Regulation of K+ Nutrition in Plants

F on ie s in Plan Science | www. on ie sin.o g 1 Ma ch 2019 | Volume 10 | A icle 281 REVIEW published: 20 Ma ch 2019 doi: 10.3389/ pls.2019.00281 Edi ed by: Lam-Son T an, RIKEN, Japan Re iewed by: Manuel Nie es-Co dones, Cen e o Edaphology and Applied Biology o Segu a, Spanish Na ional Resea ch Council (CSIC), Spain Fe nando Aleman, The Sc ipps Resea ch Ins i u e, Uni edS a es *Co espondence: José M. Pa do [email p o ec ed] Special y sec ion: This a icle was submi ed o Plan Abio ic S ess, a sec ion o he jou nal F on ie s in Plan Science Recei ed: 07 Decembe 2018 Accep ed: 20 Feb ua y 2019 Published: 20 Ma ch 2019 Ci a ion: Ragel P, Radda z N, Leidi EO, Quin e o FJ and Pa do JM (2019) Regula ion o K+ Nu i ion in Plan s. F on . Plan Sci. 10:281. doi: 10.3389/ pls.2019.00281 Regula ion o K+ Nu i ion in Plan s PaulaRagel1,2, Na aliaRadda z1, Edua doO.Leidi3, F anciscoJ.Quin e o1 and JoséM.Pa do1* 1 Ins i u o de Bioquímica Vege al y Fo osín esis, Consejo Supe io de In es igaciones Cien í icas y Uni e sidad de Se illa, Se ille, Spain, 2 Cen e o O ganismal S udies, Uni e si ä Heidelbe g, Heidelbe g, Ge many, 3 Ins i u o de Recu sos Na u ales y Ag obiologia de Se illa, Consejo Supe io de In es igaciones Cien i icas, Se ille, Spain Mode n ag icul u e elies on mine al e iliza ion. Unlike o he majo mac onu ien s, po assium (K+) is no inco po a ed in o o ganic ma e bu emains as soluble ion in he cell sap con ibu ing up o 10% o he d y o ganic ma e . Consequen ly, K+ cons i u es a chie osmo icum o d i e cellula expansion and o gan mo emen s, such as s oma a ape u e. Mo eo e , K+ anspo is c i ical o he con ol o cy oplasmic and luminal pH in endosomes, egula ion o memb ane po en ial, and enzyme ac i i y. No su p isingly, plan s ha e e ol ed a la ge ensemble o K+ anspo e s wi h de ined unc ions in nu ien up ake by oo s, s o age in acuoles, and ion ansloca ion be ween issues and o gans. This e iew desc ibes c i ical anspo p o eins go e ning K+ nu i ion, hei egula ion, and coo dina ed ac i i y, and summa izes ou cu en unde s anding o signaling pa hways ac i a ed by K+ s a a ion. Keywo ds: plan nu i ion, po assium, ni a e, egula ion, long-dis ance anspo INTRODUCTION Po assium (K+) is o pa amoun impo ance in plan cell physiology. K+ is an essen ial mac onu ien ha ul ills c i ical unc ions ela ed o enzyme ac i a ion, osmo ic adjus men , u go gene a ion, cell expansion, egula ion o memb ane elec ic po en ial, and pH homeos asis (Hawkes o d e  al., 2012). While he K+ concen a ion in he soil solu ion may a y widely om 0.01 o 20 mM, plan cells main ain a ela i ely cons an concen a ion o 80–100 mM in he cy oplasm (Rod iguez-Na a o, 2000). Mo eo e , plan s accumula e la ge amoun s o K+ in hei acuoles, su passing pu ely nu i ional equi emen s. Hence, K+ is he mos abundan ca ion in plan cells, comp ising up o 10% o plan d y weigh and o en exceeding he ca. 2% ha suppo s nea -maximal g ow h a es (Whi e and Ka ley, 2010). The e is a s eep cu ilinea ela ionship be ween he issue concen a ion o K+ and plan g ow h, om which a c i ical concen a ion o K+ suppo ing 90% o maximum yield can be de e mined. Abo e his concen a ion, g ow h has no co ela ion wi h he inc eased K+ con en , bu a lowe K+ concen a ions, g ow h declines apidly. Consequen ly, K+ e iliza ion is common p ac ice in mode n ag icul u e and abou 40–60% o c op yields a e a ibu able o comme cial e ilize use (S ewa e  al., 2005). Howe e , ag icul u al e iliza ion is a om being ine- uned wi h nu i ional equi emen s. K+ is aken up om he soil solu ion by oo epide mal and co ical cells. Once K+ is inside he oo symplas , i may be s o ed in acuoles, whe e i ul ills osmo ic unc ions, o is anspo ed o he shoo ia xylem (Pa do and Rubio, 2011). In u n, shoo cells may also supply s o ed K+ o edis ibu ion ia phloem. In his ansi om he soil o he di e en Ragel e al. Regula ion o K+ Nu i ion in Plan s F on ie s in Plan Science | www. on ie sin.o g 2 Ma ch 2019 | Volume 10 | A icle 281 plan o gans, K+ c osses a ious cell memb anes h ough K+- speci ic anspo sys ems (Figu e 1). Coo dina ed ope a ion o he di e en anspo sys ems wi hin he plan o secu e K+ up ake om he soil and deli e y o he di e en plan o gans equi es complex K+ sensing and signaling mechanisms. Because o he ex ao dina y di e si y o K+ anspo e s in plan cells and he physiological and de elopmen al p ocesses in which hey a e in ol ed, his e iew is ocused on he molecula mechanisms media ing K+ up ake and elease a he plasma memb ane le el, wi h an emphasis on K+ abso p ion om he soil and dis ibu ion h oughou he plan due o he ele ance o hese p ocesses in plan nu i ion. S o age o K+ in o acuoles is ea ed only b ie ly and eade s a e e e ed o o he comp ehensi e e iews desc ibing anspo sys ems ope a ing a he onoplas (Ma inoia e  al., 2012; Ahmad and Maa huis, 2014; Eisenach and De Angeli, 2017; Ma inoia, 2018). Las , because o he ex ensi e in e ac ions o ni ogen and K+ in plan mine al nu i ion, wesumma ize he coo dina ed egula ion o NO3− and K+ up ake and long-dis ance anspo in A abidopsis. Up ake and dis ibu ion o K+ in plan cells is ca ied ou by a a ie y o anspo e p o eins ca ego ized in o se e al amilies wi h a ied s uc u es and anspo mechanisms ha comp ise he channel amilies Shake -like ol age-dependen , he andem-po e (TPK), and he wo-po e channels (TPC) (Hed ich, 2012), he ca ie -like amilies KT/HAK/KUP (Nie es- Co dones e  al., 2014a; Li e  al., 2018), HKT unipo e s and sympo e s (Hamamo o e al., 2015), and ca ion-p o on an ipo e s (CPA). The CPA amily is he la ges one and includes he NHX, CHX, and KEA an ipo e s (Sze and Chan oj, 2018). In his e iew, we desc ibe he s uc u e and di e si y o he main K+ anspo e amilies whose membe s con ibu e subs an ially o K+ nu i ion. O he p o eins wi h unce ain oles o desc ip ions o anspo ac i i ies wi hou candida e p o eins ha e been omi ed. TRANSPORT PROTEIN FAMILIES INVOLVED IN K+ NUTRITION K+-Selec i e Channels The i s K+ anspo e wi h a ole in nu ien up ake was he Shake -like, ol age-ga ed, and