FERONIA regulates FLS2 plasma membrane nanoscale dynamics to modulate plant immune signaling
Posted on: 5 August 2020 , updated on: 10 August 2020
Preprint posted on 22 July 2020
Article now published in eLife at http://dx.doi.org/10.7554/eLife.74162
FERONIA is the new BAK1, and membrane nanodomains are the new thing - but the flg22/FLS2/BAK1 complex continues to serve as a platform for new discoveries
Selected by Marc Somssich
Categories: cell biology, developmental biology, plant biology
Background
20 years ago the lab of Thomas Boller made a surprise discovery when they found that 22 highly conserved amino acids from a Pseudomonas syringae pv tabaci protein can function as a potent elicitor of immune responses in plants1. Right on the heels of this discovery, they also identified the Arabidopsis thaliana receptor for this elicitor2. The elicitor is, of course, flagellin22 (flg22), and the corresponding receptor-like kinase (RLK) is FLAGELLIN-SENSING 2 (FLS2). The discovery of this sensory module established A. thaliana as a model to study pathogen perception and elicitor signaling in plants, and formed the basis for countless important discoveries since. Out of those, the identification of the co-receptor BAK1 (BRASSINOSTEROID INSENSITIVE 1(BRI1)-ASSOCIATED RECEPTOR KINASE 1), as well as the observation that the FLS2-BAK1 interaction is actually triggered by their ligand flg22, might just be the most important one3. BAK1, at the time known only as co-receptor for the brassinosteroid receptor BRI1, subsequently turned out to be a co-receptor for several pathways, demonstrating the inter-connectedness of signaling pathways in plants and enabling researchers to study these connections4. BAK1 became the ‘one for all’ co-receptor4. With its links to brassinosteroid signaling, this also enabled plant scientists to study the trade-off between growth and immunity5. Protein-protein interaction studies remained a great tool to find more components of the flg22 pathway, and through many more publications, the complex signaling events occurring downstream of the flg22/FLS2/BAK1 complex were pieced together bit by bit in the following years6. Another thing that has become increasingly clear in recent years is that sub-domains in the plasma membrane (PM) not only exist, but are actually important as signaling platforms – something many plant scientists were only ready to accept years after the ‘lipid raft’ debacle, and after changing the name for these domains to PM nanodomains7,8. One advancement that aided in this acceptance was modern (close-to-)super resolution microscopy7. Techniques such as VA-TIRF with single-particle tracking and AiryScan deconvolution helped to finally visualize such nanodomains, and once again the flg22/FLS2/BAK1 complex was among the first studied examples of a receptor module that signals from such a nanodomain (the corresponding paper was also preLighted here9)10. Next to this emergence of PM nanodomains in recent years, the RLK FERONIA also suddenly rose from a protein implicated in pollen tube guidance to a universal co-receptor involved in pretty much every pathway researchers seem to be looking at, and yes, of course also in FLS2/BAK1 signaling (here, I would like to cite an updated ‘One for all’ review – but this is still missing from the literature)11,12. So once again, the flg22/FLS2/BAK1 complex will help to generate new insights, this time into how FER exerts its function as a somewhat universal co-receptor on a molecular level11,12.
Key findings of this preprint
Previously it was shown that FER and LORELEI-LIKE-GPI ANCHORED PROTEIN 1 (LLG1) associate with FLS2, and facilitate flg22-induced FLS2-BAK1 complex formation12. However, perception of the RAPID ALKALINIZATION FACTOR 23 (RALF23) peptide by FER/LLG1 negatively regulates FLS2/BAK1 complex formation12. Now in this new study, Julien Gronnier and colleagues aim to explain this contrasting function on a molecular level11.
They started out by testing if FER is involved in signaling events downstream of the FLS2/BAK1 complex by determining if its intracellular kinase domain is required for its function. However, a kinase-dead variant of FER is still able to support flg22-triggered complex formation and signaling activation. Similarly, the extracellular domain of FER, which was suggested to bind pectin and serve as cell wall integrity sensor, is also dispensable for this immune signaling pathway. These experiments suggest that FER is likely to be a scaffold with structural importance for the FLS2/BAK1 complex.
LEUCIN-RICH REPEAT EXTENSIN (LRX) proteins are implicated to function in association with Catharanthus roseus RECEPTOR-LIKE KINASE (CrRLK) proteins, such as FER13. Since lrx3,4,5 triple mutants have some phenotypic similarities with fer mutants, and LRXs can bind RALF peptides, the authors decided to investigate a possible role for these LRXs in the flagellin pathway13. And indeed, they found that FLS2/BAK1 complex formation and signaling are similarly impaired in lrx3,4,5 triple mutants as they are in fer mutants, while the triple mutant is als insensitive to RALF23-induced immune signaling. These observations suggest that LRX3,4,5 are potential co-receptors for FER, and the authors do confirm the interaction of LRX4 with FER.
