Global geographic distribution and host range of fusarium circinatum, the causal agent of pine pitch canker

Review Global Geographic Distribution and Host Range of Fusarium circinatum, the Causal Agent of Pine Pitch Canker Rein Drenkhan 1,*, Beccy Ganley 2, Jorge Martín-García3,4 , Petr Vahalík5, Kalev Adamson 1, Katarína Adamˇcíková6, Rodrigo Ahumada 7, Lior Blank 8, Helena Bragança 9, Paolo Capretti 10, Michelle Cleary 11 , Carolina Cornejo 12, Kateryna Davydenko 13,14, Julio J. Diez 3,4 , Hatice Tu˘gba Do˘gmu¸s Lehtijärvi 15, Miloˇn Dvoˇrák5, Rasmus Enderle 16 , Gerda Fourie 17, Margarita Georgieva 18, Luisa Ghelardini 10 , Jarkko Hantula 19, Renaud Ioos 20 , Eugenia Iturritxa 21, Loukas Kanetis 22 , Natalia N. Karpun 23, András Koltay 24 , Elena Landeras 25, Svetlana Markovskaja 26, Nebai Mesanza 21, Ivan Milenkovi´c 27,28 , Dmitry L. Musolin 29 , Konstantinos Nikolaou 30, Justyna A. Nowakowska 31 , Nikica Ogris 32 , Funda Oskay 33 , Tomasz Oszako 34 , Irena Papazova-Anakieva 35, Marius Paraschiv 36, Matias Pasquali 37 , Francesco Pecori 38, Trond Rafoss 39, Kristina Raitelaityt˙ e26, Rosa Raposo 4,40, Cecile Robin 41 , Carlos A. Rodas 42, Alberto Santini 38, Antonio V. Sanz-Ros 4,43 , Andrey V. Selikhovkin 29,44, Alejandro Solla 45 , Mirkka Soukainen 46, Nikoleta Soulioti 47, Emma T. Steenkamp 17, Panaghiotis Tsopelas 47, Aleksandar Vemi´c 27, Anna Maria Vettraino 48 , Michael J. Wingfield 17 , Stephen Woodward 49, Cristina Zamora-Ballesteros 50 and Martin S. Mullett 28,51 1Institute of Forestry and Rural Engineering, Estonian University of Life Sciences, Fr. R. Kreutzwaldi 5, 51006 Tartu, Estonia; kalev[email protected] 2The New Zealand Institute for Plant and Food Research Limited, 412 No.1 Road RD2, 3182 Te Puke, New Zealand; Beccy[email protected] 3Department of Plant Production and Forest Resources, University of Valladolid, Avenida de Madrid 44, 34071 Palencia, Spain; [email protected] (J.M.-G.); jdcaser[email protected] (J.J.D.) 4 Sustainable Forest Management Research Institute, University of Valladolid – INIA, Avenida de Madrid 44, 34071 Palencia, Spain; [email protected] (R.R.); [email protected] (A.V.S.-R.) 5Faculty of Forestry and Wood Technology, Mendel University in Brno, Zemˇedˇelská3, 61300 Brno, Czech Republic; petr[email protected] (P.V.); [email protected] (M.D.) 6Department of Plant Pathology and Mycology, Institute of Forest Ecology, Slovak Academy of Sciences, Akademická2, 949 01 Nitra, Slovakia; [email protected] 7Bioforest S.A., Km. 15 S/N, Camino a Coronel, 403 0000 Concepcion, Chile; [email protected] 8Department of Plant Pathology and Weed Research, Agricultural Research Organization, Volcani Center, HaMaccabim Rd 68, 7528809 Rishon LeZion, Israel; [email protected].il 9Instituto Nacional de Investigação Agrária e Veterinária, I.P. (INIAV, I.P.) & GREEN-IT Bioresources for Sustainability, ITQB NOVA. Av da República, Quinta do Marquês, 2780-159 Oeiras, Portugal; [email protected] 10 Department of Agriculture, Food, Environment and Forestry, Universitàdegli Studi di Firenze, Piazzale delle Cascine, 18, 50144 Firenze, Italy; paolo.capr[email protected] (P.C.); [email protected] (L.G.) 11 Southern Swedish Forest Research Centre, Swedish University of Agricultural Sciences, Sundsvägen 3, 23053 Alnarp, Sweden; [email protected] 12 WSL Swiss Federal Research Institute, Zürcherstrasse 111, 8903 Birmensdorf, Switzerland; [email protected] 13 Department of Forest Protection, G. M. Vysotskiy Ukrainian Research Institute of Forestry and Forest Melioration, 61024 Kharkiv, Ukraine; [email protected] 14 Department of Forest Mycology and Plant Pathology, Swedish University of Agricultural Sciences, 75007 Uppsala, Sweden 15 Faculty of Forestry, Isparta University of Applied Sciences, 32260 Isparta, Turkey; [email protected] Forests 2020,11, 724; doi:10.3390/f11070724 www.mdpi.com/journal/forests Forests 2020,11, 724 2 of 40 16 Institute for Plant Protection in Horticulture and Forests, Federal Research Centre for Cultivated Plants (JKI), Messeweg 11/12, 38104 Braunschweig, Germany; [email protected] 17 Department of Biochemistry, Genetics and Microbiology, Forestry and Agricultural Biotechnology Institute (FABI), University of Pretoria, Lynwoond and University Roads, 0028 Pretoria, South Africa; [email protected] (G.F.); [email protected] (E.T.S.); [email protected] (M.J.W.) 18 Department of Forest Entomology, Phytopathology and Game fauna, Forest Research Institute, Bulgarian Academy of Sciences, 132 St. Kliment Ohridski Blvd, 1756 Sofia, Bulgaria; margaritageor[email protected] 19 Department of Natural Resources, Natural Resources Institute Finland (Luke), Latokartanonkaari 9, 00790 Helsinki, Finland; [email protected] 20 ANSES Plant Health Laboratory, Unit of Mycology, Domaine de Pixérécourt, Bât. E., 54220 Malzéville, France; [email protected] 21 Forestry Science Department, Neiker Institute, Campus Agroalimentario de Arkaute, S/N 01080 Arkaute, Álava, Spain; [email protected] (E.I.); [email protected] (N.M.) 22 Department of Agricultural Sciences, Biotechnology & Food Science, Cyprus University of Technology, Arch. Kyprianos Str. 30, 3603 Limassol, Cyprus; [email protected] 23 Russian Research Institute of Floriculture and Subtropical Crops, J¯ anis Fabriciuss str., 2/28, 354002 Sochi, Russia; [email protected] 24 Forest Protection Department, NARIC Forest Research Institute, Hegyalja u. 18, 3232 M á trafüred, Hungary; [email protected] 25 Laboratorio de Sanidad Vegetal, Gobierno del Principado de Asturias, C/Lucas Rodríguez Pire, 4-bajo, 33011 Oviedo, Spain; [email protected]g 26 Institute of Botany, Nature Research Centre, Žaliu˛ju˛ ežeru˛ 49, 08412 Vilnius, Lithuania; [email protected] (S.M.); [email protected] (K.R.) 27 Department of Forest Protection, Faculty of Forestry, University of Belgrade, Kneza Višeslava 1, 11030 Belgrade, Serbia; [email protected] (I.M.); aleksandar[email protected] (A.V.) 28 Phytophthora Research Centre, Mendel University in Brno, Zemˇedˇelská3, 61300 Brno, Czech Republic; [email protected] or [email protected] 29 Department of Forest Protection, Wood Science and Game Management, Saint Petersburg State Forest Technical University, Institutskiy per., 5, 194021 Saint Petersburg, Russia; [email protected] (D.L.M.); [email protected] (A.V.S.) 30 Department of Forests, Ministry of Agriculture, Rural Development and Environment, Loukis Akritas 26, 1414 Nicosia, Cyprus; [email protected].cy 31 Institute of Biological Sciences, Faculty of Biology and Environmental Sciences, Cardinal Stefan Wyszynski University in Warsaw, Wóycickiego 1/3 Street, 01-938 Warsaw, Poland; [email protected] 32 Department of Forest Protection, Slovenian Forestry Institute, Veˇcna pot 2, 1000 Ljubljana, Slovenia; [email protected] 33 Faculty of Forestry, Çankırı Karatekin University, 18200 Çankırı, Turkey; [email protected] 34 Department of Forest Protection, Forest Research Institute in S˛ekocin Stary, Braci Le´snej 3, 05-090 Raszyn, Poland; [email protected].pl 35 Faculty of Forestry, Ss. Cyril and Methodius University in Skopje, 16 Makedonska brigada br.1, 1000 Skopje, Republic of North Macedonia; [email protected] 36 Department of Forest Protection, National Institute for Research and Development in Forestry – Bras ,ov Station, Clos ,ca 13, 500040 Bras ,ov, Romania; [email protected] 37 Department of Food, Environmental and Nutritional Sciences, University of Milan, Via Celoria 2, 20133 Milano, Italy; [email protected] 38 Institute for Sustainable Plant Protection – C.N.R., Via Madonna del Piano, 10, 50019 Sesto Fiorentino, Italy; [email protected].it (F.P.); [email protected] (A.S.) 39 Biotechnology and Plant Health Division, Norwegian Institute of Bioeconomy Research, 1431 Ås, Norway; [email protected] 40 Centre of Forest Research, National Institute for Agricultural and Food Research and Technology (INIA), C. Coruna, 28040 Madrid, Spain 41 INRAE, Univ. Bordeaux, BIOGECO, F-33610 Cestas, France; cecile.r[email protected] 42 Forest Health Protection Programme, Smurfit Kappa Colombia – University of Pretoria, Calle 15 N ◦ 18 -109. Yumbo – Valle Colombia, 760502 Cali, Colombia; Carlos.r[email protected] Forests 2020,11, 724 3 of 40 43 Plant Pathology Laboratory, Calabazanos Forest Health Center (Regional Government of Castilla y León), Polígono Industrial de Villamuriel S/N, Villamuriel de Cerrato, 34190 Palencia, Spain 44 Department of Biogeography and Environmental Protection, Saint Petersburg State University, Universitetskaya emb., 13B, 199034 Saint Petersburg, Russia 45 Faculty of Forestry, University of Extremadura, Avenida Virgen del Puerto 2, 10600 Plasencia, Spain; [email protected] 46 Laboratory and Research Division, Plant Analytics Unit, Finnish Food Authority, Mustialankatu 3, 00790 Helsinki, Finland; [email protected] 47 Institute of Mediterranean Forest Ecosystems, Terma Alkmanos, 11528 Athens, Greece; [email protected] (N.S.); [email protected] (P.T.) 48 Department for Innovation in Biological, Agro-food and Forest Systems (DIBAF), University of Tuscia, Via S. Camillo de Lellis, 01100 Viterbo, Italy; [email protected] 49 School of Biological Sciences, University of Aberdeen, Cruickshank Building, St. Machar Drive, Aberdeen AB24 3UU, UK; s.woodwar[email protected] 50 Department of Vegetal Production and Forestry Resources, College of Agricultural and Forestry Engineering, University of Valladolid, Av Madrid 44, 34004 Palencia, Spain; cristinazamoraballester[email protected] 51 Forest Research Forest Research, Alice Holt Lodge, Surrey, Farnham GU10 4LH, UK *Correspondence: r[email protected] Received: 27 May 2020; Accepted: 25 June 2020; Published: 1 July 2020   Abstract: Fusarium circinatum, the causal agent of pine pitch canker (PPC), is currently one of the most important threats of Pinus spp. globally. This pathogen is known in many pine-growing regions, including natural and planted forests, and can affect all life stages of trees, from emerging seedlings to mature trees. Despite the importance of PPC, the global distribution of F. circinatum is poorly documented, and this problem is also true of the hosts within countries that are affected. The aim of this study was to review the global distribution of F. circinatum, with a particular focus on Europe. We considered (1) the current and historical pathogen records, both positive and negative, based on confirmed reports from Europe and globally; (2) the genetic diversity and population structure of the pathogen; (3) the current distribution of PPC in Europe, comparing published models of predicted disease distribution; and (4) host susceptibility by reviewing literature and generating a comprehensive list of known hosts for the fungus. These data were collated from 41 countries and used to compile a specially constructed geo-database. A review of 6297 observation records showed that F. circinatum and the symptoms it causes on conifers occurred in 14 countries, including four in Europe, and is absent in 28 countries. Field observations and experimental data from 138 host species revealed 106 susceptible host species including 85 Pinus species, 6 non-pine tree species and 15 grass and herb species. Our data confirm that susceptibility to F. circinatum varies between different host species, tree ages and environmental characteristics. Knowledge on the geographic distribution, host range and the relative susceptibility of different hosts is essential for disease management, mitigation and containment strategies. The findings reported in this review will support countries that are currently free of F. circinatum in implementing effective procedures and restrictions and prevent further spread of the pathogen. Keywords: invasive pathogen; climate change; interactive map of pathogen; susceptibility 1. Introduction Fusarium circinatum (teleomorph Gibberella circinata Nirenberg and O’Donnell [ 1 ]) is an invasive pathogen that causes a disease known as pine pitch canker (PPC). This fungus is a quarantine organism, included in the EPPO (European and Mediterranean Plant Protection Organization) A2 list and regulated in the EU (European Union) [ 2 ]. In nurseries and the wider environment, the pathogen Forests 2020,11, 724 4 of 40 affects pines (Pinus spp.) and Douglas-fir (Pseudotsuga menziesii) [ 3 , 4 ]. It has also been isolated from asymptomatic plants (Poaceae, Asteraceae, Lamiaceae, Rosaceae) growing close to PPC-affected trees in pine stands [ 