Root Tropisms: Investigations on Earth and in Space to Unravel Plant Growth Direction

Root Tropisms: Investigations on Earth and in Space to Unravel Plant Growth Direction Lucius Wilhelminus Franciscus Muthert 1 , Luigi Gennaro Izzo 1 *, Martijn van Zanten 2 and Giovanna Aronne 1 1 Department of Agricultural Sciences, University of Naples Federico II, Naples, Italy, 2 Molecular Plant Physiology, Institute of Environmental Biology, Utrecht University, Utrecht, Netherlands Root tropisms are important responses of plants, allowing them to adapt their growth direction. Research on plant tropisms is indispensable for future space programs that envisage plant-based life support systems for long-term missions and planet colonization. Root tropisms encompass responses toward or away from different environmental stimuli, with an underexplored level of mechanistic divergence. Research into signaling events that coordinate tropistic responses is complicated by the consistent coincidence of various environmental stimuli, often interacting via shared signaling mechanisms. On Earth the major determinant of root growth direction is the gravitational vector, acting through gravitropism and overruling most other tropistic responses to environmental stimuli. Critical advancements in the understanding of root tropisms have been achieved nullifying the gravitropic dominance with experiments performed in the microgravity environment. In this review, we summarize current knowledge on root tropisms to different environmental stimuli. We highlight that the term tropism must be used with care, because it can be easily confused with a change in root growth direction due to asymmetrical damage to the root, as can occur in apparent chemotropism, electrotropism, and magnetotropism. Clearly, the use of Arabidopsis thaliana as a model for tropism research contributed much to our understanding of the underlying regulatory processes and signaling events. However, pronounced differences in tropisms exist among species, and we argue that these should be further investigated to get a more comprehensive view of the signaling pathways and sensors. Finally, we point out that the Cholodny-Went theory of asymmetric auxin distribution remains to be the central and unifying tropistic mechanism after 100 years. Nevertheless, it becomes increasingly clear that the theory is not applicable to all root tropistic responses, and we propose further research to unravel commonalities and differences in the molecular and physiological processes orchestrating root tropisms. Keywords: Arabidopsis, Cholodny-Went, directional growth, gravitropism, microgravity Frontiers in Plant Science | www.frontiersin.org February 2020 | Volume 10 | Article 18071 Edited by: Valérie Legué, Université Clermont Auvergne, France Reviewed by: Francisco Javier Medina, Superior Council of Scientific Investigations, Spain John Z. Kiss, University of North Carolina at Greensboro, United States *Correspondence: Luigi Gennaro Izzo [email protected] Specialty section: This article was submitted to Plant Abiotic Stress, a section of the journal Frontiers in Plant Science Received: 22 July 2019 Accepted: 24 December 2019 Published: 21 February 2020 Citation: Muthert LWF, Izzo LG, van Zanten M and Aronne G (2020) Root Tropisms: Investigations on Earth and in Space to Unravel Plant Growth Direction. Front. Plant Sci. 10:1807. doi: 10.3389/fpls.2019.01807 REVIEW published: 21 February 2020 doi: 10.3389/fpls.2019.01807 INTRODUCTION Although plants are sessile organisms, their organs including roots are not motionless. Movements of plant have fascinated scientists for ages (Whippo and Hangarter, 2006). This includes Charles Darwin who laid the foundations for accurate studies on movements of different plant organs in response to external directional stimuli, especially light and gravity (Darwin and Darwin, 1880). One particular type of plant movement are tropistic responses, defined as “a directional growth response to a directional stimulus”(Gilroy, 2008). Tropistic responses are distinguished from nastic responses by being directional relative to the stimulus. Tropisms can be classified as “positive”or “negative”according to the exhibited growth toward or away from the directional stimulus, respectively (Schrank, 1950; Gilroy, 2008). Root tropisms are exerted through differentially-regulated cell growth on opposite sides of the root tip in specific root zones (Gilroy and Masson, 2008). Until the early 2000s the traditional anatomical view identified three main zones in the root tip, directly distal from the root cap: the root apical meristematic zone (MZ), the elongation zone (EZ), and the differentiation zone (DZ), which was based on the premise that cell elongation initiates immediately after the apical meristem (Dolan and Davies, 2004). However, evidence of a distinct cell population in the part of the EZ more distal from the base of the root has been presented in the last three decades. This region was dubbed distal elongation zone (DEZ) initially, and later transition zone (TZ), due to its unique characteristics (Ishikawa and Evans, 1993; Verbelen et al., 2006;Baluška et al., 2010). In the current view, four zones are thus identified, each characterized by specific cell types, cellular activities, and specific responses to tropistic signals (Figure 1,Table 1). The root cap consists of the columella and the lateral root cap surrounding the MZ, a zone of active cell divisions which is followed by the TZ (Figure 1). The cells in the TZ undergo isodiametric cell growth with nuclei located in the center of the cells, similar to the meristem. Following the TZ, cells in the EZ rapidly elongate and nuclei are pushed toward the lateral cell walls due to the formation of large central vacuoles. Cells progressively slow down their elongation and finally reach their mature lengths within the differentiation zone (DZ), which is characterized by root hair development (Figure 1)(Verbelen et al., 2006). In the late nineteenth and early twentieth century, several phenomenological studies on tropisms were conducted. During the final decades of the twentieth century, the focus moved to studies on the molecular mechanisms of root tropisms, enabled by new techniques in molecular genetics and supported in the FIGURE 1 | Schematic representation of a longitudinal cross section of an Arabidopsis root apex, indicating the four distinct developmental zones: the meristematic zone (MZ; pink), the transition zone (TZ; purple), also known as distal elongation zone (DEZ), the elongation zone (EZ; blue), and the differentiation zone (DZ; green). The root cap is indicated in gray and consists of the columella root cap (COL) and the lateral root cap (LRC) that, together with the MZ, surround the quiescent center (QC). Known or suspected sensor and action regions are indicated alongside the root. Tropisms within parentheses are likely not sensu stricto tropisms. BL, blue light; RL, red light. *Specific localization in the cortex of the EZ. **Suspected localizations. Muthert et al. Root Tropisms Frontiers in Plant Science | www.frontiersin.org February 2020 | Volume 10 | Article 18072 first decade of the twenty-first century by special research environments such as the International Space Station (ISS) (Wolverton and Kiss, 2009;Kiss, 2015). Currently, research