The WAK-like protein RFO1 acts as a sensor of the pectin methylation status in Arabidopsis cell walls to modulate root growth and defense

Huerta, Apolonio; Sáncho-Andrés, Gloria; Montesinos, Juan Carlos; Silva‐Navas, Javier; Bassard, Solène; Pau-Roblot, Corinne; Kesten, Christopher; Schlechter, R.; Dora, Susanne; Ayupov, Temurkhan; Pelloux, Jérôme; Santiago, Julia; Sánchez-Rodríguez, Clara

doi:10.1016/j.molp.2023.03.015

Cited by 20 publications

(7 citation statements)

References 114 publications

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“…Interestingly, a recent report showed that BR signaling modulates FER plasma membrane localization (Chaudhary et al 2023) indicating that RALF and BR signaling regulate each other providing a molecular circuit coordinating morphogenesis. In addition, more research is required to unravel whether RALF signaling also involves the previously identified BR-regulating wall monitoring cell-surface receptors RLP44 (Wolf et al 2014) and RFO1/WAKL22 (Huerta et al 2023), or whether they correspond to parallel signaling pathways converging towards BR signaling. It will also be particularly interesting to reveal whether the regulation of BRI1-BAK1 association and cell anisotropy by FER involves antagonist RALF peptides, as proposed in the context of immune signaling (Stegmann et al 2017) and recently demonstrated in the context of reproduction (Lan et al 2023).…”

Section: Resultsmentioning

confidence: 99%

“…In recent years, however, several lines of evidence point towards the predominant role of wall monitoring cell-surface receptors in this process. Indeed, the RECEPTOR-LIKE PROTEIN 44 (RLP44) and the WALL-ASSOCIATED KINASE (WAK)-like RLK RESISTANCE TO FUSARIUM OXYSPORUM 1 (RFO1)/WAKL22 mediate the activation of BRI1 signaling in response to pectin modification (Wolf et al 2014; Huerta et al 2023). In rice ( Oryza sativa ) changes in pectin alleviate the inhibition of OsBRI1 signaling by the WALL-ASSOCIATED KINASE 11 (OsWAK11) (Yue et al 2022).…”

Section: Introductionmentioning

confidence: 99%

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A RALF-Brassinosteroid morpho-signaling circuit regulates Arabidopsis hypocotyl cell shape

Biermann,

von Arx,

Xhelilaj

et al. 2024

Preprint

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Plant cells survey and modulate their cell wall to control their shape and anisotropic growth. Signaling mediated by the plant steroid hormones brassinosteroids (BR) plays a central role in coordinating cell wall status and cell growth, and alterations in the cell wall BR feedback loop leads to life-threatening defects in tissue and cellular integrity. How the status of the cell wall is relayed to BR signaling remains largely unclear. Increasing evidence shows that RAPID ALKALANIZATION FACTORs (RALFs), a class of secreted peptides, play structural and signaling roles at the cell surface. Here we show that perception of RALF23 promotes the formation and signaling of the main BR receptor complex formed by BRASSINOSTEROID INSENSITIVE 1 (BRI1) and BRI1 BRASSINOSTEROID INSENSITIVE1 BRASSINOSTEROID ASSOCIATED KINASE 1 (BAK1). The loss of the plasma membrane localized RALF receptor complex FERONIA (FER) LORELEI LIKE GPI anchor protein 1 (LLG1) leads to defects in cell expansion and anisotropy, as well as uncontrolled BRI1 BAK1 complex formation and signaling. RALF23 bioactivity relies on pectin status and its perception induces changes in pectin composition and the activity of pectin-modifying enzymes. Our observations suggest a model in which RALF23 functions as a cell wall informed signaling cue initiating a feedback loop that solicits BR signaling, modifies the cell wall, and coordinates cell morphogenesis.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

A RALF-Brassinosteroid morpho-signaling circuit regulates Arabidopsis hypocotyl cell shape