5 – 7 ]. Additionally, artificial inoculation trials have shown the potential for F. circinatum to infect a wide range of plant genera, e.g., Abies,Larix,Libocedrus,Picea [ 3 , 8 – 10 ], although natural infections of species in these taxa have not been reported. Fusarium circinatum can affect all stages of pine development. Being seed-borne [ 11 ], it can cause seed and seedling mortality (preand post-emergence damping-off, respectively), and lignified seedling decay (late damping-off) [ 12 ]. The pathogen also causes dieback of branches and stems on young and mature trees where the main symptoms are copious resin (‘pitch’) production from cankers, hence the common name “pine pitch canker disease” [ 13 – 15 ]. Infection is usually via wounds through which spores gain entry into the plant tissue [ 16 , 17 ]. However, wounds are not always necessary for infection although they are for disease development [ 18 ]. The dispersal of the infective propagules occurs via agents such as insects, water, and wind [ 19 – 21 ]. However, the main avenues for long-distance movement of the fungus are associated with human activities, particularly plant trade and movement of contaminated soil and equipment [22,23]. Pine pitch canker was first described in the Southeast USA (North and South Carolina) in 1945 [ 24 ], where outbreaks tended to occur in poorly managed stands or after severe drought events [ 17 ]. Since then, F. circinatum has been recorded in Africa, Asia, South America, and Southern Europe, although information concerning its distribution in these regions is often not easily accessible or uniformly presented [ 25 – 27 ]. However, the pathogen is now known from most pine growing regions, generally with high incidence in Mediterranean and sub-tropical climates and some spread into temperate regions [ 28 ]. Because its spread and establishment is strongly dependent on climatic conditions, primarily temperature and humidity [ 4 , 28 , 29 ], F. circinatum is unlikely to spread to cooler, northern latitudes despite the presence of susceptible hosts in these areas [ 29 , 30 ]. Nevertheless, global trade has exacerbated the spread of many forest pathogens, and this trend seems set to continue [ 31 , 32 ]. Introduction of the pathogen via anthropogenic activities into nurseries or areas with suitable microclimates could lead to disease spread into what have hitherto been thought of as generally less suitable areas. The European COST Action FP1406 “Pine pitch canker—strategies for management of Gibberella circinata in greenhouses and forests (PINESTRENGTH)” brought together scientists and stakeholders from 36 countries to establish a European-focused network dedicated to increasing our understanding of F. circinatum and its effects on pine. The main objectives were to increase knowledge on the biology, ecology, and spread pathways of F. circinatum; to evaluate the potential to develop effective and environmentally friendly prevention and mitigation strategies and to deliver these outcomes to stakeholders and policy makers. In this regard, updated information on the geographic distribution and host range of the pathogen, as well as on the relative susceptibility of different hosts, were considered. These factors represent important elements of disease management, mitigation and containment strategies. This would potentially also allow countries currently free of the pathogen to implement effective procedures and restrictions to prevent its introduction. In this review, we considered the global distribution of F. circinatum, with a particular focus on Europe. More specifically the objectives were to (1) determine presently available and historical pathogen records, based on the confirmed reports from Europe and globally, (2) review the global populations and genetic diversity of the pathogen, (3) compare the current distribution of PPC in Europe with published models of predicted disease distribution; and (4) provide a comprehensive and up to date list of susceptible hosts. 2. The Geographic Distribution of F. circinatum The occurrence of F. circinatum is well known for some countries, while information regarding its distribution globally or within many countries is scattered or poorly documented, and in some cases records are erroneous. To present the current distribution of F. circinatum, a geo-database for the Forests 2020,11, 724 5 of 40 pathogen was developed and used to generate an interactive map (see Supplementary Materials and interactive map: http://bit.do/phytoportal). The geo-database contains geographic coordinates of 6297 sampling or observation records from 106 different hosts in 41 countries (including states): Africa (1 country), North and South America (7 countries), Asia (5 countries, including the Asian part of the Russian Federation and the Asian part of Turkey), Europe (28 countries including the European part of the Russian Federation and the European part of Turkey), and Oceania (2 countries). The interactive map shows the presence and first reports of F. circinatum in 14 countries, including four in Europe (Figure 1; Table 1). In 12 countries (Brazil, Chile, Colombia, France, Italy, Japan, Mexico, Portugal, Spain, South Africa, Uruguay, and USA[not allstates]), thepresence of F. circinatum was confirmedusingmolecular methods, and in two countries (South Korea and Haiti) the presence of the pathogen was verified using classical morphological approaches (e.g., vegetative and reproductive traits). In France and Italy, F. circinatum has been found in nurseries and at public gardens, and in both of these European countries the pathogen is considered officially eradicated [ 27 ] (Figure 2; Table 1). PPC was considered absent in 28 countries (24 European countries, Australia, New Zealand, Turkey and Israel) after rigorous field observations and/or laboratory testing (see http://bit.do/phytoportal). Countries for which no data on presence or absence were available were not considered to be positive or negative. The data were obtained as described in the instructions of the geo-database for F. circinatum distribution (see Supplementary Materials, Table S1). A summary of pathogen distribution by continent is presented below. 2.1. Europe In Europe, F. circinatum has been reported in four countries: Spain [ 33 , 34 ], Italy [ 35 ], France [ 36 ], and Portugal [ 37 ]. The first record of F. circinatum in Europe was in 1995 on nursery seedlings of P. radiata and P. halepensis in Galicia, northern Spain [ 33 ]. In 1997, the pathogen was evidently found in a nursery in the Basque Country, northern Spain, causing mortality of P. radiata seedlings [ 38 – 40 ], but F. circiantum presence was formally identified in 2004 [ 34 ]. The disease reappeared in northern Spain, in Asturias, some years later (2003–2004) on nursery seedlings of P. radiata and P. pinaster [ 34 ]. In 2004, the pathogen was reported for the first time in the forest environment, where it caused PPC of P. radiata in a 20-year-old forest plantation in Cantabria, northern Spain [ 34 ]. Thus, F. circinatum has been present for over 20 years in Spanish nurseries and over 10 years in forests. In 2006, an eradication and control programme was launched to limit its spread in Spain, and in 2007 the EU adopted measures to prevent its spread to other member states [ 2 ]. Measures undertaken included the elimination of infected material and the establishment of an intensive and continuous monitoring programme in forests and of plant reproductive material from both public and private entities. In Castilla y Le ó n, F. circinatum was found from 2005 to 2013, both in nurseries and forest stands, but there have been no subsequent reports of the fungus in that region (Forest Health Service, direct communication). However, the pathogen remains active in several coastal areas despite eradication attempts. If F. circinatum cannot be eradicated from these regions, it is likely that new infections will occur and the pathogen will continue to spread to inland areas [41]. In Portugal, F. circinatum was first detected in 2007 from infected seedlings of P. radiata and P. pinaster in a nursery located in the centre of the country [ 37 ]. As a consequence of this first report, following EU and national rules, an action plan was implemented by the Forest Authority to establish extraordinary phytosanitary measures, aiming to eradicate and/or control the disease. In both Portugal and Spain, after each detection of F. circinatum, an infested zone and a buffer zone (at least 1 km wide) were established around the infested site. In Portugal, the survey and programme results (Figure 1,http://bit.do/phytoportal) showed that until 2016 all positive reports of F. circinatum were obtained exclusively from nurseries. In 2016, the fungus was also detected for the first time in a plantation of P. radiata in Minho province [ 42 ] and in the same province on two P. pinaster trees in 2018 [ 42 ]. In both cases, Pinus plants in nurseries and in forests were destroyed and the surrounding area intensively surveyed with no further positive findings to date [ 27 ]. Although the lack of new Forests 2020,11, 724 6 of 40 positive records suggests that the pathogen has been successfully eliminated, it is premature to declare official eradication in the whole country. In Italy and France, F. circinatum appears to have been eradicated successfully. Pine pitch canker was reported in Italy in 2005 on ornamental plantings (Foggia, southern Italy) of the native species P. pinea and P. halepensis [ 35 ]. Infected plants were promptly removed and destroyed, and no new records of the disease have subsequently been reported in gardens, nurseries or the wider environment. In France, F. circinatum was recorded for the first time in 2005 in a private garden (Perpignany, South France) on a declining Douglas-fir tree and a few declining pine trees [ 36 ] and was considered officially eradicated in 2008 after intensive monitoring [ 43 , 44 ]. In 2009, the fungus was found on P. radiata seedlings in two French nurseries: all infected plants and plants from the same nursery beds were removed and destroyed [ 45 ]. After two years of intensive survey in and around the nurseries, the pathogen was considered eradicated [27]. The current study gathered 6297 observations from 28 European countries (http://bit.do/ phytoportal). In 24 of the 28 monitored European countries, there was no evidence of F. circinatum presence (i.e., all surveys and samples were negative) (Figures 1and 2). Both morphological and molecular methods (species-specific PCR [ 46 ] or sequencing) for F. circinatum detection were used to determine presence or absence in 18 countries. In nine countries, only visual inspection of symptoms in the field or morphological diagnosis of cultures in the laboratory was used to confirm pathogen absence or presence. However, visual inspection alone may not be sufficiently reliable for F. circinatum detection and identification because the fungus may behave as an endophyte or latent pathogen with no visible external symptoms or it can be mistaken for other pathogens that cause similar symptoms [ 7 , 47 , 48 ]. It is preferable, therefore, to combine visual surveys with molecular detection methods for reliable and more precise identification [ 46 , 49 , 50 ]. In the current study, both visual and molecular surveys were considered. 2.2. North America and South America Fusarium circinatum was first recorded on pines in southeastern North America in 1945 [ 24 ]. The pathogen was described from Pinus virginiana in North and South Carolina [ 24 ]. Pine pitch canker has subsequently been reported from other states including Alabama, Arkansas, California, Florida, Georgia, Indiana, Louisiana, Mississippi, Tennessee, Texas, and Virginia [ 26 , 29 ] (see Figures 1and 2, Table 1). In Mexico, F. circinatum was recorded for the first time in 1989 on planted P. halepensis and natural stands of P. douglasiana and P. leiophylla [ 39 ]. Consistent with the idea that F. circinatum is native to Mexico [ 51 , 52 ], the pathogen is widespread in this country with records from at least nine states (Sinaloa, Nayarit, Mexico, Nuevo Leon, Puebla, Michoacan, Jalisco, Durango, and Tamaulipas). There were no published records for the pathogen in Canada (Tod Ramsfield, personal comm.) or in the USA states of Massachusetts and Washington [27]. The first report of PPC in Haiti was in 1953 [ 53 ], although thereafter no new information is available about the disease in that country. The first report of F. circinatum in South America was in P. radiata mother plants (hedges) in nurseries of Chile in 2001 [ 54 ]. Since then, the pathogen has been found in Uruguay, Colombia, and Brazil [ 55 – 58 ]. In Chile, Uruguay, and Brazil, the pathogen has been reported only in nurseries and it has apparently not spread to the forest environment. Conversely, in Colombia, F. circinatum was first detected in 2005, affecting seedlings of P. patula,P. maximinoi, and P. tecunumanii in nursery, but was later also found in isolated trees on plantations [ 56 , 57 ]. More recently in 2017, the pathogen was reported and identified as F. circinatum causing damages in P. patula and high elevation plantations of P. tecunumanii (Carlos Rodas, unpublished). 