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YODA signalling in the early Arabidopsis embryo Thomas J. Musielak* and Martin Bayer*1 *Max Planck Institute for Developmental Biology, Department of Cell Biology, Spemannstrasse 35, 72076 Tubingen, ¨ Germany
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Abstract During early embryogenesis, flowering plants establish their principal body plan starting with an apical–basal axis. An asymmetric division of the zygote gives rise to apical and basal cells with different developmental fates. Besides WOX (WUSCHEL-RELATED HOMEOBOX) transcription factors and the plant hormone auxin, the YDA (YODA)/MAPK (mitogen-activated protein kinase) pathway plays a major role in establishing different cell fates after the first zygotic division. In the present review, we summarize the available data on YDA signalling during embryogenesis. The role of YDA in other developmental processes was taken into account to highlight possible implications for this pathway in the embryo.
Introduction Multicellular organisms form their complex body plan from a single cell. Asymmetric cell divisions are a common way to break symmetry and to create differences in daughter cells that ultimately translate into distinct cell identities [1]. This is especially true during embryogenesis where the principal body plan is formed [2]. In flowering plants, embryogenesis starts with a double fertilization event. The two sperm cells of the pollen fuse with the egg cell and the central cell of the female gametophyte respectively. The fertilized egg cell, or zygote, develops into the embryo, whereas the fertilized central cell forms the nourishing endosperm [3]. In Arabidopsis and other Brassicaceae, embryonic development follows a strict, nearly invariant, pattern of cell divisions, which can be more variable in other flowering plants [4]. Whereas the unfertilized egg cell in Arabidopsis thaliana shows a clear morphological asymmetry, the fertilized zygote undergoes a transient phase where the nucleus is positioned centrally and small vacuoles are dispersed evenly across the cell. This phase of apparent symmetry is broken when the nucleus moves towards the chalazal (apical) end and a large vacuole forms at the micropylar (basal) end of the zygote [2,5,6]. During this period, the zygote elongates approximately 3-fold before it divides asymmetrically into a smaller apical and a larger basal cell. The apical daughter cell is the founder of the spherical pro-embryo, whereas the basal cell divides a limited number of times horizontally to give rise to a rod-shaped structure called the suspensor [7]. The suspensor physically connects the embryo with maternal tissue, pushes the embryo into the surrounding endosperm and is critical for rapid development of the embryo proper, Key words: Arabidopsis thaliana, asymmetric division, embryogenesis, mitogen-activated protein kinase signalling (MAPK signalling), YODA, zygote polarity. Abbreviations: BDL, BODENLOS; bHLH, basic helix–loop–helix; BIN2, BRASSINOSTEROIDINSENSITIVE 2; BR, brassinosteroid; BRI1, BRASSINOSTEROID-INSENSITIVE 1; BSK1, BRASSINOSTEROID SIGNALLING KINASE 1; BSU1, BRI1 SUPPRESSOR 1; EPF, EPIDERMAL PATTERNING FACTOR; ER, ERECTA; ERL, ERECTA-LIKE; GRD, GROUNDED; MAPK, mitogen-activated protein kinase; MKK, MAPK kinase; PIN, PINFORMED; SPCH, SPEECHLESS; SSP, SHORT SUSPENSOR; WOX, WUSCHELRELATED HOMEOBOX; WRKY2, WRKY DNA-BINDING PROTEIN 2; YDA, YODA; YDA-CA, constitutively active YDA. 1 To whom correspondence should be addressed (email [email protected]).
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possibly by serving as conduit for nutrients [8,9]. The suspensor remains mainly extra-embryonic and only partially contributes to the embryonic root with its uppermost cell, the hypophysis [2].
