The CLAVATA receptor FASCIATED EAR2 responds to distinct CLE peptides by signaling through two downstream effectors

Like animals, plants are made up of many different types of cells, which descend from undifferentiated cells called stem cells. Thanks to these cells, plants are able to grow and develop throughout their lives. Stem cells live at the tips of the plant’s shoots and roots. They constantly divide to produce new cells to self-renew or replace specific plant cells in need of repair. Over time, they change – or differentiate – to go on to become part of tissues like leaves, roots, stems, shoots, flowers or fruits.

To maintain a continuous pool of undifferentiated stem cells and to make sure that stem cells divide at the correct pace, neighbouring cells emit signals that control the activity of stem cells. The new stem cells that remain close to these ‘maintenance signals’ continue to behave like stem cells, but those displaced away begin to differentiate. Stem cells can receive many different types of signals, but how are these signals filtered and passed onto different places within the cell?

To test this, Je, Xu et al. created maize plants that contained mutations in a number of known signalling molecules to see if these molecules used the same communication pathway. The results showed that stem cells could integrate the different signals. Even if the signals pass through the same receiver (a receptor protein called FASCIATED EAR2), each signal exits the receptor as a different message, and attaches to a different messenger protein to relay specific information about stem cell maintenance to the cell.

A next step will be to test if other plants use the same signalling pathways in the same ways to send messages between cells. A better knowledge about stem cell signals in plants could help to develop more productive crops. Previous work has found that precise control of stem cell pathways can help breed crops with more seeds or bigger fruits. These kinds of changes have been selected naturally by humans since the dawn of civilization, but we need to accelerate these advances to help meet the needs of the growing world population and improve agricultural sustainability.

Stem cell proliferation and differentiation throughout plant life is regulated by a feedback loop between the homeodomain transcription factor WUS and CLV ligand-receptor signaling (Mayer et al., 1998; Brand et al., 2000; Schoof et al., 2000; Yadav et al., 2011; Daum et al., 2014). The secretion of the diffusible glycopeptide CLV3 from the central zone (CZ) stem cells of the SAM is believed to initiate signaling through LRR receptors (Fletcher et al., 1999; Rojo et al., 2002; Kondo et al., 2006; Ohyama et al., 2009; Nimchuk et al., 2011b), which transmits the signal to restrict the expression of WUS in the organizing center (OC) cells. To balance this system, WUS non-cell-autonomously promotes stem cell fate by activation of CLV3 expression (Yadav et al., 2011; Daum et al., 2014). CLV3 is thought to be perceived by multiple receptor kinase and receptor like proteins, including the CLV1 LRR receptor-like kinase (Clark et al., 1993; Clark et al., 1997; Brand et al., 2000; Ogawa et al., 2008) and the related BAM receptors (DeYoung et al., 2006; Deyoung and Clark, 2008; Nimchuk et al., 2015; Shinohara and Matsubayashi, 2015), or by a heterodimer of the receptor like protein CLV2 and the transmembrane pseudokinase CRN (Kayes and Clark, 1998; Jeong et al., 1999; Miwa et al., 2008; Müller et al., 2008; Bleckmann et al., 2010; Zhu et al., 2010; Nimchuk et al., 2011a), or by the receptor-like kinase RPK2 (Mizuno et al., 2007; Nodine et al., 2007; Kinoshita et al., 2010). The relationship between CLV1 and CLV2 is not clear- CLV1 can form homodimers, or higher order complexes with CLV2/CRN, to signal co-operatively in the SAM (Guo et al., 2010; Somssich et al., 2015), but it seems that CLV2/CRN is not essential for CLV3 perception or for CLV1 signaling (Müller et al., 2008; Nimchuk et al., 2011b; Nimchuk, 2017). In contrast to CLV1, CLV2 does not bind CLV3 peptide directly (Shinohara and Matsubayashi, 2015), and its expression is not restricted to the SAM, suggesting that it might function as a co-receptor in additional pathways beyond CLV3 signaling. Indeed, CLV2 appears to be involved in signaling by several CLE peptides (Fiers et al., 2005; Meng and Feldman, 2010; Hazak et al., 2017) and in biotic interactions (Replogle et al., 2011; Hanemian et al., 2016), suggesting it plays diverse functions in plant development and immunity (Pan et al., 2016). The multiple roles of CLV2 promote the question of how it confers signal specificity. Two candidate downstream effectors of CLV2 have been identified. One is the transmembrane pseudokinase CRN, discovered in Arabidopsis, and the second is COMPACT PLANT2 (CT2), the heterotrimeric G protein alpha subunit, discovered in maize (Bommert et al., 2013a). However, since CRN and CT2 were identified in different species, their molecular and genetic interactions remain unknown.

