Soybean RIN4 represents a mechanistic link between plant immune and symbiotic signaling
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eLife assessment
The manuscript describes important findings supported by convincing data. The authors present persuasive genetic and biochemical evidence that supports the biological mechanism for optimal nodulation in soybean presented in this study. The results are of relevance to understanding the signaling pathway underpinning beneficial rhizobia symbiosis, while repressing the immune response. With the discussion part strengthened this paper would be of broad interest to plant biologists working on cell signaling and plant-microbe interactions.
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- Plant Biology (eLife)
Abstract
The legume-rhizobium symbiosis represents a unique and beneficial interaction between legumes and nitrogen-fixing soil bacteria, called rhizobia. The initiation and development of this symbiosis is complex and begins with recognition of key molecular signals, produced by the plant and its symbiont, which determine symbiotic compatibility. Current data suggest that the invading symbiont initially triggers plant immune responses that are subsequently suppressed. Hence, there is growing evidence that features of plant immunity may be relevant to symbiotic establishment. RIN4 is a key immune regulator in plants, regulating basal immunity and it is also targeted by pathogen effector proteins that either confer susceptibility or resistance, depending on the presence of the appropriate resistance protein. Surprisingly, we found that RIN4 was rapidly phosphorylated upon rhizobial inoculation of soybean root hairs. RNAi silencing and mutant studies indicate that RIN4 expression is essential for effective nodulation of soybean. RIN4 phosphorylation occurs within a fifteen amino acid motif, which is highly conserved within the Fabales (legumes) and Rosales orders, that comprise species capable of nitrogen-fixing endosymbiosis with rhizobia. RIN4 proteins mutated in this conserved phosphorylation site failed to support efficient soybean nodulation. Phosphorylation of this site is mediated by the symbiotic receptor-like kinase, SymRK, a well-studied member of the symbiotic signaling pathway. The data implicate RIN4 phosphorylation as a key mediator of rhizobial compatibility, interconnecting symbiotic and immune signaling pathways. The nitrogen fixing legume-rhizobium symbiosis is a cornerstone of sustainable agriculture, with ongoing efforts to transfer this unique ability to non-leguminous crop plants. Plants are surrounded by a myriad of microbes in the soil, and, therefore, require constant surveillance in order to distinguish between a pathogen or symbiont. Plants monitor for specific molecular signals that indicate pathogen or symbiont presence. We show that RIN4, a key immune regulator, plays an essential role in promoting the development of the symbiotic nitrogen-fixing relationship between soybean and its compatible symbiont Bradyrhizobium japonicum . Therefore, RIN4 is likely a key player in mediating the appropriate response upon infection by friend or foe.
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eLife assessment
The manuscript describes important findings supported by convincing data. The authors present persuasive genetic and biochemical evidence that supports the biological mechanism for optimal nodulation in soybean presented in this study. The results are of relevance to understanding the signaling pathway underpinning beneficial rhizobia symbiosis, while repressing the immune response. With the discussion part strengthened this paper would be of broad interest to plant biologists working on cell signaling and plant-microbe interactions.
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Reviewer #1 (Public Review):
The authors set out to illuminate how legumes promote symbiosis with beneficial nitrogen-fixing bacteria while maintaining a general defensive posture towards the plethora of potentially pathogenic bacteria in their environment. Intriguingly, a protein involved in plant defence signalling, RIN4, is implicated as a type of 'gatekeeper' for symbiosis, connecting symbiosis signalling with defence signalling. Although questions remain about how exactly RIN4 enables symbiosis, the work opens an important door to new discoveries in this area.
Strengths:
The study uses a multidisciplinary, state-of-the-art approach to implicate RIN4 in soybean nodulation and symbiosis development. The results support the authors' conclusions.Weaknesses:
No serious weaknesses, although the manuscript could be improved slightly from …Reviewer #1 (Public Review):
The authors set out to illuminate how legumes promote symbiosis with beneficial nitrogen-fixing bacteria while maintaining a general defensive posture towards the plethora of potentially pathogenic bacteria in their environment. Intriguingly, a protein involved in plant defence signalling, RIN4, is implicated as a type of 'gatekeeper' for symbiosis, connecting symbiosis signalling with defence signalling. Although questions remain about how exactly RIN4 enables symbiosis, the work opens an important door to new discoveries in this area.