on plant tropisms becomes critical for advancing plant-based life support systems in space considering their fundamental role in producing fresh food and recycling of air and water (Lasseur et al., 2010). More in-depth knowledge of root growth response to a directional stimulus is required to design plant-based life support facilities able to guide root growth in a desired direction, as the gravity vector is absent in space. At the same time, the possibility of performing explorative experiments in the space environment, together with the development of new technologies, is also crucial to pave the way toward the goal of deepening our fundamental understanding of plant tropisms and their underlying molecular networks on Earth (Borst and van Loon, 2009;Gómez and Izzo, 2018). Many different types of tropisms have been proposed over the years. Of these, gravitropism, phototropism, hydrotropism, halotropism, and thigmotropism are the most extensively studied. Physiological studies from around the turn of the twentieth century also investigated directional growth responses to electrical, chemical, and temperature gradients, among others (Bennett, 1904;Fitting, 1905). Some of these have received renewed attention in the 1990's, the most important of which being chemotropism, magnetotropism, electrotropism, and oxytropism. Whether these can be categorized as bona fide tropisms sensu stricto (i.e., directional growth responses to a directional stimulus (Gilroy, 2008)isin many cases still a matter of debate. However, it is certainly possible that more tropisms are still to be identified, as the recently proposed phonotropism illustrates (Rodrigo-Moreno et al., 2017). In this review, an overview of all known and proposed tropistic responses with a focus on the roots is provided, and current insight into the different types of tropisms and their underlying molecular signaling mechanisms is discussed. GRAVITROPISM Our fundamental understanding of the reliable downward movement of plant roots is based on the Cholodny-Went theory (Cholodny, 1927;Went, 1928;Orbovik and Poff, 1993). Their central premise that a differential localization of auxin causes differential elongation still stands firm (Sato et al., 2015). According to this theory, accumulation of auxin in the root tip on the side closest to the direction of the gravity vector triggers a decrease in cell elongation within the basal zone of the root cap, causing the root to bend in the direction of the gravity vector (Geisler et al., 2014;Krieger et al., 2016). An important elaboration on the Cholodny-Went theory is the auxin fountain model, that proposed how differential auxin levels in the root are established and regulated (Kramer and Bennett, 2006;Grieneisen et al., 2007;Mironova et al., 2012; Geisler et al., 2014). Most of the auxin in plant roots is synthesized in and around the columella cells (Petersson et al., 2009). According to the fountain model, auxin flows upward from these synthesis sites through the epidermis and partially flows back through the cortex, endodermis, and pericycle to the vasculature, where it returns to the root tip. When the root is not positioned in the direction of gravity, the auxin flow toward the basal oriented part is increased, while the flow to the adaxial parts decreases (Geisler et al., 2014;Swarup and Bennett, 2018). After gravitropic bending, not all plant roots are fully oriented in the direction of the gravity vector, but at various angles, based on the developmental stage and environmental circumstances. This fixed growth angle has been called the gravitropic set-point angle (GSA), which is at 0° when the root grows straight downwards (Digby and Firn, 1995). Like in most responses to environmental signals, three distinct phases are typically recognized in the process of gravitropism: perception of the stimulus, signal transmission, and growth response (Toyota and Gilroy, 2013). Sensing of the gravity vector occurs in the columella cells, located in the center of the root cap (Figure 1). There, starch-rich amyloplasts, called statoliths, sediment in aggregates within the cell in response to gravity, due to their high mass (Leitz et al., 2009). The statoliths are free to sediment through the cytoplasm, in part because the nuclei are located at the top of the cells, the vacuoles are small, and because the endoplasmic reticula (ER) lie close to the plasma membrane (Morita and Tasaka, 2004). As plastids, the amyloplasts possess a Translocon at the Outer Envelope Membrane of Chloroplasts (TOC) complex, which TABLE 1 | Root tropism sensor regions, signaling mechanism, and action regions in Arabidopsis thaliana. Tropism Sensor region Signalling Action region Gravitropism primary Columella S1 and S2 [1] CholodnyWent [2] Basal TZ [3] secondary TZ or EZ [4] Likely not C-W [5] Apical TZ [4] Hydrotropism EZ [6] Likely not C-W [7] EZ cortex [6, 3] Phototropism BL neg. Likely EZ or root cap [8, 9, 10] Likely not C-W [11] EZ [10] RL pos. Possibly root cap [12, 13] Unknown EZ [12] BL pos. Unknown Unknown Unknown Halotropism Unknown CholodnyWent [14] Likely EZ* [15, 16] Thigmotropism Strongest in root cap [17] C-W [18] EZ [17] (Electrotropism † ) primary Unknown Unknown TZ [19] secondary Unknown Unknown EZ [19] (Thermotropism † )Unknown Unknown Unknown Oxytropism Unknown Possibly C-W [20] Unknown (Phonotropism † )Unknown I.a. Ca 2+ [21] Unknown *Despite a lack of direct reporting, the action region of halotropism is likely in the EZ, as it is a Cholodny-Went tropism. † Likely not a sensu stricto tropism. [1] (Blancaflor et al., 1998), [2] (Geisler et al., 2014), [3] (Krieger et al., 2016), [4] (Wolverton et al., 2002), [5] (Wolverton et al., 2011), [6] (Dietrich et al., 2017), [7] (Shkolnik et al., 2016), [8] (Sakamoto and Briggs, 2002), [9] (Briggs and Christie, 2002), [10] (Mullen et al., 2002), [11] (Kimura et al., 2018), [12] (Kiss et al., 2003b), [13] (Salisbury et al., 2007), [14] (GalvanAmpudia et al., 2013), [15] (van den Berg et al., 2016), [16] (Yokawa et al., 2014), [17] (Massa and Gilroy, 2003), [18] (Lee et al., 2020), [19] (Wolverton et al., 2000), [20] (Eysholdt-Derzsó and Sauter, 2017), [21] (Rodrigo-Moreno et al., 2017). Muthert et al. Root Tropisms Frontiers in Plant Science | www.frontiersin.org February 2020 | Volume 10 | Article 18073 functions in gravitropism as well (Stanga et al., 2009). Disruption of the central pore protein, TOC75, or one of the receptor proteins, TOC132, strongly enhances the gravitropic deficiency of the altered response to gravity (arg1) mutant. ARG1 and its paralog ARG1-LIKE2 (ARL2) are type-II DnaJ-like peripheral membrane proteins and localize to the plasma membrane and the BFA sensitive endomembrane trafficking pathway (Boonsirichai et al., 2003;Harrison and Masson, 2008). While ARG1 is expressed throughout the whole plant, ARL2 is specifically expressed in the columella cells. Outside of the arg1 mutant background, disruption of TOC132 or TOC75 does not, or only slightly attenuate gravitropism, respectively (Stanga et al., 2009). These findings suggest a role in the early gravitropic signaling for ARG1 and the TOC complex. In accordance with the starch-statolith hypothesis, starchless Arabidopsis thaliana phosphoglucomutase (pgm)mutants displayed strongly reduced gravitropism (Caspar and Pickard, 1989). However, some