A transcriptional network that establishes apical–basal polarity of the embryo Besides their morphological differences, the apical and basal cell lineages of the first zygotic division also follow distinct genetic programmes. This is highlighted by a subset of transcription factor genes of the WOX (WUSCHELRELATED HOMEOBOX) family [10]. Both WOX2 and WOX8 are initially expressed in the egg cell and the zygote, but WOX2 expression becomes restricted to the apical cell and later to the upper half of the globular embryo, whereas WOX8 transcripts accumulate specifically in suspensor cells after the first zygotic division. Mutant wox2 embryos do not correctly separate the protoderm in the octant embryo and the positioning and formation of the cotyledons is impaired, indicating an important role in specifying apical cell identity. This is corroborated further by a total loss of apical structures in a wox1,wox2,wox3,wox5 quadruple mutant [10,11]. Single mutants of wox8 do not show any obvious embryonic phenotypes, but the double mutant wox8,wox9 displays severe embryonic defects with horizontal instead of vertical divisions in the apical cell lineage and irregular cell division planes or enlarged misshapen cells in the basal lineage [11]. WOX8 and WOX9 seem to act as inductors of WOX2 expression, since the latter is lost in wox8,wox9 mutants, but stronger apical defects in wox8,wox9 than in wox2 suggests additional WOX2-independent functions. Interestingly, neither wox2 nor the wox8,wox9 double mutant show any obvious defects in the zygote, but ectopic expression of WOX2 in a wox8,wox9 background leads to reduced zygote elongation. It is therefore speculated that the balance between the apical lineage regulator WOX2 and the basal lineage regulators WOX8 and WOX9 coordinates the asymmetrical zygotic division [11]. Upstream of WOX8 and possibly WOX9 acts the WRKY2 (WRKY DNA-BINDING PROTEIN 2) transcription factor. wrky2 Biochem. Soc. Trans. (2014) 42, 408–412; doi:10.1042/BST20130230
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mutants show abnormally localized nuclei and vacuoles in late zygotes and atypical symmetric zygotic divisions [12]. However, the asymmetry of the egg cell does not seem to be affected in this background, suggesting that both polarization processes are at least partially independent. In addition to the WRKY2–WOX8/WOX9 transcriptional network, the plant hormone auxin plays a role in the establishment of the apical–basal axis. An early involvement of auxin is indicated by lack of zygote elongation and occasional symmetric zygotic divisions in backgrounds deficient of the ARF (ADP-ribosylation factor)-GEF (guanine-nucleotide-exchange factor) GN (GNOM), which might be explained by disturbed vesicle trafficking of the auxin efflux facilitator PIN1 (PINFORMED 1) [13,14]. Notably, the involvement of auxin in the zygote is rather speculative. More direct evidence is found after the first zygotic division, when auxin is transported upwards to the apical cell by the basally expressed PIN7 [14]. According to this view, auxin accumulates in the apical cells and triggers the degradation of IAA12 (INDOLE-3-ACETIC ACID 12)/BDL (BODENLOS), which acts as a corepressor of ARF5 (AUXIN-RESPONSE FACTOR 5)/MP (MONOPTEROS) [15,16]. Loss-of-function pin7 mutations as well as stabilizing bdl mutations evoke transverse instead of vertical cell divisions in the pro-embryo at the single-cell stage, suggesting a loss of embryonic identity in the apical cell [14,17]. Lack of detectable PIN1 expression in wox8,wox9 double mutants indicates a connection between WOX transcription factors and auxin signalling and transport. As reintroduction of WOX2 in this background restores PIN1 expression and auxin distribution, it was suggested that WOX8 and WOX9 activate WOX2 expression, which in turn serves as an activator of PIN1 [11,18]. The present data suggest an interconnected transcriptional network that establishes apical–basal polarity, but how these factors function together is still far from clear (Figure 1A).
Figure 1 YODA signalling in the early embryo (A) Schematic depiction of the genetic relationship of key genes involved in setting up apical–basal polarity in the embryo. Functions of corresponding proteins indicated are outlined in the text. (B–G) Phenotypic consequences of altered YDA activity. Differential interference contrast images of embryos at the single-cell stage (B–D) and triangular stage (E–G) of wild-type (B and E), yda-1 (C and F), and constitutively active YDA-CA (D and G). Cells of the apical cell lineage are false-coloured in red, cells of the basal lineage are in green. Scale bar, 10 μm.
YODA signalling in the embryo In addition to the above-mentioned players, there is evidence for a further signalling cascade that is involved in apical–basal polarity in the early embryo that is colloquially called YODA pathway after its founding member, the MAPK (mitogenactivated protein kinase) kinase kinase gene YDA (YODA). Loss-of-function mutations in YDA affect zygote elongation and apical–basal polarity of the embryo [19]. YDA was also described for its role in regulating stomata density, but the strong dwarf phenotype of yda loss-of-function alleles indicates an even broader field of duties [19,20]. Recent studies suggest involvement of YDA in as diverse developmental processes as embryogenesis, epidermal patterning, inflorescence architecture and anther development [21–23] (Figure 2). The earliest obvious embryonic defects of yda mutants arise directly after fertilization. In yda mutants, the zygote fails to elongate, resulting in a more or less symmetric cell division. The apical cell is of a similar size to the wild-