K+-selec i e channel AKT1 (Hi sch e  al., 1998). Al hough ol age-ga ed (VG) channels o plan s a e phylogene ically ela ed o animal Shake channels, hey a e dis inc and include addi ional unc ional domains (Jegla e  al., 2018). The basic a chi ec u e o VG channels consis s o ou α-subuni s su ounding a cen al aqueous po e o K+ pe mea ion. Each subuni con ains six ansmemb ane segmen s, named S1–S6, which can bedi ided in o wo di e en modules: he i s ou α-helices o m a ol age-senso domain ha con ains mul iple posi i ely cha ged esidues ha mo es wi hin he memb ane in esponse o ol age. This mo emen is di ec ly coupled o he opening o closing o he channel. The segmen s S5, S6, and he po e loop, o m he po e domain, named P, whe e each o he ou subuni s con ibu es equally o he pe mea ion pa hway. Mo eo e , plan α-subuni s ha e a long C- e minal egion cons i u ing mo e han hal o he p o ein (Figu e 2). This cy osolic ail includes se e al unc ional domains: (1) a linke egion (C-linke ) p oximal o he po e FIGURE 1 | T anspo e s in ol ed in K+ up ake by oo s and in e -o gan pa i ion. HAK5, AKT1, and non-selec i e cyclic nucleo ide-ga ed ca ion channels (CNGC) all con ibu e o K+ nu i ion, albei a di e en anges o subs a e concen a ions, om low- o high-a ailabili y, espec i ely. K+ e lux h ough he ou wa d- ec i ying GORK channel acili a es he ine- uning o plasma memb ane elec ical po en ial, and allows epola iza ion unde ci cums ances ha p omo e depola iza ion, such as salini y s ess. In he oo s ele, he ou wa d- ec i ying SKOR channel eleases K+ in o he xylem essels o nu ien deli e y o he shoo s. The ni a e anspo e NRT1.5 acili a es K+ uploading in o he xylem ei he by elec ical coupling wi h o he K+-selec i e anspo e s o di ec ly ac ing as K+/H+ an ipo e . In ae ial issues, an a ay o K+-in lux channels and KT/HAK/KUP ca ie s allow he up ake o he incoming K+ in o g een cells. K+ is s o ed inside acuoles by NHX exchange s and eleased back o he cy osol by TPK and TPC1 channels, and possibly also by KT/HAK/KUP ca ie s a he onoplas ( he acuole in oo cells is omi ed o simplici y). The plasma memb ane ou wa d K+ channel AKT2 eleases K+ in o he phloem o e u ning K+ o he oo and o acili a e he uploading o pho osyn ha es in o he phloem sap. Ragel e al. Regula ion o K+ Nu i ion in Plan s F on ie s in Plan Science | www. on ie sin.o g 3 Ma ch 2019 | Volume 10 | A icle 281 ha ansduces con o ma ional changes ha ga e he channel and ha may also de e mine he a ge memb ane (Nie es- Co dones e  al., 2014b; Jegla e  al., 2018); (2) a conse ed and essen ial cyclic nucleo ide-binding homology domain (CNBHD) whose unc ion is no he binding o cNMP bu o media e he in e ac ions be ween subuni s wi hin he channel e ame ; (3) an anky in domain ( ound in only six ou o he nine A abidopsis VG channels), which may media e he binding o in e ac ing p o eins (Michaely and Benne , 1992); and (4) a dis al KT/KHA domain ich in hyd ophobic and acidic esidues, ha is unique o plan K+ channels, and is in ol ed in channel e ame iza ion and clus e ing a he memb ane (Da am e  al., 1997; Eh ha d e  al., 1997; Zimme mann e  al., 2001; D eye e  al., 2004). Plan ol age-ga ed K+ channels a e di ided in o h ee sub amilies ega ding hei esponse o he memb ane po en ial (D eye and Uozumi, 2011): (1) Inwa d- ec i ying (Kin) channels ha in A abidopsis include AKT1, AKT6, KAT1, and KAT2; hey open a hype pola ized memb ane po en ials allowing he up ake o K+. (2) Ou wa d- ec i ying (Kou ) channels ha media e K+ elease because hey open a depola ized memb ane po en ials; his g oup is composed o SKOR and GORK channels. (3) Weakly ec i ying (Kweak) channels ha can media e bo h K+ up ake and elease, and whose A abidopsis ep esen a i e is AKT2. In addi ion, he A abidopsis KC1 (KAT3) is an elec ically silen Shake -like p o ein ha in e ac s wi h and egula es unc ionali y o he Kin channels AKT1, KAT1, KAT2, and AKT2, bu no he Kou channels (Jeanguenin e al., 2011). This in e ac ion nega i ely shi s he ac i a ion h eshold o Kin channels and dec eases he mac oscopic inwa d conduc ance compa ed o ha o homome ic channels (D eye e al., 1997; Duby e  al., 2008; Geige e  al., 2009). He e ome iza ion o di e en subuni s o Kin channels is o g ea impo ance o inc ease he unc ional di e si y and egula ion o di e en cell ypes (D eye e al., 1997; Vé y and Sen enac, 2003; Xicluna e  al., 2007; Jeanguenin e  al., 2008; Lebaudy e  al., 2008; Lebaudy e  al., 2010). Al hough his beha io has also been sugges ed o ou wa d- ec i ie (Kou ) channels, he e ome iza ion has been epo ed only among subuni s o Kin o Kou , p e en ing o ma ion o he e ome ic s uc u es be ween he wo subuni ypes (D eye e  al., 2004). K+-Up ake Ca ie s P o eins o he KT/HAK/KUP amily a e p esen in plan s, ungi, bac e ia, and e en i uses (G eine e  al., 2011; San a- Ma ia e  al., 2018), and hey a e o en associa ed wi h K+ anspo ac oss memb anes and K+ supply. In bac e ial genomes, K+ ca ie s o his amily a e encoded by single-copy genes named kup. In Esche ichia coli, kup is a cons i u i e low-a ini y up ake sys em ha ope a es as K+-H+ sympo e (Zakha yan and T chounian, 2001). In ungi, he homologous p o eins a e encoded by HAK1-like genes p esen as one- o wo-copy in AB C FIGURE 2 | Topological models o he main ion anspo e s in ol ed in K+ nu i ion. (A) Vol age-ga ed K+ channels con ain six ansmemb ane domains (S1–S6); S4 is he ol age-senso cha ac e ized by he a ay o posi i ely cha ged amino acids (+). The long C- e minal ail con ains se e al conse ed domains: C-linke , a cyclic nucleo ide binding homologous domain (CNBHD), an anky in domain (ANK), and a inal egion ich in hyd ophobic and acidic esidues (KHA). (B) HKT anspo e s ha e a channel-like s uc u e ha con ains ou iden ical subuni s (a–d), each comp ising wo ansmemb ane helices (M1 and M2) connec ed by he P-loop in ol ed in ion selec i i y. (C) KT/HAK/KUP anspo e s ha e 12 pu a i e ansmemb ane domains (TMs). TM1-5 and TM6-10 a e p edic ed o old in he same con o ma ion bu showing in e se symme y. Ragel e al. Regula ion o K+ Nu