The CLV-WUS pathway is widely conserved (Somssich et al., 2016; Soyars et al., 2016). In maize, THICK TASSEL DWARF1 (TD1) and FEA2 are CLV1 and CLV2 orthologs, and function similarly to restrict inflorescence shoot meristem proliferation (Taguchi-Shiobara et al., 2001; Bommert et al., 2005). Two maize WUS orthologs, ZmWUS1 and ZmWUS2, have been predicted by phylogenetic analysis, and a ZmWUS1 reporter is expressed in the presumptive organizing center of the inflorescence shoot meristem (Je et al., 2016), but these genes have not been functionally characterized (Nardmann and Werr, 2006). In rice, FLORAL ORGAN NUMBER 1 (FON1), the CLV1 ortholog, and FON2, the CLV3 ortholog, similarly function in floral development in a common pathway, as expected (Suzaki et al., 2004; Chu et al., 2006; Suzaki et al., 2006; Suzaki et al., 2008; Suzaki et al., 2009), whereas a second rice CLE peptide gene, FON2-LIKE CLE PROTEIN1 (FCP1) controls stem cell proliferation independent of FON1 (Suzaki et al., 2008). The rice WUS homolog, TILLERS ABSENT1/MONOCULM3 functions in axillary shoot meristem formation (Tanaka et al., 2015; Lu et al., 2015), and WUS function in the shoot apical meristems appears to have been taken over by the WUSCHEL RELATED HOMEOBOX4 (WOX4) gene (Ohmori et al., 2013).

How specificity is achieved is a common question in signal transduction pathways. Recently, we identified a distinct CLV receptor, FASCIATED EAR3 (FEA3) in maize and Arabidopsis, and found that FEA3 controls responses to the maize FCP1 (ZmFCP1) CLE peptide (Je et al., 2016). Here, we show that the maize CLV2 ortholog FEA2 also participates in ZmFCP1 signaling, in addition to controlling responses to the maize CLV3 ortholog, ZmCLE7 (Je et al., 2016). To ask how specificity from these different CLE peptide inputs is achieved, we first isolated mutant alleles of the maize CRN gene. Consistent with results in Arabidopsis (Miwa et al., 2008; Müller et al., 2008; Bleckmann et al., 2010; Zhu et al., 2010; Nimchuk et al., 2011a), we found that fea2 was epistatic to Zmcrn in control of meristem size, but Zmcrn;ct2 double mutants showed an additive enhanced phenotype, suggesting they act in parallel pathways, despite the fact that FEA2 binds both ZmCRN and CT2 in co-immunoprecipitation (co-IP) experiments. Strikingly, ct2 and Zmcrn mutants were resistant to different CLE peptides, ZmCLE7 and ZmFCP1, respectively, but fea2 was resistant to both, suggesting that FEA2 controls responses to different CLE peptides by acting through different downstream effectors.

A major question in signal transduction is how multiple inputs can be translated into distinct outputs. CLV-WUS feedback signaling is the central regulatory pathway in shoot meristem development, and perception of CLV3 peptide involves the CLV1 receptor-like kinase and the CLV2 receptor-like protein together with the CRN pseudokinase (Brand et al., 2000; Schoof et al., 2000; Miwa et al., 2008; Müller et al., 2008; Bleckmann et al., 2010; Zhu et al., 2010; Nimchuk et al., 2011a). However, genetic evidence in both maize and Arabidopsis suggests these receptors function independently, and CLV2, and its maize ortholog FEA2, respond to multiple CLE peptides (Bommert et al., 2005; Fiers et al., 2005; Müller et al., 2008; Guo et al., 2010; Meng and Feldman, 2010; Je et al., 2016; Hazak et al., 2017). So how is the information conferred by these different signals kept separate during transmission through a common receptor?

To address this question and further decipher the FEA2 signaling pathway, we isolated mutants in the maize CRN ortholog, ZmCRN, by reverse genetics and by cloning a newly identified fasciated ear mutant fea*148. ZmCRN was predicted to encode a membrane localize pseudokinase, like CRN in Arabidopsis (Nimchuk et al., 2011a), and characterization of the mutants indicated that ZmCRN similarly functioned as a negative regulator of stem cell proliferation. We found that fea2 was epistatic to Zmcrn and that FEA2 and ZmCRN interacted directly, using Co-IP and BiFC assays of proteins transiently overexpressed in N. benthamiana, suggesting that ZmCRN is a signaling component in the FEA2 pathway. Natural variation in the CLV-WUS pathway underlies yield improvements in different crop species including tomato, maize and mustard (Bommert et al., 2013b; Fan et al., 2014; Xu et al., 2015; Je et al., 2016), and FEA2 is a quantitative trait locus (QTL) for kernel row number (KRN) (Bommert et al., 2013b). In this study, we used a maize association panel of 368 diverse inbred lines to show that ZmCRN also had significant association with KRN under multiple environments (Li et al., 2013; Liu et al., 2015), suggesting that ZmCRN contributes to quantitative variation in this trait. Therefore, ZmCRN could be manipulated for maize yield enhancement.