type, but the basal cell is much smaller and a large vacuole is often lacking, giving the basal cell the appearance of embryonic cells (Figure 1C). Additionally, yda embryos are occasionally positioned perpendicular to the normal axis of growth [19]. Up to the eight-cell stage, yda embryos undergo a morphologically normal development in the apical cell lineage, but show an irregular development of the basal cells. In some cases, the basal cell remains completely undivided, whereas, in other cases, longitudinal cell divisions are observed (Figure 1F). These cells appear in their morphology often more similar to cells of the embryo proper, and loss of expression of suspensor identity markers supports this notion further [19]. In constitutively active versions of YDA C The
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(YDA-CA), which lack a regulatory domain in the Nterminal region of the protein, the suspensor is longer than in wild-type and often consists of more cells (Figures 1D and 1G). In severe cases, the zygote develops to a file of cells, giving the whole embryo a suspensor-like appearance [19]. Taken together, these phenotypes indicate that YDA signalling is necessary for zygote elongation and subsequently promotes suspensor identity in the basal cells of the early embryo. How YDA influences zygote elongation and establishes suspensor identity is still unclear, owing to the fact that, so far, we only know a handful of genes that are involved in this pathway. Originally, some of the known players were discovered for their role in the leaf epidermal YDA pathway. The MAPKs MPK3 and MPK6 act redundantly downstream of YDA during stomata development, as mpk6 single as well as mpk3,mpk6 double mutants show increased stomatal density and clusters of stomata on the leaf surface [24]. In addition, mpk3,mpk6 double mutants also show an embryonic phenotype similar to yda loss-of-function, demonstrating that these MAPKs are also participating in the embryonic YDA pathway. Double mutants of MKK4 (MAPK KINASE 4) and MKK5 show similar epidermal defects to those of mpk3,mpk6 mutants, and genetic evidence places these genes redundantly downstream of YDA and upstream of MPK3/MPK6 [24]. Although it has not been published explicitly for the embryo, it seems plausible that these MAPKs also work together with YDA in the embryonic pathway. MKK7 and MKK9 also function together with YDA during leaf epidermal patterning, but whether they play a role in the embryo has not been addressed [25]. Taken together, the YDA–MAPK module in the embryo seems to consist at least of YDA, MKK4/MKK5 and MPK3/MPK6, but which proteins are phosphorylated by these kinases is unknown, since no direct targets of the YDA pathway in the embryo have been identified so far. The RWP-RK transcription factor GRD (GROUNDED) seems to act downstream of YDA in a common pathway as was shown by genetic studies [26,27]. grd mutants resemble yda mutants in the aspects of zygote elongation and impaired suspensor formation. Furthermore, genetic markers for suspensor identity (WOX8 and SUC3) are lost or reduced in their expression as in yda, whereas embryonic markers (ZWILLE) expand in their expression [26]. YDA-CA does not suppress the effect of grd mutations, which indicates that GRD is necessary for YDA function and tentatively suggests that it acts downstream in a common pathway. However, transcription of GRD is independent of YDA and it is not a direct target of the YDA/MAPK cascade [26]. Ectopic overexpression of GRD in seedlings induces the expression of early-embryo-specific genes, leading to the formation of embryo-like structures [27]. This strongly suggests that GRD confers embryonic cell identity, but how it works together with YDA is not clear. GRD shows strong synergistic interaction with WOX8/9. In a wox8,wox9 + / − ,grd triple mutant, approximately 50% of the embryos arrest at the two- to four-cell stage, whereas the rest display a grd-like phenotype. The arrest phenotype C The
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is more frequent than in the grd single or the wox8,wox9 double mutants alone, suggesting that these transcription factors possibly act in a co-operative manner [26]. However, how the WOX transcription factors and the YDA pathway establish apical–basal polarity in the embryo remains unclear. Whereas downstream targets of the YDA pathway in the embryo are so far unknown, the membraneassociated receptor-like cytoplasmic kinase SSP (SHORT SUSPENSOR) has been reported to act upstream of YDA [28]. Loss-of-function ssp mutants exhibit similar, but weaker, embryonic phenotypes as yda, indicating the possible existence of further redundant components of the YDA pathway. As hyperactive YDA variants (YDA-CA) can complement the ssp loss-of-function phenotype, it is assumed that it works genetically upstream of YDA. As in yda and grd, the expression of genetic markers for basal cell identity is down-regulated or partially lost in suspensor cells of ssp mutant embryos [26,28]. Although SSP is normally not expressed there, its ectopic expression in leaves results in an epidermis entirely consisting of pavement cells, reminiscent of the YDA-CA phenotype. This effect depends on functional YDA and SSP protein, suggesting that SSP is capable of activating the YDA pathway and that upstream components of the YDA pathway are somewhat conserved between the embryo and leaf [28]. For proper function, SSP needs to be membrane-localized by N-terminal myristoylation and palmitoylation. Besides this, a C-terminal tetratricopeptide domain, a protein–protein interaction motif, seems to be essential for SSP function. Interestingly, the kinase domain of SSP lacks several canonical residues, and mutations that generally abolish kinase activity have no effect on SSP function [28]. SSP is therefore considered to be a pseudokinase, although biochemical experiments have not yet been reported. Nonetheless, the presence of the kinase domain is necessary, and larger deletions in this domain are not tolerated. Hence it is conceivable that SSP acts as a scaffold or interaction platform. Since the interaction partners of SSP are unknown, our understanding of how SSP participates in YDA activation is very limited.