2.3. Asia In Asia, F. circinatum is known to be present only in Japan and South Korea [ 59 , 60 ]. There are no records of the pathogen in the Russian Far East, nor in western Asia (e.g., Israel and Turkey, including the European part of Turkey) (see Figures 1and 2, Table 1). In Japan, PPC was first recorded in 1981 Forests 2020,11, 724 7 of 40 on native P. luchensis trees on Amami ¯ Oshima and Okinawa Islands [ 60 ]. In South Korea, PPC was reported from natural stands and plantations of P. rigida in the mid-1990s where it caused tree mortality in Seoul and Kangwon Provinces [59]. 2.4. Africa In Africa, F. circinatum has been reported only from South Africa, where it was documented for the first time in 1991 [ 12 ]. The pathogen was responsible for an outbreak of root and root collar disease on P. patula seedlings in a single nursery, and has subsequently spread to most pine seedling production nurseries in the country [ 4 ]. Accordingly, various management strategies have been investigated and developed to limit the occurrence and spread of F. circinatum in commercial forestry, e.g., nursery hygiene practices to limit the build-up of inoculum [ 61 – 63 ] and the use of chemical and biologically derived compounds to boost plant defence responses [ 64 ]. However, F. circinatum remains a major challenge to seedling production and plantation establishment in South Africa [65,66]. In 2005, PPC was detected for the first time outside the nursery environment on established trees in a plantation of P. radiata and it is now commonly found on this species in the Western Cape Province in South Africa [ 67 , 68 ]. The pathogen has since been detected also in plantations of P. greggii in the Eastern Cape and KwaZulu-Natal Provinces where localized outbreaks of PPC have occurred [ 66 , 68 , 69 ]. Additionally, in the summer rainfall area of the country, localised outbreaks of PPC have been recorded in plantations of P. patula, which is the most widely planted Pinus species in South Africa [ 70 ]; Steenkamp and Wingfield, unpublished]. To limit losses related to PPC, considerable effort has been dedicated to develop and deploy planting stock that is tolerant or more resistant to PPC. These include less susceptible families of P. patula [ 71 – 73 ] and certain families of P. maximinoi, P. pseudostrobus, low-elevation P. tecunumanii, and P. elliottii var. elliottii [ 65 , 74 ]. Various hybrids have also been evaluated, with low-elevation P. tecunumanii × patula,P. elliottii × caribaea, and P. patula × oocarpa showing low levels of susceptibility to infection by F. circinatum [ 75 , 76 ], and many of these hybrids have already been deployed commercially. 2.5. Oceania Fusarium circinatum has not been found in Oceania. In both Australia and New Zealand, surveillance programmes regularly monitor pine and Douglas-fir seedlings and mature trees for unwanted organisms including F. circinatum. Suspect samples are tested using morphological and molecular methods and, to date, all samples tested have proven negative for F. circinatum (see Figures 1 and 2). Both countries have strict border biosecurity regulations, and at least one potential introduction of the pathogen has been prevented. In this case, F. circinatum was detected in 2004 on scions of Douglas-fir from California, and the pre-border detection required the infected material to be destroyed before it was imported into New Zealand [77]. Forests 2020,11, 724 8 of 40 Figure 1. Historical dispersal of Fusarium circinatum according to the date the pathogen was first recorded in the country (see Table 1for details). The data are based on literature and monitoring records. Figure 2. Global distribution of Fusarium circinatum showing where the pathogen is present, eradicated, not found or data are not available. See the interactive map: http://bit.do/phytoportal for detailed locations within countries. Forests 2020,11, 724 9 of 40 Table 1. Geographic distribution, by country, of Fusarium circinatum (FC) including the type of planting, year found, host species affected, and the method used to identify the pathogen. Continent/ Country/State Year of First Record of FC in Nursery and/or Wider Environment Host Species Type of Planting/Sampling Site Identification Method References or Data Holder Europe France 2005 1, 2 Pseudotsuga menziesii, Pinus sp. Urban greenery species-specific PCR, sequence analysis [37] France 2008 2P. menziesii Nursery species-specific PCR, sequence analysis [44] Italy 2005 1, 2 P. halepensis, P. pinea Urban greenery species-specific PCR [36] Portugal 2007 1, 2 Pinus radiata, P. pinaster Nursery species-specific PCR, sequence analysis [38] Portugal 2016 2P. radiata Forest plantation species-specific PCR, sequence analysis [42] Spain 1995 1P. radiata, P. halepensis Nursery, in Galicia visual observation [34] Spain 1997 P. radiata Nurseries, in Basque Country mycelial morphology [39] Spain 2003 P. radiata, P. pinaster Nursery, in Asturias species-specific PCR [35] Spain 2004 P. radiata Plantation, in Cantabria species-specific PCR [35] Spain 2005 P. sylvestris, P. nigra, P. pinaster, P. pinea Nurseries in Castilla y León morphological traits, species-specific PCR Regional Forest Health Service Spain 2005 P. sylvestris, P. nigra, P. pinea, P. radiata Forest plantations, in Castilla y León morphological traits, species-specific PCR Regional Forest Health Service Asia Japan 1981 1P. luchuensis Forest, Amamioshima Island (Ryukyu Archipelago) and the Okinawa island mycelial morphology [60] South Korea 1995 1P. rigida Urban greenery, forest mycelial morphology [59] Africa South Africa 1991 1P. patula Nursery, Ngodwana Mpumalanga Province mycelial morphology [12] South Africa 2005 P. radiata Plantation, Tokai, Western Cape Province species-specific PCR, sequence analysis [67] South Africa 2007 P. greggii Plantation, Ugie, Eastern Cape Province sequence analysis [68,69] South Africa 2014 P. patula Plantation, Louis Trichardt, Limpopo Province sequence analysis [70] North America Haiti 1953 1P. occidentalis Natural forest mycelial morphology [53] Mexico 1989 1P. douglasiana, P. halepensis, P. leiophylla, P. greggii, P. patula Forest plantation and natural stand unknown, probably visual observation [40] Forests 2020,11, 724 16 of 40 Figure 4. European climatic suitability for Fusarium circinatum based on the CLIMEX model parameters ofGanley etal.[ 28 ]using higherresolutionclimaticdata[ 133 ]. TheEuropeandistribution ofnon-nursery F. circinatum findings is shown as red dots in the main figure, while the inset displays the dataset used by Ganley et al. [28] in the original CLIMEX modelling. Table 2. Minimum, average and maximum values of climatic and topographical variables from the dataset of Hijmans et al. [ 134 ] and new observations of current distribution of Fusarium circinatum from the geo-database presented in the current study. Minimum Average Maximum Altitude −3 m a.s.l. 262 m a.s.l. 3619 m a.s.l. Annual mean temperature 6.2 ◦C 13.7◦C 25.4 ◦C Mean temperature of the warmest month 12.4 ◦C 24.7 ◦C 36.5 ◦C Mean temperature of the coldest month −14.2 ◦C 4.8 ◦C 16.7 ◦C Annual precipitation sum 324 mm 1259 mm 3062 mm Precipitation sum of the wettest month 51 mm 154 mm 583 mm Precipitation sum of the driest month 0 mm 57 mm 151 mm 6. Host Range Knowledge of the host range of F. circinatum has been growing steadily, and recently reports of non-pine hosts have increased. For the purpose of this review, all known hosts of F. circinatum and their susceptibility ratings were compiled and assessed (Tables 3–6). The host list and susceptibility ratings were based on results of both field observations and experimental inoculations reported in peer-reviewed and “grey” literature, as well as from unpublished studies and the geo-database records compiled in this study. Such an extensive and integrated list has not previously been published because the information is scattered throughout numerous sources. We summarized these results and included data for 138 hosts (including 18 Pinus hybrids) tested in growth chamber, greenhouse, nursery and field inoculations or survey data from the wider environment. Taxa from which data have been gathered include 96 species in the genus Pinus (including Pinus hybrids), 24 other tree species in 15 genera (Abies,Cedrus,Chamaecyparis, xCupressocyparis, Cupressus,Eucalyptus,Larix,Libocedrus,Picea,Podocarpus,Pseudotsuga,Sequoia,Sequoiadendron,Thuja, and Widdringtonia) and 18 grass and herb species (see Tables 3–6;http://bit.do/phytoportal). In total, Forests 2020,11, 724 17 of 40 F. circinatum has been reported to infect 106 different plant species, including 67 Pinus species and 18 Pinus hybrids (Tables 3–5), as well as 6 non-pine tree species and 15 grass and herb species (Table 6). Overall, levels of susceptibility vary with the plant’s age class, from recently emerged seedlings to mature trees. This variation is primarily due to the different behaviour of, and type of disease caused by, F. circinatum on plants of different ages. In pine seedlings, for example, F. circinatum essentially causes root disease (manifested as preand post-emergence, as well as late, damping-off), which is mainly seen in nursery situations, while the predominant symptom of infection in older or established pine trees are resinous cankers on the above-ground plant parts. Many species affected as seedlings in a nursery situation have not been seen to be affected as mature trees in a forest situation (Wingfield, unpublished). Because the behaviour and disease cycle of F. circinatum is likely to differ significantly in these two settings, the susceptibility ratings of seedlings and young plants (Table 3) were treated separately from those of older or mature trees (Table 4). Nevertheless, as nursery production is the primary route of F. circinatum transmission to the wider environment, a summary of the susceptibility ratings for both seedlings and mature trees is given below. This treatment allows for an assessment of the highest and lowest risk species that may serve as ‘carriers’ of the pathogen from the nursery to the forest and exhibit the disease in both settings. 