i ion in Plan s F on ie s in Plan Science | www. on ie sin.o g 4 Ma ch 2019 | Volume 10 | A icle 281 mos species. In con as o bac e ial kup, ungal HAK genes a e s ongly induced by K+ s a a ion and he encoded p o eins media e high-a ini y K+ anspo (Beni o e  al., 2011). In plan s, hese anspo e s a e known as KT, HAK, o KUP (KT/HAK/KUP amily) and hey a e ep esen ed by mul iple genes in hei genomes. Membe s o his amily ha e been widely associa ed wi h high-a ini y K+ up ake om he soil, while o he s may unc ion in bo h low-a ini y and/o high- a ini y anspo (Luan e  al., 2009; Ve y e  al., 2014) and o he oles ela ed, o example, o K+ ansloca ion, con ol o wa e mo emen a he plan le el, sal ole ance, osmo ic/ d ough esponses, anspo o o he alkali ca ions, and de elopmen al p ocesses in plan s, such as oo hai g ow h and auxin dis ibu ion (Li e al., 2018; San a-Ma ia e al., 2018). These di e se unc ions o KT/HAK/KUP anspo e s may all esul om hei c i ical oles in cellula K+ homeos asis. KT/HAK/KUP genes a e no p esen in animal cells, wha could indica e ha hey a e c ucial o K+ anspo in o ganisms acing ex e nal solu ions wi h luc ua ing and e y low K+ concen a ions, o en in he μM ange (Ashley e  al., 2006). Based on he p esen knowledge, KT/HAK/KUP genes a e p esen in all plan genomes, which con as s wi h ha in he o he kingdoms, whe e hey a e only p esen in ce ain species (G abo , 2007; G eine e al., 2011). This di e ence may e lec he impo ance o hese anspo e s o he plan ’s way o li e. KT/HAK/KUP anspo e s o land plan s a e classi ied acco ding o hei sequence homology in o six clus e s o clades (I–VI), wi h clade VI including only membe s o b yophy es (San a-Ma ia e al., 2018). Phylogene ic analysis shows ha all KT/HAK/KUPs om algae di e ge om land plan clades, sugges ing ha he di e si ica ion in o hese g oups ook place a e he coloniza ion o land by g een o ganisms (San a-Ma ia e  al., 2018). The KT/HAK/KUP g oup om angiospe ms displays a high and a he a iable numbe o membe s in he di e en plan species genomes ha ha e been sequenced so a . Fo ins ance, he e a e 13 genes in A abidopsis, 16 in peach, 17 in g ape ine, 20 in Medicago, 21 in Cassa a, 27 in ice, maize, and B achypodium, and 57 in Panicum i ga um (Song e  al., 2015; Nie es-Co dones e  al., 2016a,c; Ou e  al., 2018). Membe s o KT/HAK/KUP amily in angiospe m a e classi ied among clades I–V (Nie es-Co dones e  al., 2016c). The KT/HAK/KUP anspo e s in ol ed in K+ up ake om he soil a e clus e ed in o a dis inc subg oup o clade I, e med Ia (Nie es-Co dones e  al., 2016c) and ha we call he ein HAK1-like anspo e s by analogy wi h he ungal coun e pa s. This subg oup includes ba ley H HAK1 (San a-Ma ía e  al., 1997; Gie h and Mäse , 2007), A abidopsis A HAK5 (Rubio e  al., 2000; Gie h e  al., 2005), ice OsHAK1 and OsHAK5 (Bañuelos e  al., 2002), peppe CaHAK1 (Ma inez-Co de o e  al., 2004), oma o LeHAK5 (Nie es-Co dones e  al., 2007), and Thellungiella ThHAK5 (Alemán e al., 2009b). High-a ini y K+ anspo has been demons a ed o all he HAK1-like anspo e s in he e ologous exp ession sys ems (Nie es-Co dones e  al., 2014a). On he o he hand, A KUP7, belonging o clade V, could bein ol ed in K+ up ake om low o mode a e ex e nal K+ concen a ions (Han e al., 2016), and hus he pa icipa ion in K+ up ake om soil o p o eins om di e en clades should no bedisca ded. In e es ingly, o he membe s o clade Icould be ela ed wi h K+ up ake by cells om specialized issues. DmHAK5 om Venus ly aps is implica ed in he up ake o K+ eleased om he diges ed p ey in he bi-lobed cap u e o gan (Sche ze e al., 2015), whe eas he quinoa CqHAK5-like d i es K+ in lux in o cells o he lea sal bladde s o con ibu e o he osmo ic balance o he cy osol agains he osmo ic p essu e o he sal -con aining acuoles (Bohm e  al., 2018). KT/HAK/KUP anspo e s a e phylogene ically ela ed o he supe amily o acid-polyamine-o ganoca ion (APC) anspo e s ha comp ises seconda y ac i e anspo p o eins esponsible o unipo , sympo , and an ipo o a wide ange o subs a es (Vas e ma k e  al., 2014). Taking as empla e c ys al s uc u es o p oka yo ic APC anspo e s, compu a ional 3D modeling o A KUP7 (Ahn e al., 2004; Al-Younis e al., 2015; San a-Ma ia e  al., 2018), A KUP4/TRH1 (Da as e  al., 2015), OsHAK1 (Rai e al., 2017), A KUP1/TRH1 (San a-Ma ia e al., 2018), A HAK5 (San a-Ma ia e  al., 2018), and H HAK1 (San a-Ma ia e  al., 2018) has been epo ed. The s uc u al models (Figu e 2) show he p esence o common a ibu es among all o hem: (1) a hyd ophobic co e con aining 10–14 ansmemb ane (TM) segmen s; and (2) h ee cy osolic domains— he N- and C- e mini and a egion con aining app oxima ely 70 esidues si ua ed be ween second and hi d TMs (loop II–III). Al hough, he s uc u e o he po e egion has no been desc ibed ye , se e al wo ks ha e analyzed he e ec o mu a ions on he unc ion o hese anspo e s (San a-Ma ia e  al., 2018). So a , esul s indica ed ha se e al pa s o he p o ein may con ibu e o se ing he Vmax o he anspo e and ha he egion including om N- e minus o loop II–III may con ibu e in de e mining i s Km. Fu he mo e, sequence alignmen s show ha , al hough he e is no ex ensi e sequence conse a ion, 40 amino acid esidues a e conse ed in exac ly he same posi ion in all he euka yo ic HAK anspo e s and in he Kup bac e ial anspo e s (Rod iguez-Na a o, 2000). Six o hese conse ed esidues a e included in a highly conse ed mo i in he i s ansmemb ane domain whose consensus sequence is GVVYGDLGTSPLY ( he amino acids conse ed in all p o eins a e in bold) (Rod iguez-Na a o, 2000). A helical-wheel ep esen a ion o his ansmemb ane agmen loca es h ee glycine esidues on he same side o he helix, which in he case o a e ame ic s uc u e may ope a e as a subs a e selec i i y il e analogous o he GXGYGD mo i highly conse ed in K+ channels. Rega ding his, i has been sugges ed ha A KUP4/TRH1 may o m homodime s (Da as e al., 2015), likely in ol ing he in e ac ion be ween C- e minus domains and less likely be ween loops II–III. Con a y o VG channels ha a e all a ge ed o he plasma memb ane, KT/HAK/KUP anspo e s