gravitropic responsiveness remained in the pgm mutants, suggesting that statolith movement alone may not be sufficient to account for all gravity sensing (Caspar and Pickard, 1989;Kiss et al., 1989). There are several theories about how the directional sedimentation of the statoliths affects processes in the cell to alter auxin flows (Strohm et al., 2012;Su et al., 2017). According to Leitz et al. (2009), the sedimentation of statoliths on the cortical ER causes ~200 nm indents, resulting in local expansion of the membrane surface of 15–20%. Mechanosensitive ion channels, particularly those for Ca 2+ , could be activated by this membrane distortion (Hamill and Martinac, 2001). The ER, where the statoliths sediment, is also a major storage compartment for Ca 2+ (Urbina et al., 2006). This could connect the sedimentation of the statoliths to the later biphasic Ca 2+ pulse characteristic of gravitropic signaling (Plieth and Trewavas, 2002). A detailed discussion of Ca 2+ kinetics in gravitropism is summarized in Tatsumi et al. (2014). The protoplast-pressure model is a modification of the ER membrane distortion theory, stating that the pressure of protoplast on the plasma membrane causes mechanosensitive ion channels to open, instead of local pressure exerted by statoliths (Wayne and Staves, 1996;Yoder et al., 2001;Perbal and Driss-Ecole, 2003). Statoliths do however add extra ballast to protoplasts, enabling the application of more pressure on the plasma membrane. Accordingly, 5gacceleration was sufficient to fully restore gravitropism after starchless pgm mutants were exposed to hypergravity conditions during centrifugation (Fitzelle and Kiss, 2001). The alternative ligand-receptor interaction model adds to both the local and protoplast-pressure membrane distortion theories in explaining more directly how secondary messengers are activated. The ligand-receptor interaction model proposes that the contact between a ligand on the membrane of the statoliths and a receptor on the outer membrane of the ER results in the activation of cortical ER ion channels after sedimentation (Strohm et al., 2012). A promising candidate for interaction with this putative ER receptor was the TOC132 receptor protein, extending into the cytosol from the TOC complex on the statolith membrane (Stanga et al., 2009). However, the cytosolic domain of TOC132 turned out not to be necessary for a full gravitropic response (Strohm et al., 2014). Despite indications that the ligand-receptor model holds true for the alga Chara globularis, to the best of our knowledge, no evidence for the ligand-receptor interaction model has been presented in flowering plants so far (Braun, 2002). Recently, the membrane phospholipid phospholipase C2 (PLC2) was shown to influence polar distribution of PIN2 in theearlygravitropicsignalingcascade(Chen et al., 2019). Gravitropic defects of Arabidopsis roots with inhibited PLC activity were previously reported, indicating that PLCs are involved in gravitropism (Andreeva et al., 2010). However, this was possibly due to these seedlings also displaying severe morphological and growth defects. PLC2 is known to produce the common secondary messenger inositol 1,4,5-trisphosphate (InsP 3 ) and 1,2-diacyglycerol (DAG) from the hydrolysis of phosphatidylinositol 4,5-bisphosphate (PtdInsP 2 )(DeWald et al., 2001). InsP 3 is involved in the early stages of gravitropism, before the establishment of the auxin asymmetry (Perera et al., 2006). By generating transgenic lines expressing human type I InsP 5-ptase, which hydrolyses InsP 3 , levels of InsP 3 were reduced by at least 90%. This caused a decrease in establishment of auxin asymmetry, resulting in a slower and 30% decreased gravitropic response compared to wild-type Arabidopsis (Perera et al., 2006). Furthermore, InsP 3 has been shown to influence gene expression in reaction to a gravitropic stimulus (Salinas-Mondragon et al., 2010). Of the downregulated genes, a substantial number is related to plastids and mitochondria. Of the upregulated genes, several are transcription factors and protein kinases linked to Ca 2+ regulation (Salinas-Mondragon et al., 2010). This link between InsP 3 and Ca 2+ is corroborated by the observed close association between the two secondary messengers in both timing and effect in relation to PIN regulation (Zhang J. et al., 2011). However, although an InsP 3 -gated Ca 2+ release channel in the ER membrane has been identified in mammalian cells, no such direct link has yet been found in plants (Zhang S. et al., 2011). Changes in pH are also involved in the early gravitropic signaling. While the root cap apoplast pH decreased from 5.5 to 4.5, the pH of columella cell cytoplasm increased from 7.2 to 7.6 after gravitropic stimulation (Fasano et al., 2001). Preventing the pH increase of columella cytoplasm through the release of caged protons also delayed the onset of gravitropism. Mutants lacking ALTERED RESPONSE TO GRAVITY (ARG1) did not display this pH change in the root cap and show reduced and delayed gravitropism (Boonsirichai et al., 2003). Both ARG1 and plasma membrane H + -ATPases are localized to the plasma membrane and the BFA sensitive endomembrane trafficking pathway, which could be connected to the effect of ARG1 on cytoplasm pH (Boonsirichai et al., 2003). Using the microgravity (µg) environment of the ISS, the involvement of the cytoskeleton in gravitropism has been established. In microgravity, lentil (Lens culinaris) amyloplasts were clustered in the proximal part of the columella cells, which was contrary to the random distribution of amyloplasts in the Muthert et al. Root Tropisms Frontiers in Plant Science | www.frontiersin.org February 2020 | Volume 10 | Article 18074 plants grown on a clinostat; i.e., a rotating device used to simulate a low gravity environment for plant growth (Perbal and Driss-Ecole, 1989). This result indicated involvement of actomyosin in the positioning of amyloplasts, which was later corroborated (DrissEcole et al., 2000). It also showed that the randomization of the gravity vector achieved by the clinostat does not elicit the same effects as the -virtualabsence of the gravity vector in µgconditions (Sievers and Hejnowics, 1992;Hoson et al., 1997). In microgravity conditions, statoliths do not have sedimenting amyloplasts. Thus these cellsalsolackanasymmetrical distributionofauxin in theroot (Ferl and Paul, 2016). Several papers also indicated that actin in the cytoskeleton has a significant role in gravity signaling, as pressure exerted by sedimentation of statoliths on actin polymers could conduct a physical pressure signal toward the plasma membrane or ER membrane, causing ion channels to open (Yoder et al., 2001; Perbal and Driss-Ecole, 2003). Additionally, the ARP3 subunit of the Actin-Related Protein 2/3 (ARP2/3) complex is involved in regulating amyloplast sedimentation kinetics, as Arabidopsis distorted1 (dis1) mutants lacking ARP3 display a delayed response to gravitropic stimulation (Zou et al., 2016). However, the exact role of the cytoskeleton deserves more attention, as pharmacological experiments gave contradictory results, showing both inhibition and promotion of gravitropism (Ma and Hasenstein, 2006;Blancaflor, 2013). A detailed overview of studies of early gravitropic signaling is summarized in Nakamura et al. (2019). Once