6.1. Host Susceptibility Ratings In this work, host susceptibility rating was based on the following categories: high, moderate-high, moderate, low-moderate, low, highly variable, unknown, and resistant. A host was considered resistant if no F. circinatum symptoms were detected after inoculation trials and natural infection with the fungus does not occur. The highly variable susceptibility category was assigned to the hosts (seedlings, young plants, young or mature trees) for which ranking varied in different studies from resistant to susceptible. Moreover, we did not include in these ratings endophytic infections, or asymptomatic plants (plants infected but seemingly healthy), as there is still very limited information about this particular lifestyle trait for F. circinatum. The presence or absence of F. circinatum and severity of disease for 96 different Pinus taxa (including species, subspecies, varieties, and hybrids), either experimentally tested or observed, is reported (Tables 3–5). Unambiguous susceptibility rankings were obtained for 21 Pinus spp. (i.e., high susceptibility—three species; moderate susceptibility—four species; low susceptibility—13 species; resistant—one species) and 14 Pinus hybrids (i.e., moderate susceptibility—three hybrids; low susceptibility—11 hybrids). Nineteen Pinus species and seven Pinus hybrids were classified as having variable susceptibility, because different studies placed them in different susceptibility categories, while for 28 species the susceptibility classification was unknown. No symptoms of disease were observed on an additional 10 Pinus taxa (P. cembra,P. contorta var. latifolia,P. heldreichii,P. mugo subsp. mugo,P. mugo subsp. rotundata,P. nigra subsp. nigra,P. nigra subsp. pallasiana,P. peuce, P. sylvestris var. hamata, and P. wallichiana) which were monitored and systematically inspected for F. circinatum in the field (http://bit.do/phytoportal). Because these trees were monitored in areas where the pathogen has not been reported, the susceptibility or resistance status remains unknown. It can therefore be concluded that 67 Pinus species and 18 Pinus hybrids are known to be susceptible to F. circinatum based on artificial inoculation and natural infection observations (see Tables 3–5). Susceptibility ratings for F. circinatum were analysed separately for different age classes of Pinus and non-Pinus hosts; i.e., seedlings and young plants (recently emerged pine seedling and plants, ≤10 years old) or mature trees ( ≥ 11 years). When only seedlings and plants of Pinus were considered, a total of 18 species were rated as highly susceptible, four as moderate-highly susceptible, 17 as moderately susceptible, seven as moderately-low susceptible, 22 as low susceptible, and one as resistant (P. koraiensis) to F. circinatum. Twelve Pinus species known to be hosts of F. circinatum and nine of the species have unknown susceptibility at the seedling stage (Table 3). When mature trees were considered separately, only a single pine species (P. radiata) was rated as highly susceptible, five species were rated as having low-moderate susceptibility, and four as having low susceptibility to Forests 2020,11, 724 18 of 40 F. circinatum. Twenty-six mature Pinus species known to be hosts of F. circinatum and 23 of species have unknown susceptibility rating to F. circinatum (Table 4). Three Pinus species in both age classes have highly variable susceptibility to F. circinatum (Tables 3and 4). Two pine species, P. densiflora and P. koraiensis, have been recorded as resistant to F. circinatum in 3–4 year old seedling inoculation trials conducted in greenhouses [ 59 , 135 ]. However, F. circinatum has been isolated from P. densiflora trees in Japan although the susceptibility of this host as a mature tree was not rated [ 136 ]. Therefore, we consider P. densiflora to have highly variable susceptibility to F. circinatum and the only truly resistant Pinus species to be P. koraiensis. Non-pine tree species are generally only weakly susceptible or are resistant to F. circinatum. The susceptibility of non-pine hosts to F. circinatum was tested or observed on 24 tree and 18 herbaceous species (Table 6). Three conifer species (Larix kaempferi,Libocedrus decurrens,Pseudotsuga menziesii) were categorised as having low level of susceptibility. Another three conifer species (Abies alba,Larix decidua, Picea abies) were considered as having highly variable susceptibility because recently emerged seedlings were classed as susceptible to F. circinatum, whereas 2-year-old and older plants were considered resistant [ 8 – 10 ]. All other non-pine hosts, 18 non-pine tree species in 10 different genera, as well as three herbaceous species, were classed as resistant to F. circinatum (Table 6). Although only three herbaceous plant species are classified as resistant to F. circinatum (Table 6), it must be noted that only a very limited number of herbaceous plants have been tested in this respect in pathogenicity assays. Fifteen species of herbaceous plants are known hosts of F. circinatum in the wider environment, but their levels of susceptibility are unknown [ 5 – 7 , 26 , 137 ]. An additional consideration is that in some P. radiata plantations infected with F. circinatum, a number of herbaceous plants (Table 6) have been reported to be infected endophytically with F. circinatum [ 7 ]. It is thus clear that the full host range of F. circinatum, and susceptibility of each species, has yet to be elucidated. Forests 2020,11, 724 19 of 40 Table 3. Susceptibility list of Pinus species seedlings and young plants (recently emerged pine seedling and plants, ≤10 years old) to Fusarium circinatum. Susceptibility/Host Species1Common English Names Subgenus; Section; Subsection2 Type of Infection Growth or Test Conditions Seedlings and/or Plant Age3References Susceptibility high Pinus brutia Ten. Turkish pine, Calabrian pine, East Mediteranean pine, Brutia pine Pinus; Pinus; Halepenses Artificial Growth chamber 2 years J. Martín-García, unpublished Pinus cembroides Zucc. Pinyon pine, Mexican nut pine Strobus; Parrya; Cembroides Artificial Greenhouse Unknown [138] Pinus douglasiana Martínez Gordon’s pine, Douglas pine Pinus; Pinus; Ponderosae; ‘Pseudostrobus Group’ Artificial Greenhouse Unknown [138] Pinus greggii Engelm. ex Parl. Gregg’s pine Pinus; Pinus; Oocarpae; ‘Oocarpa Group’ Artificial Field 2 years [76] Pinus halepensis Mill. Aleppo pine Pinus; Pinus; Halepenses Artificial Growth chamber 2 years J. Martín-García, unpublished Pinus hartwegii Lindl. Endlicher pine Pinus; Pinus; Ponderosae; ‘Montezumae Group’ Artificial Greenhouse Unknown [138] Pinus herrerae Martínez Herrera’s pine Pinus; Pinus; Oocarpae; ‘Teocote Group’ Artificial Greenhouse 12 weeks [139] Pinus montezumae Lamb. Montezuma pine Pinus; Pinus; Ponderosae; ‘Montezumae Group’ Artificial Greenhouse Unknown [138] Pinus mugo Turra Mountain pine, dwarf mountain pine Pinus; Pinus, Pinus Artificial Growth chamber Recently emerged [9] Pinus mugo Turra subsp. uncinata (Ramond ex DC.) Domin. Swiss mountain pine Pinus; Pinus, Pinus Artificial Growth chamber Recently emerged [8] Pinus nigra J.F.Arnold Austrian pine, black pine Pinus; Pinus; Pinus Artificial Growth chamber Recently emerged, 2 years [8], J. Martín-García, unpublished Pinus patula Schiede ex Schltdl. & Cham. Patula pine, Jelecote pine, Mexican weeping pine, spreading-leaved pine Pinus; Pinus; Oocarpae; ‘Oocarpa Group’ Artificial Greenhouse 7–10 m [71,75,140] Pinus pinaster Aiton Maritime pine Pinus; Pinus; Pinus Artificial Growth chamber Recently emerged, 2 years [ 8 , 141 ], J. Mart í n-Garc í a, unpublished Pinus pseudostrobus Lindl. Smooth-bark Mexican pine Pinus; Pinus; Ponderosae; ‘Pseudostrobus Group’ Artificial Greenhouse Unknown [138] Pinus radiata D. Don Monterey pine, radiata pine, insignis pine Pinus; Pinus; Attenuatae Artificial Growth chamber, greenhouse, field Recently emerged, 3 months, 1 year, 2 years, 2–3 years, 3–4 years, unknown [8,76,80,88,139,142,143] Pinus strobus L. Eastern white pine, northern white pine, white pine, Weymouth pine (British), and soft pine Strobus; Strobus;Strobi Artificial Growth chamber Recently emerged [8] Pinus sylvestris L. Scots/Scotch pine Pinus; Pinus; Pinus Artificial Growth chamber, greenhouse Recently emerged, 1.5 years, 2 years [8,10] J. Martín-García, unpublished Pinus taeda L. Loblolly pine Pinus; Pinus; Australes Artificial Greenhouse 1 year [88] Forests 2020,11, 724 20 of 40 Table 3. Cont. Susceptibility/Host Species1Common English Names Subgenus; Section; Subsection2 Type of Infection Growth or Test Conditions Seedlings and/or Plant Age3References Susceptibility moderate-high Pinus leiophylla Schiede ex Schltdl. & Cham. Chihuahua pine, smooth-leaf pine, yellow pine Pinus; Pinus; Leiophyllae Artificial Field 5–8 years [144] Pinus patula Schiede ex Schltdl. & Cham. Patula pine, Jelecote pine, Mexican weeping pine, spreading-leaved pine Pinus; Pinus; Oocarpae; ‘Oocarpa Group’ Artificial Greenhouse, Field 3 months, 21 weeks, 2 years [76,145,146] Pinus pinaster Aiton Maritime pine, cluster pine Pinus; Pinus; Pinus Artificial Greenhouse 6 months, 3 years [141,147] Pinus taeda L. Loblolly pine Pinus; Pinus; Australes Artificial Greenhouse, Field 21 weeks, 4 years [88,147] Susceptibility moderate Pinus banksiana Lamb. Jack pine, scrub pine Pinus; Pinus; Contortae Artificial Greenhouse 3.5 years [148] Pinus devoniana Lindl. Michoacán pine Pinus; Pinus; Ponderosae ‘Montezumae Group’ Artificial Greenhouse, field 12 weeks [97,139] Pinus echinata Mill. Shortleaf pine Pinus; Pinus; Australes Artificial Greenhouse 3–4 years [135] Pinus elliottii Engelm. Slash pine Pinus; Pinus; Australes Artificial Greenhouse, field 7–9 months, 8 years [74,75,144] Pinus greggii Engelm. ex Parl. Gregg’s pine Pinus; Pinus; Oocarpae; ‘Oocarpa Group’ Artificial Greenhouse 7 months [75] Pinus halepensis Mill. Aleppo pine Pinus; Pinus; Halepenses Artificial Greenhouse 2 years, 3–4 years, unknown [138,142,143] Pinus kesiya Royle ex Gordon Khasia pine, Khasi pine, Benguet pine Pinus; Pinus; Pinus Artificial Field 2 years [76] Pinus leiophylla Schiede ex Schltdl. & Cham. Chihuahua pine, smooth-leaf pine, yellow pine Pinus; Pinus; Leiophyllae Artificial Greenhouse Unknown [138] Pinus mugo Turra subsp. uncinata (Ramond ex DC.) Domin. Swiss mountain pine Pinus; Pinus, Pinus Artificial Greenhouse 2 years [148] Pinus nigra J.F.Arnold Austrian pine, black pine Pinus; Pinus; Pinus Artificial Field Unknown [8] Pinus palustris Mill. Longleaf pine Pinus; Pinus; Australes Natural Nursery Recently emerged [149] Pinus pinaster Aiton Maritime pine, cluster pine Pinus; Pinus; Pinus Artificial Greenhouse, field 2 years, Unknown [8,143] Pinus pringlei Shaw Pringle´s pine Pinus; Pinus; Oocarpae; ‘Oocarpa Group’ Artificial Greenhouse Unknown [138] Pinus strobus L. Eastern white pine, northern white pine, white pine, Weymouth pine (British), and soft pine Strobus; Strobus;Strobi Artificial Greenhouse 3.5 years [150] Pinus sylvestris L. Scots/Scotch pine Pinus; Pinus; Pinus Artificial Greenhouse 2 years, 3.5 years [143,150] Pinus tecunumanii F.Schwerdtf. ex Eguiluz & J.P.Perry Schwerdtfeger’s Pine, Tecun Uman Pine Pinus; Pinus; Oocarpae; ‘Oocarpa Group’ Artificial Greenhouse 3 months, 12 weeks, 6–8 months (high elevation origin) [139,145,146] Pinus virginiana Mill. Virginia pine, Jersey pine, scrub pine Pinus; Pinus; Contortae Artificial Greenhouse 3–4 years [135] Forests 2020,11, 724 21 of 40 Table 3. Cont. Susceptibility/Host Species1Common English Names Subgenus; Section; Subsection2 Type of Infection Growth or Test Conditions Seedlings and/or Plant Age3References Susceptibility low-moderate Pinus caribaea Morelet Caribbean pine Pinus; Pinus; Australes Artificial Greenhouse 7 months [75] Pinus elliottii Engelm. Slash pine Pinus; Pinus; Australes Artificial Field 2 years [76] Pinus mugo Turra subsp. uncinata (Ramond ex DC.) Domin. Swiss mountain pine Pinus; Pinus, Pinus Artificial Field Unknown [8] Pinus pinaster Aiton Maritime pine, cluster pine Pinus; Pinus; Pinus Artificial Greenhouse 2 years [148] Pinus sylvestris L. Scots/Scotch pine Pinus; Pinus; Pinus Artificial Growth chamber, greenhouse Recently emerged, 2 years [9,148] Pinus taeda L. Loblolly pine Pinus; Pinus; Australes Artificial Greenhouse 7–9 months, 1 year [74,151] Pinus thunbergii Parl. black pine, Japanese black pine, Japanese pine Pinus; Pinus; Pinus Artificial Greenhouse 3–4 years [135] Susceptibility low Pinus ayacahuite Ehrenb. ex Schltdl. Mexican white pine, ayacahuite pine Strobus; Strobus; Strobi Artificial Greenhouse Unknown [138] Pinus canariensis C.Sm. Canary Island pine Pinus; Pinus; Canarienses Artificial Greenhouse 2–3 years, 3–4 years [3,142] Pinus caribaea Morelet Caribbean pine Pinus; Pinus; Australes Artificial Greenhouse 3 months [139] Pinus clausa (Chapm. ex Engelm.) Vasey ex Sarg. Sand pine, Florida spruce pine, Alabama pine Pinus; Pinus; Contortae Artificial, natural Greenhouse, field 18 months, 6–8 years [82] Pinus glabra Walter Spruce pine Pinus; Pinus; Australes Artificial, natural Greenhouse, field 5 months, unknown [152] Pinus jaliscana Perez de la Rosa Jalisco pine Pinus; Pinus; Oocarpae; ‘Oocarpa Group’ Artificial Greenhouse 3 months [139] Pinus luchuensis Mayr Luchu/Ryukyu pine Pinus; Pinus; Pinus Artificial Greenhouse 2 years [136] Pinus maximinoi H.E. Moore Thinleaf pine Pinus; Pinus; Ponderosae; ‘Pseudostrobus Group’ Artificial Greenhouse 3 months, 7 months, 8–9 months [56,74,145] Pinus monophylla Torr. & Frém. Singleleaf pinyon pine Strobus; Parrya; Cembroides Natural Field Unknown [79] Pinus nigra J.F.Arnold Austrian pine, black pine Pinus; Pinus; Pinus Artificial Greenhouse 2 years, 3.5 years [143,150,153] Pinus occidentalis Sw. Western Indian pine Pinus; Pinus; Australes Natural Field