YDA activation by an unusual parent-of-origin effect The SSP expression pattern suggests an interesting mechanism of YDA activation in the zygote. Although SSP is solely transcribed in sperm cells and its transcripts appear to accumulate there at high levels, no SSP protein could be detected in pollen [28,29]. After fertilization, an SSP protein fusion to YFP can be detected transiently in the membrane of the zygote. Allele-specific reverse transcription–PCR identifies only paternally derived SSP transcripts in ovules at this stage [28]. This strongly suggests that paternally inherited SSP transcripts are translated after fertilization in the zygote, whereas their precocious translation in sperm cells is suppressed before fertilization. How this is achieved and how this repression is released in the zygote is yet unclear. Similarly to the artificial situation in leaves where
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Figure 2 Schematic depiction of the architecture of YDA signalling pathways involved in different developmental processes including a basic outline of the BRI1 signalling pathway to highlight signalling cross-talk During embryo, epidermis and inflorescence development, the different YDA signalling pathways contain common and context-specific components. Downstream transcription factors are depicted in the nucleus. To reduce complexity, only a selection of signalling components is shown. Their functional description is given in the text. BAK1, BRI1-ASSOCIATED RECEPTOR KINASE 1; BZR, BRASSINAZOLE-RESISTANT; EPFL, EPF-LIKE; TMM, TOO MANY MOUTHS.
the presence of SSP leads to YDA activity, the transient SSP accumulation in the zygote might lead to YDA activation, serving as a temporal cue to synchronize YDA activity with the fertilization event.
YDA signalling during stomata development In the leaf epidermis, the YDA pathway acts as a negative regulator of stomata development [30]. It controls the entry division that initiates stomata development by MPK3/MPK6dependent phosphorylation of the bHLH (basic helix– loop–helix) transcription factor SPCH (SPEECHLESS) [31] (Figure 2). Furthermore, it restricts the developmental progression of meristemoids to guard mother cells, possibly by regulating the activity of the bHLH transcription factor MUTE, although MUTE does not appear to be a direct MAPK target on the basis of in vitro data [25]. Genetic data suggest that the epidermal YDA pathway includes a cascade consisting of YDA and MKK4/MKK5, as well as MKK7/MKK9 and MPK3/MPK6 [20,24,25]. This module is activated by leucine-rich receptor-like kinases of the ER (ERECTA) family, including ER, ERL1 (ERECTA-LIKE1) and ERL2 which perceive extracellular small cysteine-rich peptides of the EPF-like family including
EPF1 (EPIDERMAL PATTERNING FACTOR 1) and EPF2 [32,33]. By inhibiting SPCH activity, the YDA pathway promotes pavement cell identity. yda loss-offunction mutants show clusters of stomata whereas YDA-CA variants evoke leaves that entirely lack stomata [20].
Signalling cross-talk It has been shown recently that YDA activity in the leaf epidermis can be influenced by components of the BR (brassinosteroid) signalling pathway, suggesting cross-talk between these two signalling cascades [34] (Figure 2). On the basis of current evidence, BIN2 (BRASSINOSTEROIDINSENSITIVE 2) seems to be the main connection between these two pathways, since it can directly phosphorylate and negatively regulate the activity of YDA, MKK4 and MKK5, as well as SPCH [35–37]. This cross-talk between BR and YDA signalling suggests an intriguing signalling mechanism that might explain how SSP can activate YDA. SSP evolved as a paralogue of the BSK1 (BRASSINOSTEROID SIGNALLING KINASE 1) gene in the last whole-genome duplication of the Brassicaceae [38]. As the name indicates, BSK1 is a signalling component of the BRI1 (BRASSINOSTEROID-INSENSITIVE 1) receptor pathway [39]. Upon perception of brassinolid, BSK1 is phosphorylated by the leucine-rich repeat receptor-like kinase BRI1 and recruits the Kelch-repeat containing phosphatases BSU1 (BRI1 SUPPRESSOR 1) and members of the BSL (BSU1LIKE) family [39,40]. These can dephosphorylate and therefore negatively regulate the activity of the GSK3 (glycogen synthase kinase 3)-like kinase BIN2 [40]. In the context of the BR–YDA cross-talk, BSK1 phosphorylation would lead to reduced activity of BIN2 and therefore increased activity of YDA. Since SSP is a paralogue of BSK1, it is tempting to speculate whether YDA activation by SSP possibly includes a similar mechanism involving BIN2. This would mean that SSP hijacked this connection between BR and YDA signalling and could be a late addition to an already pre-existing more ancient YDA pathway. With the architecture of YDA signalling pathways in other developmental contexts in mind, it is intuitive to speculate about so far undiscovered receptor-like kinases in the embryo acting upstream of YDA and possibly independently of SSP. If these indeed exist, what extracellular signal they might perceive and from which tissue their ligands could originate is unfortunately speculative at this moment.
Conclusion Besides auxin and a transcriptional network including WRKY2, WOX2, WOX8 and WOX9, the YDA/MAPK signalling pathway acts as a key regulator to specify apical– basal polarity in the early embryo. At the moment, our knowledge of the inner workings of this pathway is still rather cryptic, and further work is needed to understand how YDA C The
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is activated and how this translates into apical–basal polarity of the embryo.
Acknowledgements We apologize to our colleagues whose work we could not present here and thank Steffen Lau for a critical reading of the paper before submission.
Funding Work in our laboratory is funded by the German Research Foundation (Deutsche Forschungsgemeinschaft) [grant number BA 3356/2-1] and the Max Planck Society.