Previously, we identified the alpha subunit of the heterotrimeric G protein, CT2, as an additional interactor of FEA2. fea2 is epistatic to ct2 in meristem regulation, similar to its genetic interaction with Zmcrn, and FEA2 interacts with CT2 in vivo, revealing that CT2, like ZmCRN, is a candidate downstream signaling component of FEA2 (Bommert et al., 2013a). Although fea2 was epistatic both to ct2 and to Zmcrn, we found that ct2; Zmcrn double mutants had an additive interaction, suggesting they function in parallel, and that the FEA2 signaling pathway branches into these two different downstream signaling components. This idea was supported by peptide assays in different mutants, which suggested that ZmCRN and CT2 function specifically in ZmFCP1 or ZmCLE7 signaling, respectively, while FEA2 is involved in both. Although we used high peptide concentrations, the activity of CLE peptides is known to be enhanced by triarabinosylation (Ohyama et al., 2009; Matsubayashi, 2011; Xu et al., 2015; Corcilius et al., 2017), and indeed we found that similarly modified ZmCLE7 peptide was about 10 fold more potent than the non-modified form (Figure 5—figure supplement 2).

Consistently with our findings, ZmCRN, CT2 and FEA2 were expressed broadly in the SAM in overlapping domains (Figure 2—figure supplement 5). These data suggest a novel mechanism in plant receptor signaling, where a single receptor, FEA2, can transmit signals from two different CLE peptides, ZmFCP1 and ZmCLE7, through two different downstream components, ZmCRN and CT2. We thereby shed light on how distinct signaling by different peptides can be achieved through a common receptor. As a candidate receptor or co-receptor for different peptides, FEA2 does not have any close homologs in the maize genome (Figure 6—figure supplement 1), similar to CLV2 in Arabidopsis, and the relatively mild phenotype of fea2 mutants may be due to compensation by partially redundant parallel signaling pathways, such as through FEA3 (Je et al., 2016). Our results are largely consistent with findings in Arabidopsis, that CRN is dispensable for CLV3 perception and signaling (Nimchuk, 2017), and that CLV2/CRN can function with other CLE ligand-receptor complexes (Hazak et al., 2017). However, in Arabidopsis CRN is required for CLV2 trafficking to the plasma membrane (Bleckmann et al., 2010). Our results suggest that the maize CLV2 ortholog FEA2 still functions (with CT2) in a crn mutant, so is presumably on the plasma membrane even in the absence of ZmCRN.

How then can a single receptor recognize different signals and transmit them differentially? The most obvious answer depends on the hypothesis that FEA2 and CLV2 are co-receptors that function with LRR RLKs, which binds CLE peptides directly (Figure 6). This hypothesis is supported by the finding that CLV1 binds CLV3 with high affinity, but CLV2 is unable to bind CLE peptides (Shinohara and Matsubayashi, 2015), and that CLV2/CRN can function with different CLE ligand-receptor complexes (Hazak et al., 2017). There are conflicting results surrounding the interaction between CLV2 and CLV1; some experiments detect their physical interaction, but many of them use over-expression and are prone to false positive results, and clv2 and clv1 act additively in double mutant combinations (Kayes and Clark, 1998; Müller et al., 2008). This genetic result suggests they act separately, and the same is true for the orthologs FEA2 and TD1 in maize (Bommert et al., 2005). A possible explanation for these conflicting findings is that CLV2 may act with multiple CLE receptor RLKs. This model is supported by the observation that CLV1 homologs, the BAMs, function redundantly with CLV1, so multiple LRR RLKs do indeed function in meristem size control. This also explains why all intermediate and strong clv1 alleles are dominant negative, as they likely interfere with the activity of other receptor kinase(s) that have functional overlap with CLV1 (Diévart et al., 2003; Nimchuk et al., 2015).

