RALF22 promotes plant immunity and amplifies the Pep3 immune signal.
FER
Pep3
RALF22
Sclerotinia sclerotiorum
plant immunity
reactive oxygen species
Journal
Journal of integrative plant biology
ISSN: 1744-7909
Titre abrégé: J Integr Plant Biol
Pays: China (Republic : 1949- )
ID NLM: 101250502
Informations de publication
Date de publication:
Nov 2023
Nov 2023
Historique:
received:
04
05
2023
accepted:
04
09
2023
medline:
22
11
2023
pubmed:
12
9
2023
entrez:
12
9
2023
Statut:
ppublish
Résumé
Rapid alkalinization factors (RALFs) in plants have been reported to dampen pathogen-associated molecular pattern (PAMP)-triggered immunity via suppressing PAMP-induced complex formation between the pattern recognition receptor (PRR) and its co-receptor BAK1. However, the direct and positive role of RALFs in plant immunity remains largely unknown. Herein, we report the direct and positive roles of a typical RALF, RALF22, in plant immunity. RALF22 alone directly elicited a variety of typical immune responses and triggered resistance against the devastating necrotrophic fungal pathogen Sclerotinia sclerotiorum in a FERONIA (FER)-dependent manner. LORELEI (LRE)-like glycosylphosphatidylinositol (GPI)-anchored protein 1 (LLG1) and NADPH oxidase RBOHD were required for RALF22-elicited reactive oxygen species (ROS) generation. The mutation of cysteines conserved in the C terminus of RALFs abolished, while the constitutive formation of two disulfide bridges between these cysteines promoted the RALF22-elicited ROS production and resistance against S. sclerotiorum, demonstrating the requirement of these cysteines in the functions of RALF22 in plant immunity. Furthermore, RALF22 amplified the Pep3-induced immune signal by dramatically increasing the abundance of PROPEP3 transcript and protein. Supply with RALF22 induced resistance against S. sclerotiorum in Brassica crop plants. Collectively, our results reveal that RALF22 triggers immune responses and augments the Pep3-induced immune signal in a FER-dependent manner, and exhibits the potential to be exploited as an immune elicitor in crop protection.
Substances chimiques
Arabidopsis Proteins
0
Reactive Oxygen Species
0
LLG1 protein, Arabidopsis
0
GPI-Linked Proteins
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
2519-2534Subventions
Organisme : National Natural Science Foundation of China
ID : 31871947
Organisme : Zhejiang Science and Technology Major Program on Agricultural New Variety Breeding
ID : 2021C02064
Organisme : Zhejiang Provincial Natural Science Foundation of China
ID : LZ18C14002
Informations de copyright
© 2023 Institute of Botany, Chinese Academy of Sciences.
Références
Abarca, A., Franck, C.M., and Zipfel, C. (2021). Family-wide evaluation of RAPID ALKALINIZATION FACTOR peptides. Plant Physiol. 187: 996-1010.
Bi, C., Ma, Y., Wu, Z., Yu, Y.T., Liang, S., Lu, K., and Wang, X.F. (2017). Arabidopsis ABI5 plays a role in regulating ROS homeostasis by activating CATALASE 1 transcription in seed germination. Plant Mol. Biol. 94: 197-213.
Bolton, M.D., Thomma, B.P., and Nelson, B.D. (2006). Sclerotinia sclerotiorum (Lib.) de Bary: Biology and molecular traits of a cosmopolitan pathogen. Mol. Plant Pathol. 7: 1-16.
Campbell, L., and Turner, S.R. (2017). A comprehensive analysis of RALF proteins in green plants suggests there are two distinct functional groups. Front. Plant Sci. 8: 37.
Choi, H.W., and Klessig, D.F. (2016). DAMPs, MAMPs, and NAMPs in plant innate immunity. BMC Plant Biol. 16: 2332.