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Biochemical Society Transactions (2014) Volume 42, part 2
YODA signalling in the early Arabidopsis embryo Thomas J. Musielak* and Martin Bayer*1 *Max Planck Institute for Developmental Biology, Department of Cell Biology, Spemannstrasse 35, 72076 Tubingen, ¨ Germany
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Abstract During early embryogenesis, flowering plants establish their principal body plan starting with an apical–basal axis. An asymmetric division of the zygote gives rise to apical and basal cells with different developmental fates. Besides WOX (WUSCHEL-RELATED HOMEOBOX) transcription factors and the plant hormone auxin, the YDA (YODA)/MAPK (mitogen-activated protein kinase) pathway plays a major role in establishing different cell fates after the first zygotic division. In the present review, we summarize the available data on YDA signalling during embryogenesis. The role of YDA in other developmental processes was taken into account to highlight possible implications for this pathway in the embryo.
Introduction Multicellular organisms form their complex body plan from a single cell. Asymmetric cell divisions are a common way to break symmetry and to create differences in daughter cells that ultimately translate into distinct cell identities [1]. This is especially true during embryogenesis where the principal body plan is formed [2]. In flowering plants, embryogenesis starts with a double fertilization event. The two sperm cells of the pollen fuse with the egg cell and the central cell of the female gametophyte respectively. The fertilized egg cell, or zygote, develops into the embryo, whereas the fertilized central cell forms the nourishing endosperm [3]. In Arabidopsis and other Brassicaceae, embryonic development follows a strict, nearly invariant, pattern of cell divisions, which can be more variable in other flowering plants [4]. Whereas the unfertilized egg cell in Arabidopsis thaliana shows a clear morphological asymmetry, the fertilized zygote undergoes a transient phase where the nucleus is positioned centrally and small vacuoles are dispersed evenly across the cell. This phase of apparent symmetry is broken when the nucleus moves towards the chalazal (apical) end and a large vacuole forms at the micropylar (basal) end of the zygote [2,5,6]. During this period, the zygote elongates approximately 3-fold before it divides asymmetrically into a smaller apical and a larger basal cell. The apical daughter cell is the founder of the spherical pro-embryo, whereas the basal cell divides a limited number of times horizontally to give rise to a rod-shaped structure called the suspensor [7]. The suspensor physically connects the embryo with maternal tissue, pushes the embryo into the surrounding endosperm and is critical for rapid development of the embryo proper, Key words: Arabidopsis thaliana, asymmetric division, embryogenesis, mitogen-activated protein kinase signalling (MAPK signalling), YODA, zygote polarity. Abbreviations: BDL, BODENLOS; bHLH, basic helix–loop–helix; BIN2, BRASSINOSTEROIDINSENSITIVE 2; BR, brassinosteroid; BRI1, BRASSINOSTEROID-INSENSITIVE 1; BSK1, BRASSINOSTEROID SIGNALLING KINASE 1; BSU1, BRI1 SUPPRESSOR 1; EPF, EPIDERMAL PATTERNING FACTOR; ER, ERECTA; ERL, ERECTA-LIKE; GRD, GROUNDED; MAPK, mitogen-activated protein kinase; MKK, MAPK kinase; PIN, PINFORMED; SPCH, SPEECHLESS; SSP, SHORT SUSPENSOR; WOX, WUSCHELRELATED HOMEOBOX; WRKY2, WRKY DNA-BINDING PROTEIN 2; YDA, YODA; YDA-CA, constitutively active YDA. 1 To whom correspondence should be addressed (email [email protected]).
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possibly by serving as conduit for nutrients [8,9]. The suspensor remains mainly extra-embryonic and only partially contributes to the embryonic root with its uppermost cell, the hypophysis [2].