perceived by the statoliths, the gravitropic signal generates a differential auxin distribution in the root. This process is dependent on the auxin influx carrier AUX1, which is expressed in the root tip and elongation zone (EZ, also known as the central elongation zone) (Marchant, 1999). Interestingly, recent experiments indicated that auxin is not only involved in the regulation of the gravitropic response, but also indirectly in gravitropic perception. Through the TIR1/AFB auxin receptor signaling pathway, auxin regulates the PHOSPHOGLUCOMUTASE (PGM), ADENOSINE DIPHOSPHATE GLUCOSE PYROPHOSPHORYLASE (ADG) and STARCH SYNTHASE 4 (SS4) starch synthesis genes that are responsible for the establishment of statoliths in the cell (Zhang et al., 2019). The change in auxin flow direction in roots that are not orientated toward the gravity vector is mediated by relocation of the PIN-FORMED3 (PIN3) and PIN7 auxin efflux carrier proteins (Friml et al., 2002;Kleine-Vehn et al., 2010). When the root is positioned vertically, these proteins are present at all sides of the columella cells. During gravistimulation, vesicles from endosomal compartments containing these PIN proteins relocate to the then lowest part of the cell, thereby providing increased efflux of auxin at that side, and decreased efflux on the opposite (upward oriented) parts of the cell (Geldner et al., 2001; Friml, 2010). For the relocation of PIN3 in the gravity sensing columella cells, ARG1 and ARL2 are necessary (Harrison and Masson, 2008).The innermost columella cells of the second tier are thought to have the most influence on the redirection of auxin (Blancaflor et al., 1998). Next to roles for PIN3 and PIN7, changes in auxin flux affect the localization and degradation of PIN2 proteins that mediate the basipetal auxin flow. High auxin levels cause PIN2 proteins to be retained longer in the plasma membrane (Paciorek et al., 2005; Abas et al., 2006). Auxin has also been shown to increase proteasomal degradation of PIN2 proteins, suggesting a complex homeostatic mechanism that controls the extension of the polar auxin distribution from the columella cells to the EZ (Abas et al., 2006). Alongside increased auxin, PLC2 is also needed for proper retainment of PIN2 in the plasma membrane (Chen et al., 2019). Additionally, plc2 mutants have reduced auxin content and reduced responsiveness to exogenous auxin. After relocation and degradation of PIN proteins in the root cap, the differential auxin distribution is extended toward the EZ, due to the auxin fountain mechanism (Grieneisen et al., 2007). In the basal part of the transition zone (TZ, also known as the distal elongation zone or DEZ), most of the gravitropic bending takes place in response to the auxin asymmetry (Figure 1)(Krieger et al., 2016). Based on experiments where gravitropism was induced while the root tip was maintained at a constant angle against the gravity vector, Wolverton et al. (2002) proposed that a second gravity sensor could be located in the apical part of the TZ that contributes ~20% to the total gravitropic curvature (Figure 1). This has been called the “dual motors and sensors”theory. During gravistimulation, the electrical properties of the TZ changed markedly, indicating that this alternative gravity sensor could involve electrical signals (Ishikawa and Evans, 1990a;Collings et al., 1992). The presence of a second sensor and motor could also explain why pgm1 mutants retained one third of the rate of wild type gravitropism, without a need for an auxin gradient (Kiss et al., 1996;Wolverton et al., 2011). Ion channel activity of plant cells and their selective retention of charges cause electric currents in their cellular environment, which are altered by increased asymmetric proton efflux during gravitropism (Ishikawa and Evans, 1990a;Baluška and Mancuso, 2013). The electrical current density and orientation differ among different regions of maize (Zea mays) roots, as Collings et al. (1992) have noted. The TZ exhibits an inward oriented current, which is contrary to the outward orientation in the meristem, EZ, and basal end of the elongation zone. A similar pattern has been recorded for cress (Lepidium sativum) (Weisenseel et al., 1992). However, while the role of electrical currents in gravitropism is comparable, differences between species are apparent, as blocking of Ca 2+ channels in maize had no effect on gravitropism, while limiting Ca 2+ availability abolished gravitropism in cress (Collings et al., 1992;Weisenseel et al., 1992). Within minutes after gravistimulation, the electrical current symmetry is disturbed. An increased proton efflux then creates a strong outward current at the upper surface of the horizontal root, near the root tip. In maize, this phenomenon has been observed at 1 to 2.5 mm from the root tip and in cress at 0 to 4 mm from the root tip (Collings et al., 1992;Weisenseel et al., 1992). This location partly corresponds to the location of the TZ. No basipetally propagating wave of proton efflux was detected in maize. Instead, it seemed that the efflux was synchronized in the youngest cells of the EZ, which is around 2.5 mm distal from the Muthert et al. Root Tropisms Frontiers in Plant Science | www.frontiersin.org February 2020 | Volume 10 | Article 18075 root tip in maize (Collings et al., 1992). While this increase in proton efflux in the TZ is linked by both Collings et al. (1992) and Weisenseel et al. (1992) to cell growth by apoplast acidification, the cytoskeletal rearrangements that are required for elongation are almost completely absent in the TZ. Because of this, the zone is also named the transition zone (TZ) instead of the distal elongation zone (Baluška et al., 2010;Baluška and Mancuso, 2013). As there is little elongation in the TZ, the bending in this second gravitropic motor and sensor region likely requires a different mechanism, as proposed by Wolverton et al. (2002). According to Baluška et al. (2010), the progression of cells into and through the TZ is decreased on the lower side and increased on the upper side of a horizontally oriented root. These differences in developmental speed then cause the root to bend at the TZ. Interestingly, the TZ has a peak of so called “brefeldin A (BFA)-induced compartments”that form because the BFA compound blocks endoplasmic reticulum to Golgi apparatus transport upon pharmacological application (Klausner et al., 1992). This peak precisely coincides with the location of TZ bending (Baluška et al., 2010). Since proper PIN2 localization also functions through a BFA-sensitive pathway, PIN2 retention in the TZ could have a critical role in the TZ gravitropic bending response (Abas et al., 2006). In response to the established auxin asymmetry, root growth is altered asymmetrically. It is proposed that a large part of this change is caused by Ca 2+ waves that elicit a change in pH (Monshausen et al., 2011). Within 2 to 6 min after reorientation, the upper flank epidermis experienced a Ca 2+ level reduction and a pH decrease. The lower flank epidermis experiences the reverse, within the same time window (Monshausen and Sievers, 2002;Monshausen et al., 2011). The Ca 2+ level reduction and a pH changes are likely connected to cell wall loosening, allowing for expansion when auxin levels are high (Monshausen et al., 2011). Gravitropic curvature