ha e been epo ed in di e en subcellula compa men s (Table 1). The majo i y o he cha ac e ized anspo e s o he KT/HAK/KUP amily a e loca ed in he plasma memb ane, al hough no all o hem a e in ol ed in K+ nu i ion. Fo ins ance, A KUP4/TRH1 seems o pa icipa e in auxin anspo ela ed wi h oo g a i opism and oo hai de elopmen (Rigas e al., 2013), whe eas A KUP6 ac s in la e al oo ini ia ion and de elopmen in he auxin and ABA c oss alk signaling pa hways (Osakabe e  al., 2013). Ragel e al. Regula ion o K+ Nu i ion in Plan s F on ie s in Plan Science | www. on ie sin.o g 5 Ma ch 2019 | Volume 10 | A icle 281 HKT P o eins The ample epe oi e o anspo e s encoded in he genome o plan s includes p o eins ha a e collec i ely known as High a ini y K+ T anspo e s (HKTs; Figu e 2) despi e he ac ha hese p o eins acili a e Na+-selec i e unipo o Na+-K+ sympo wi h a channel-like ac i i y (Beni o e  al., 2014). Phylogene ic and unc ional analyses dis inguished wo HKT sub amilies (Pla en e  al., 2006). Membe s o sub amily I (HKT1) a e ubiqui ous in plan s, Na+-selec i e, and mos ly in ol ed in Na+ eci cula ion h ough ascula issues, as bes exempli ied by A HKT1;1 (Suna pi e  al., 2005). Membe s o sub amily II (HKT2) ha e been ound only in monoco yledonous species. Al hough hey a e all K+-pe meable, mechanis ically HKT2s can ope a e as ei he Na+-K+ sympo e s o K+-selec i e unipo e s [ e iewed by Beni o e al. (2014)]. HKT2-like p o eins o ce eals ha e been in ol ed in K+ nu i ion. K+ UPTAKE BY ROOTS The up ake o K+ by oo s (o en measu ed wi h ubidium as ace ) exhibi s a biphasic kine ics in esponse o inc easing ex e nal concen a ions co esponding o high- and low-a ini y anspo sys ems, which wo k a low (<1 mM) and high (>1mM) ex e nal K+ concen a ions espec i ely (Eps ein e al., 1963; Gie h and Mäse , 2007). A high concen a ion in he soil solu ion, K+ c osses he memb ane mos ly h ough channels. The channels simply gi e a pa h o he ions allowing hem o mo e down he elec ochemical g adien . A low K+ concen a ion, ac i e anspo e sys ems a e needed in o de o pull K+ inside he cell agains i s elec ochemical g adien . Howe e , s udies in se e al plan species ha e shown ha channels may be in ol ed in K+ up ake in he high-a ini y ange o K+ concen a ions (Rubio e  al., 2010) as long as he memb ane is su icien ly hype pola ized, i.e. highly elec onega i e inside (Hi sch e  al., 1998; Spalding e  al., 1999; Gie h and Mäse , 2007; Rubio e  al., 2010). The sensi i i y o NH4+ is an impo an cha ac e is ic o high- a ini y K+ up ake media ed by ca ie s ha has been used as a ool o he iden i ica ion o addi ional high-a ini y anspo sys ems (San a-Ma ía e al., 1997; Nie es-Co dones e al., 2007). NH4+-sensi i e and -insensi i e componen s o high-a ini y K+ up ake ha e been iden i ied in A abidopsis (Spalding e al., 1999), ba ley (San a-Ma ia e  al., 2000), peppe (Ma inez-Co de o e  al., 2005), and ice (Bañuelos e al., 2002; Chen e  al., 2015). Resul s indica e ha he NH4+-sensi i e componen o K+ up ake is likely media ed by KT/HAK/KUP anspo e s (HAK1-like anspo e s), whe eas inwa d- ec i ie K+ channels (AKT1-like channels) cons i u e he NH4+-insensi i e pa hway (San a-Ma ia e al., 2000; Nie es-Co dones e al., 2014a). Toge he , AKT1-like channels and HAK1-like anspo e s a e now hough o cons i u e he main sys ems o K+ up ake in plan s unde low-K+ concen a ions (Table 2). Howe e , he NH4+-sensi i e and -insensi i e pa hways appea o con ibu e di e en ly o high- a ini y K+ up ake depending on he plan species and he ionic ex e nal concen a ion o anspo ed subs a es, mainly K+, NH4+, and Na+ (Aleman e  al., 2011; Nie es-Co dones e  al., 2016c). Among he inwa d- ec i ying K+ channels o A abidopsis, only AKT1 and A KC1 a e abundan ly exp essed in oo issues (Rein anz e al., 2002). A KC1 exp essed alone emains in he endoplasmic e iculum, bu i can be ec ui ed o he plasma memb ane o egula e AKT1 ac i i y (Duby e  al., 2008; Geige e  al., 2009; Honsbein e  al., 2009; Wang e  al., 2010). In addi ion, AKT1 is posi i ely egula ed by he p o ein kinase complex comp ising he kinase CIPK23 and one o he wo al e na i e calcium- dependen egula o y subuni s CBL1 and CBL9 (Li e  al., 2006; TABLE 1 | Sub-cellula loca ion o selec ed A abidopsis, ba ley, ice, and Physcomi ella pa ens KT/HAK/KUP anspo e s. T anspo e /loca ion Plasma memb ane Tonoplas ER-like memb anes Thylakoid memb anes Re e ences A HAK5 √Qi e al., 2008 A KUP4/TRH1 √√√ Rigas e al., 2013 A KUP5 √Jaquinod e al., 2007; Whi eman e al., 2008 A KUP6 √Osakabe e al., 2013 A KUP7 √ √ Han e al., 2016 A KUP8 √Jaquinod e al., 2007; Whi eman e al., 2008 A KUP12 √ √ Kle mann e al., 2004; Jaquinod e al., 2007; Whi eman e al., 2008 H HAK1 √Senn e al., 2001 OsHAK1 √Chen e al., 2015 OsHAK5 √Yang e al., 2014 OsHAK10 √Bañuelos e al., 2002 OsHAK21 √Shen e al., 2015 PpHAK2 √Ha o e al., 2013 PpHAK3 √Ha o e al., 2013 Ragel e al. Regula ion o K+ Nu i ion in Plan s F on ie s in Plan Science | www. on ie sin.o g 6 Ma ch 2019 | Volume 10 | A icle 281 Xu e  al., 2006). AKT1 possesses an in insic K+ senso educing channel conduc ance a submillimola ex e nal K+ concen a ions. Despi e his K+ senso , upon ac i a ion by he CIPK/CBL complex a low ex e nal K+, he homome ic AKT1 channels open a ol ages posi i e o EK, a condi ion po en ially esul ing in cellula K+ leakage (Geige e  al., 2009). Inco po a ion o he A KC1 subuni in o he channel complex, howe e , shi s he ol age dependence o AKT1 owa d mo e nega i e po en ials (ca. −70mV) o p e en K+ loss (Geige e  al., 2009; Wang e  al., 2010; Wang e al., 2016). In o he wo ds, AKT1/KC1 he e ome iza ion ende s he channel mo e e icien a blocking K+ pe mea ion in he ou wa d di ec ion. The physical in e ac ion o he CIPK23/CBL1 complex is speci ic o AKT1 channels and does no in ol e he A KC1 subuni . The gain-o - unc ion mu a ion A KC1-D (G322D subs i u ion in ansmemb ane S6) was eco e ed in he cipk23 mu an backg ound. A KC1-D enhanced he inhibi ion o AKT1 channel ac i i y and es ic ed K+ leakage h ough AKT1 unde low-K+ condi ions, he eby inc easing