Subtilase-mediated biogenesis of the expanded family of SERINE RICH ENDOGENOUS PEPTIDES.
Journal
Nature plants
ISSN: 2055-0278
Titre abrégé: Nat Plants
Pays: England
ID NLM: 101651677
Informations de publication
Date de publication:
04 Dec 2023
04 Dec 2023
Historique:
received:
10
12
2022
accepted:
03
11
2023
pubmed:
5
12
2023
medline:
5
12
2023
entrez:
4
12
2023
Statut:
aheadofprint
Résumé
Plant signalling peptides are typically released from larger precursors by proteolytic cleavage to regulate plant growth, development and stress responses. Recent studies reported the characterization of a divergent family of Brassicaceae-specific peptides, SERINE RICH ENDOGENOUS PEPTIDES (SCOOPs), and their perception by the leucine-rich repeat receptor kinase MALE DISCOVERER 1-INTERACTING RECEPTOR-LIKE KINASE 2 (MIK2). Here, we reveal that the SCOOP family is highly expanded, containing at least 50 members in the Columbia-0 reference Arabidopsis thaliana genome. Notably, perception of these peptides is strictly MIK2-dependent. How bioactive SCOOP peptides are produced, and to what extent their perception is responsible for the multiple physiological roles associated with MIK2 are currently unclear. Using N-terminomics, we validate the N-terminal cleavage site of representative PROSCOOPs. The cleavage sites are determined by conserved motifs upstream of the minimal SCOOP bioactive epitope. We identified subtilases necessary and sufficient to process PROSCOOP peptides at conserved cleavage motifs. Mutation of these subtilases, or their recognition motifs, suppressed PROSCOOP cleavage and associated overexpression phenotypes. Furthermore, we show that higher-order mutants of these subtilases show phenotypes reminiscent of mik2 null mutant plants, consistent with impaired PROSCOOP biogenesis, and demonstrating biological relevance of SCOOP perception by MIK2. Together, this work provides insights into the molecular mechanisms underlying the functions of the recently identified SCOOP peptides and their receptor MIK2.
Identifiants
pubmed: 38049516
doi: 10.1038/s41477-023-01583-x
pii: 10.1038/s41477-023-01583-x
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Gatsby Charitable Foundation
ID : n/a
Organisme : RCUK | Biotechnology and Biological Sciences Research Council (BBSRC)
ID : BB/P012574/1
Organisme : EC | EU Framework Programme for Research and Innovation H2020 | H2020 Priority Excellent Science | H2020 European Research Council (H2020 Excellent Science - European Research Council)
ID : 773153
Organisme : EC | EU Framework Programme for Research and Innovation H2020 | H2020 Priority Excellent Science | H2020 European Research Council (H2020 Excellent Science - European Research Council)
ID : 724321
Organisme : Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (Swiss National Science Foundation)
ID : 31003A_182625
Organisme : Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (Swiss National Science Foundation)
ID : 310030_184769
Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer Nature Limited.
Références
Matsubayashi, Y. Posttranslationally modified small-peptide signals in plants. Annu. Rev. Plant Biol. 65, 385–413 (2014).
pubmed: 24779997
doi: 10.1146/annurev-arplant-050312-120122
Olsson, V. et al. Look closely, the beautiful may be small: precursor-derived peptides in plants. Annu. Rev. Plant Biol. 70, 153–186 (2019).
pubmed: 30525926
doi: 10.1146/annurev-arplant-042817-040413
Tavormina, P., De Coninck, B., Nikonorova, N., De Smet, I. & Cammue, B. P. The plant peptidome: an expanding repertoire of structural features and biological functions. Plant Cell 27, 2095–2118 (2015).
pubmed: 26276833
pmcid: 4568509
doi: 10.1105/tpc.15.00440
Stührwohldt, N., Ehinger, A., Thellmann, K. & Schaller, A. Processing and formation of bioactive CLE40 peptide are controlled by posttranslational proline hydroxylation. Plant Physiol. 184, 1573–1584 (2020).
pubmed: 32907884
pmcid: 7608152
doi: 10.1104/pp.20.00528
Stührwohldt, N. et al. The biogenesis of CLEL peptides involves several processing events in consecutive compartments of the secretory pathway. eLife 9, e55580 (2020).