in roots is also partially dependent on a transcriptional response to high auxin, enabled through decreased repression of auxin response factors (ARFs) by AUX/IAA proteins (Su et al., 2017). Reactive oxygen species (ROS) have been shown to accumulate in root tips of gravistimulated maize in response to auxin (Joo et al., 2001). This accumulation was strongly reduced when phosphatidylinositol 3-kinase (PtdIns 3-kinase) activity was blocked, leading to reduced gravitropic reaction of the roots (Joo et al., 2005). A later report specified that the accumulation of ROS was higher at the concave or lower side of the root in the TZ after gravistimulation (Krieger et al., 2016). Other than the involvement of PtdIns 3-kinase and its product, phosphatidylinositol 3-phosphate (PtdIns3P), little is known about the asymmetric ROS gradient generated in response to gravitropically increased auxin levels. Asymmetric increase of nitric oxide (NO) levels, centered around the TZ of the lower root side, is crucial for root gravitropism (París et al., 2018). When NO was reduced by adding a NO scavenger to the medium, cells of gravistimulated roots did not exhibit a PIN2 asymmetry in their plasma membranes. However, growth of Arabidopsis in general was also severely inhibited, prohibiting the drawing of sound conclusions on the specificity of NO effects on root gravitropism (París et al., 2018). Similarly, an asymmetric increase of gibberellic acid (GA) levels is found at the lower side of gravistimulated roots (Löfke et al., 2013). Higher auxin levels at the lower side of the root cause a decrease in cycling of PIN2 to the lytic vacuole in the EZ (Kleine-Vehn et al., 2008). High GA levels seem to influence PIN2 retainment in the plasma membrane in the same way, by preventing PIN protein trafficking to the lytic vacuole (Löfke et al., 2013). The relative contribution to gravitropic bending in the EZ of this GA-mediated PIN2 stabilization, compared to the effects of auxin, has however not been determined yet. Although gravitropism is the most studied tropism in plants, there are still important gaps in the knowledge of the signaling cascade. The sensory mechanism for primary gravitropism is known, but it remains largely elusive how the signal is transduced to InsP 3 and later Ca 2+ signals. Clearly, auxin asymmetry explains large parts of the gravitropic bending in the EZ. The picture is however complicated by the initiation of gravitropic curvature in the TZ. Additionally, the (possible) roles of various other signals, such as Ca 2+ , pH, ROS, NO, and GA levels, which are all to a certain extend altered asymmetrically in the EZ of gravistimulated roots, are poorly understood. Whether and how these signaling pathways connect to auxin signaling, or regulate gravitropic responses via parallel pathways, remains to be elucidated. Finally, as these secondary messengers are not necessarily confined to the columella, they could also constitute hubs for interaction of related tropism signaling pathways (Table 2)(Fasano et al., 2002;Salinas-Mondragon et al., 2010). HYDROTROPISM Water acquisition is an important function of plant roots (Miyazawa et al., 2011). Because water availability in the soil is often spatially and temporally patchy, roots of many species can exert directional root growth toward water; i.e., hydrotropism. Even though hydrotropism has been described as early as 1887 (Von Sachs, 1887), the underlying mechanisms have not yet been fully elucidated (Eapen et al., 2005;Shkolnik and Fromm, 2016). One of the main reasons for this, is that gravitropism is often dominant over hydrotropic responses, making it difficult to study hydrotropism in isolation (Takahashi, 1997). The few reports published on hydrotropism in a natural environment have not observed a directional growth toward water where it was expected (Loomis and Ewan, 1936;Cole and Mahall, 2006). As Takahashi et al. (2009) proposes, this can be due to the balance between the influences of gravity and water being different between species. Hydrotropism has however been observed under lab conditions. Hydrotropism appears not to function according to the Cholodny-Went theory, as no apparent changes in auxin distribution were observed in roots exhibiting hydrotropism (Shkolnik and Fromm, 2016;Shkolnik et al., 2016). Accordingly, pharmacologic application of auxin influx and efflux inhibitors did not affect hydrotropism, while it drastically decreased the root gravitropic responses (Shkolnik Muthert et al. Root Tropisms Frontiers in Plant Science | www.frontiersin.org February 2020 | Volume 10 | Article 18076 et al., 2016). However, application of the auxin antagonists a- (phenylethyl-2-one)-indole-3-acetic (PEO-IAA), auxinole, and the auxin response inhibitor PCIB gave contradicting results (Kaneyasu et al., 2007;Shkolnik et al., 2016). Possibly, components of auxin signaling are thus necessary, although hydrotropism may not depend on the establishment of an auxin gradient for differential growth per se. Also contrary to the Cholodny-Went theory is the likely localization of both a hydrotropic sensor and response area in the EZ of Arabidopsis roots (Figure 1)(Krieger et al., 2016). While de novo gene expression in columella cells is not necessary for hydrotropism, laser ablation of stories 1 and 2 of the columella cells did severely decrease the hydrotropic response (Miyazawa et al., 2008). In contrast, preventing de novo gene expression in TZ cells did suppress hydrotropic curvature (Miyazawa et al., 2008). In a later study, laser ablation of the root meristem and columella cells had however no effect on hydrotropism in Arabidopsis (Dietrich et al., 2017). Possibly, multiple sensory regions for water gradients are present in Arabidopsis with the EZ and TZ seeming prominently involved. Several Arabidopsis mutations have been identified that cause attenuation of the hydrotropic response; no hydrotropic response 1 (nhr1), mizu-kussei 1 (miz1), mizu-kussei 2 (miz2), and altered hydrotropic response 1 (ahr1) (Eapen et al., 2003; Kobayashi et al., 2007;Miyazawa et al., 2009a;Saucedo et al., 2012). The miz1 and miz2 mutants may be specifically disturbed in hydrotropic functioning, as they exhibited a normal response to gravity, and a wild type-like root cap organization. The highly conserved MIZ1 protein is likely located at the cytosolic side of the ER of columella cells and lateral root cap, as well as the TZ, but its molecular function remains unknown (Yamazaki et al., 2012). As miz1 roots show increased levels of auxin, it is thought that MIZ1 has a role in reducing auxin levels (Cassab et al., 2013). This effect of MIZ1 indicates that auxin levels are regulated in hydrotropism, although not asymmetrically (Dietrich, 2018). The miz2 mutation was identified as a weak GNOM mutant allele, involved in facilitating membrane trafficking (Geldner et al., 2003;Miyazawa et al., 2009b). No change in PIN1 localization was observed in miz2 mutants, even though the ADP ribosylation factor guanine-nucleotide exchange factor (ARF-GEF) GNOM functions in the continuous recycling of PIN1 (Geldner et al., 2003;Miyazawa et al., 2009b). It has, therefore, been proposed that the effect of GNOM on hydrotropism may be distinct from its role in auxin distribution (Moriwaki et al., 2014). In contrast to miz1 and miz2, little is known