he ole ance o nu ien s ess (Wang e  al., 2016). Al hough he double mu an ak 1 KC1-D was sensi i e o low-K+, indica ing ha KC1-D ac ion is h ough AKT1, an addi ional indi ec e ec o mu a ion KC1-D h ough HAK5 canno be uled ou . By inhibi ing AKT1 and shi ing i s ol age dependence owa d a mo e nega i e di ec ion, he plasma memb ane could become hype pola ized in he KC1-D mu an , he eby enhancing he exp ession and ac i i y o HAK5 and imp o ing ne K+ up ake. Se e al mechanisms o AKT1 deac i a ion ha e been p oposed. The PP2C- ype p o ein phospha ase AIP1 in e ac s wi h and inac i a es he AKT1 channel, coun e ac ing he ac i a ion by CIPK23in oocy es (Lee e al., 2007). In p inciple, hese indings a e e idence o a phospho yla ion/dephospho yla ion swi ch ha egula es AKT1 channel ac i i y, bu i should be no ed ha no phospho yla ion o AKT1 by CIPK23 and dephospho yla ion by AIP1 has been demons a ed conclusi ely (Hashimo o e al., 2012). Ins ead, ou componen s, CIPKs, CBLs, PP2Cs, and AKT1, appea o in e ac mu ually and o m a molecula complex whose speci ic composi ion could ul ima ely egula e channel ac i i y (Lan e  al., 2011). In his model, PP2C phospha ases in e ac wi h he kinase domain o CIPKs o coun e ac kinase- media ed ac i a ion o AKT1. Upon calcium signaling, CBLs in e ac wi h PPC2C o inhibi hei phospha ase ac i i y while simul aneously ac i a ing he pa ne ing CIPKs. On he o he hand, CBL10, a egula o y subuni o CIPK24/SOS2 bu no o CIPK23, also in e ac s di ec ly wi h AKT1 and nega i ely modula es AKT1 ac i i y by compe ing wi h CIPK23 o bind AKT1 (Ren e  al., 2013). Since CBL10 unc ion is ela ed o salini y s ess a he han o mine al nu i ion (Kim e  al., 2007; Quan e  al., 2007; Lin e  al., 2009), his c oss- egula ion may cons i u e a mechanism o p e en salini y-induced K+ loss hough AKT1. In line wi h his, he ni ic oxide (NO) ha accumula es unde salini y s ess also inhibi s he K+ up ake media ed by AKT1. The link is indi ec since NO igge ed he accumula ion o py idoxal 5′-phospha e (PLP), an ac i e o m o i amin B6, ha in u n ep essed he ac i i y o AKT1in Xenopus oocy es and A abidopsis oo p o oplas s (Xia e  al., 2014). In A abidopsis, he ol age-ga ed channel GORK (gua d cell ou wa d- ec i ying K+) is he majo ou wa d- ec i ying K+ channel in gua d cells whe e i con ibu es o K+ e lux o dec easing u go and s oma al closu e (Ache e al., 2000; Hosy e  al., 2003). In addi ion, GORK is exp essed in oo ou e cell laye s (epide mal, oo hai s, and co ex) o A abidopsis and hus GORK is conside ed a majo pa hway o s ess- induced K+ leakage om oo cells, e.g. by exposu e o oo s o high sal (I ashikina e  al., 2001; Demidchik e  al., 2010; Demidchik e al., 2014). P oduc ion o hyd oxyl adicals (HO˙) in salinized oo s s imula es a d ama ic K+ e lux media ed by GORK om oo cells (Demidchik e  al., 2010). The oxida i e and sal s esses cause p og ammed cell dea h (PCD) and collapse memb ane po en ial in oo cells o A abidopsis haliana in a K+-dependen manne . Acco dingly, he A abidopsis go k1-1 mu an showed no K+ ou wa dly di ec ed cu en s in esponse o HO˙. Besides, a e exposu e o high NaCl le els, he mu an go k1-1 displayed lowe ac i i y o p o eases and endonucleases o PCD, which in he wild ype was d ama ically enhanced by K+ loss in oo cells (Demidchik e  al., 2010). Bo h he exp ession le el and channel ac i i y o GORK a e signi ican ly up egula ed by inc easing le els o he abscisic acid (ABA) and jasmona e. S imuli ha ele a ed endogenous ABA concen a ions, e.g. d ough , osmo ic s ess, o cold, led o he up- egula ion o GORK ansc ip s (Becke e al., 2003; Suhi a, 2004) while ea men wi h salicylic acid inhibi ed he p esence o ac i e GORK channels and imp o ed salini y ole ance h ough p e en ion o K+ e lux. Recen s udies demons a ed ha calcium-dependen p o ein kinase 21 (CPK21) phospho yla ed GORK and sugges ed ha 14-3-3 p o eins con ol GORK ac i i y h ough binding wi h CPK21. This kinase phospho yla es h ee amino acid esidues in he C- e minus o GORK, T344, S518, and S649. Binding o 14-3-3 o CPK21 s ongly s imula ed i s kinase ac i i y and inc eased TABLE 2 | Compa ison o AKT1 channels and HAK1/HAK5 anspo e s om A abidopsis and ice wo king a di e en anges o ex e nal K+ concen a ions. The up ake sys ems wo king in addi ion o AKT1 and HAK1/HAK5 likely include CHX exchange s (Zhao e al., 2008) and cyclic nucleo ide-ga ed channels (CNGC) ha may con ibu e o K+ abso p ion when he ex e nal K+ concen a ion is su icien ly high (Caballe o e al., 2012). Ex e nal [K+] A abidopsis Rice <10μM A HAK5 OsHAK1 10–100μM A HAK5 A KUP7 A AKT1 OsHAK1 OsHAK5 OsAKT1 100–200μM A HAK5 A AKT1 OsHAK1 OsHAK5 OsAKT1 200μM–1mM A AKT1 OsHAK1 OsHAK5 OsAKT1 1–10mM A AKT1 O he sys ems (CHX, CNGC) OsAKT1 Unknown sys ems >10mM O he sys ems (CHX, CNGC) Unknown sys ems Ragel e al. Regula ion o K+ Nu i ion in Plan s F on ie s in Plan Science | www. on ie sin.o g 7 Ma ch 2019 | Volume 10 | A icle 281 GORK phospho yla ion ( an Klee e  al., 2018). On he o he hand, he phospha ase A PP2CA in e ac s physically wi h GORK inhibi ing i s cu en (Le oulon e  al., 2016). Thus, A PP2CA could ha e an an agonis ole o CPK21 on he egula ion o GORK ( an Klee e  al., 2018). These esul s imply ha he salini y-induced memb ane depola iza ion oge he wi h he Ca2+- and CPK21-dependen phospho yla ion ac oge he o ac i a e GORK and o epola ize he plasma memb ane by means o eleasing pa o he cy osolic K+. Mo eo e , he peak o he sal -induced K+-e lux in he aha2 mu an , de oid o a majo iso o m o he plasma memb ane H+-ATPase, was s onge and mo e sus ained han in he wild- ype, sugges ing ha H+-pumps ake o e memb ane epola iza ion a e he ini ial K+-loss o e-enac K+ up ake ( an Klee e  al., 2018). Recen ly, Sapona o e  al. (2017) showed ha 14-3-3 p o eins a e also capable o modula ing KAT1, al hough in his case 14-3-3 bound di ec ly o he KAT1 C- e minus a ec ing bo h he ol age dependency o he channel and he numbe o channel molecules in he memb ane (So oco nola e al., 2008). K+-H+ sympo has long been conside ed he likely ca aly ic mechanism