A transcriptional network that establishes apical–basal polarity of the embryo Besides their morphological differences, the apical and basal cell lineages of the first zygotic division also follow distinct genetic programmes. This is highlighted by a subset of transcription factor genes of the WOX (WUSCHELRELATED HOMEOBOX) family [10]. Both WOX2 and WOX8 are initially expressed in the egg cell and the zygote, but WOX2 expression becomes restricted to the apical cell and later to the upper half of the globular embryo, whereas WOX8 transcripts accumulate specifically in suspensor cells after the first zygotic division. Mutant wox2 embryos do not correctly separate the protoderm in the octant embryo and the positioning and formation of the cotyledons is impaired, indicating an important role in specifying apical cell identity. This is corroborated further by a total loss of apical structures in a wox1,wox2,wox3,wox5 quadruple mutant [10,11]. Single mutants of wox8 do not show any obvious embryonic phenotypes, but the double mutant wox8,wox9 displays severe embryonic defects with horizontal instead of vertical divisions in the apical cell lineage and irregular cell division planes or enlarged misshapen cells in the basal lineage [11]. WOX8 and WOX9 seem to act as inductors of WOX2 expression, since the latter is lost in wox8,wox9 mutants, but stronger apical defects in wox8,wox9 than in wox2 suggests additional WOX2-independent functions. Interestingly, neither wox2 nor the wox8,wox9 double mutant show any obvious defects in the zygote, but ectopic expression of WOX2 in a wox8,wox9 background leads to reduced zygote elongation. It is therefore speculated that the balance between the apical lineage regulator WOX2 and the basal lineage regulators WOX8 and WOX9 coordinates the asymmetrical zygotic division [11]. Upstream of WOX8 and possibly WOX9 acts the WRKY2 (WRKY DNA-BINDING PROTEIN 2) transcription factor. wrky2 Biochem. Soc. Trans. (2014) 42, 408–412; doi:10.1042/BST20130230
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mutants show abnormally localized nuclei and vacuoles in late zygotes and atypical symmetric zygotic divisions [12]. However, the asymmetry of the egg cell does not seem to be affected in this background, suggesting that both polarization processes are at least partially independent. In addition to the WRKY2–WOX8/WOX9 transcriptional network, the plant hormone auxin plays a role in the establishment of the apical–basal axis. An early involvement of auxin is indicated by lack of zygote elongation and occasional symmetric zygotic divisions in backgrounds deficient of the ARF (ADP-ribosylation factor)-GEF (guanine-nucleotide-exchange factor) GN (GNOM), which might be explained by disturbed vesicle trafficking of the auxin efflux facilitator PIN1 (PINFORMED 1) [13,14]. Notably, the involvement of auxin in the zygote is rather speculative. More direct evidence is found after the first zygotic division, when auxin is transported upwards to the apical cell by the basally expressed PIN7 [14]. According to this view, auxin accumulates in the apical cells and triggers the degradation of IAA12 (INDOLE-3-ACETIC ACID 12)/BDL (BODENLOS), which acts as a corepressor of ARF5 (AUXIN-RESPONSE FACTOR 5)/MP (MONOPTEROS) [15,16]. Loss-of-function pin7 mutations as well as stabilizing bdl mutations evoke transverse instead of vertical cell divisions in the pro-embryo at the single-cell stage, suggesting a loss of embryonic identity in the apical cell [14,17]. Lack of detectable PIN1 expression in wox8,wox9 double mutants indicates a connection between WOX transcription factors and auxin signalling and transport. As reintroduction of WOX2 in this background restores PIN1 expression and auxin distribution, it was suggested that WOX8 and WOX9 activate WOX2 expression, which in turn serves as an activator of PIN1 [11,18]. The present data suggest an interconnected transcriptional network that establishes apical–basal polarity, but how these factors function together is still far from clear (Figure 1A).
Figure 1 YODA signalling in the early embryo (A) Schematic depiction of the genetic relationship of key genes involved in setting up apical–basal polarity in the embryo. Functions of corresponding proteins indicated are outlined in the text. (B–G) Phenotypic consequences of altered YDA activity. Differential interference contrast images of embryos at the single-cell stage (B–D) and triangular stage (E–G) of wild-type (B and E), yda-1 (C and F), and constitutively active YDA-CA (D and G). Cells of the apical cell lineage are false-coloured in red, cells of the basal lineage are in green. Scale bar, 10 μm.
YODA signalling in the embryo In addition to the above-mentioned players, there is evidence for a further signalling cascade that is involved in apical–basal polarity in the early embryo that is colloquially called YODA pathway after its founding member, the MAPK (mitogenactivated protein kinase) kinase kinase gene YDA (YODA). Loss-of-function mutations in YDA affect zygote elongation and apical–basal polarity of the embryo [19]. YDA was also described for its role in regulating stomata density, but the strong dwarf phenotype of yda loss-of-function alleles indicates an even broader field of duties [19,20]. Recent studies suggest involvement of YDA in as diverse developmental processes as embryogenesis, epidermal patterning, inflorescence architecture and anther development [21–23] (Figure 2). The earliest obvious embryonic defects of yda mutants arise directly after fertilization. In yda mutants, the zygote fails to elongate, resulting in a more or less symmetric cell division. The apical cell is of a similar size to the wild-