about the ahr1 mutant, which displays no hydrotropism when confronted with a water gradient. The root meristem and EZ length, cell cycle duration, and primary growth of arh1 mutants are not decreased following hydrotropic stimulation, as is the case for the wild type (Salazar-Blas et al., 2017). Upon addition of cytokinins, normal hydrotropic growth was restored in arh1 mutants, indicating a critical role for cytokinins in hydrotropism (Saucedo et al., 2012). Recently, Dietrich et al. (2017) identified a critical role for two subclass III Snf1-related kinases (SnRK2s) in the response of Arabidopsis to hydrotropic stimuli. SnRK2s function upstream of transcription factors in abscisic acid (ABA) phytohormone signaling (Cutler et al., 2010). While high ABA levels decrease root elongation, at low water potential, low ABA levels increase elongation (Rowe et al., 2016). Specifically, SnRK2.2 and SnRK2.3 play critical roles, as the snrk2.2 snrk2.3 double mutant displayed severely inhibited hydrotropism. Strikingly, SnRK2.2 and MIZ1 expression is only needed in the cortex of the TZ and EZ (Dietrich et al., 2017). These results hint to a central role for ABA levels in the elongation and transition zone of the root cortex during hydrotropism, independent from the root meristem. A detailed overview of the components involved in hydrotropism is found in Cassab et al. (2013). Using natural variation in hydrotropic responses among Arabidopsis accessions, Miao et al. (2018) identified H + efflux near the root tip as an indicator for hydrotropism. Increases in H 2 O 2 flux and Ca 2+ influx in the same root region during hydrotropism were only observed in the strongly hydrotropic Wassilewskija (Ws) accession. Transcriptomic analysis indicated an important role for brassinosteroids and epigenetic regulation in hydrotropism in this accession. Indeed, the strong hydrotropic response of Ws was reduced when brassinosteroid perception TABLE 2 | Secondary messengers and phytohormones (potentially) involved in Arabidopsis thaliana root tropisms. With the following abbreviations: inositol 1,4,5-trisphosphate (InsP 3 ), phospholipase Dz2 (PLDz2), phosphatidylinositol 3phosphate (PtdIns3P), and phosphatidic acid (PA). Tropism Secondary messengers Phytohormones Gravitropism primary Ca 2+ [1] , InsP 3[2] , NO [3] ,pH [1] , PLDz2 [4] , PtdIns3P [5] , ROS [6] Auxin [7] , gibberellic acid [8] secondary Unknown Unknown Hydrotropism Ca 2+ [9] , PLDz2 [4] , ROS [6] ABA [10] , auxin? [11, 12] , brassinosteroids [13] , cytokinin [14] , ethylene? [15] Phototropism BL neg. Ca 2+ ? [16] , Flavonoids [17] Cytokinin [18] RL pos. Unknown Unknown BL pos. Unknown Unknown Halotropism Ca 2+ ? [19] , Flavonoids [20] , H 2 O 2 ? [19] , PLDz2 [21] Unknown Thigmotropism Ca 2+ [22] ,pH [22] , ROS [22, 23] Auxin [24] , ethylene [25] (Electrotropism † )Unknown Unknown (Thermotropism † )Unknown Unknown Oxytropism Unknown Auxin? [26] , ethylene [26] (Phonotropism † )Ca 2+ [27] ,K + [27] , superoxide (O 2- ) [27] Unknown † Likely not a sensu stricto tropism. [1] (Monshausen et al., 2011), [2] (Perera et al., 2006), [3] (París et al., 2018), [4] (Taniguchi et al., 2010), [5] (Joo et al., 2005), [6] (Krieger et al., 2016), [7] (Sato et al., 2015), [8] (Löfke et al., 2013), [9] (Takano et al., 1997), [10] (Dietrich et al., 2017), [11] (Shkolnik et al., 2016), [12] (Kaneyasu et al., 2007), [13] (Miao et al., 2018), [14] (Saucedo et al., 2012), [15] (Rowe et al., 2016), [16] (Pedmale et al., 2010), [17] (Silva-Navas et al., 2016), [18] (Silva-Navas et al., 2016), [19] (Shabala et al., 2015), [20] (Petrella et al., 2018), [21] (Galvan-Ampudia et al., 2013), [22] (Monshausen et al., 2009), [23] (Kurusu et al., 2013), [24] (Lee et al., 2020), [25] (Yamamoto et al., 2008), [26] (Eysholdt-Derzsó and Sauter, 2017), [27] (Rodrigo-Moreno et al., 2017). The compounds thought to be involved on the basis of little or only indirect evidence, or with controversy, are followed by a question mark. Muthert et al. Root Tropisms Frontiers in Plant Science | www.frontiersin.org February 2020 | Volume 10 | Article 18077 was partially deficient. Increased activity of brassinosteroidactivated plasma membrane H + -ATPases was likely linked to the increased H+ efflux of Ws during hydrotropism. Although an increase of brassinosteroid levels was assumed from the expression of a brassinosteroid biosynthesis control gene, the actual brassinosteroid levels, as well as the function and localization of H + ,Ca 2+ , and ROS during hydrotropism remains to be investigated. The plasma membrane-associated cation-binding protein 1 (PCaP1) potentially functions as a signaling hub in hydrotropism (Tanaka-Takada et al., 2019). This protein is capable of binding Ca 2+ ,Ca 2+ /calmodulin, and PtdInsP 2 and is usually stably associated with the plasma membrane, despite that the protein lacks a transmembrane domain. During hydrotropism, PCaP1 localization in the EZ shifted to the cytoplasm. While hydrotropic bending is controlled in the EZ cortex, the change in PCaP1 localization is especially apparent in the endodermis (Dietrich et al., 2017). This position, combined with the initial membrane localization and the ability to bind Ca2+, points toward a potential central role in the hydrotropic signal transduction pathway. While it is also able to bind the InsP3 precursor PtdInsP 2 , no role for InsP 3 has been confirmed in hydrotropism. It is also possible that the InsP 3 binding capability represents a link to the gravitropic signaling mechanism, which needs to be suppressed before hydrotropic bending can take place. Our understanding of hydrotropism is not as advanced as that of gravitropism, while significant interaction between the tropisms are apparent (Takahashi, 2003). One of the remaining open questions is how asymmetric signals are formed in the root in response to water patchiness and how these signals are transduced. The natural variation in hydrotropic competence of Arabidopsis accessions provide a valuable resource for hydrotropism research, in addition to the four known hydrotropic mutants (Miao et al., 2018). Additionally, experiments in space allow for the investigation of hydrotropic signaling without the interference from gravitropism. PHOTOTROPISM Plants evolved the ability to sense—and respond to—different characteristics of light, such as quantity, quality, duration (photoperiod), and direction, which is mediated by specialized photoreceptor proteins (Galvão and Fankhauser, 2015). Shoots and/or leaves of many plant species can optimize the amount of energy perceived through directional growth when exposed to non-uniform light conditions; called phototropism (Liscum et al., 2014). Already in the nineteenth century it was recognized that roots of some species grow away from light, while others grow toward the light (Von Sachs, 1868). The first response is known as negative phototropism, the second as positive phototropism. Light conditions perceived in the shoot can also influence root growth and development via e.g., the master photomorphogenesis repressor COP1, influencing root apical meristem proliferation through modulation of PIN1 and PIN2 distribution (Sassi et al., 2012;van Gelderen et al., 2018). Roots can be exposed to light directlyaswell,despite theirundergroundlocalization.Notonlycan light penetrate up to a few centimeters