o plan KT/HAK/KUP anspo e s based on he demons a ion ha K+-H+ sympo ope a es in K+-s a ed Neu ospo a c assa and on he modynamical conside a ions ega ding he s eep K+ g adien ha KT/HAK/KUP p o eins a e able o achie e ac oss cell memb anes ha exceeds wha could be eached by coupling he K+ up ake o he memb ane po en ial solely (Rod iguez-Na a o, 2000). Un il ecen ly, e o s o exp ess plan KT/HAK/KUP p o eins in Xenopus oocy es o measu e K+ cu en s had ailed, bu wo k wi h he DmHAK5 anspo e om Venus ly aps showed ha co-exp ession o he co esponding cRNA wi h ha o CBL9/CIPK23 (bu no DmHAK5 alone) gene a ed inwa d K+ and Rb+ cu en s in Xenopus oocy es ha we e s imula ed by low ex e nal pH (Sche ze e al., 2015). Mo eo e , sal bladde s o he halophy e Chenopodium quinoa ha accumula e sal s o e y high concen a ions exp ess a HAK-like ac i i y d i ing high-a ini y and selec i e K+ up ake ha was dependen on acidic ex e nal pH and by he CIPK23/CBL1 kinase module o A abidopsis (Bohm e al., 2018). Elec ophysiological eco dings in ice oo s showed ha he ac i i y o OsHAK1 was s ongly elec ogenic and depola izing. Plo s o he OsHAK1-dependen K+-induced memb ane depola iza ion had a slope o 29 mV pe decade o ex e nal K+ concen a ion, sugges ing he co- anspo o wo mono alen ca ions (a 59 mV slope is o be expec ed om an unip o anspo mo ing only single K+ ions) (Nie es-Co dones e al., 2017). Toge he , hese da a s ongly sugges ha plan KT/ HAK/KUP p o eins ope a e as K+-H+ sympo e s. Residues in ol ed in K+ binding and/o anspo ha e no been iden i ied; howe e , mu an p o eins wi h esidue subs i u ions o membe s o he KT/HAK/KUP amily ha e been desc ibed as showing modi ied a ini y o K+, Na+, and/o Cs+, o inc eased Vmax (Aleman e  al., 2014). HAK1-like anspo e s a e subjec o complex ansc ip ional and pos - ansla ional egula ions, al hough s udies ha e been ca ied ou almos exclusi ely in A abidopsis A HAK5 (Jung e  al., 2009; Rubio e  al., 2014; Ragel e  al., 2015). Unde any s ess condi ions ha di ec ly a ec K+ acquisi ion, such as K+ dep i a ion o salini y, high-a ini y K+ up ake sys ems should be ansc ip ionally o pos - ansla ionally ac i a ed in o de o main ain he K+ supply and K+/Na+ homeos asis. Acco dingly, all cha ac e ized HAK1-like anspo e s exhibi low exp ession le els in oo s unde con ol condi ions, a e highly up- egula ed upon K+ dep i a ion and apidly down- egula ed when K+ is esupplied ( e iewed by (Li e  al., 2018)). Fu he mo e, i has been commonly obse ed ha o he ions, pa icula ly NH4+, NO3−, Na+, and Pi, also egula e he exp ession o HAK1-like genes and no always in he same way (Nie es-Co dones e  al., 2019). Fo example, NH4+ educes he ansc ip ional induc ion by K+ s a a ion o he peppe CaHAK1 (Ma inez-Co de o e  al., 2005) and A abidopsis A HAK5 (Qi e  al., 2008), bu enhances he exp ession o LeHAK5 in oma o (Nie es-Co dones e  al., 2007). The p esence o NaCl p e en s he induc ion o LeHAK5 by K+ s a a ion (Nie es-Co dones e  al., 2007), bu p o okes a s ong and ansien up- egula ion o H HAK1 (Fulgenzi e  al., 2008). Thus, he A abidopsis model canno be comple ely ex ended o o he plan species, c ops among hem. In con as o HAK1-like anspo e s, KT/HAK/KUP p o eins belonging o clus e s II–V show di e se exp ession pa e ns and mos o hem do no exhibi ansc ip ional egula ion in esponse o K+ de iciency (Ahn e  al., 2004; Li e  al., 2018). Fo example, A KUP7 (clus e V, plasma memb ane) ansc ip is no induced by low-K+ (Han e al., 2016) and A KUP12 (clus e III, chlo oplas ) is down- egula ed a e K+ esupply (A mengaud e  al., 2004). Rega ding he ansc ip ional egula ion o genes encoding HAK1-like anspo e s, i has been shown ha he e ec o he nu ien de iciency and sal s esses on ansc ip ional exp ession o A HAK5 and LeHAK5 is associa ed wi h changes in he oo cell memb ane po en ials (Nie es-Co dones e  al., 2008; Rubio e  al., 2014); he hype pola iza ion o he plasma memb ane o oo cells induces ansc ip ion o bo h genes. Suppo ing his, ThHAK5 o Thellungiella halophila (sal c ess, a.k.a. Eu ema salsuginea) is exp essed o highe le els han A HAK5 unde sal s ess, while oo s o T. halophila main ained a mo e nega i e memb ane po en ial han A abidopsis oo s (Volko and Am mann, 2006; Alemán e  al., 2009b; Rubio e al., 2014). Besides memb ane hype pola iza ion, he exp ession o A HAK5 is also induced, unde K+-limi ing condi ions, as esul o signaling cascades ha in ol e ROS p oduc ion, phy oho mones, and ansc ip ion ac o s. Low-K+ s ess, alike o he nu ien -dep i ed condi ions, p omo es an inc ease o e hylene ha posi i ely egula es ROS p oduc ion in oo s (Shin and Schach man, 2004; Jung e  al., 2009). Roo s dep i ed o K+ induce he exp ession o genes in ol ed in e hylene biosyn hesis and signaling, and in ROS me abolism, p omo ing wo- old highe le els o e hylene and he inc ease in hyd ogen pe oxide (H2O2) concen a ions. Bo h e hylene and ROS gi e ise o enhanced ansc ip ion o HAK5 in A abidopsis and oma o (Rodenas e  al., 2018). In A abidopsis, H2O2 p oduced by he NADPH oxidase RHD2/RbohC egula es he exp ession o A HAK5 in esponse o K+ de iciency (Shin and Schach man, 2004) and i has been p oposed ha pe oxidase RCI3 (Ra e Cold Inducible gene 3) con ibu es o ROS p oduc ion du ing A abidopsis oo esponse o K+ de iciency (Kim e  al., 2010). In he case o e hylene-induced A HAK5 ansc ip ion, he in e media ies in e hylene signaling CTR1 (Cons i u i e T iple Ragel e al. Regula ion o K+ Nu i ion in Plan s F on ie s in Plan Science | www. on ie sin.o g 8 Ma ch 2019 | Volume 10 | A icle 281 Response (1) and EIN2 (E hylene Insensi i e (2) a e pa ially in ol ed. Resul s also sugges he exis ence o o he signaling pa hways o an EIN2-independen e hylene ou e ha may play an impo an ole in low-K+ signaling (Jung e al., 2009). Gene ic hie a chy indica es ha e hylene signaling ac s ups eam o ROS when plan s a e dep i ed o K+ (Jung e  al., 2009). Ne e heless, i has also been specula ed ha a posi i e eedback may s imula e e hylene-induced ROS p oduc ion (Wang e al., 2002). O he ho mones ha e been shown o be