type, but the basal cell is much smaller and a large vacuole is often lacking, giving the basal cell the appearance of embryonic cells (Figure 1C). Additionally, yda embryos are occasionally positioned perpendicular to the normal axis of growth [19]. Up to the eight-cell stage, yda embryos undergo a morphologically normal development in the apical cell lineage, but show an irregular development of the basal cells. In some cases, the basal cell remains completely undivided, whereas, in other cases, longitudinal cell divisions are observed (Figure 1F). These cells appear in their morphology often more similar to cells of the embryo proper, and loss of expression of suspensor identity markers supports this notion further [19]. In constitutively active versions of YDA C The
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(YDA-CA), which lack a regulatory domain in the Nterminal region of the protein, the suspensor is longer than in wild-type and often consists of more cells (Figures 1D and 1G). In severe cases, the zygote develops to a file of cells, giving the whole embryo a suspensor-like appearance [19]. Taken together, these phenotypes indicate that YDA signalling is necessary for zygote elongation and subsequently promotes suspensor identity in the basal cells of the early embryo. How YDA influences zygote elongation and establishes suspensor identity is still unclear, owing to the fact that, so far, we only know a handful of genes that are involved in this pathway. Originally, some of the known players were discovered for their role in the leaf epidermal YDA pathway. The MAPKs MPK3 and MPK6 act redundantly downstream of YDA during stomata development, as mpk6 single as well as mpk3,mpk6 double mutants show increased stomatal density and clusters of stomata on the leaf surface [24]. In addition, mpk3,mpk6 double mutants also show an embryonic phenotype similar to yda loss-of-function, demonstrating that these MAPKs are also participating in the embryonic YDA pathway. Double mutants of MKK4 (MAPK KINASE 4) and MKK5 show similar epidermal defects to those of mpk3,mpk6 mutants, and genetic evidence places these genes redundantly downstream of YDA and upstream of MPK3/MPK6 [24]. Although it has not been published explicitly for the embryo, it seems plausible that these MAPKs also work together with YDA in the embryonic pathway. MKK7 and MKK9 also function together with YDA during leaf epidermal patterning, but whether they play a role in the embryo has not been addressed [25]. Taken together, the YDA–MAPK module in the embryo seems to consist at least of YDA, MKK4/MKK5 and MPK3/MPK6, but which proteins are phosphorylated by these kinases is unknown, since no direct targets of the YDA pathway in the embryo have been identified so far. The RWP-RK transcription factor GRD (GROUNDED) seems to act downstream of YDA in a common pathway as was shown by genetic studies [26,27]. grd mutants resemble yda mutants in the aspects of zygote elongation and impaired suspensor formation. Furthermore, genetic markers for suspensor identity (WOX8 and SUC3) are lost or reduced in their expression as in yda, whereas embryonic markers (ZWILLE) expand in their expression [26]. YDA-CA does not suppress the effect of grd mutations, which indicates that GRD is necessary for YDA function and tentatively suggests that it acts downstream in a common pathway. However, transcription of GRD is independent of YDA and it is not a direct target of the YDA/MAPK cascade [26]. Ectopic overexpression of GRD in seedlings induces the expression of early-embryo-specific genes, leading to the formation of embryo-like structures [27]. This strongly suggests that GRD confers embryonic cell identity, but how it works together with YDA is not clear. GRD shows strong synergistic interaction with WOX8/9. In a wox8,wox9 + / − ,grd triple mutant, approximately 50% of the embryos arrest at the two- to four-cell stage, whereas the rest display a grd-like phenotype. The arrest phenotype C The
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is more frequent than in the grd single or the wox8,wox9 double mutants alone, suggesting that these transcription factors possibly act in a co-operative manner [26]. However, how the WOX transcription factors and the YDA pathway establish apical–basal polarity in the embryo remains unclear. Whereas downstream targets of the YDA pathway in the embryo are so far unknown, the membraneassociated receptor-like cytoplasmic kinase SSP (SHORT SUSPENSOR) has been reported to act upstream of YDA [28]. Loss-of-function ssp mutants exhibit similar, but weaker, embryonic phenotypes as yda, indicating the possible existence of further redundant components of the YDA pathway. As hyperactive YDA variants (YDA-CA) can complement the ssp loss-of-function phenotype, it is assumed that it works genetically upstream of YDA. As in yda and grd, the expression of genetic markers for basal cell identity is down-regulated or partially lost in suspensor cells of ssp mutant embryos [26,28]. Although SSP is normally not expressed there, its ectopic expression in leaves results in an epidermis entirely consisting of pavement cells, reminiscent of the YDA-CA phenotype. This effect depends on functional YDA and SSP protein, suggesting that SSP is capable of activating the YDA pathway and that upstream components of the YDA pathway are somewhat conserved between the embryo and leaf [28]. For proper function, SSP needs to be membrane-localized by N-terminal myristoylation and palmitoylation. Besides this, a C-terminal tetratricopeptide domain, a protein–protein interaction motif, seems to be essential for SSP function. Interestingly, the kinase domain of SSP lacks several canonical residues, and mutations that generally abolish kinase activity have no effect on SSP function [28]. SSP is therefore considered to be a pseudokinase, although biochemical experiments have not yet been reported. Nonetheless, the presence of the kinase domain is necessary, and larger deletions in this domain are not tolerated. Hence it is conceivable that SSP acts as a scaffold or interaction platform. Since the interaction partners of SSP are unknown, our understanding of how SSP participates in YDA activation is very limited.