in the upper layers of some soils (Mandoli et al., 1990), the plant itself can also guide light through the stem tothe roots due to the “stem pipe effect”(Mandoli et al., 1984;Lee et al., 2016). Aside from the above-mentioned phenomena, roots can also be exposed to light shortly after germination in the top layer of the soil or because cracks in the soil emerge that trigger a phototropic reaction. The precise evolutionary function of phototropism in roots is still under debate, although an increased root efficiency and enhanced seedling survival under dry conditions have been suggested as fitness benefits to the plant (Galen et al., 2007;Kutschera and Briggs, 2012). Some of the principles and signaling pathways involved in the well-studied shoot phototropism responses also account for root responses to light (Esmon et al., 2005;Briggs, 2014). However, there are also clear differences, as for instance shoots, but not the roots, display distinctly different phototropic reactions to low fluence rate and high fluence rate light exposure (Parks et al., 2001). Moreover, the blue light photoreceptor PHOTOTROPIN2 (PHOT2/NPL1), important for high fluence light shoot phototropism, does not appear to be present in the root (Sakai et al., 2001;Kong et al., 2006). In addition, over 3,000 light-responsive genes are differentially expressed between hypocotyls and roots of Arabidopsis seedlings (Ma et al., 2005). A recent discussion of root and shoot phototropism in response to blue light is provided in Morrow et al. (2018). Roots of many species respond with positive or negative phototropic growth to red and blue light, while others are insensitive. Early studies demonstrated that roots of about half of the tested species (circa 292) did not react to unidirectional white light, while the other half showed negative phototropism, and only a handful of species displayed a positive response (Hubert and Funke, 1937;Kutschera and Briggs, 2012). Most recent work focused on Arabidopsis, which mainly displays a negative blue light root phototropism (Zhang et al., 2013). The difference between plant species could be caused by the absence or presence of a functional phototropic mechanism for a specific part of the light spectrum, by a different light intensity threshold, or by a difference in balance between responses to diverse tropistic stimuli. Roots of individuals of the same species likely react similarly to light stimuli. Still, Kutschera and Briggs (2012) noticed distinct groups of cress reacting with positive, negative or no phototropism. However, these seedlings were grown in hydroculture, which constitutes a potentially detrimental flooding-like condition (Ashraf, 2012;Sauter, 2013). Indeed, Hubert and Funke (1937) had already rearranged their experimental setup after noticing such damaging effects of hydroculture on roots and found no differences in phototropic response of different cress individuals. Some researchers have advocated for interpreting the far more abundant negative tropistic reaction to light as a stress reaction (Yokawa et al., 2014). Negative phototropism combined with increased root growth would then constitute an “escape Muthert et al. Root Tropisms Frontiers in Plant Science | www.frontiersin.org February 2020 | Volume 10 | Article 18078 tropism”(Yokawa et al., 2013). As an increase in ROS is part of several stress responses, the increase of ROS in illuminated roots is seen as an indication that root illumination can be considered a stress condition, justifying the term “escape tropism.”However, ROS is also an important part of gravitropic signaling (Krieger et al., 2016). Therefore, the ROS increase under light could represent regular physiological phototropic signaling rather than a stress indicator. Different light sensors and signaling pathways are in place that mediate blue light and red light phototropisms (BLPT, RLPT) (Goyal et al., 2013). PHOTOTROPIN1 (PHOT1/ NPH1) is a sensor for BLPT in roots and is, in Arabidopsis, predominantly localized in the internal tissues of the EZ (Figure 1)(Liscum and Briggs, 1995;Briggs and Christie, 2002). Upon blue light stimulation of Arabidopsis roots, PHOT1 is autophosphorylated at the plasma membrane and around 20% dissociates from the membrane (Sakamoto and Briggs, 2002; Knieb et al., 2004). In maize, only local root cap illumination is able to achieve white light-induced phototropic curvature in the EZ (Mullen et al., 2002). Therefore, it is possible that the expression pattern of phot1 is different in maize, or there is an unknown link between the root cap and PHOT1 in the EZ. Despite the clear role for phototropins, the BLPT signaling cascade has not been fully elucidated. Following autophosphorylation, PHOT1 binds to PHYTOCHROME KINASE SUBSTRATE 1 (PKS1) together with ROOT PHOTOTROPISM2 (RTP2), a membrane-bound putative scaffolding protein (Inada et al., 2004;Boccalandro et al., 2008). NON-PHOTOTROPIC HYPOCOTYL 3 (NPH3) is dephosphorylated by blue-light-activated PHOT1, which functions as a substrate adapter for a CULLIN3-based E3 ubiquitin ligase (CRL3) (Pedmale and Liscum, 2007;Roberts et al., 2011). Under low-intensity blue light, this CRL3-NPH3 complex monoor multiubiquitinates PHOT1, which could be connected to PHOT1 dissociation from the plasma membrane (Knieb et al., 2004;Roberts et al., 2011). Under high-intensity blue light, PHOT1 is polyubiquitinated, marking it for 26S proteasome-mediated degradation. This likely functions as a mechanism of receptor desensitization (Roberts et al., 2011). One prevalent model connected PHOT1 activation to asymmetrical PIN2 distribution through altered trafficking (Wan et al., 2012). In this model, NPH3 functions as a point of interaction for gravitropic and phototropic signaling, that influences PIN2 distribution. In addition, PIN3 polarization is influenced through a GNOM-dependent trafficking pathway (Zhang et al., 2013). By changing the polarity and symmetrical distributions of PIN2 and PIN3, BLPT could function according to the Cholodny-Went theory, through the generation of auxin asymmetry (Pedmale et al., 2010;Zhang et al., 2014). However, a recent study by Kimura et al. (2018) presented critical notes to this model. An asymmetrical increase in auxin was found on the illuminated side of the root, in agreement with some earlier studies (Zhang et al., 2013;Zhang et al., 2014). However, Kimura et al. (2018) attests that this is a gravitropic reaction following the initial phototropic bending. Due to the BLPT-driven reorientation of the root, gravitropism would be activated, generating auxin asymmetry and opposing phototropic curvature. Inhibition or attenuation of auxin production and transport using pharmacological and genetic experiments was also found to increase BLPT, as it obstructed gravitropism (Kimura et al., 2018). These results suggest that auxin asymmetry may not be necessary, but instead antagonistic for establishing phototropic curvature in the root. One possible mechanism involved in phototropism is the increase of flavonols in the TZ of the illuminated side of the root (Silva-Navas et al., 2016). This establishment of an asymmetric gradient of flavonols (e.g., quercetin and kaempferol) affects auxin signaling, PLETHORA gradient, and superoxide radical content. The resulting reduction of cell proliferation in the illuminated side