Biermann,

von Arx,

Xhelilaj

et al. 2024

Preprint

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“…In addition to 5 WAKs, there are at least 21 WAK-likes (WAKLs) in Arabidopsis. To date, clear evidence is missing that WAKLs are also able to bind cell wall fragments (Kohorn, 2016), with the exception of WAKL22/RESISTANCE TO FUSARIUM OXYSPORUM 1 (RFO1) and WAKL14 (Huerta et al ., 2023; Ma et al ., 2024). However, based on their phylogenetic relationship, WAKLs are obvious candidates to test for further genetic redundancy.…”

Section: Discussionmentioning

confidence: 99%

Arabidopsis WALL-ASSOCIATED KINASES are not required for oligogalacturonide-induced signaling and immunity

Herold,

Hua,

Kohorn

et al. 2024

Preprint

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Carbohydrate-based cell wall signaling impacts plant growth, development, and stress responses; however, how cell wall signals are perceived and transduced remains poorly understood. Several cell wall breakdown products have been described as typical damage-associated molecular patterns (DAMPs) that activate plant immunity, including pectin-derived oligogalacturonides (OGs). Receptor kinases (RKs) of the WALL-ASSOCIATED KINASE (WAK) family have been shown to bind pectin and OGs, and were previously proposed as OG receptors. However, unambiguous genetic evidence for the role of WAKs in OG responses is lacking. Here, we investigated the role of Arabidopsis WAKs in OG perception using a novel deletion mutant of the clustered WAK family. Using a combination of immune assays for early and late pattern-triggered immunity (PTI), we show that WAKs are dispensable for OG-induced signaling and immunity, indicating that they are not bona fide OG receptors.

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“…In addition, GO enrichment and WGCNA analyses of qua2 and cesa3 je5 showed differences ( qua2 included cell wall biosynthesis and pectin metabolism, whereas the cesa3 je5 mutant included jasmonic acid biosynthesis in addition to cell wall biogenesis) that hint at unique CWI signaling responses to wall defects. This may partly be explained by the fact that pectin has cross‐linking sites and can act as a ligand for RLKs (Feng et al, 2018 ; Huerta et al, 2023 ; Kohorn et al, 2009 ; Lin et al, 2022 ). This suggests the presence of distinct CWI pathways that might inspire the future engineering of stress‐resilient cell walls and plants.…”

Section: Discussionmentioning

confidence: 99%

A core of cell wall proteins functions in wall integrity responses in Arabidopsis thaliana

Ajayi,

Zelinsky,

Anderson

2024

Plant Direct

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Cell walls surround all plant cells, and their composition and structure are tightly regulated to maintain cellular and organismal homeostasis. In response to wall damage, the cell wall integrity (CWI) system is engaged to ameliorate effects on plant growth. Despite the central role CWI plays in plant development, our current understanding of how this system functions at the molecular level is limited. Here, we investigated the transcriptomes of etiolated seedlings of mutants of Arabidopsis thaliana with defects in three major wall polysaccharides, pectin (quasimodo2), cellulose (cellulose synthase3je5), and xyloglucan (xyloglucan xylosyltransferase1 and 2), to probe whether changes in the expression of cell wall‐related genes occur and are similar or different when specific wall components are reduced or missing. Many changes occurred in the transcriptomes of pectin‐ and cellulose‐deficient plants, but fewer changes occurred in the transcriptomes of xyloglucan‐deficient plants. We hypothesize that this might be because pectins interact with other wall components and/or integrity sensors, whereas cellulose forms a major load‐bearing component of the wall; defects in either appear to trigger the expression of structural proteins to maintain wall cohesion in the absence of a major polysaccharide. This core set of genes functioning in CWI in plants represents an attractive target for future genetic engineering of robust and resilient cell walls.

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The WAK-like protein RFO1 acts as a sensor of the pectin methylation status in Arabidopsis cell walls to modulate root growth and defense

Cited by 20 publications

References 114 publications

A RALF-Brassinosteroid morpho-signaling circuit regulates Arabidopsis hypocotyl cell shape

A RALF-Brassinosteroid morpho-signaling circuit regulates Arabidopsis hypocotyl cell shape

Arabidopsis WALL-ASSOCIATED KINASES are not required for oligogalacturonide-induced signaling and immunity

A core of cell wall proteins functions in wall integrity responses in Arabidopsis thaliana

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