Schardon, K. et al. Precursor processing for plant peptide hormone maturation by subtilisin-like serine proteinases. Science 354, 1594–1597 (2016).
pubmed: 27940581
doi: 10.1126/science.aai8550
Reichardt, S., Piepho, H. P., Stintzi, A. & Schaller, A. Peptide signaling for drought-induced tomato flower drop. Science 367, 1482–1485 (2020).
pubmed: 32217727
doi: 10.1126/science.aaz5641
Doll, N. M. et al. A two-way molecular dialogue between embryo and endosperm is required for seed development. Science 367, 431–435 (2020).
pubmed: 31974252
doi: 10.1126/science.aaz4131
Stührwohldt, N. & Schaller, A. Regulation of plant peptide hormones and growth factors by post-translational modification. Plant Biol. 21, 49–63 (2019).
pubmed: 30047205
doi: 10.1111/plb.12881
Rzemieniewski, J. & Stegmann, M. Regulation of pattern-triggered immunity and growth by phytocytokines. Curr. Opin. Plant Biol. 68, 102230 (2022).
Hou, S., Liu, D. & He, P. Phytocytokines function as immunological modulators of plant immunity. Stress Biol. 1, 8 (2021).
Gust, A. A., Pruitt, R. & Nürnberger, T. Sensing danger: key to activating plant immunity. Trends Plant Sci. 22, 779–791 (2017).
pubmed: 28779900
doi: 10.1016/j.tplants.2017.07.005
Gully, K. et al. The SCOOP12 peptide regulates defense response and root elongation in Arabidopsis thaliana. J. Exp. Bot. 70, 1349–1365 (2019).
pubmed: 30715439
pmcid: 6382344
doi: 10.1093/jxb/ery454
Hou, S. et al. The Arabidopsis MIK2 receptor elicits immunity by sensing a conserved signature from phytocytokines and microbes. Nat. Commun. 12, 5494 (2021).
pubmed: 34535661
pmcid: 8448819
doi: 10.1038/s41467-021-25580-w
Rhodes, J. et al. Perception of a divergent family of phytocytokines by the Arabidopsis receptor kinase MIK2. Nat. Commun. 12, 705 (2021).
pubmed: 33514716
pmcid: 7846792
doi: 10.1038/s41467-021-20932-y
Guillou, M.-C. et al. The PROSCOOP10 gene encodes two extracellular hydroxylated peptides and impacts flowering time in Arabidopsis. Plants (Basel) 11, 3354 (2022).
Zhang, J. et al. EWR1 as a SCOOP peptide activates MIK2-dependent immunity in Arabidopsis.J. Plant Inter. 17, 562–568 (2022).
Guillou, M. C. et al. SCOOP12 peptide acts on ROS homeostasis to modulate cell division and elongation in Arabidopsis primary root. J. Exp. Bot. 73, 6115–6132 (2022).
pubmed: 35639812
doi: 10.1093/jxb/erac240
Stahl, E. et al. The MIK2/SCOOP signaling system contributes to Arabidopsis resistance against herbivory by modulating jasmonate and indole glucosinolate biosynthesis. Front. Plant Sci. 13, 852808 (2022).
pubmed: 35401621
pmcid: 8984487
doi: 10.3389/fpls.2022.852808
Julkowska, M. M. et al. Natural variation in rosette size under salt stress conditions corresponds to developmental differences between Arabidopsis accessions and allelic variation in the LRR-KISS gene. J. Exp. Bot. 67, 2127–2138 (2016).
pubmed: 26873976
pmcid: 4809279
doi: 10.1093/jxb/erw015
Van der Does, D. et al. The Arabidopsis leucine-rich repeat receptor kinase MIK2/LRR-KISS connects cell wall integrity sensing, root growth and response to abiotic and biotic stresses. PLoS Genet. 13, e1006832 (2017).
pubmed: 28604776
pmcid: 5484538
doi: 10.1371/journal.pgen.1006832
Engelsdorf, T. et al. The plant cell wall integrity maintenance and immune signaling systems cooperate to control stress responses in Arabidopsis thaliana. Sci. Signal. 11, eaao3070 (2018).
pubmed: 29945884
doi: 10.1126/scisignal.aao3070
Coleman, A. D. et al. The Arabidopsis leucine-rich repeat receptor-like kinase MIK2 is a crucial component of early immune responses to a fungal-derived elicitor. New Phytol. 229, 3453–3466 (2021).
pubmed: 33253435
doi: 10.1111/nph.17122
Stintzi, A. & Schaller, A. Biogenesis of post-translationally modified peptide signals for plant reproductive development. Curr. Opin. Plant Biol. 69, 102274 (2022).
pubmed: 35977439
doi: 10.1016/j.pbi.2022.102274
Royek, S. et al. Processing of a plant peptide hormone precursor facilitated by posttranslational tyrosine sulfation. Proc. Natl Acad. Sci. USA 119, e2201195119 (2022).
pubmed: 35412898
pmcid: 9169856
doi: 10.1073/pnas.2201195119
Bailey, T. L. & Gribskov, M. Combining evidence using p-values: application to sequence homology searches. Bioinformatics 14, 48–54 (1998).