Despite not knowing the details of specific CLE-receptor interactions, our data show that FEA2 can transmit different peptide signals through two distinct downstream signaling components that most likely converge on the regulation of ZmWUS expression to regulate stem cell proliferation in meristem development (Figure 6). This suggests a new working model for meristem size regulation, in which ligand binding can be transmitted by a common co-receptor working with different RLKs coupled to distinct signaling proteins. Our model differs from most well-studied ligand-receptor signaling pathways, in which the signaling pathways usually converge (Couto and Zipfel, 2016). For instance, different microbial ligands such as flagellin and Elongation Factor Thermo unstable (EF-Tu) are specifically recognized by the FLAGELLIN-SENSITIVE 2 (FLS2)-BRI1 ASSOCIATED RECEPTOR KINASE (BAK1) or EF-Tu RECEPTOR (EFR)-BAK1 RLK complexes, respectively, while signal transduction requires a shared set of cytosolic kinases, including BOTRYTIS-INDUCED KINASE 1 (BIK1) (Aarts et al., 1998; Lu et al., 2010). Nevertheless, a similar principle can be drawn from the different signaling pathways mediated by BAK1, which functions as a co-receptor for the brassinosteroid (BR) receptor, BR INSENSITIVE 1 (BRI1) or for FLS2. After ligand perception, BR signaling through the BAK1-BRI1 complex is transmitted through the receptor-like cytoplasmic kinase (RLCK) BRASSINOSTEROID-SIGNALING KINASE 1 (BSK1), and flagellin signaling through the BAK1-FLS2 complex is transmitted through a different RLCK, BIK1 (Li et al., 2002; Nam and Li, 2002; Chinchilla et al., 2007; Lu et al., 2010; Wang, 2012; Sun et al., 2013). Our study also reveals another source of variation in meristem receptor signaling, by highlighting the role of an additional CLE peptide, ZmFCP1. The role of FCP1 in meristem maintenance has been characterized in both maize and rice (Suzaki et al., 2008; Je et al., 2016), but not yet in Arabidopsis.

In summary, multiple receptor signaling pathways appear to be required to for the perception of different CLE peptide signals to fine tune meristem development. This complex system of multiple peptides, receptors and downstream components presumably confers robustness on the meristem structure, as well as providing flexibility to control meristem development according to different physiological or developmental cues. For example, meristem size responds to stress and developmental transitions, such as floral induction, and different signaling pathways may confer such responsiveness. Our results help explain how meristem size regulation is orchestrated by multiple CLE peptides and receptors, as observed in many species including Arabidopsis, rice, maize and tomato (Ito et al., 2006; Strabala et al., 2006; Suzaki et al., 2009; Nimchuk et al., 2015; Xu et al., 2015). They also support the idea that meristem signaling components are highly conserved between diverse plant species, and a major challenge is to understand how differential regulation of these common components leads to diversity in meristem organization and size across diverse plant taxa.

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Author details

1. Byoung Il Je

   1. Cold Spring Harbor Laboratory, Cold Spring Harbor, United States
   2. Department of Horticultural Bioscience, College of Natural Resource and Life Science, Pusan National University, Miryang, Republic of Korea

   Contribution

   Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Writing—original draft, Writing—review and editing

   Contributed equally with

   Fang Xu

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-6661-5855

2. Fang Xu

   Cold Spring Harbor Laboratory, Cold Spring Harbor, United States

   Contribution

   Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Writing—review and editing

   Contributed equally with

   Byoung Il Je

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-0767-1272

3. Qingyu Wu

   Cold Spring Harbor Laboratory, Cold Spring Harbor, United States

   Contribution

   Data curation, Methodology

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-3064-2445

4. Lei Liu

   Cold Spring Harbor Laboratory, Cold Spring Harbor, United States

   Contribution

   Data curation, Methodology

   Competing interests

   No competing interests declared

5. Robert Meeley

   DuPont Pioneer, Agricultural Biotechnology, Johnston, United States

   Contribution

   Conceptualization, Formal analysis, Methodology

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-4496-1888

6. Joseph P Gallagher

   University of Massachusetts Amherst, Amherst, United States

   Contribution

   Conceptualization, Methodology

   Competing interests

   No competing interests declared

7. Leo Corcilius

   The University of Sydney, Camperdown, Australia

   Contribution

   Conceptualization, Methodology

   Competing interests

   No competing interests declared

8. Richard J Payne

   The University of Sydney, Camperdown, Australia

   Contribution

   Conceptualization, Methodology

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-3618-9226

9. Madelaine E Bartlett

   University of Massachusetts Amherst, Amherst, United States

   Contribution

   Conceptualization, Methodology

   Competing interests

   No competing interests declared

10. David Jackson

    Cold Spring Harbor Laboratory, Cold Spring Harbor, United States

    Contribution

    Conceptualization, Data curation, Formal analysis, Supervision, Funding acquisition, Investigation, Methodology, Writing—original draft, Writing—review and editing

    For correspondence

    jacksond@cshl.edu

    Competing interests

    No competing interests declared

    "This ORCID iD identifies the author of this article:" 0000-0002-4269-7649

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