Unknown [53] Pinus oocarpa Schiede ex Schltdl. Ocote pine, Egg-cone pine, hazelnut pine Pinus; Pinus; Oocarpae; ‘Oocarpa Group’ Artificial Greenhouse 3 months, 7 months [75,139,145] Pinus pringlei Shaw Pringle’s pine Pinus; Pinus; Oocarpae; ‘Oocarpa Group’ Artificial Greenhouse 7 months [75] Pinus pseudostrobus Lindl. syn. Pinus oaxacana Mirov Smooth-bark Mexican pine Pinus; Pinus; Ponderosae; ‘Pseudostrobus Group’ Natural, artificial Field, greenhouse Unknown, 7 months [74,97] Pinus pungens Lamb. Table mountain pine Pinus; Pinus; Australes Artificial Unknown Unknown [53] Pinus resinosa Aiton Red pine, Norway pine Pinus; Pinus; Pinus Artificial Greenhouse 3.5 years [150] Pinus rigida Mill. Pitch pine Pinus; Pinus; Australes Artificial Greenhouse 3–4 years [135] Forests 2020,11, 724 22 of 40 Table 3. Cont. Susceptibility/Host Species1Common English Names Subgenus; Section; Subsection2 Type of Infection Growth or Test Conditions Seedlings and/or Plant Age3References Susceptibility low-moderate Pinus serotina Michx. Pond pine, marsh pine, pocosin pine Pinus; Pinus; Australes Artificial Greenhouse 1 year [53,151] Pinus sylvestris L. Scots/Scotch pine Pinus; Pinus; Pinus Artificial Field 2 years, Unknown [8] Pinus taeda L. Loblolly pine Pinus; Pinus; Australes Artificial Field 8 years [140] Pinus tecunumanii F.Schwerdtf. ex Eguiluz & J.P.Perry Schwerdtfeger’s Pine, Tecun Uman Pine Pinus; Pinus; Oocarpae; ‘Oocarpa Group’ Artificial Greenhouse, field 3 months, 12 weeks, 6–8 months, 8 years (low-elevation origin) [56,74,139,144–146] Pinus thunbergii Parl. Black pine, Japanese black pine, Japanese pine Pinus; Pinus; Pinus Artificial Greenhouse 3–4 years [142] Resistant Pinus koraiensis Siebold and Zucc. Korean pine Strobus; Strobus; Cembrae Artificial Greenhouse 3 years [59] Highly variable susceptibility Pinus densiflora Siebold and Zucc. Japanese red pine, Korean red pine Pinus; Pinus; Pinus Artificial Greenhouse 3–4 years [59,135,136] Pinus muricata D. Don Bishop pine Pinus; Pinus; Attenuatae; Artificial Greenhouse Unknown [79] Pinus pinea L. Italian stone pine, umbrella pine Pinus; Pinus; Pineae Artificial Greenhouse, growth chambers 6 months, 2 years, 3-4 years [35,37,143,154], J. Martín-García, unpublished Susceptible, unknown susceptibility rate Pinus attenuata Lemmon Knobcone pine, Narrowcone pine Pinus; Pinus; Attenuatae Artificial Greenhouse Unknown [79,154] Pinus brutia Ten. var. eldarica (Medw.) Silba Eldarica pine Pinus; Pinus; Halepenses Artificial Greenhouse Unknown [79] Pinus canariensis C.Sm. Canary Island pine Pinus; Pinus; Canarienses Artificial Greenhouse Unknown [79] Pinus contorta Douglas ex Loudon Shore pine, lodgepole pine Pinus; Pinus; Contortae Artificial Greenhouse Unknown [141] Pinus coulteri D. Don Coulter pine, big-cone pine Pinus; Pinus; Ponderosae; ‘Sabinianae Group’ Artificial Greenhouse Unknown [79,154] Pinus halepensis Mill. Aleppo pine Pinus; Pinus; Halepenses Artificial Nursery 2 years [35] Pinus jeffreyi A.Murray bis Jeffrey pine Pinus; Pinus; Ponderosae Artificial Greenhouse Unknown [79] Pinus lambertiana Douglas Sugar pine Strobus; Strobus; Strobi Artificial Greenhouse Unknown [79] Pinus nigra J.F. Arnold subsp. laricio (Poir.) Maire Corsican pine Pinus; Pinus; Pinus Natural Nursery <6 months A.V. Sanz-Ros, unpublished Pinus pinaster Aiton Maritime pine, cluster pine Pinus; Pinus; Pinus Artificial Nursery 2 years [36] Pinus ponderosa Douglas ex Loudon Ponderosa pine, bull pine, blackjack pine Pinus; Pinus; Ponderosae Artificial Greenhouse Unknown [79] Pinus sabiniana Douglas ex D. Don Gray/foothill/digger pine Pinus; Pinus; Ponderosae; ‘Sabinianae Group’ Artificial Greenhouse Unknown [79] 1Host taxonomy is based on Zanoni, Farjon [155]; 2Subgenus; Section; Subsection is based on Price et al. [156]; 3Seedlings and plants age: w—week, m—month, y—year. Forests 2020,11, 724 23 of 40 Table 4. Susceptibility list of Pinus species mature trees (≥11 years) to Fusarium circinatum. Susceptibility/Host Species1Sampling Site Status of Host Tree Age, Years Reference Susceptibility high Pinus radiata D. Don Plantation, unknown Exotic, native Unknown, 20y [12,34,128,154,157] Susceptibility low-moderate Pinus discolor D.K. Bailey & Hawksw. Unknown Native Unknown [138] Pinus douglasiana Martinéz Unknown Native Unknown [138] Pinus durangensis Martinéz Unknown Native Unknown [138] Pinus halepensis Mill. Unknown Exotic Unknown [138] Pinus leiophylla Schiede ex Schltdl. & Cham. Unknown Native Unknown [138] Susceptibility low Pinus ayacahuite Ehrenb. ex Schltdl. Unknown Native Unknown [138] Pinus canariensis C. Sm. Urban trees Exotic Unknown [154] Pinus luchuensis Mayr Greenhouse Native 11–19 years [136] Pinus pinaster Aiton Plantation Native Unknown Highly variable susceptibility Pinus densiflora Siebold and Zucc. Unknown Native Unknown [136] Pinus muricata D. Don Unknown, Plantation Native Unknown, 12-13 years [80,153] Pinus pinea L. Plantation, urban trees Exotic, native Unknown [35,154] Susceptible, unknown susceptibility rate Pinus arizonica Engelm. Plantation, natural forest Native Unknown [43,97,138] Pinus armandii Franch. Natural forest Native Unknown [136] Pinus attenuata Lemm Unknown Native Unknown [154,158] Pinus canariensis C. Sm. Unknown Exotic Unknown [15,80] Pinus cembroides Zucc. Unknown Native Unknown [138] Pinus contorta Douglas ex Loudon Unknown Native Unknown [154] Pinus contorta Douglas ex Loudon var. contorta Natural forest Native Unknown [158] Pinus coulteri D. Don Unknown Native Unknown [154] Pinus elliottii Engelm. var. densa (Little and Dorman) E. Murray Plantation Native Unknown [17] Pinus elliottii Engelm. var. elliottii Plantation, natural forest Native, exotic Unknown [13,159] Pinus greggii Engelm. ex Parl. Unknown Exotic Unknown [74,76] Pinus halepensis Mill. Unknown, urban trees Exotic, native Unknown [35,80] Pinus hartwegii Lindl. Plantation and natural forest Native Unknown [40,138] Forests 2020,11, 724 24 of 40 Table 4. Cont. Susceptibility/Host Species1Sampling Site Status of Host Tree Age, Years Reference Susceptible, unknown susceptibility rate Pinus kesiya Royle. ex Gordon Plantation Exotic Unknown [56] Pinus leiophylla Schiede ex Schltdl. & Cham. var. leiophylla Natural forest Native Unknown [120] Pinus montezumae Lamb. Unknown Native Unknown [138] Pinus patula Schiede ex Schltdl. & Cham. Plantation Exotic Unknown [56] Pinus ponderosa Douglas ex Lawson Plantation Native Unknown [154] Pinus pringlei Shaw Unknown Native Unknown [138] Pinus pseudostrobus Lindl. Unknown Native Unknown [138] Pinus pseudostrobus Lindl. var. apulcensis (Lindl.) Shaw Plantation and natural forest Native Unknown [40,97,138] Pinus radiata ×attenuata Natural forest Native Unknown [158] Pinus sabiniana Douglas ex D. Don Unknown Native Unknown [154,158] Pinus taeda L. Unknown, greenhouse Native Unknown, 21 years [151,160] Pinus thunbergii Parl. Roadside, golf course Native Unknown [161] Pinus torreyana Parry ex Carrière Unknown Native Unknown [154,158] 1Host taxonomy is based on Zanoni, Farjon [155]. Forests 2020,11, 724 25 of 40 6.2. Species with Variable Susceptibility Ratings Susceptibility ratings were variable for 19 Pinus species and seven Pinus hybrids due to the fact that different studies classified them in different susceptibility categories (see Tables 3–5). Variable susceptibility ranging from susceptible to resistant was found in two mature pine hosts: P. muricata and P. pinea. The highest discrepancy between susceptible ratings was noted for species classified as having both high and low susceptibility: P. nigra,P. pseudostrobus, P. sylvestris, and P. taeda. Two Pinus species (P. pinaster and P. mugo subsp. uncinata) were ranked as having both high and low-moderate susceptibility. Slight differences in susceptibility ratings, i.e., those in adjacent ranking categories, were recorded for 11 pine hosts: P. canariensis,P. caribaea,P. elliottii,P. greggii,P. halepensis,P. leiophylla,P. patula, P. pringlei,P. strobus,P. tecunumanii, and P. thunbergii (Tables 3and 4). These minor discrepancies in susceptibility ratings are most likely due to experimental variation and interpretation of the categories by various authors and are not discussed further in this review, while the species with greater discrepancies in susceptibility ratings are discussed in more detail below. Among the seven Pinus hybrids, we found ambiguous classifications for those with P. tecunumanii and P. greggii as one of the parental species (Table 5). Seeds for these two Pinus species have been sourced from different locations in Mexico, and susceptibility to F. circinatum varies based on seed sources [ 139 ]. Pinus tecunumanii originated from high elevations, and P. greggii from northern Mexico (i.e., P. greggii var. greggi), are respectively more susceptible to F. circinatum than low-elevation P. tecunumanii and P. greggii from southern Mexico (i.e., P. greggii var. australis) [ 75 , 76 ]. Failure to mention such provenance information has accordingly resulted in apparently inconsistent pathogenicity data in some published studies. Mature P. pinea was rated as resistant to F. circinatum by Gordon et al. [ 154 ], but in urban conditions in Italy the host was considered susceptible [ 34 ]. Furthermore, seedlings of P. pinea were rated as having low susceptibility [ 37 , 142 , 143 , 148 ] and unknown susceptibility [ 35 ], but P. pinea seedlings of Spanish origin (6 months, 12–14 cm) were very susceptible and taller seedlings (6 months, >16 cm) of the same origin were resistant (Mart í n-Garc í a, unpublished). Therefore, we consider that P. pinea has highly variable susceptibility. The results of P. muricata inoculation tests by Schmale & Gordon [ 153 ] indicated a wide range of variation in susceptibility: 27% of P. muricata trees were considered resistant, while others were susceptible to F. circinatum. In other studies, P. muricata seedlings and mature trees were shown to be susceptible to F. circinatum [ 79 , 80 ]. Thus, we considered P. muricata to be highly variable in susceptibility to F. circinatum. Pinus sylvestris seedlings, both recently emerged and 1.5-year-old seedlings, of Spanish, Czech, and Scottish origin, were classified as highly susceptible in growth chamber and greenhouse experiments by Martinez-Alvarez et al. [ 8 ], Mart í n-Garc í a et al. [ 10 ], and Woodward, unpublished. In contrast, low susceptibility of P. sylvestris seedlings of the Spanish origin was observed in a field trial [ 8 ]. No data are available for the susceptibility of mature P. sylvestris trees. Pinus nigra seedlings of different provenances were highly susceptible to F. circinatum in growth chamber experiments [ 8 ], Mart í n-Garc í a, unpublished. In contrast, in greenhouse experiments 2and 3.5-years old seedlings of P. nigra were found to have low levels of susceptibility [ 143 , 150 ]. This discrepancy could be a result of different environmental conditions (temperature, humidity) in the growth chamber and greenhouse as compared to field conditions. These kinds of experiments should be done under the same environmental conditions. The variation in susceptibility of 2-year-old P. nigra seedlings of Spanish origin was quite high between individuals, indicating that some individuals in this species may be at higher risk of damage from F. circinatum [ 143 ]. Less than sixmonths-old seedlings of P. nigra subsp. laricio of the Spanish origin were found naturally (not artificially inoculated) infected in nurseries (Sanz-Ros, unpublished), and this was considered as unknown susceptibility. No data are available for the susceptibility of mature P. nigra. One-year-old P. taeda seedlings in South Africa were found to be susceptible to F. circinatum [ 88 ], in contrast to other studies showing that P. taeda was highly tolerant to F. circinatum in South Africa [ 76 , 139 ]. Seven-month-old seedlings of P. pseudostrobus were ranked as having low susceptibility Forests 2020,11, 724 32 of 40 greenhouse inoculations. Tree age clearly plays an important role in susceptibility to F. circinatum, and much work needs to be done to fully understand the interaction between host, environment and pathogen and their interactive influences on susceptibility and severity of infection. Thus, the results in this study clearly support the need for standard protocols to be applied in pathogenicity tests to compare data in different conditions (including laboratories) and