in ol ed in K+ dep i a ion signaling and esponse, o ins ance jasmonic acid (A mengaud e  al., 2004), auxin (Jung e  al., 2009; Hong e  al., 2013), ABA (Kim e  al., 2010), cy okinins (Nam e  al., 2012), and gibbe ellins h ough DELLA p o eins (Oli e uk e al., 2017). Cy okinins a e known o egula e mac onu ien homeos asis by con olling he exp ession o ni a e, phospha e, and sul a e anspo e s. Cy okinin con en dec eases unde K+-s a ed condi ions, and cy okinin-de icien mu an s, unde same condi ions, display enhanced accumula ion o bo h ROS and A HAK5 ansc ip s (Nam e  al., 2012). By con as , cy okinin- ecep o mu an s los he esponsi eness o low-K+, including ROS accumula ion and oo hai g ow h. In e es ingly, he cy okinin/e hylene a io is posi i ely co ela ed wi h oma o shoo biomass, sugges ing ha he balance be ween bo h ho mones is impo an in de e mining he plan igo a low-K+ supply, bu wi h an in e se ole in oma o compa ed o A abidopsis, whe e cy okinin/e hylene a io was nega i ely co ela ed wi h ole ance o K+ dep i a ion (Jung e  al., 2009; Nam e  al., 2012). In addi ion o low nu ien condi ions, sal s ess (and p esumably o he abio ic s esses) esul s in modi ica ions o A HAK5 exp ession o he low-K+ esponse. Mild sal s ess does no induce A HAK5 exp ession bu i s exp ession le els g adually inc eased ollowing an inc ease in NaCl concen a ions (Ahn e  al., 2004; Hong e al., 2013). This sugges s ha plan s may ecognize high Na+ le els as K+ dep i a ion. Howe e , he induc ion o A HAK5 exp ession by low K+ was supp essed by sal s ess in A abidopsis (Nie es-Co dones e  al., 2010), bu no in T. halophila (Alemán e  al., 2009a). As discussed abo e, unde sal s ess condi ions, T. halophila egis e s a mo e nega i e oo memb ane po en ial han A. haliana (Volko and Am mann, 2006), which may explain he exp ession o ThHAK5 unde hese condi ions (Alemán e  al., 2009a). In ecen yea s, se e al ansc ip ion ac o s (TFs), and hei a ge sequences, ha e been iden i ied in he A HAK5 p omo e . Among hem, ARF2 (Auxin Response Fac o 2) is he only one desc ibed so a o wo k as nega i e egula o o A HAK5 ansc ip ion (Zhao e  al., 2016). In e es ingly, ARF2 has been ound o bein ol ed in many phy oho mone-signaling pa hways, bu i seems no o pa icipa e in auxin signaling. Unde K+- su icien condi ions, channel-media ed K+ up ake would beene ge ically mo e a o able han sympo h ough A HAK5, and hence A HAK5 should be shu down (Zhao e  al., 2016). In hose condi ions, ARF2 binds o he auxin- esponsi e elemen s (AuxREs) wi hin he A HAK5 p omo e and ep esses ansc ip ion. When plan s a e subjec ed o low-K+ s ess, ARF2 is apidly phospho yla ed by an unknown kinase and loses DNA binding ac i i y. ARF2 is emo ed om he A HAK5 p omo e , which elie es he ep ession on A HAK5 ansc ip ion. In u n, o he TFs bind o he A HAK5 p omo e and ac i a e i s ansc ip ion. These TFs up- egula ing A HAK5 exp ession unde K+ s a a ion include RAP2.11, which binds o he e hylene- esponsi e elemen (ERE) and he GCC-box o he A HAK5 p omo e , and whose exp ession is s imula ed by e hylene and ROS, alike A HAK5 (Kim e al., 2012). TFs DDF2, JLO, bHLH121, and TFII_A also in e ac wi h he ups eam egion o A HAK5, bu he speci ic binding mo i o each o hem has no been iden i ied ye (Hong e  al., 2013). All o hese ansc ip ion ac o s a e su icien o ac i a e A HAK5 exp ession in he e ologous sys ems, bu none o hem is absolu ely equi ed. When K+ is esupplied, ARF2 becomes dephospho yla ed again and ep esses A HAK5 exp ession (Zhao e  al., 2016). Thus, i is appa en ha egula ion o he ac i i y o TFs ac ing on A HAK5 ansc ip ion (posi i ely o nega i ely) is necessa y o de e mine coope a i ely he accumula ion o he co esponding ansc ip s (San a-Ma ia e  al., 2018). Al hough a gene al nu ien dep i a ion s imulus is su icien o he ansc ip ional ac i a ion o A HAK5 and LeHAK5 genes, a educ ion o in e nal K+ is equi ed o he induc ion o a unc ional HAK5-media ed high-a ini y K+ up ake in A abidopsis and oma o oo s (Rubio e  al., 2014), sugges ing he exis ence o pos - ansc ip ional egula ion in plan a. Recen ly, i was shown ha ac i a ion o high-a ini y K+ up ake media ed by A HAK5 (Ragel e  al., 2015), DmHAK5 om Venus ly aps (Sche ze e  al., 2015), and CqHAK om quinoa (Bohm e  al., 2018) is media ed by he CBL-in e ac ing p o ein kinase (CIPK)/ calcineu in B-like p o ein (CBL) complex comp ising CIPK23 and CBL1/9 p o eins o A abidopsis. No ably, his CIPK23/CBL1,9 module also ac i a es AKT1 channel, ha oge he wi h A HAK5 cons i u es he main K+ up ake pa hway in A abidopsis oo s (Xu e  al., 2006; Lee e  al., 2007). Bo h he p o ein kinase A CIPK23 and he Ca2+ senso A CBL1 a e necessa y and su icien o ac i a ion o he high-a ini y K+ anspo e A HAK5 in yeas (Ragel e  al., 2015). Besides A CBL1, o he CBLs (A CBL8/9/10) a e able o bind A CIPK23 and ac i a e A HAK5 o complemen K-up ake de ec i e yeas g ow h. The educ ion in he K+ concen a ion p oduces a speci ic Ca2+ signa u e in he cy osol (Figu e 3) (Behe a e  al., 2017) ha would be eco ded by A CBL1, p omo ing CIPK23/CBL1 complex o ma ion, and he ac i a ion o A HAK5 by phospho yla ion a he cy osolic N- e minus (Ragel e  al., 2015), in a simila way ha was desc ibed o AKT1 (Xu e  al., 2006; Lee e  al., 2007). The enhancemen o g ow h a low-K+ o yeas cells co-exp essing A HAK5, A CIPK23, and A CBL1 seems o esul om modi ica ion o he kine ic p ope ies o he anspo e (Km dec ease and Vmax inc ease), likely h ough he phospho yla ion-induced con o ma ional changes o A HAK5 (Ragel e al., 2015). Howe e , since physical in e ac ion be ween CIPK23/CBL1 and A HAK5 is also equi ed o ull ac i a ion o A HAK5in yeas , he a icking o he anspo e o plasma memb ane has been p oposed as a second mechanism o A HAK5 egula ion by CIPK23/CBL1 complex. Suppo ing his idea, he A HAK5 p o ein was mainly de ec ed in he endoplasmic e iculum o K+-su icien plan s, while K+ s a a ion p oduced an en ichmen o A HAK5 p o ein in he plasma memb ane (Qi e  al., 2008). Ragel e al. Regula ion o K+ Nu i ion in Plan s F on ie s in Plan Science | www. on