pubmed: 9520501
doi: 10.1093/bioinformatics/14.1.48
Bjornson, M., Pimprikar, P., Nürnberger, T. & Zipfel, C. The transcriptional landscape of Arabidopsis thaliana pattern-triggered immunity. Nat. Plants 7, 579–586 (2021).
pubmed: 33723429
pmcid: 7610817
doi: 10.1038/s41477-021-00874-5
Yu, Z. et al. The Brassicaceae-specific secreted peptides, STMPs, function in plant growth and pathogen defense. J. Integr. Plant Biol. 62, 403–420 (2020).
pubmed: 31001913
doi: 10.1111/jipb.12817
Yadeta, K. A., Valkenburg, D. J., Hanemian, M., Marco, Y. & Thomma, B. P. The Brassicaceae-specific EWR1 gene provides resistance to vascular wilt pathogens. PLoS ONE 9, e88230 (2014).
pubmed: 24505441
pmcid: 3914955
doi: 10.1371/journal.pone.0088230
Neukermans, J. et al. ARACINs, Brassicaceae-specific peptides exhibiting antifungal activities against necrotrophic pathogens in Arabidopsis. Plant Physiol. 167, 1017–1029 (2015).
pubmed: 25593351
pmcid: 4348783
doi: 10.1104/pp.114.255505
Petre, B. Toward the discovery of host-defense peptides in plants. Front. Immun. 11, 1825 (2020).
doi: 10.3389/fimmu.2020.01825
Fletcher, J. C. Recent advances in Arabidopsis CLE peptide signaling. Trends Plant Sci. 25, 1005–1016 (2020).
pubmed: 32402660
doi: 10.1016/j.tplants.2020.04.014
Liu, J. X., Srivastava, R., Che, P. & Howell, S. H. Salt stress responses in Arabidopsis utilize a signal transduction pathway related to endoplasmic reticulum stress signaling. Plant J. 51, 897–909 (2007).
pubmed: 17662035
pmcid: 2156172
doi: 10.1111/j.1365-313X.2007.03195.x
Liu, J. X., Srivastava, R., Che, P. & Howell, S. H. An endoplasmic reticulum stress response in Arabidopsis is mediated by proteolytic processing and nuclear relocation of a membrane-associated transcription factor, bZIP28. Plant Cell 19, 4111–4119 (2007).
pubmed: 18156219
pmcid: 2217655
doi: 10.1105/tpc.106.050021
Ghorbani, S. et al. The SBT6.1 subtilase processes the GOLVEN1 peptide controlling cell elongation. J. Exp. Bot. 67, 4877–4887 (2016).
pubmed: 27315833
pmcid: 4983112
doi: 10.1093/jxb/erw241
Abarca, A., Franck, C. M. & Zipfel, C. Family-wide evaluation of RAPID ALKALINIZATION FACTOR peptides. Plant Physiol. 187, 996–1010 (2021).
pubmed: 34608971
pmcid: 8491022
doi: 10.1093/plphys/kiab308
Sénéchal, F. et al. Arabidopsis PECTIN METHYLESTERASE17 is co-expressed with and processed by SBT3.5, a subtilisin-like serine protease. Ann. Bot. 114, 1161–1175 (2014).
pubmed: 24665109
pmcid: 4195543
doi: 10.1093/aob/mcu035
Hruz, T. et al. Genevestigator v3: a reference expression database for the meta-analysis of transcriptomes. Adv. Bioinformatics 2008, 420747 (2008).
pubmed: 19956698
pmcid: 2777001
doi: 10.1155/2008/420747
Schaller, A. et al. From structure to function – a family portrait of plant subtilases. New Phytol. 218, 901–915 (2018).
pubmed: 28467631
doi: 10.1111/nph.14582
Ramírez, V., López, A., Mauch-Mani, B., Gil, M. J. & Vera, P. An extracellular subtilase switch for immune priming in Arabidopsis. PLoS Pathog. 9, e1003445 (2013).
pubmed: 23818851
pmcid: 3688555
doi: 10.1371/journal.ppat.1003445
Kourelis, J. et al. A homology-guided, genome-based proteome for improved proteomics in the alloploid Nicotiana benthamiana. BMC Genomics 20, 722 (2019).
pubmed: 31585525
pmcid: 6778390
doi: 10.1186/s12864-019-6058-6
von Groll, U., Berger, D. & Altmann, T. The subtilisin-like serine protease SDD1 mediates cell-to-cell signaling during Arabidopsis stomatal development. Plant Cell 14, 1527–1539 (2002).
doi: 10.1105/tpc.001016
Cedzich, A. et al. The protease-associated domain and C-terminal extension are required for zymogen processing, sorting within the secretory pathway, and activity of tomato subtilase 3 (SlSBT3). J. Biol. Chem. 284, 14068–14078 (2009).
