Perception of a conserved family of plant signalling peptides by the receptor kinase HSL3

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    Evaluation Summary:

    Beginning with transcriptome data, Rhodes et al. identify a new family of peptides with signalling function called CTNIP in the model plant Arabidopsis thaliana. They use an elegant biochemical capture approach to pinpoint the SERK-dependent LRR receptor kinase HSL3 as the only receptor for these peptides. They provide convincing genetic and biochemical evidence that HSL3 binds CTNIP and that CTNIP perception triggers HSL3-dependent cytoplasmic calcium influx, ROS production and transcriptional changes. Furthermore, they provide initial evidence that the CTNIP-HSL3 module may participate in regulating root growth.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 agreed to share their name with the authors.)

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Abstract

Plant genomes encode hundreds of secreted peptides; however, relatively few have been characterised. We report here an uncharacterised, stress-induced family of plant signalling peptides, which we call CTNIPs. Based on the role of the common co-receptor BRASSINOSTEROID INSENSITIVE 1-ASSOCIATED KINASE 1 (BAK1) in CTNIP-induced responses, we identified in Arabidopsis thaliana the orphan receptor kinase HAESA-LIKE 3 (HSL3) as the CTNIP receptor via a proteomics approach. CTNIP-binding, ligand-triggered complex formation with BAK1, and induced downstream responses all involve HSL3. Notably, the HSL3-CTNIP signalling module is evolutionarily conserved amongst most extant angiosperms. The identification of this novel signalling module will further shed light on the diverse functions played by plant signalling peptides and will provide insights into receptor-ligand co-evolution.

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  1. Author Response

    Reviewer #3 (Public Review ):

    Rhodes et al. explored novel signalling peptides by searching genes encoding small proteins having signal peptide, which are transcriptionally induced upon biotic elicitor treatments in Arabidopsis thaliana. They found that small potentially secreted proteins, designate as CTNIPs based on the conserved sequence motif, are transcriptionally induced upon 7 different elicitors. In A. thaliana, 5 CTINPs are encoded in the genome, and CTNIP4 is strongly induced upon the elicitor treatments. Chemically synthesized signal peptide-deleted CTNIP proteins except for CTNIP5 show the activities to induce Ca2+ influx and MAP kinases phosphorylation in A. thaliana, which are the hallmarks of elicitor-induced immune signalling. The authors found that CTNIP4 can induce ROS burst in a BAK1-dependent …

  2. Evaluation Summary:

    Beginning with transcriptome data, Rhodes et al. identify a new family of peptides with signalling function called CTNIP in the model plant Arabidopsis thaliana. They use an elegant biochemical capture approach to pinpoint the SERK-dependent LRR receptor kinase HSL3 as the only receptor for these peptides. They provide convincing genetic and biochemical evidence that HSL3 binds CTNIP and that CTNIP perception triggers HSL3-dependent cytoplasmic calcium influx, ROS production and transcriptional changes. Furthermore, they provide initial evidence that the CTNIP-HSL3 module may participate in regulating root growth.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 agreed to …

  3. Reviewer #1 (Public Review):

    Using transcriptome data reporting responses to biotic stress Rhodes et al identified a new family of small peptides, called CTNIPs, which elicit cytoplasmic Ca2+-influx and MAP-kinase phosphorylation in a bak1 dependent manner. Based on the requirement of BAK1, they searched for BAK1-interactors in the presence of CTNIP using a combination of BAK1-pulldown with proteomics and identified the orphan receptor-like kinase HSL3. They use a combination of biochemical binding assays, protein modelling and genetics (based on root growth responses to the peptides) to confirm that HSL3 is indeed the receptor of CTNIPs. Thus, the study provides a novel small peptide ligand-receptor pair, with a likely function in the regulation of directional root growth. The work is thoroughly conducted and includes several …

  4. Reviewer #2 (Public Review):

    Rhodes et al., use an elegant biochemical capture approach to identify the SERK-dependent LRR receptor kinase HSL3 as the only receptor for the newly identified CTNIP peptides in Arabidopsis, and in other species. This idea is based on their finding that synthetic CTNIP peptides trigger cytoplasmic calcium influx and ROS production in wild-type but not bak1-5 mutant Arabidopsis plants. Using the BAK1 co-receptor and the synthetic peptide they identify HSL3 as a major BAK1 signaling complex component and then elegantly demonstrate in vivo and in vitro that CTNIPs are direct ligands targeting the HSL3 extracellular domain. HSL3, despite its name, is thus no receptor for IDA/IDL peptides but for a new family of peptides with possible roles in stress responses and in root development. While most experiments are …

  5. Reviewer #3 (Public Review):

    Rhodes et al. explored novel signalling peptides by searching genes encoding small proteins having signal peptide, which are transcriptionally induced upon biotic elicitor treatments in Arabidopsis thaliana. They found that small potentially secreted proteins, designate as CTNIPs based on the conserved sequence motif, are transcriptionally induced upon 7 different elicitors. In A. thaliana, 5 CTINPs are encoded in the genome, and CTNIP4 is strongly induced upon the elicitor treatments. Chemically synthesized signal peptide-deleted CTNIP proteins except for CTNIP5 show the activities to induce Ca2+ influx and MAP kinases phosphorylation in A. thaliana, which are the hallmarks of elicitor-induced immune signalling. The authors found that CTNIP4 can induce ROS burst in a BAK1-dependent manner in A. thaliana, …