increase knowledge on the biology and epidemiology of F. circinatum. Knowledge of the centre of origin and source populations of F. circinatum can aid in sourcing resistant species or valuable genetic material. Combined with information regarding introduction pathways, it can also help prevent further introductions by focusing quarantine measures and monitoring efforts where they are most effective. Given the risks posed by the movement of the pathogen, there is an urgent need for routine surveillance of Pinus and other species known to be susceptibletoF. circinatum, aswellasresearchontheimportanceofsoil,nativeinsects,andasymptomatic nursery plants for the spread of the disease [ 166 ]. Without maintained levels of surveillance, it is highly probable the pathogen will continue spreading to new areas and extending its host range. Supplementary Materials: The following are available online at http://www.mdpi.com/1999-4907/11/7/724/s1, supporting information to Geo-database, Table S1: Data fields of the international Fusarium circinatum (FC) geo-database (for more information see: http://bit.do/phytoportal), GIS and map analyses, and statistical analyses. Author Contributions: All authors sent monitoring data of the pathogen for geo-database and interactive map. Writing: R.D., M.S.M., B.G,J.M.G., P.V. Review: allauthors. Editing: S.W., K.A. (Katar í na Adamˇc í kov á ). All authors have read and agreed to the published version of the manuscript. Funding: This study was financially supported by COST Action FP1406 (PINESTRENGTH), the Estonian Science Foundation grant PSG136, the Forestry Commission, United Kingdom, the Phytophthora Research Centre Reg. No. CZ.02.1.01/0.0/0.0/15_003/0000453, a project co-financed by the European Regional Development Fund. ANSES is supported by a grant managed by the French National Research Agency (ANR) as part of the “Investissements d’Avenir” programme (ANR-11-LABX-0002-01, Laboratory of ExcellenceARBRE). SW was partly supported by BBSRC Grant reference BB/L012251/1 “Promoting resilience of UK tree species to novel pests & pathogens: ecological & evolutionary solutions (PROTREE)” jointly funded by BBSRC, Defra, ESRC, the Forestry Commission, NERC and the Scottish Government, under the Tree Health and Plant Biosecurity Initiative. Annual surveys in Switzerland were financially supported by the Swiss Federal Office for the Environment FOEN. Acknowledgments: Andrea Kunova and Cristina Pizzatti are acknowledged for the assistance in the sampling. Thanks are due to Dina Ribeiro and Helena Marques from ICNF-Portuguese Forest Authority for providing location coordinates. We thank three anonymous reviwers for valuable corrections and suggestions. Conflicts of Interest: The authors declare no conflict of interest. References 1. Geiser, D.M.; Aoki, T.; Bacon, C.W.; Baker, S.E.; Bhattacharyya, M.K.; Brandt,M.E.; Brown,D.W.; Burgess, L.W.; Chulze, S.; Coleman, J.J.; et al. One Fungus, One Name: Defining the Genus Fusarium in a Scientifically Robust Way That Preserves Longstanding Use. Phytopathology 2013,103, 400–408. [CrossRef] 2. Vettraino, A.M.; Potting, R.; Raposo, R. EU Legislation on Forest Plant Health: An Overview with a Focus on Fusarium circinatum.Forests 2018,9, 568. [CrossRef] 3. Garc í a-Serna, I. Diplodia pinea (Desm.) Kickx y Fusarium circinatum Niremberg & O’Donell, Principales Hongos de Chancro de las Masas Forestales de Pinus radiata D. Don del Pa í s Vasco. Ph.D. Thesis, University of the Basque Country, Bilbao, Spain, 2011. 4. Wingfield, M.J.; Hammerbacher, A.; Ganley, R.J.; Steenkamp, E.T.; Gordon, T.R.; Wingfield, B.D.; Coutinho, T. Pitch canker caused by Fusarium circinatum—A growing threat to pine plantations and forests worldwide. Australas. Plant Pathol. 2008,37, 319–334. [CrossRef] 5. Swett, C.L.; Gordon, T. First Report of Grass Species (Poaceae) as Naturally Occurring Hosts of the Pine Pathogen Gibberella circinata.Plant Dis. 2012,96, 908. [CrossRef] 6. Swett, C.L.; Porter, B.; Fourie, G.; Steenkamp, E.T.; Gordon, T.R.; Wingfield, M.J. Association of the pitch canker pathogen Fusarium circinatum with grass hosts in commercial pine production areas of South Africa. South. For. J. For. Sci. 2014,76, 161–166. [CrossRef] Forests 2020,11, 724 33 of 40 7. Hernandez-Escribano, L.; Iturritxa, E.; Elvira-Recuenco, M.; Berbegal, M.; Campos, J.A.; Renobales, G.; Garcia, I.; Raposo, R. Herbaceous plants in the understory of a pitch canker-affected Pinus radiata plantation are endophytically infected with Fusarium circinatum.Fungal Ecol. 2018,32, 65–71. [CrossRef] 8. Mart í nezÁ lvarez, P.; Pando, V.; Diez, J.J. Alternative species to replace Monterey pine plantations affected by pitch canker caused by Fusarium circinatum in northern Spain. Plant Pathol. 2014 ,63, 1086–1094. [CrossRef] 9. Mart í n-Garc í a, J.; Paraschiv, M.; Flores-Pacheco, J.A.; Chira, D.; D í ez, J.J.; Fern á ndez, M. Susceptibility of Several Northeastern Conifers to Fusarium circinatum and Strategies for Biocontrol. Forests 2017 ,8, 318. [CrossRef] 10. Mart í n-Garc í a, J.; Lukaˇceviˇcov á , A.; Flores-Pacheco, J.A.; D í ez, J.J.; Dvoˇr á k, M. Evaluation of the Susceptibility of Several Czech Conifer Provenances to Fusarium circinatum.Forests 2018,9, 72. [CrossRef] 11. Storer, A.J.; Gordon, T.R.; Clark, S.L. Clark Association of the pitch canker fungus, Fusarium subglutinans f. sp. pini, with Monterey pine seeds and seedlings in California. Plant Pathol. 1998,47, 649–656. [CrossRef] 12. Viljoen, A. First Report of Fusarium subglutinans f. sp. pini on Pine Seedlings in South Africa. Plant Dis. 1994 , 78, 309. [CrossRef] 13. Wikler, K.; Storer, A.; Newman, W.; Gordon, T.; Wood, D. The dynamics of an introduced pathogen in a native Monterey pine (Pinus radiata) forest. For. Ecol. Manag. 2003,179, 209–221. [CrossRef] 14. Gordon, T.R. Biology and Management of Gibberella circinata, the cause of pitch canker in pines. In Control of Fusarium Diseases; Alves-Santos, F.M., Diez, J.J., Eds.; Research Signpost: Kerala, India, 2011; pp. 195–207. 15. Bezos, D.; Mart í nez-Alvarez, P.; Fern á ndez, M.; Diez, J.J. Epidemiology and management of pine pitch canker disease in Europe—A review. Baltic For 2017,23, 279–293. 16. Kelley, W.D. Incidence of Pitch Canker Among Clones of Loblolly Pine in Seed Orchards. Plant Dis. 1982 , 66, 1171. [CrossRef] 17. Dwinell, L.D. Pitch Canker: A Disease Complex of Southern Pines. Plant Dis. 1985,69, 270. [CrossRef] 18. Swett, C.L.; Reynolds, G.J.; Gordon, T.R. Infection without wounding and symptomless shoot colonization of Pinus radiata by Fusarium circinatum, the cause of pitch canker. For. Pathol. 2018,48, 1–7. [CrossRef] 19. Kuhlman, E.G.; Dianis, S.D.; Smith, T.K. Epidemiology of pitch canker disease in a loblolly pine seed orchard in North Carolina. Phytopathology 1982,72, 1212–1216. [CrossRef] 20. Runion, G.B.; Bruck, R.I. Associations of the pine tip moth with pitch canker of loblolly pine. Phytopathology 1985,75, 1339. 21. Aguayo, J.; Fourrier-Jeandel, C.; Capdevielle, X.; V é tillard, F.; Piou, D.; Iturritxa, E.; Robin, C. Assessment of molecular detection of Fusarium circinatum in insects and passive spore traps in Pinus radiata plantations. For. Pathol. 2020,50, e12574. [CrossRef] 22. Mart í n-Rodrigues, N.; Sanchez-Zabala, J.; Salcedo, I.; Majada, J.; Gonz á lez-Murua, C.; Duñabeitia, M.K. New insights into radiata pine seedling root infection byFusarium circinatum. Plant Pathol. 2015 ,64, 1336–1348. [CrossRef] 23. Zamora-Ballesteros, C.; D í ez, J.J.; Mart í n-Garc í a, J.; Witzell, J.; Solla, A.; Ahumada, R.; Capretti, P.; Cleary, M.; Drenkhan, R.; Dvoˇr á k, M.; et al. Pine Pitch Canker (PPC): Pathways of Pathogen Spread and Preventive Measures. Forests 2019,10, 1158. [CrossRef] 24. Hepting, G.H.; Roth, E.R. Pitch canker, a new disease of southern pines. J. For. 1946,44, 742–744. 25. Anonymous. DP 22: Fusarium circinatum. ISPM 27 Diagnostic Protocols for Regulated Pests; Iternational Plant Protection Convention (IPPC): Rome, Italy, 2017; p. 22. 26. CABI. Gibberella Circinata (Pitch Canker). Available online: https://www.cabi.org/isc/datasheet/25153 (accessed on 27 May 2020). 27. EPPO. Fusarium circinatum. Available online: https://gd.eppo.int/taxon/GIBBCI/distribution (accessed on 27 May 2020). 28. Ganley, R.J.; Watt, M.; Manning, L.; Iturritxa, E. A global climatic risk assessment of pitch canker disease. Can. J. For. Res. 2009,39, 2246–2256. [CrossRef] 29. Baker, R.; Candresse, T.S.; Erzs é bet Dormannsn é , E.; Gilioli, G.; Gr é goire, J.; Jeger, M.J. Risk assessment of Gibberella circinata for the EU territory and identification and evaluation of risk management options. EFSA 2010,8, 1620. 30. Möykkynen, T.; Capretti, P.; Pukkala, T. Modelling the potential spread of Fusarium circinatum, the causal agent of pitch canker in Europe. Ann. For. Sci. 2014,72, 169–181. [CrossRef] Forests 2020,11, 724 34 of 40 31. Santini, A.; Ghelardini, L.; de Pace, C.; Desprez-Loustau, M.L.; Capretti, P.; Chandelier, A.; Cech, T.; Chira, D.; Diamandis, S.; Gaitniekis, T.; et al. Biogeographical patterns and determinants of invasion by forest pathogens in Europe. New Phytol. 2012,197, 238–250. [CrossRef] [PubMed] 32. Wingfield, M.; Brockerhoff, E.G.; Wingfield, B.D.; Slippers, B. Planted forest health: The need for a global strategy. Science 2015,349, 832–836. [CrossRef] 33. Collar Urquijo, J. Informe de la reuni ó n del grupo de trabajo de laboratorios de diagn ó stico y prospecciones fitosanitarias. Almería1995,7. 34. Landeras, E.; Garcia, P.; Fern á ndez, Y.; Braña, M.; Fern á ndez-Alonso, O.; M é ndez-Lodos, S.; P é rez-Sierra, A.; Leon, M.; Abad-Campos, P.; Berbegal, M.; et al. Outbreak of Pitch Canker Caused by Fusarium circinatum on Pinus spp. in Northern Spain. Plant Dis. 2005,89, 1015. [CrossRef] 35. Carlucci, A.; Colatruglio, L.; Frisullo, S. First Report of Pitch Canker Caused by Fusarium circinatum on Pinus halepensis and P. pinea in Apulia (Southern Italy). Plant Dis. 2007,91, 1683. [CrossRef] 36. EPPO. First Report of Gibberella Circinata in France; EPPO Reporting Service; EPPO Global Database: Paris, France, 2006; p. 104. 37. Bragança, H.; Diogo, E.; Moniz, F.; Amaro, P. First Report of Pitch Canker on Pines Caused by Fusarium circinatum in Portugal. Plant Dis. 2009,93, 1079. [CrossRef] [PubMed] 38. Lauricica, J.M.; Muguruza, J.R. Presencia de Fusarium Subglutinan ssp. Pinien Viveros de Pino Radiata en Bizkaia. In Proceedings of the Actas XIV Reuni ó n Anual del Grupo de Trabajo Fitosanitario de Forestales Parques YJardines Zaragoza, Zaragoza, Spain, 18–20 November 1997; pp. 301–303. 39. Dwinell, L.D.; Adams, D.; Guerra-Santos, J.J.; Aguirre, J.R.M. Pitch Canker Disease of Pinus radiata. In Proceedings of the ICPP98—7th International Congress of Plant Pathology, London, UK, 9–16 August 1998; Available online: http://www.bspp.org.uk/icpp98/3.7/30.html (accessed on 27 April 2020). 40. Dwinell, L.D. Global distribution of the pitch canker fungus. In Current and Potential Impacts of Pitch Canker in Radiata pine, IMPACT Monterey Workshop, Monterey, CA, USA, 30 November–3 December 1998; Devey, M.E., Matheson, A.C., Gordon, T.R., Eds.; CSIRO Forestry and Forest Products: Canberra, Australia, 1999; pp. 54–57. 41. EPPO. Update of the Situation of Fusarium circinatum in Spain; EPPO Reporting Service; EPPO Global Database: Paris, France, 2019; p. 196. 42. EPPO. Update of the Situation of Fusarium circinatum in Portugal; EPPO Reporting Service; EPPO Global Database: Paris, France, 2019; p. 170. 43. EPPO. Gibberella Circinata Eradicated in France; EPPO Reporting Service; EPPO Global Database: Paris, France, 2008; p. 103. 44. EPPO. Situation of Gibberella circinata in France; EPPO Reporting Service; EPPO Global Database: Paris, France, 2009; p. 093. 45. EPPO. Gibberella circinata Detected Again in France; EPPO Reporting Service; EPPO Global Database: Paris, France, 2010; p. 034. 46. Ioos, R.; Aloi, F.; Piškur, B.; Guinet, C.; Mullett, M.; Berbegal, M.; Bragança, H.; Cacciola, S.O.; Oskay, F.; Cornejo, C.; et al. Transferability of PCR-based diagnostic protocols: An international collaborative case study assessing protocols targeting the quarantine pine pathogen Fusarium circinatum.Sci. Rep. 2019 ,9, 8195. [CrossRef] [PubMed] 47. Elvira-Recuenco, M.; Cacciola, S.; Sanz-Ros, A.V.; Garbelotto, M.; Aguayo, J.; Solla, A.; Mullett, M.; Drenkhan, T.; Oskay, F.; Kaya, A.G.A.; et al. Potential Interactions between Invasive Fusarium circinatum and Other Pine Pathogens in Europe. Forests 2019,11, 7. [CrossRef] 48. Field Guide. Pine Pitch Canker. Available online: https://drive.google.com/file/d/1rA7EPEUzaBXikevC_ skV9cpuu0VuCAYZ/view (accessed on 27 April 2020). 