Strengths:
The study uses a multidisciplinary, state-of-the-art approach to implicate RIN4 in soybean nodulation and symbiosis development. The results support the authors' conclusions.Weaknesses:
No serious weaknesses, although the manuscript could be improved slightly from technical and communication standpoints. -
Reviewer #2 (Public Review):
Summary:
The study by Toth et al. investigates the role of RIN4, a key immune regulator, in the symbiotic nitrogen fixation process between soybean and rhizobium. The authors found that SymRK can interact with and phosphorylate GmRIN4. This phosphorylation occurs within a 15 amino acid motif that is highly conserved in N-fixation clades. Genetic studies indicate that GmRIN4a/b play a role in root nodule symbiosis. Based on their data, the authors suggest that RIN4 may function as a key regulator connecting symbiotic and immune signaling pathways.Overall, the conclusions of this paper are well supported by the data, although there are a few areas that need clarification.
Strengths:
• This study provides important insights by demonstrating that RIN4, a key immune regulator, is also required for symbiotic …Reviewer #2 (Public Review):
Summary:
The study by Toth et al. investigates the role of RIN4, a key immune regulator, in the symbiotic nitrogen fixation process between soybean and rhizobium. The authors found that SymRK can interact with and phosphorylate GmRIN4. This phosphorylation occurs within a 15 amino acid motif that is highly conserved in N-fixation clades. Genetic studies indicate that GmRIN4a/b play a role in root nodule symbiosis. Based on their data, the authors suggest that RIN4 may function as a key regulator connecting symbiotic and immune signaling pathways.Overall, the conclusions of this paper are well supported by the data, although there are a few areas that need clarification.
Strengths:
• This study provides important insights by demonstrating that RIN4, a key immune regulator, is also required for symbiotic nitrogen fixation.
• The findings suggest that GmRIN4a/b could mediate appropriate responses during infection, whether it is by friendly or hostile organisms.Weaknesses:
• The study did not explore the immune response in the rin4 mutant. Therefore, it remains unknown how GmRIN4a/b distinguishes between friend and foe. -
Reviewer #3 (Public Review):
Summary:
This manuscript by Toth et al reveals a conserved phosphorylation site within the RIN4 (RPM1-interacting protein 4) R protein that is exclusive to two of the four nodulating clades, Fabales and Rosales. The authors present persuasive genetic and biochemical evidence that phosphorylation at the serine residue 143 of GmRIN4b, located within a 15-aa conserved motif with a core five amino acids 'GRDSP' region, by SymRK, is essential for optimal nodulation in soybean. While the experimental design and results are robust, the manuscript's discussion fails to clearly articulate the significance of these findings. Results described here are important to understand how the symbiosis signaling pathway prioritizes associations with beneficial rhizobia, while repressing immunity-related signals.Strengths:
The …Reviewer #3 (Public Review):
Summary:
This manuscript by Toth et al reveals a conserved phosphorylation site within the RIN4 (RPM1-interacting protein 4) R protein that is exclusive to two of the four nodulating clades, Fabales and Rosales. The authors present persuasive genetic and biochemical evidence that phosphorylation at the serine residue 143 of GmRIN4b, located within a 15-aa conserved motif with a core five amino acids 'GRDSP' region, by SymRK, is essential for optimal nodulation in soybean. While the experimental design and results are robust, the manuscript's discussion fails to clearly articulate the significance of these findings. Results described here are important to understand how the symbiosis signaling pathway prioritizes associations with beneficial rhizobia, while repressing immunity-related signals.Strengths:
The manuscript asks an important question in plant-microbe interaction studies with interesting findings.Overall, the experiments are detailed, thorough, and very well-designed. The findings appear to be robust.
The authors provide results that are not overinterpreted and are instead measured and logical.
Weaknesses:
No major weaknesses. However, a well-thought-out discussion integrating all the findings and interpreting them is lacking; in its current form, the discussion lacks 'boldness'. The primary question of the study - how plants differentiate between pathogens and symbionts - is not discussed in light of the findings. The concluding remark, "Taken together, our results indicate that successful development of the root nodule symbiosis requires cross-talk between NF-triggered symbiotic signaling and plant immune signaling mediated by RIN4," though accurate, fails to capture the novelty or significance of the findings, and left me wondering how this adds to what is already known. A clear conclusion, for eg, the phosphorylation of RIN4 isoforms by SYMRK at S143 modulates immune responses during symbiotic interactions with rhizobia, or similar, is needed. -