Daudi, A., Cheng, Z., O Brien, J.A., Mammarella, N., Khan, S., Ausubel, F.M., and Bolwell, G.P. (2012). The apoplastic oxidative burst peroxidase in Arabidopsis is a major component of pattern-triggered immunity. Plant Cell 24: 275-287.
de Torres, Z.M., Littlejohn, G., Jayaraman, S., Studholme, D., Bailey, T., Lawson, T., Tillich, M., Licht, D., Bölter, B., Delfino, L., et al. (2015). Chloroplasts play a central role in plant defence and are targeted by pathogen effectors. Nat. Plants. 1: 15074.
Du, C., Li, X., Chen, J., Chen, W., Li, B., Li, C., Wang, L., Li, J., Zhao, X., Lin, J., et al. (2016). Receptor kinase complex transmits RALF peptide signal to inhibit root growth in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A 113: E8326-E8334.
Flury, P., Klauser, D., Schulze, B., Boller, T., and Bartels, S. (2013). The anticipation of danger: Microbe-associated molecular pattern perception enhances AtPep-triggered oxidative burst. Plant Physiol. 161: 2023-2035.
Guo, H., Nolan, T.M., Song, G., Liu, S., Xie, Z., Chen, J., Schnable, P.S., Walley, J.W., and Yin, Y. (2018). FERONIA receptor kinase contributes to plant immunity by suppressing jasmonic acid signaling in Arabidopsis thaliana. Curr. Biol. 28: 3316-3324.
Gust, A.A., Pruitt, R., and Nürnberger, T. (2017). Sensing danger: Key to activating plant immunity. Trends Plant Sci. 22: 779-791.
Hander, T., Fernández-Fernández, Á.D., Kumpf, R.P., Willems, P., Schatowitz, H., Rombaut, D., Staes, A., Nolf, J., Pottie, R., Yao, P., et al. (2019). Damage on plants activates Ca2+-dependent metacaspases for release of immunomodulatory peptides. Science 363: eaar7486.
Haruta, M., Sabat, G., Stecker, K., Minkoff, B.B., and Sussman, M.R. (2014). A peptide hormone and its receptor protein kinase regulate plant cell expansion. Science 343: 408-411.
Hou, S., Wang, X., Chen, D., Yang, X., Wang, M., Turrà, D., Di Pietro, A., and Zhang, W. (2014). The secreted peptide PIP1 amplifies immunity through Receptor-Like Kinase 7. PLoS Pathog. 10: e1004331.
Huffaker, A., Dafoe, N.J., and Schmelz, E.A. (2011). ZmPep1, an ortholog of Arabidopsis elicitor peptide 1, regulates maize innate immunity and enhances disease resistance. Plant Physiol. 155: 1325-1338.
Huffaker, A., Pearce, G., Veyrat, N., Erb, M., Turlings, T.C., Sartor, R., Shen, Z., Briggs, S.P., Vaughan, M.M., Alborn, H.T., et al. (2013). Plant elicitor peptides are conserved signals regulating direct and indirect antiherbivore defense. Proc. Natl. Acad. Sci. U.S.A 110: 5707-5712.
Hu, X.L., Lu, H., Hassan, M.M., Zhang, J., Yuan, G., Abraham, P.E., Shrestha, H.K., Villalobos, S.M., Chen, J.G., Tschaplinski, T.J., et al. (2021). Advances and perspectives in discovery and functional analysis of small secreted proteins in plants. Hortic. Res. 8: 130.
Klauser, D., Desurmont, G.A., Glauser, G., Vallat, A., Flury, P., Boller, T., Turlings, T.C., and Bartels, S. (2015). The Arabidopsis Pep-PEPR system is induced by herbivore feeding and contributes to JA-mediated plant defence against herbivory. J. Exp. Bot. 66: 5327-5336.
Li, C., Wu, H.M., and Cheung, A.Y. (2016). FERONIA and her pals: Functions and mechanisms. Plant Physiol. 171: 2379-2392.
Li, P., Zhao, L., Qi, F., Htwe, N.M.P.S., Li, Q., Zhang, D., Lin, F., Shang-Guan, K., and Liang, Y. (2021). The receptor-like cytoplasmic kinase RIPK regulates broad-spectrum ROS signaling in multiple layers of plant immune system. Mol. Plant 14: 1-16.