YDA activation by an unusual parent-of-origin effect The SSP expression pattern suggests an interesting mechanism of YDA activation in the zygote. Although SSP is solely transcribed in sperm cells and its transcripts appear to accumulate there at high levels, no SSP protein could be detected in pollen [28,29]. After fertilization, an SSP protein fusion to YFP can be detected transiently in the membrane of the zygote. Allele-specific reverse transcription–PCR identifies only paternally derived SSP transcripts in ovules at this stage [28]. This strongly suggests that paternally inherited SSP transcripts are translated after fertilization in the zygote, whereas their precocious translation in sperm cells is suppressed before fertilization. How this is achieved and how this repression is released in the zygote is yet unclear. Similarly to the artificial situation in leaves where
Regulation of Fertilization and Early Seed Development
Figure 2 Schematic depiction of the architecture of YDA signalling pathways involved in different developmental processes including a basic outline of the BRI1 signalling pathway to highlight signalling cross-talk During embryo, epidermis and inflorescence development, the different YDA signalling pathways contain common and context-specific components. Downstream transcription factors are depicted in the nucleus. To reduce complexity, only a selection of signalling components is shown. Their functional description is given in the text. BAK1, BRI1-ASSOCIATED RECEPTOR KINASE 1; BZR, BRASSINAZOLE-RESISTANT; EPFL, EPF-LIKE; TMM, TOO MANY MOUTHS.
the presence of SSP leads to YDA activity, the transient SSP accumulation in the zygote might lead to YDA activation, serving as a temporal cue to synchronize YDA activity with the fertilization event.
YDA signalling during stomata development In the leaf epidermis, the YDA pathway acts as a negative regulator of stomata development [30]. It controls the entry division that initiates stomata development by MPK3/MPK6dependent phosphorylation of the bHLH (basic helix– loop–helix) transcription factor SPCH (SPEECHLESS) [31] (Figure 2). Furthermore, it restricts the developmental progression of meristemoids to guard mother cells, possibly by regulating the activity of the bHLH transcription factor MUTE, although MUTE does not appear to be a direct MAPK target on the basis of in vitro data [25]. Genetic data suggest that the epidermal YDA pathway includes a cascade consisting of YDA and MKK4/MKK5, as well as MKK7/MKK9 and MPK3/MPK6 [20,24,25]. This module is activated by leucine-rich receptor-like kinases of the ER (ERECTA) family, including ER, ERL1 (ERECTA-LIKE1) and ERL2 which perceive extracellular small cysteine-rich peptides of the EPF-like family including
EPF1 (EPIDERMAL PATTERNING FACTOR 1) and EPF2 [32,33]. By inhibiting SPCH activity, the YDA pathway promotes pavement cell identity. yda loss-offunction mutants show clusters of stomata whereas YDA-CA variants evoke leaves that entirely lack stomata [20].
Signalling cross-talk It has been shown recently that YDA activity in the leaf epidermis can be influenced by components of the BR (brassinosteroid) signalling pathway, suggesting cross-talk between these two signalling cascades [34] (Figure 2). On the basis of current evidence, BIN2 (BRASSINOSTEROIDINSENSITIVE 2) seems to be the main connection between these two pathways, since it can directly phosphorylate and negatively regulate the activity of YDA, MKK4 and MKK5, as well as SPCH [35–37]. This cross-talk between BR and YDA signalling suggests an intriguing signalling mechanism that might explain how SSP can activate YDA. SSP evolved as a paralogue of the BSK1 (BRASSINOSTEROID SIGNALLING KINASE 1) gene in the last whole-genome duplication of the Brassicaceae [38]. As the name indicates, BSK1 is a signalling component of the BRI1 (BRASSINOSTEROID-INSENSITIVE 1) receptor pathway [39]. Upon perception of brassinolid, BSK1 is phosphorylated by the leucine-rich repeat receptor-like kinase BRI1 and recruits the Kelch-repeat containing phosphatases BSU1 (BRI1 SUPPRESSOR 1) and members of the BSL (BSU1LIKE) family [39,40]. These can dephosphorylate and therefore negatively regulate the activity of the GSK3 (glycogen synthase kinase 3)-like kinase BIN2 [40]. In the context of the BR–YDA cross-talk, BSK1 phosphorylation would lead to reduced activity of BIN2 and therefore increased activity of YDA. Since SSP is a paralogue of BSK1, it is tempting to speculate whether YDA activation by SSP possibly includes a similar mechanism involving BIN2. This would mean that SSP hijacked this connection between BR and YDA signalling and could be a late addition to an already pre-existing more ancient YDA pathway. With the architecture of YDA signalling pathways in other developmental contexts in mind, it is intuitive to speculate about so far undiscovered receptor-like kinases in the embryo acting upstream of YDA and possibly independently of SSP. If these indeed exist, what extracellular signal they might perceive and from which tissue their ligands could originate is unfortunately speculative at this moment.
Conclusion Besides auxin and a transcriptional network including WRKY2, WOX2, WOX8 and WOX9, the YDA/MAPK signalling pathway acts as a key regulator to specify apical– basal polarity in the early embryo. At the moment, our knowledge of the inner workings of this pathway is still rather cryptic, and further work is needed to understand how YDA C The
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is activated and how this translates into apical–basal polarity of the embryo.
Acknowledgements We apologize to our colleagues whose work we could not present here and thank Steffen Lau for a critical reading of the paper before submission.
Funding Work in our laboratory is funded by the German Research Foundation (Deutsche Forschungsgemeinschaft) [grant number BA 3356/2-1] and the Max Planck Society.
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