Finally, the authors utilized TIRF-microscopy with single-particle tracking to demonstrate that FER, like FLS2, localizes to plasma membrane nanodomains, which restrict the mobility of the proteins in the PM. Given the hypothesized role for FER as a scaffold for FLS2, they analyze the mobility of FLS2 in a fer mutant, and show that the receptor is now more mobile within the PM, suggesting that FER normally restricts the movement of FLS2 to the nanodomain. This would explain the observation that FLS2/BAK1 complex formation is impaired in a fer mutant, as the receptors are now no longer sequestered in the nanodomain, and therefore less likely to be in close proximity. This is further supported by the fact that RALF23 peptide treatment resulted in internalization of FER, which was also accompanied with an increase in FLS2 mobility in the PM.
Conclusions
From the research presented here, it appears that FER and its LRX co-receptor sequester FLS2 and BAK1 in PM nanodomains, thereby keeping them in close proximity to enable a rapid assembly of the active FLS2/BAK1 signaling platform in the event of a pathogenic attack. Perception of RALF23 by a FER/LLG1/LRX complex results in the endocytosis of this receptor, and therefore the partial release of FLS2 from the nanodomain. This makes RALF23 a negative regulator of FLS2/BAK1 immune signaling, which could serve to dampen the immune response, and prevent over-activation, which would impair plant development. This hypothesis needs further testing, however. For example, it would be interesting to see if elicitor-triggered FLS2/BAK1 activation is actually followed by FER/LLG1/LRX4 activation and internalization, even without the addition of external RALF23, which would indicate that this pathway gets activated as part of a negative feedback loop. Also, the potential cell wall integrity sensor function of FER and the LRXs could provide a link to damage-associated molecular pattern signaling pathways, with CrRLKs and LRXs thereby connecting damage- and pathogen-associated molecular pattern pathways. Similarly, with FER being implicated in countless other pathways, it will be interesting to see if this role as an anchor point to PM nanodomains is a general model for FER function, or if FER is more of a ‘Jack of all trades’. The fact that kinase function is not required for FERs role in the flagellin pathway, but is required for others, does suggests the latter, with FER functioning differently in different contexts. Certainly FER, and of course the FLS2/BAK1 complex, will provide us with many more insights in the coming years.
References
- Felix G, Duran JD, Volko S, Boller T. Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J. 1999;18: 265–276. Available at doi:10.1046/j.1365-313X.1999.00265.x
- Gómez-Gómez L, Boller T. FLS2: An LRR Receptor-like Kinase Involved in the Perception of the Bacterial Elicitor Flagellin in Arabidopsis. Mol Cell. 2000;5: 1003–1011. Available at doi:10.1016/S1097-2765(00)80265-8
- Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nürnberger T, Jones JDG, et al. A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature. 2007;448: 497–500. Available at doi:10.1038/nature05999
- Chinchilla D, Shan L, He P, De Vries SC, Kemmerling B. One for all: the receptor-associated kinase BAK1. Trends Plant Sci. 2009;14: 535–41. Available at doi:10.1016/j.tplants.2009.08.002
- Lozano-Durán R, Zipfel C. Trade-off between growth and immunity: role of brassinosteroids. Trends Plant Sci. 2015;20: 12–19. Available at doi:10.1016/j.tplants.2014.09.003
- Couto D, Zipfel C. Regulation of pattern recognition receptor signalling in plants. Nat Rev Immunol. Nature Publishing Group; 2016; Available at doi:10.1038/nri.2016.77
- Gronnier J, Gerbeau-Pissot P, Germain V, Mongrand S, Simon-Plas F. Divide and Rule: Plant Plasma Membrane Organization. Trends Plant Sci. Elsevier Ltd; 2018;xx: 1–19. Available at doi:10.1016/j.tplants.2018.07.007
- Goñi FM. “Rafts”: a nickname for putative transient nanodomains. Chem Phys Lipids. Elsevier Ireland Ltd; 2018; Available at doi:10.1016/j.chemphyslip.2018.11.006
- Somssich M. preLight: The cell wall regulates dynamics and size of plasma-membrane nanodomains in Arabidopsis. preLights. 2019;: 1–3. doi:10.1242/prelights.6238
- McKenna JF, Rolfe DJ, Webb SED, Tolmie AF, Botchway SW, Martin-Fernandez ML, et al. The cell wall regulates dynamics and size of plasma-membrane nanodomains in Arabidopsis. Proc Natl Acad Sci U S A. 2019;: 201819077. Available at doi:10.1073/pnas.1819077116
- Gronnier J, Franck CM, Stegmann M, Defalco TA, Cifuentes A, Dünser K, et al. FERONIA regulates FLS2 plasma membrane nanoscale dynamics to modulate plant immune signaling. bioRxiv. 2020; Available at doi:10.1101/2020.07.20.212233
- Stegmann M, Monaghan J, Smakowska-Luzan E, Rovenich H, Lehner A, Holton NJ, et al. The receptor kinase FER is a RALF-regulated scaffold controlling plant immune signaling. Science. 2017;355: 287–289. Available at doi:10.1126/science.aal2541
- Herger A, Dünser K, Kleine-Vehn J, Ringli C. Leucine-Rich Repeat Extensin Proteins and Their Role in Cell Wall Sensing. Curr Biol. 2019;29: R851–R858. Available at doi:10.1016/j.cub.2019.07.039
doi: https://doi.org/10.1242/prelights.23746
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