ie sin.o g 9 Ma ch 2019 | Volume 10 | A icle 281 In he e ologous sys ems, he A abidopsis CIPK23/CBL1,9 complex enabled he ac i a ion o a ious membe s om clade Io KT/ HAK/KUP anspo e s, such as peppe CaHAK1 (Ragel e  al., 2015) and Venus ly ap DmHAK5 (Sche ze e  al., 2015), bu no o oma o SlHAK5 o he Eu ema salsuginea EsHAK5 (Ragel e al., 2015). These esul s sugges ed ha he ac i a ion mechanism by CIPK23/CBLs complexes is e olu iona ily conse ed, bu no he phospho yla ion si e and/o he a ge sequence ecogni ion, which may a y among dis an plan species. Acco dingly, a quime ic oma o HAK5 p o ein ha con ained he 15 i s amino acids o CaHAK1 could be ac i a ed by CIPK23/CBL1 in yeas (Ragel e  al., 2015). Since he wo main con ibu o s o K+ up ake in A abidopsis, AKT1 and HAK5, a e egula ed by he CIPK23/CBL1,9 complex, he coo dina ed egula ion o hese anspo sys ems dese es a en ion. Unde K+-su icien condi ions, K+ up ake by HAK5 would beene ge ically mo e expensi e han pe mea ion h ough he AKT1 channel. The H+-pumping ac i i y o plasma memb ane ATPases, which is used o many seconda y anspo p ocesses, c ea es pe se an elec ical cha ge (nega i e inside) ha su ices o d aw signi ican amoun s o K+ in o he cy osol. A a egula s eady memb ane po en ial o −120 o −180mV, oo epide mal cells could sus ain a 100–1,000- old inwa d-di ec ed g adien o K+. Howe e , coupling K+ up ake o H+ in lux no only e u ns H+ o he cy oplasm bu also is mo e depola izing han simple K+ pe mea ion, which in u n imposes a g ea e demand on he H+-pumps and ATP consump ion. We specula e ha unde such condi ions o K+ su iciency, he plasma memb ane is no hype pola ized (o no enough), signaling phy oho mones a e no p oduced, and he e o e ansc ip ion o HAK5 is no ac i a ed. AKT1 would be ope a ional h ough he physical in e ac ion wi h CIPK23 (and possibly o he CIPKs) (Lee e  al., 2007). As he K+ concen a ion ou side dec eases, he unc ion o AKT1 becomes inc easingly hampe ed and ull ac i a ion by he Ca2+- dependen CIPK23/CBL1,9 complex is equi ed o sus ain K+ up ake, while he KC1 sa egua d p e en s K+ leakage h ough AKT1 (Wang e al., 2016). CIPK23 is known o display di e en s a es o ac i a ion, depending on ac o s ha a ec he ac i a ion o CIPKs by ups eam kinases (Ba ajas-Lopez e  al., 2018) and CBL binding (Cha es-Sanjuan e  al., 2014). Thus, a mild K+ dep i a ion may p oduce a pa ially ac i a ed CIPK23 ha would becompe en o ac i a ing AKT1 bu no HAK5, whe eas se e e K+ dep i a ion leads o HAK5 ansc ip ion and o ull ac i a ion o CIPK23, which would hen becompe en o ac i a ing HAK5 (Ragel e al., 2015). The CIPK23 is i sel induced ansc ip ionally by low-K+ s ess (Xu e  al., 2006), which could also enhance he esponse o nu i ional s ess. The pa icipa ion o Ca2+ senso s in high-a ini y K+ up ake could mechanis ically connec K+ s a a ion wi h o he abio ic s esses, o ins ance: salini y, wa e a ailabili y, oxygen de iciency (hypoxia) o absence (anoxia), mechanical s ess, cold s ess, hea y me al s ess, and o he nu ien dep i a ions, all sha ing cy osolic ee Ca2+ as a second messenge (Wilkins e  al., 2016). Cu en hinking is ha he speci ici y o Ca2+ signaling is de e mined by he ampli ude and du a ion (and possible oscilla ion) o he cy osolic Ca2+ inc ease, o en e e ed o as he “calcium signa u e” ha is elici ed by he s imulus. K+ de iciency e okes wo successi e Ca2+ signals in oo s exhibi ing di e en spa ial and empo al speci ici y (Behe a e  al., 2017). The i s one is cha ac e ized by a ansien and as Ca2+ inc ease wi hin 1 min in he pos me is ema ic elonga ion zone (mos p ominen ly in he ascula issue and endode mis), ollowed by a Ca2+ e u n nea ly o basal concen a ions in <7 min. The second wa e (seconda y Ca2+ FIGURE 3 | Regula o y ci cui y egula ing A HAK5 exp ession and ac i i y. K+ s a a ion is p obably sensed as hype pola iza ion o he plasma memb ane, which, oge he wi h ele a ed e hylene and ROS le els, leads o exp ession o he HAK5 gene. Se e al ansc ip ional ac i a o and ep esso ac o s ha e been iden i ied, bu hei placemen in speci ic signaling pa hways is unce ain. Subsequen ly, calmodulin-like (CML) and calcineu in B-like (CBL) Ca2+-binding p o eins ec ui and ac i a e p o ein kinases ILK1 and CIPK23 ha acili a e he a icking o HAK5 o he plasma memb ane and i s biochemical ac i a ion, espec i ely. CIPK23 also s imula es he K+-up ake channel AKT1. K+ eplenishmen depola izes he memb ane and e u ns he sys em o homeos a ic le els. Ragel e al. Regula ion o K+ Nu i ion in Plan s F on ie s in Plan Science | www. on ie sin.o g 16 Ma ch 2019 | Volume 10 | A icle 281 o cen al impo ance o plan nu i ion and dese e addi ional esea ch. The a ailabili y o no el gene ically encoded K+ senso s (Bischo e al., 2017) ha could be a ge ed o a ious cellula compa men s o p ede ined cells and issues will be powe ul ools o moni o he dynamics o cellula K+ wi h unp eceden ed spa io empo al esolu ion. AUTHOR CONTRIBUTIONS All au ho s ha e con ibu ed o li e a u e sea ch, discussion, and w i ing o he manusc ip . PR and JP assembled all sec ions. PR and FQ p epa ed he Figu es. All au ho s checked and app o ed he manusc ip . FUNDING This wo k was suppo ed by g an BIO2015-70946-R o FQ, and by g an s BFU2015-64671-R and BIO2016-81957-REDT om AEI-MINECO (co- inanced by he Eu opean Regional De elopmen Fund), and he SSAC g an PJ01318205 om he Ru al De elopmen Adminis a ion, Republic o Ko ea, o JP. ACKNOWLEDGMENTS We acknowledge suppo o he publica ion ee by he CSIC Open Access Publica ion Suppo Ini ia i e h ough i s Uni o In o ma ion Resou ces o Resea ch (URICI). REFERENCES Ache, P., Becke , D., I ashikina, N., Die ich, P., Roel sema, M. R. G., and Hed ich, R. (2000). GORK, a delayed ou wa d ec i ie exp essed in gua d cells o A abidopsis haliana, is a K+-selec i e, K+-sensing ion channel. FEBS Le . 486, 93–98. doi: 10.1016/S0014-5793(00)02248-1 Ahmad, I., and Maa huis, F. J. (2014). Cellula and issue dis ibu ion o po assium: physiological ele ance, mechanisms and egula ion. J. 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