pubmed: 19332543
pmcid: 2682855
doi: 10.1074/jbc.M900370200
Ottmann, C. et al. Structural basis for Ca
pubmed: 19805099
pmcid: 2749846
doi: 10.1073/pnas.0907587106
Stührwohldt, N., Schardon, K., Stintzi, A. & Schaller, A. A toolbox for the analysis of peptide signal biogenesis. Mol. Plant 10, 1023–1025 (2017).
pubmed: 28735025
doi: 10.1016/j.molp.2017.07.005
Tian, M., Huitema, E., Da Cunha, L., Torto-Alalibo, T. & Kamoun, S. A Kazal-like extracellular serine protease inhibitor from Phytophthora infestans targets the tomato pathogenesis-related protease P69B. J. Biol. Chem. 279, 26370–26377 (2004).
pubmed: 15096512
doi: 10.1074/jbc.M400941200
Tian, M., Benedetti, B. & Kamoun, S. A second Kazal-like protease inhibitor from Phytophthora infestans inhibits and interacts with the apoplastic pathogenesis-related protease P69B of tomato. Plant Physiol. 138, 1785–1793 (2005).
pubmed: 15980196
pmcid: 1176446
doi: 10.1104/pp.105.061226
Paulus, J. K. et al. Extracellular proteolytic cascade in tomato activates immune protease Rcr3. Proc. Natl Acad. Sci. USA 117, 17409–17417 (2020).
pubmed: 32616567
pmcid: 7382257
doi: 10.1073/pnas.1921101117
Stührwohldt, N., Bühler, E., Sauter, M. & Schaller, A. Phytosulfokine (PSK) precursor processing by subtilase SBT3.8 and PSK signaling improve drought stress tolerance in Arabidopsis. J. Exp. Bot. 72, 3427–3440 (2021).
pubmed: 33471900
doi: 10.1093/jxb/erab017
Stegmann, M. et al. RGI-GOLVEN signaling promotes cell surface immune receptor abundance to regulate plant immunity. EMBO Rep. 23, e53281 (2022).
pubmed: 35229426
pmcid: 9066070
doi: 10.15252/embr.202153281
Zhang, H. et al. A plant phytosulfokine peptide initiates auxin-dependent immunity through cytosolic Ca
pubmed: 29511053
pmcid: 5894845
doi: 10.1105/tpc.17.00537
Igarashi, D., Tsuda, K. & Katagiri, F. The peptide growth factor, phytosulfokine, attenuates pattern-triggered immunity. Plant J. 71, 194–204 (2012).
pubmed: 22353039
doi: 10.1111/j.1365-313X.2012.04950.x
Ranf, S. et al. Microbe-associated molecular pattern-induced calcium signaling requires the receptor-like cytoplasmic kinases, PBL1 and BIK1. BMC Plant Biol. 14, 374 (2014).
pubmed: 25522736
pmcid: 4279983
doi: 10.1186/s12870-014-0374-4
Lampropoulos, A. et al. GreenGate—a novel, versatile, and efficient cloning system for plant transgenesis. PLoS ONE 8, e83043 (2013).
pubmed: 24376629
pmcid: 3869738
doi: 10.1371/journal.pone.0083043
Gleave, A. P. A versatile binary vector system with a T-DNA organisational structure conducive to efficient integration of cloned DNA into the plant genome. Plant Mol. Biol. 20, 1203–1207 (1992).
pubmed: 1463857
doi: 10.1007/BF00028910
Castel, B., Tomlinson, L., Locci, F., Yang, Y. & Jones, J. D. G. Optimization of T-DNA architecture for Cas9-mediated mutagenesis in Arabidopsis. PLoS ONE 14, e0204778 (2019).
pubmed: 30625150
pmcid: 6326418
doi: 10.1371/journal.pone.0204778
Frickey, T. & Lupas, A. CLANS: a Java application for visualizing protein families based on pairwise similarity. Bioinformatics 20, 3702–3704 (2004).
pubmed: 15284097
doi: 10.1093/bioinformatics/bth444
Kesten, C. et al. Pathogen-induced pH changes regulate the growth-defense balance in plants. EMBO J. 38, e101822 (2019).
pubmed: 31736111
pmcid: 6912046
doi: 10.15252/embj.2019101822
Huerta, A. I., Kesten, C., Menna, A. L., Sancho-Andrés, G. & Sanchez-Rodriguez, C. In-plate quantitative characterization of Arabidopsis thaliana susceptibility to the fungal vascular pathogen fusarium oxysporum. Curr. Protoc. Plant Biol. 5, e20113 (2020).
pubmed: 32598078
doi: 10.1002/cppb.20113