Liu, C., Shen, L., Xiao, Y., Vyshedsky, D., Peng, C., Sun, X., Liu, Z., Cheng, L., Zhang, H., Han, Z., et al. (2021). Pollen PCP-B peptides unlock a stigma peptide-receptor kinase gating mechanism for pollination. Science 372: 171-175.
Liu, F., Li, X., Wang, M., Wen, J., Yi, B., Shen, J., Ma, C., Fu, T., and Tu, J. (2018). Interactions of WRKY15 and WRKY33 transcription factors and their roles in the resistance of oilseed rape to Sclerotinia infection. Plant Biotechnol. J. 16: 911-925.
Logemann, E., Birkenbihl, R.P., Rawat, V., Schneeberger, K., Schmelzer, E., and Somssich, I.E. (2013). Functional dissection of the PROPEP2 and PROPEP3 promoters reveals the importance of WRKY factors in mediating microbe-associated molecular pattern-induced expression. New Phytol. 198: 1165-1177.
Mecchia, M.A., Santos-Fernandez, G., Duss, N.N., Somoza, S.C., Boisson-Dernier, A., Gagliardini, V., Martínez-Bernardini, A., Fabrice, T.N., Ringli, C., Muschietti, J.P., et al. (2017). RALF4/19 peptides interact with LRX proteins to control pollen tube growth in Arabidopsis. Science 358: 1600-1603.
Meng, X., and Zhang, S. (2013). MAPK cascades in plant disease resistance signaling. Annu. Rev. Phytopathol. 51: 245-266.
Merino, M.C., Guidarelli, M., Negrini, F., De Biase, D., Pession, A., and Baraldi, E. (2019). Induced expression of the Fragaria ×ananassa rapid alkalinization factor-33-like gene decreases anthracnose ontogenic resistance of unripe strawberry fruit stages. Mol. Plant Pathol. 20: 1252-1263.
Moussu, S., Broyart, C., Santos-Fernandez, G., Augustin, S., Wehrle, S., Grossniklaus, U., and Santiago, J. (2020). Structural basis for recognition of RALF peptides by LRX proteins during pollen tube growth. Proc. Natl. Acad. Sci. U.S.A 117: 7494-7503.
Pearce, G., Moura, D.S., Stratmann, J., and Ryan, C.A. (2001). RALF, a 5-kDa ubiquitous polypeptide in plants, arrests root growth and development. Proc. Natl. Acad. Sci. U.S.A 98: 12843-12847.
Pearce, G., Yamaguchi, Y., Munske, G., and Ryan, C.A. (2010). Structure-activity studies of RALF, rapid alkalinization factor, reveal an essential-YISY-motif. Peptides 31: 1973-1977.
Segonzac, C., and Monaghan, J. (2019). Modulation of plant innate immune signaling by small peptides. Curr. Opin. Plant Biol. 51: 22-28.
Bartels, S., and Boller, T. (2015). Quo vadis, Pep? Plant elicitor peptides at the crossroads of immunity, stress, and development. J. Exp. Bot. 66: 5183-5193.
Shang-Guan, K., Wang, M., Htwe, N.M.P.S., Li, P., Li, Y., Qi, F., Zhang, D., Cao, M., Kim, C., Weng, H., et al. (2018). Lipopolysaccharides trigger two successive bursts of reactive oxygen species at distinct cellular locations1. Plant Physiol. 176: 2543-2556.
Sharma, A., Hussain, A., Mun, B., Imran, Q.M., Falak, N., Lee, S., Kim, J.Y., Hong, J.K., Loake, G.J., Ali, A., et al. (2016). Comprehensive analysis of plant rapid alkalization factor (RALF) genes. Plant Physiol. Bioch. 106: 82-90.
Shen, W., Liu, J., and Li, J.F. (2019). Type-II metacaspases mediate the processing of plant elicitor peptides in Arabidopsis. Mol. Plant 12: 1524-1533.