49. Loit, K.; Adamson, K.; Bahram, M.; Puusepp, R.; Anslan, S.; Kiiker, R.; Drenkhan, R.; Tedersoo, L. Relative Performance of MinION (Oxford Nanopore Technologies) versus Sequel (Pacific Biosciences) Third-Generation Sequencing Instruments in Identification of Agricultural and Forest Fungal Pathogens. Appl. Environ. Microbiol. 2019,85, 01368-19. [CrossRef] [PubMed] 50. Tedersoo, L.; Drenkhan, R.; Anslan, S.; Morales-Rodriguez, C.; Cleary, M. High-throughput identification and diagnostics of pathogens and pests: Overview and practical recommendations. Mol. Ecol. Resour. 2018 , 19, 47–76. [CrossRef] [PubMed] Forests 2020,11, 724 35 of 40 51. Guerra-Santos, J.J. El Cancro Resinoso Causado por Subglurinans (Wollenw y Reink) Nelson, Toussoun y Marasas, Una Nueva Enfermedad de Pinus spp., en Mexico. Master’s Thesis, Universidad Autonoma Chapingo, Chapingo, Mexico, 1995. 52. Wikler, K.; Gordon, T.R. An initial assessment of genetic relationships among populations of Fusarium circinatum in different parts of the world. Can. J. Bot. 2000,78, 709–717. 53. Hepting, G.H.; Roth, E.R. Host relations and spread of the pine pitch canker disease. Phytopathology 1953 , 43, 475. 54. Wingfield, M.; Jacobs, A.; Coutinho, T.; Ahumada, R.; Wingfield, B.D. First report of the pitch canker fungus, Fusarium circinatum, on pines in Chile. Plant Pathol. 2002,51, 397. [CrossRef] 55. Alonso, R.; Bettucci, L. First report of the pitch canker fungus Fusarium circinatum affecting Pinus taeda seedlings in Uruguay. Australas. Plant Dis. Notes 2009,4, 91–92. 56. Steenkamp, E.T.; Rodas, C.A.; Kvas, M.; Wingfield, M. Fusarium circinatum and pitch canker of Pinus in Colombia. Australas. Plant Pathol. 2012,41, 483–491. [CrossRef] 57. Rodas, C.A. Important Pest and Diseases of Plantation Grown Pinus and Eucalyptus in Colombia and Their Control. PhD. Thesis, University of Pretoria, Pretoria, South Africa, 2013. 58. Pfenning, L.; Costa, S.D.S.; de Melo, M.P.; Costa, H.; Ventura, J.A.; Auer, C.G.; dos Santos, Á .F. First report and characterization of Fusarium circinatum, the causal agent of pitch canker in Brazil. Trop. Plant Pathol. 2014,39, 210–216. [CrossRef] 59. Lee, J.K.; Lee, S.H.; Sung, I.Y.; Lee, Y.W. First report of pitch canker disease on Pinus rigida in Korea. Plant Pathol. J. 2000,16, 52–54. 60. Kobayashi, T.; Muramoto, M. Pitch canker of Pinus luchuensis, a new disease of Japanese forests. For. Pests 1989,40, 169–173. 61. Morris, A.; Fourie, G.; Greyling, I.; Steenkamp, E.T.; Jones, N.B. Re-use of seedling containers and Fusarium circinatum association with asymptomatic Pinus patula planting stock. South. For. J. For. Sci. 2014 ,76, 177–187. [CrossRef] 62. Fourie, G.; Wingfield, M.J.; Wingfield, B.D.; Jones, N.B.; Morris, A.; Steenkamp, E.T. Culture-independent detection, and quantification of Fusarium circinatum in a pine-producing seedling nursery. South. For. J. For. Sci. 2014,76, 137–143. [CrossRef] 63. Jones, N.B.; Ford, C.; Light, M.E.; Nadel, R.; Greyling, I.; Fourie, G.; Wingfield, M.J.; Morris, A. Effect on nursery and field performance of Pinus patula seedlings after inoculation with Fusarium circinatum.South. For. J. For. Sci. 2014,76, 125–136. [CrossRef] 64. Fitza, K.; Payn, K.; Steenkamp, E.T.; Myburg, A.; Naidoo, S. Chitosan application improves resistance to Fusarium circinatum in Pinus patula.S. Afr. J. Bot. 2013,85, 70–78. [CrossRef] 65. Mitchell, R.; Steenkamp, E.T.; Coutinho, T.; Wingfield, M. The pitch canker fungus, Fusarium circinatum: Implications for South African forestry. South. For. J. For. Sci. 2011,73, 1–13. [CrossRef] 66. Fru, F.F.; Steenkamp, E.T.; Wingfield, M.J.; Santana, Q.C.; Roux, J. Unique clones of the pitch canker fungus, Fusarium circinatum, associated with a disease outbreak in a new region of South Africa. Eur. J. Plant Pathol. 2017,148, 97–107. [CrossRef] 67. Coutinho, T.; Steenkamp, E.T.; Mongwaketsi, K.; Wilmot, M.; Wingfield, M.J. First outbreak of pitch canker in a South African pine plantation. Australas. Plant Pathol. 2007,36, 256. [CrossRef] 68. Steenkamp, E.T.; Makhari, O.M.; Coutinho, T.; Wingfield, B.D.; Wingfield, M. Evidence for a new introduction of the pitch canker fungus Fusarium circinatum in South Africa. Plant Pathol. 2013,63, 530–538. [CrossRef] 69. Santana, Q.C.; Coetzee, M.P.A.; Wingfield, B.D.; Wingfield, M.; Steenkamp, E.T. Nursery-linked plantation outbreaks and evidence for multiple introductions of the pitch canker pathogen Fusarium circinatum into South Africa. Plant Pathol. 2015,65, 357–368. [CrossRef] 70. Fru, F.F.; Steenkamp, E.T.; Wingfield, M.; Roux, J. High genetic diversity of Fusarium circinatum associated with the first outbreak of pitch canker on Pinus patula in South Africa. South. For. J. For. Sci. 2018 ,81, 69–78. [CrossRef] 71. Mitchell, R.; Wingfield, M.; Steenkamp, E.T.; Coutinho, T. Tolerance of Pinus patula full-sib families to Fusarium circinatum in a greenhouse study. South. For. J. For. Sci. 2012,74, 247–252. [CrossRef] 72. Nel, A.; Hodge, G.R.; Mongwaketsi, K.E.; Kanzler, A. Genetic parameters for Fusarium circinatum tolerance within open pollinated families of Pinus patula tested at screening facilities in South Africa and the USA. South. For. 2014,76, 145–150. [CrossRef] Forests 2020,11, 724 36 of 40 73. Mitchell, R.G.; Wingfield, M.; Steenkamp, E.T.; Roux, J.; Verryn, S.; Coutinho, T. Comparison of the tolerance of Pinus patula seedlings and established trees to infection by Fusarium circinatum. South. For. J. For. Sci. 2014,76, 151–159. [CrossRef] 74. Mitchell, R.G.; Wingfield, M.; Hodge, G.R.; Steenkamp, E.T.; Coutinho, T. Selection of Pinus spp. in South Africa for tolerance to infection by the pitch canker fungus. New For. 2011,43, 473–489. [CrossRef] 75. Mitchell, R.G.; Wingfield, M.J.; Hodge, G.R.; Steenkamp, E.T.; Coutinho, T.A. The tolerance of Pinus patula × Pinus tecunumanii, and other pine hybrids, to Fusarium circinatum in greenhouse trials. New For. 2013 , 44, 443–456. [CrossRef] 76. Roux, J.; Eisenberg, B.; Kanzler, A.; Nel, A.; Coetzee, V.; Kietzka, E.; Wingfield, M.J. Testing of selected South African Pinus hybrids and families for tolerance to the pitch canker pathogen, Fusarium circinatum.New For. 2006,33, 109–123. [CrossRef] 77. Ormsby, M. Pitch canker in quarantine—A biosecurity success story. Biosecurity 2004,51, 10. 78. Smith, S. Plant Health Clinic News. 2013. Available online: https://www.uaex.edu/yard-garden/plant-healthclinic/docs/2013_Plant_Health_Clinic_Newsletters/plant%20health%20clinic%20newsletter%2013.pdf (accessed on 27 May 2020). 79. McCain, A.H.; Koehler, C.S.; Tjosvold, S.A. Pitch canker threatens California pines. Calif. Agric. 1987 , 41, 22–23. 80. Correll, J.C. Pitch Canker Disease in California: Pathogenicity, Distribution, and Canker Development on Monterey Pine (Pinus radiata). Plant Dis. 1991,75, 676. [CrossRef] 81. Huang, J.W. Fungi Associated with Damping-offof Slash Pine Seedlings in Georgia. Plant Dis. 1990,74, 27. [CrossRef] 82. Blakeslee, G.; Jokela, E.; Hollis, C.; Wilson, D.; Lante, W.; Allen, J. Pitch Canker in Young Loblolly Pines: Influence of Precommercial Thinning and Fertilization on Disease Incidence and Severity. South. J. Appl. For. 1999,23, 139–143. [CrossRef] 83. McCay-Buis, T.S.; Abney, T.S.; Cummings, R.B.; Huber, D.M. Pitch canker disease of white pine seedlings in Indiana. Phytopathology 1994,84, 1122. 84. Starkey, D.; Meeker, J.; Mangini, A. Pitch Canker of Southern Pines and Recent Cases in Florida, Louisiana, Mississippi, and Texas. In USDA Forest Service Proceedings RMRS-P; USDA Forest Service: Fort Collins, CO, USA, 2007; Volume 50, pp. 97–103. 85. Dwinell, L.D. Susceptibility of southern pines to infection by Fusarium moniliforme var. subglutinans. Plant Dis. Repor. 1978,62, 108–111. 86. Kuhlman, E.G.; Dwinell, L.D.; Nelson, P.E.; Booth, C. Characterization of the Fusarium causing pitch canker of southern pines. Mycologia 1978,70, 1131–1143. [CrossRef] 87. Correll, J.C.; Gordon, T.R.; McCain, A.H. Genetic diversity in California and Florida populations of the pitch pine canker fungus Fusarium subglutinans var. pini. Phytopathology 1992,82, 415–420. [CrossRef] 88. Viljoen, A. Characterization of Fusarium Isolates from Gladiolus Corms Pathogenic to Pines. Plant Dis. 1995 , 79, 1240. [CrossRef] 89. Britz, H.; Coutinho, T.; Wingfield, M.J.; Marasas, W.F.O.; Gordon, T.R.; Leslie, J.F. Fusarium subglutinans f. sp. pini Represents a Distinct Mating Population in theGibberella fujikuroi Species Complex. Appl. Environ. Microbiol. 1999,65, 1198–1201. [CrossRef] 90. Nirenberg, H.I.; O’Donnell, K. New Fusarium species and combinations within the Gibberella fujikuroi species complex. Mycologia 1998,90, 434–458. [CrossRef] 91. O’Donnell, K.; Cigelnik, E.; Nirenberg, H.I. Molecular systematic and phylogeography of the Gibberella fujikuroi species complex. Mycologia 1998,90, 465–493. [CrossRef] 92. Britz, H.; Coutinho, T.A.; Wingfield, M.J.; Marasas, W.F.O. Validation of the description of Giberella circinata and morphological differentiation of the anamorph Fusarium circinatum.Sydowia 2002,54, 9–22. 93. Nelson, P.E.; Toussoun, T.A.; Marasas, W.F.O. Fusarium species: An Illustrated Manual of Identification; Penn State University Press: University Park, PA, USA, 1983. 94. Hawksworth, D.L. A new dawn for the naming of fungi: Impacts of decisions made in Melbourne in July 2011 on the future publication and regulation of fungal names. IMA Fungus 2011 ,2, 155–162. [CrossRef] [PubMed] Forests 2020,11, 724 37 of 40 95. O’Donnell, K.; Rooney, A.; Proctor, R.H.; Brown, D.W.; McCormick, S.P.; Ward, T.J.; Frandsen, R.J.N.; Lysøe, E.; Rehner, S.A.; Aoki, T.; et al. Phylogenetic analyses of RPB1 and RPB2 support a middle Cretaceous origin for a clade comprising all agriculturally and medically important fusaria. Fungal Genet. Boil. 2013 ,52, 20–31. [CrossRef] [PubMed] 96. Kvas, M.; Marasas, W.F.O.; Wingfield, B.D.; Wingfield, M.J.; Steenkamp, E.T. Diversity, and evolution of Fusarium species in the Gibberella fujikuroi complex. Fungal Divers. 2009,34, 1–21. 97. Guerra-Santos, J.J. Pitch canker on Monterey pine in Mexico. In Current and Potential Impacts of Pitch Canker in Radiata pine, Proceedings of the IMPACT Monterey Workshop, Monterey, CA, USA, 30 November–3 December 1998; Devey, M.E., Matheson, A.C., Gordon, T.R., Eds.; CSIRO Forestry and Forest Products: Canberra, Australia, 1999; pp. 58–61. 98. Iltis, H.H. Homeotic Sexual Translocations and the Origin of Maize (Zea Mays, Poaceae): A New look at an old problem. Econ. Bot. 2000,54, 7–42. [CrossRef] 99. Swett, C.L.; Gordon, T.R. Endophytic association of the pine pathogen Fusarium circinatum with corn (Zea mays). Fungal Ecol. 2015,13, 120–129. [CrossRef] 100. Herron, D.; Wingfield, M.; Wingfield, B.D.; Rodas, C.; Marincowitz, S.; Steenkamp, E.T. Novel taxa in the Fusarium fujikuroi species complex from Pinus spp. Stud. Mycol. 2015,80, 131–150. [CrossRef] 101. Perry, J.P.; Graham, A.; Richardson, D. The history of pines in Mexico and Central America. In Ecology and Biogeography of Pinus; Richardson, D.M., Ed.; Cambridge University Press: Cambridge, UK, 2000; pp. 137–149. 102. Millar, C.I. Impact of the Eocene on the Evolution of Pinus L. Ann. Mo. Bot. Gard. 1993,80, 471. [CrossRef] 103. Leslie, J.F. Gibberella fujikuroi: Available populations and variable traits. Can. J. Bot. 1995 ,73, 282–291. [CrossRef] 104. Martin, S.H.; Wingfield, B.D.; Wingfield, M.J.; Steenkamp, E.T. Structure, and evolution of the Fusarium mating type locus: New insights from the Gibberella fujikuroi complex. Fungal Genet. Boil. 2011 ,48, 731–740. [CrossRef] [PubMed] 105. Covert, S.F.; Briley, A.; Wallace, M.; McKinney, V.T. Partial MAT-2 Gene Structure, and the Influence of Temperature on Mating Success in Gibberella circinata.Fungal Genet. Boil. 1999 ,28, 43–54. [CrossRef] [PubMed] 106. Wilken, P.M.; Steenkamp, E.T.; Wingfield, M.J.; de Beer, Z.W.; Wingfield, B.D. Which MAT gene? Pezizomycotina (Ascomycota) mating-type gene nomenclature reconsidered. Fungal Boil. Rev. 2017,31, 199–211. [CrossRef] 107. Leslie, J.F.; Summerell, B.A. The Fusarium Laboratory Manual; Blackwell Publishing Ltd.: Oxford, UK, 2006. 