of the root then causes curvature. Furthermore, cytokinin could be involved through regulation of flavonol biosynthesis, as the cytokinin receptor cre1 ahk1 double mutant displayed reduced BLPT and flavonol accumulation (Silva-Navas et al., 2016). Recently, a previously unknown positive blue-light phototropic response was identified in Arabidopsis in a microgravity environment (Vandenbrink et al., 2016). The response was only detectableatgravitylevelsbelow0.3gandalreadyattenuatedaround 0.1g. In addition, pre-treatment with 1 h of red light enhanced the positive blue light phototropism (Kiss et al., 2012;Vandenbrink et al., 2016). As both the phyA and phyB mutants displayed wild type-like curvature, it is likely that another phytochrome is responsible for this red-light mediated enhancement (Vandenbrink et al., 2016). Candidates include phyD and phyE, being both highly expressed in the root tip, with phyD also being expressed throughout the EZ (Salisbury et al., 2007). In addition to blue light, Arabidopsis roots also respond to unilateral red light with positive tropistic curvature. For this positive red light phototherapy (RLPT) it is also necessary to attenuate gravitropism, either through rotation on a so called “ROTATO”feedback system, that keeps the root tip aligned with the gravity vector based on rotation after image processing and feedback, the use of a mutant (e.g., pgm1) or microgravity conditions (Ruppel et al., 2001;Kiss et al., 2003a;Vandenbrink et al., 2016). Interestingly, positive RLPT has an inverse relationship with the strength of gravity, in contrast to the apparent 0.1–0.3gthreshold for positive BLPT (Vandenbrink et al., 2016). Mutations in phyA and phyB only partially inhibited the RLPT response, indicating a possible additive effect of phyA and phyB in RLPT (Kiss et al., 2003b;Kiss et al., 2012; Vandenbrink et al., 2016). The location of positive red-light phototropic curvature was found to be at the basal edge of the EZ (Figure 1)(Kiss et al., 2003b). PKS1 is one of the few proteins known to be involved in the process (Molas and Kiss, 2008). Under red light exposure PKS1 expression is increased in a phyA-dependent manner (Boccalandro et al., 2008). However, experiments with phyA/B pks1 double mutants indicate that the function of PKS1 in RLPT is separate from both phytochromes. In addition, overexpression of PKS1 led to negative curvature in response to unilateral red light (Molas and Kiss, 2008). Whether or not red-light phototropism functions according to the Cholodny-Went theory and how it interacts with blue light Muthert et al. Root Tropisms Frontiers in Plant Science | www.frontiersin.org February 2020 | Volume 10 | Article 18079 approach could be to target WAVY GROWTH 2 (WAV2),as WAV2 inhibits root tip rotation and thereby enhances linear growth (Mochizuki et al., 2005). This causes wav2 mutants to respond to gravity, light, touch, and hydrotropic stimulation with a larger bending angle than wild type Arabidopsis (Takahashi et al., 2002;Mochizuki et al., 2005). In this framework, although the use of clinostats proved to be informative for certain parameters, findings will have to be validated in true microgravity environments, necessitating space-based research (Sievers and Hejnowics, 1992;Hoson et al., 1997;Kraft et al., 2000). Complicating the investigation of tropisms in a microgravity environment such as the ISS, are the changes in plant growth caused by the absence of gravity, that are not related to gravitropism. These changes have for instance been revealed at the cellular and molecular level in biological systems in which tropisms cannot be defined, such as cultured cells in vitro (Zupanska et al., 2017;Kamal et al., 2018). Apart from changes in fundamental processes such as cell cycle regulation, ribosome biogenesis, and epigenetics, levels of cytokinin were also altered in microgravity (Ferl and Paul, 2016;Kamal et al., 2018). Additional spaceflight experiments have indicated the occurrence of many other substantial gene expression changes, with many differentially regulated genes connected to pathogen defense and cell wall reorganization (Johnson et al., 2017; Zupanska et al., 2019). Part of these transcriptome changes could influence tropistic functioning as well, changing the behaviour of plant roots in response to stimuli in a space environment. A part of the “spaceflight transcriptome”is in fact dependent on the early gravitropic signaling component ARG1 (Zupanska et al., 2017). Moreover, the ARG1 paralog ARL2 is upregulated in gravitropism and downregulated in response to touch, indicating a complex molecular cross talk between microgravity adaptation and tropistic responses. Despite several experiments have been performed on tropism interactions, knowledge about the localization of tropistic effects and the signals involved is far from complete (Tables 1 and 2). At the same time, identifying secondary messengers can lead to possible identification of new gradients able to establish tropistic bending. For example, ROS are implicated in gravitropism, hydrotropism, and thigmotropism, while also able to control the balance between cell proliferation and differentiation (Tsukagoshi et al., 2010). Similarly, flavonols, forming a gradient during negative phototropism, are able to influence auxin signaling, ROS content, and the meristem regulating PLETHORA protein gradient (Galinha et al., 2007;Silva-Navas et al., 2016). In this regard, the accumulated wealth of information from gene expression studies holds a potential for the identification of new, or shared, signaling components which could be pursued (Kimbrough et al., 2004;Salinas-Mondragon et al., 2010;Strohm et al., 2014;Toal et al., 2018). Other important prerequisites include information about the response ranges and their relation to stimulus strength combined with knowledge about the relative strength of tropisms when occurring simultaneously. Especially considering the need for compensation of gravitropism in microgravity conditions, better understanding of the interactions among tropisms is necessary. Literally and figuratively back on Earth, the Cholodny-Went theory of differential auxin distribution still stands firm as the starting point into many investigations of tropisms, as it remains the dominant theory for explaining root tropisms, while nearing its 100-year anniversary. At the same time, however, it becomes increasingly clear that the Cholodny-Went theory is not generally applicable to all root tropism responses to diverse environmental stimuli. Future research therefore will have to refine the theory and further determine commonalities and differences in the molecular and physiological processes orchestrating root tropisms, before efficient translation to microgravity and reduced gravity situations can be made. AUTHOR CONTRIBUTIONS LM, LI, and GA contributed conception and design of the review. LM organized the reference database and wrote the draft of the manuscript. LI, MZ, and GA contributed to manuscript writing and revision. LM and LI designed the figure and tables. All authors read and approved the submitted version and declare no competing interests. REFERENCES Abas, L., Benjamins, R., Malenica, N., Paciorek, T., Wišniewska, J., Moulinier– Anzola, J. C., et al. (2006). 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