Stegmann, M., Monaghan, J., Smakowska-Luzan, E., Rovenich, H., Lehner, A., Holton, N., Belkhadir, Y., and Zipfel, C. (2017). The receptor kinase FER is a RALF-regulated scaffold controlling plant immune signaling. Science 355: 287-289.
Tanaka, K., and Heil, M. (2021). Damage-associated molecular patterns (DAMPs) in plant innate immunity: Applying the danger model and evolutionary perspectives. Annu. Rev. Phytopathol. 59: 53-75.
Tang, D., Kang, R., Coyne, C.B., Zeh, H.J., and Lotze, M.T. (2012). PAMPs and DAMPs: Signal 0s that spur autophagy and immunity. Immunol. Rev. 249: 158-175.
Tang, D., Wang, G., and Zhou, J. (2017). Receptor kinases in plant-pathogen interactions: More than pattern recognition. Plant Cell 29: 618-637.
Tavormina, P., De Coninck, B., Nikonorova, N., De Smet, I., and Cammue, B.P.A. (2015). The plant peptidome: An expanding repertoire of structural features and biological functions. Plant Cell 27: 2095-2118.
Thynne, E., Saur, I.M.L., Simbaqueba, J., Ogilvie, H.A., Gonzalez-Cendales, Y., Mead, O., Taranto, A., Catanzariti, A., McDonald, M.C., Schwessinger, B., et al. (2017). Fungal phytopathogens encode functional homologues of plant rapid alkalinization factor (RALF) peptides. Mol. Plant Pathol. 18: 811-824.
Tintor, N., Ross, A., Kanehara, K., Yamada, K., Fan, L., Kemmerling, B., Nürnberger, T., Tsuda, K., and Saijo, Y. (2013). Layered pattern receptor signaling via ethylene and endogenous elicitor peptides during Arabidopsis immunity to bacterial infection. Proc. Natl. Acad. Sci. U.S.A 110: 6211-6216.
Wang, Z., Fang, H., Chen, Y., Chen, K., Li, G., Gu, S., and Tan, X. (2014). Overexpression of BnWRKY33 in oilseed rape enhances resistance to Sclerotinia sclerotiorum. Mol. Plant Pathol. 15: 677-689.
Xiao, Y., Stegmann, M., Han, Z., DeFalco, T.A., Parys, K., Xu, L., Belkhadir, Y., Zipfel, C., and Chai, J. (2019). Mechanisms of RALF peptide perception by a heterotypic receptor complex. Nature 572: 270-274.
Xu, H., Zhang, C., Li, Z., Wang, Z., Jiang, X., Shi, Y., Tian, S., Braun, E., Mei, Y., Qiu, W., et al. (2018). The MAPK kinase kinase GmMEKK1 regulates cell death and defense responses1. Plant Physiol. 178: 907-922.
Yamaguchi, K., and Kawasaki, T. (2021). Pathogen- and plant- derived peptides trigger plant immunity. Peptides 144: 170611.
Yuan, M., Ngou, B.P.M., Ding, P., and Xin, X. (2021). PTI-ETI crosstalk: An integrative view of plant immunity. Curr. Opin. Plant Biol. 62: 102030.
Zhang, X.R., Xu, Y.P., and Cai, X.Z. (2018). SlCNGC1 and SlCNGC14 suppress xanthomonas oryzae pv. oryzicola-induced hypersensitive response and non-host resistance in tomato. Front. Plant Sci. 9: 285.
Zhang, X., Peng, H., Zhu, S., Xing, J., Li, X., Zhu, Z., Zheng, J., Wang, L., Wang, B., Chen, J., et al. (2020). Nematode-encoded RALF peptide mimics facilitate parasitism of plants through the FERONIA receptor kinase. Mol. Plant 13: 1434-1454.
Zhao, C., Zayed, O., Yu, Z., Jiang, W., Zhu, P., Hsu, C., Zhang, L., Tao, W.A., Lozano-Durán, R., and Zhu, J. (2018). Leucine-rich repeat extensin proteins regulate plant salt tolerance in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A 115: 13123-13128.
Zipfel, C. (2014). Plant pattern-recognition receptors. Trends Immunol. 35: 345-351.