108. Leslie, J.F.; Klein, K.K. Female Fertility and Mating Type Effects on Effective Population Size and Evolution in Filamentous Fungi. Genetics 1996,144, 557–567. 109. Berbegal, M.; P é rez-Sierra, A.; Armengol, J.; Grünwald, N.J. Evidence for Multiple Introductions and Clonality in Spanish Populations of Fusarium circinatum.Phytopathology 2013,103, 851–861. [CrossRef] 110. Iturritxa, E.; Ganley, R.J.; Wright, J.; Heppe, E.; Steenkamp, E.T.; Gordon, T.R.; Wingfield, M.J. A genetically homogenous population of Fusarium circinatum causes pitch canker of Pinus radiata in the Basque Country, Spain. Fungal Boil. 2011,115, 288–295. [CrossRef] 111. Britz, H.; Wingfield, M.J.; Coutinho, T.; Marasas, W.F.O.; Leslie, J.F. Female Fertility and Mating Type Distribution in a South African Population of Fusarium subglutinans f. sp. pini. Appl. Environ. Microbiol. 1998,64, 2094–2095. [CrossRef] 112. Britz, H.; Coutinho, T.; Wingfield, B.D.; Marasas, W.F.O.; Wingfield, M. Diversity, and differentiation in two populations of Gibberella circinata in South Africa. Plant Pathol. 2005,54, 46–52. [CrossRef] 113. Leslie, J.F. Fungal Vegetative Compatibility. Annu. Rev. Phytopathol. 1993,31, 127–150. [CrossRef] 114. Viljoen, A.; Wingfield, M.J.; Gordon, T.R.; Marasas, W.F.O. Genotypic diversity in a South African population of the pitch canker fungus Fusarium subglutinans f.sp. pini. Plant Pathol. 1997,46, 590–593. [CrossRef] 115. Santana, Q.C.; Coetzee, M.P.A.; Steenkamp, E.T.; Mlonyeni, O.X.; Hammond, G.N.A.; Wingfield, M.J.; Wingfield, B.D. Microsatellite discovery by deep sequencing of enriched genomic libraries. Biotechniques 2009,46, 217–223. [CrossRef] [PubMed] 116. Gordon, T.; Storer, A.; Okamoto, D. Population structure of the pitch canker pathogen, Fusarium subglutinans f. sp. pini, in California. Mycol. Res. 1996,100, 850–854. [CrossRef] 117. Muramoto, M. Pitch Canker of Pinus luchuensis in Japan. Plant Dis. 1990,74, 530. [CrossRef] 118. Gordon, T.R. Pitch Canker Disease of Pines. Phytopathology 2006,96, 657–659. [CrossRef] [PubMed] 119. Mullett, M.; Perez-Sierra, A.; Armengol, J.; Berbegal, M. Phenotypical and Molecular Characterisation of Fusarium circinatum: Correlation with Virulence and Fungicide Sensitivity. Forests 2017,8, 458. [CrossRef] Forests 2020,11, 724 38 of 40 120. Britz, H.; Couhnho, T.; Gordon, T.; Wingfield, M. Characterisation of the pitch canker fungus, Fusarium circinatum, from Mexico. S. Afr. J. Bot. 2001,67, 609–614. [CrossRef] 121. Adamson, K.; Mullett, M.; Solheim, H.; Barnes, I.; Müller, M.M.; Hantula, J.; Vuorinen, M.; Kacergius, A.; Markovskaja, S.; Musolin, D.; et al. Looking for relationships between the populations of Dothistroma septosporum in northern Europe and Asia. Fungal Genet. Boil. 2018,110, 15–25. [CrossRef] 122. Laas, M.; Adamson, K.; Drenkhan, R. A look into the genetic diversity of Lecanosticta acicola in northern Europe. Fungal Biol. 2019,123, 773–782. [CrossRef] 123. Wallin, J.R.; Waggoner, P.E. The influence of climate on the development and spread of Phytophthora infestans in artificially inoculated potato plots. Plant Dis. Rep. 1950,190, 19–33. 124. Hanso, M.; Drenkhan, R. Diplodia pinea is a new pathogen on Austrian pine (Pinus nigra) in Estonia. Plant Pathol. 2009,58, 797. [CrossRef] 125. Hanso, M.; Drenkhan, R. Lophodermium needle cast, insect defoliation and growth responses of young Scots pines in Estonia. For. Pathol. 2011,42, 124–135. [CrossRef] 126. Hanso, M.; Drenkhan, R. Simple visualization of climate change for improving the public perception in forest pathology/Kliimamuutuste visualiseerimise lihtne viis seoste paremaks tajumiseks metsapatoloogias. For. Stud. 2013,58, 37–45. [CrossRef] 127. McDonald, M.J. Temperature effects on Fusarium subglutinans f.sp. pini infection on juvenile Pinus radiata (Monterey pine) and influence on growth of Fusarium subglutinans f.sp. pini isolates from California and Florida. Master’s Thesis, San Jose State University, San Jose, CA, USA, 1994. 128. Gordon, T.; Kirkpatrick, S.C.; Petersen, J.C.; Friel, C.J. Potential diversity in vegetative compatibility groupings in the California population of Gibberella circinata.Mycol. Res. 2006,110, 936–940. [CrossRef] [PubMed] 129. Blank, L.; Mart í n-Garc í a, J.; Bezos, D.; Vettraino, A.M.; Krasnov, H.; Lomba, J.M.; Fern á ndez, M.; Diez, J.J. Factors Affecting the Distribution of Pine Pitch Canker in Northern Spain. Forests 2019,10, 305. [CrossRef] 130. Watt, M.; Ganley, R.J.; Kriticos, D.J.; Manning, L.K. Dothistroma needle blight and pitch canker: The current and future potential distribution of two important diseases of Pinus species. Can. J. For. Res. 2011 ,41, 412–424. [CrossRef] 131. Serra-Varela, M.J.; Al í a, R.; P ó rtoles, J.; Gonzalo, J.; Soliño, M.; Grivet, D.; Raposo, R. Incorporating exposure to pitch canker disease to support management decisions of Pinus pinaster Ait. in the face of climate change. PLoS ONE 2017,12, e0171549. [CrossRef] 132. Drenkhan, R.; Tomešov á -Haataja, V.; Fraser, S.; Bradshaw, R.E.; Vahal í k, P.; Mullett, M.; Mart í n-Garc í a, J.; Bulman, L.S.; Wingfield, M.J.; Kirisits, T.; et al. Global geographic distribution and host range of Dothistroma species: A comprehensive review. For. Pathol. 2016,46, 408–442. [CrossRef] 133. New, M.; Lister, D.; Hulme, M.; Makin, I. A high-resolution data set of surface climate over global land areas. Clim. Res. 2002,21, 1–25. [CrossRef] 134. Hijmans, R.J.; Cameron, S.E.; Parra, J.L.; Jones, P.G.; Jarvis, A. Very high-resolution interpolated climate surfaces for global land areas. Int. J. Clim. 2005,25, 1965–1978. [CrossRef] 135. Kim, Y.-S.; Woo, K.-S.; Koo, Y.-B.; Yeo, J.-K. Variation in susceptibility of six pine species and hybrids to pitch canker caused by Fusarium circinatum.For. Pathol. 2008,38, 419–428. [CrossRef] 136. Muramoto, M.; Tashiro, T.; Minamihashi, H. Distribution of Fusarium moniliforme var. subglutinans in Kagoshima Prefecture and its pathogenicity to pines. J. Jpn. For. Soc. 1993,75, 1–9. 137. Swett, C.L.; Gordon, T.R. Colonization of corn (Zea mays) by the pitch canker pathogen, Fusarium circinatum: Insights into the evolutionary history of a pine pathogen. Phytopathology 2009,99, S126–S127. 138. Guerra-Santos, J.J.; Cibrian-Tovar, D. El Cancro Resinoso por Fusarium subglutinans (Wollenw y Reink) Nelson, Tousson y Marasas, Una nueva Enfermedad de Pinus spp. en Mexico; Revista Chapingo (Mexico). In Serie Ciencias Forestales y del Ambiente; Universidad Autonoma Chapingo: Chapingo, Mexico, 1998; pp. 279–284. 139. Hodge, G.; Dvorak, W. Differential responses of Central American and Mexican pine species and Pinus radiata to infection by the pitch canker fungus. New For. 2000,19, 241–258. [CrossRef] 140. Porter, B.; Wingfield, M.; Coutinho, T. Susceptibility of South African native conifers to the pitch canker pathogen, Fusarium circinatum.S. Afr. J. Bot. 2009,75, 380–382. [CrossRef] 141. Vivas, M.; Zas, R.; Solla, A. Screening of Maritime pine (Pinus pinaster) for resistance to Fusarium circinatum, the causal agent of Pitch Canker disease. Forests 2011,85, 185–192. [CrossRef] Forests 2020,11, 724 39 of 40 142. Gordon, T.R.; Okamoto, D.; Storer, A.J.; Wood, D.L. Susceptibility of Five Landscape Pines to Pitch Canker Disease, Caused by Fusarium subglutinans f. sp. pini.HortScience 1998,33, 868–871. [CrossRef] 143. Iturritxa, E.; Ganley, R.J.; Raposo, R.; Mesanza, N.; Kirkpatrick, S.C.; Gordon, T.; Garc í a-Serna, I. Resistance levels of Spanish conifers against Fusarium circinatum and Diplodia pinea.For. Pathol. 2013 ,43, 488–495. [CrossRef] 144. Dvorak, W.; Hodge, G.; Kietzka, J. Genetic variation in survival, growth, and stem form of Pinus leiophylla in Brazil and South Africa and provenance resistance to pitch canker. South. Hemisphere For. J. 2007 ,69, 125–135. [CrossRef] 145. Hodge, G.R.; Dvorak, W.S. Variation in pitch canker resistance among provenances of Pinus patula and Pinus tecunumanii from Mexico and Central America. New For. 2006,33, 193–206. [CrossRef] 146. Dvorak, W.S.; Potter, K.M.; Hipkins, V.D.; Hodge, G. Genetic Diversity and Gene Exchange in Pinus oocarpa, a Mesoamerican Pine with Resistance to the Pitch Canker Fungus (Fusarium circinatum). Int. J. Plant Sci. 2009,170, 609–626. [CrossRef] 147. Elvira-Recuenco, M.; Iturritxa, E.; Majada, J.; Alia, R.; Raposo, R. Adaptive Potential of Maritime Pine (Pinus pinaster) Populations to the Emerging Pitch Canker Pathogen, Fusarium circinatum.PLoS ONE 2014 , 9, e114971. [CrossRef] [PubMed] 148. Iturritxa, E.; Mesanza, N.; Elvira-Recuenco, M.; Serrano, Y.; Quintana, E.; Raposo, R. Evaluation of genetic resistance in Pinus to pitch canker in Spain. Australas. Plant Pathol. 2012,41, 601–607. [CrossRef] 149. Carey, W.A.; Oak, S.W.; Enebak, S.A. Pitch canker ratings of longleaf pine clones correlate with Fusarium circinatum infestation of seeds and seedling mortality in containers. For. Pathol. 2005 ,35, 205–212. [CrossRef] 150. Enebak, S.A.; Stanosz, G.R. Responses of conifer species of the Great Lakes region of North America to inoculation with the pitch canker pathogen Fusarium circinatum.For. Pathol. 2003,33, 333–338. [CrossRef] 151. Broaddus, J.B. Branch Dieback and Cone and Seed Infection Caused by Fusarium moniliforme var. subglutinans in a Loblolly Pine Seed Orchard in South Carolina. Phytopathology 1985,75, 1104. [CrossRef] 152. Enebak, S.A.; Carey, W.A. Pitch Canker Caused by Fusarium circinatum Identified on Spruce Pine in Alabama. Plant Dis. 2003,87, 449. [CrossRef] 153. Schmale, D.G.; Gordon, T. Variation in susceptibility to pitch canker disease, caused by Fusarium circinatum, in native stands of Pinus muricata.Plant Pathol. 2003,52, 720–725. [CrossRef] 154. Gordon, T.; Storer, A.J.; Wood, D.L. The Pitch Canker Epidemic in California. Plant Dis. 2001 ,85, 1128–1139. [CrossRef] 155. Zanoni, T.A.; Farjon, A. World Checklist and Bibliography of Conifers. Brittonia 1999,51, 76. [CrossRef] 156. Price, A.; Liston, A.; Strauss, S.H. Evolution, phylogeny, and systematics. In Ecology and Biogeography of Pinus; Richardson, D.M., Ed.; Cambridge University Press: Cambridge, UK, 1998; pp. 49–68. 157. Garc í a, D.B.; Lomba, J.M.; Mart í nezÁ lvarez, P.; Fern á ndez, M.; Diez, J.J. Effects of Pruning in Monterrey Pine Plantations Affected by Fusarium circinatum.For. Syst. 2012,21, 481. [CrossRef] 158. Storer, A.J.; Gordon, T.; Dallara, P.L.; Wood, D. Pitch canker kills pines, spreads to new species and regions. Calif. Agric. 1994,48, 9–13. [CrossRef] 159. Fisher, R.F.; Garbett, W.S.; Underhill, E.M. Effects of Fertilization on Healthy and Pitch Canker-Infected Pines. South. J. Appl. For. 1981,5, 77–79. [CrossRef] 160. Dwinell, L.D.; Ryan, P.L.; Kuhlman, E.G. Pitch canker of loblolly pine in seed orchards. In Proceedings of the 14th Southern Forest Tree Improvement Conference, Gainesville, FL, USA, 14–16 June 1977; pp. 130–137. 161. Woo, K.S.; Yoon, J.H.; Han, S.U.; Kim, C.S. Assessment of pathogenic variation against pitch canker pathogen, Fusarium circinatum in Pinus thunbergii and responses of natural selection Pinus × rigitaeda to branch inoculation in a seed orchard. Plant Pathol. J. 2010,26, 299–305. [CrossRef] 162. Vivas, M.; Nunes, C.; Coimbra, M.A.; Solla, A. Maternal effects and carbohydrate changes of Pinus pinaster after inoculation with Fusarium circinatum.Trees 2013,28, 373–379. [CrossRef] 163. Ford, C.; Jones, N.B.; Chirwa, P.W. Pinus patula and pine hybrid hedge productivity in South Africa: A comparison between two vegetative propagation systems exposed to natural infection by Fusarium circinatum.South. For. J. For. Sci. 2014,76, 167–175. [CrossRef] 164. Kanzler, A.; Nel, A.; Ford, C. Development and commercialisation of the Pinus patula x P. tecunumanii hybrid in response to the threat of Fusarium circinatum.New For. 2014,45, 417–437. [CrossRef] Forests 2020,11, 724 40 of 40 165. Dick, M.A.; Simpson, J.A. Fusarium circinatum as a Cause of Damping-off: Exploring the Host Range. Unpublished Report. 2003. Available online: http://www.nzfoa.org.nz/images/stories/pdfs/content/fhrc_ reports/2002-04.pdf (accessed on 11 February 2020). 166. Fern á ndez-Fern á ndez, M.; Naves, P.; Musolin, D.L.; Selikhovkin, A.V.; Cleary, M.; Chira, D.; Paraschiv, M.; Gordon, T.; Solla, A.; Papazova-Anakieva, I.; et al. Pine Pitch Canker and Insects: Regional Risks, Environmental Regulation, and Practical Management Options. Forests 2019,10, 649. [CrossRef] © 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).