Rice NLR Protein XinN1, Induced by a Pattern Recognition Receptor XA21, Confers Enhanced Resistance to Bacterial Blight

Overview

Journal Plant Cell Rep

Publisher Springer

Date 2024 Feb 20

PMID 38376569

Authors

Hyeran Moon

A-Ram Jeong

Chang-Jin Park

Affiliations

Soon will be listed here.

Abstract

Rice CC-type NLR XinN1, specifically induced by a PRR XA21, activates defense pathways against Xoo. Plants have evolved two layers of immune systems regulated by two different types of immune receptors, cell surface located pattern recognition receptors (PRRs) and intracellular nucleotide-binding domain leucine-rich repeat-containing receptors (NLRs). Plant PRRs recognize conserved molecular patterns from diverse pathogens, resulting in pattern-triggered immunity (PTI), whereas NLRs are activated by effectors secreted by pathogens into plant cells, inducing effector-triggered immunity (ETI). Rice PRR, XA21, recognizes a tyrosine-sulfated RaxX peptide (required for activation of XA21-mediated immunity X) as a molecular pattern secreted by Xanthomonas oryzae pv. oryzae (Xoo). Here, we identified a rice NLR gene, XinN1, that is specifically induced during the XA21-mediated immune response against Xoo. Transgenic rice plants overexpressing XinN1 displayed increased resistance to infection by Xoo with reduced lesion length and bacterial growth. Overexpression of autoactive mutant of XinN1 (XinN1) also displayed increased resistance to Xoo, accompanied with severe growth retardation and cell death. In rice protoplast system, overexpression of XinN1 or XinN1 significantly elevated reactive oxygen species (ROS) production and cytosolic-free calcium (Ca) accumulations. In addition, XinN1 overexpression additionally elevated the ROS burst caused by the interaction between XA21 and RaxX-sY and induced the transcription of PTI signaling components, including somatic embryogenesis receptor kinases (OsSERKs) and receptor-like cytoplasmic kinases (OsRLCKs). Our results suggest that XinN1 induced by the PRR XA21 activates defense pathways and provides enhanced resistance to Xoo in rice.

Citing Articles

Rice E3 ubiquitin ligases: From key modulators of host immunity to potential breeding applications.

Yan Y, Wang H, Bi Y, Song F Plant Commun. 2024; 5(12):101128.

PMID: 39245936 PMC: 11671762. DOI: 10.1016/j.xplc.2024.101128.

References

Bai S, Liu J, Chang C, Zhang L, Maekawa T, Wang Q . Structure-function analysis of barley NLR immune receptor MLA10 reveals its cell compartment specific activity in cell death and disease resistance. PLoS Pathog. 2012; 8(6):e1002752. PMC: 3369952. DOI: 10.1371/journal.ppat.1002752. View

Bari R, Jones J . Role of plant hormones in plant defence responses. Plant Mol Biol. 2008; 69(4):473-88. DOI: 10.1007/s11103-008-9435-0. View

Bart R, Chern M, Park C, Bartley L, Ronald P . A novel system for gene silencing using siRNAs in rice leaf and stem-derived protoplasts. Plant Methods. 2006; 2:13. PMC: 1524957. DOI: 10.1186/1746-4811-2-13. View

Bendahmane A, Farnham G, Moffett P, Baulcombe D . Constitutive gain-of-function mutants in a nucleotide binding site-leucine rich repeat protein encoded at the Rx locus of potato. Plant J. 2002; 32(2):195-204. DOI: 10.1046/j.1365-313x.2002.01413.x. View

Bi G, Su M, Li N, Liang Y, Dang S, Xu J . The ZAR1 resistosome is a calcium-permeable channel triggering plant immune signaling. Cell. 2021; 184(13):3528-3541.e12. DOI: 10.1016/j.cell.2021.05.003. View

Bjornson M, Pimprikar P, Nurnberger T, Zipfel C . The transcriptional landscape of Arabidopsis thaliana pattern-triggered immunity. Nat Plants. 2021; 7(5):579-586. PMC: 7610817. DOI: 10.1038/s41477-021-00874-5. View

Boller T, He S . Innate immunity in plants: an arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science. 2009; 324(5928):742-4. PMC: 2729760. DOI: 10.1126/science.1171647. View

Bolus S, Akhunov E, Coaker G, Dubcovsky J . Dissection of Cell Death Induction by Wheat Stem Rust Resistance Protein Sr35 and Its Matching Effector AvrSr35. Mol Plant Microbe Interact. 2019; 33(2):308-319. PMC: 7309591. DOI: 10.1094/MPMI-08-19-0216-R. View

Bradford M . A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976; 72:248-54. DOI: 10.1016/0003-2697(76)90527-3. View

10.

Burger M, Chory J . Stressed Out About Hormones: How Plants Orchestrate Immunity. Cell Host Microbe. 2019; 26(2):163-172. PMC: 7228804. DOI: 10.1016/j.chom.2019.07.006. View

11.

Chang M, Chen H, Liu F, Fu Z . PTI and ETI: convergent pathways with diverse elicitors. Trends Plant Sci. 2021; 27(2):113-115. DOI: 10.1016/j.tplants.2021.11.013. View

12.

Chern M, Fitzgerald H, Yadav R, Canlas P, Dong X, Ronald P . Evidence for a disease-resistance pathway in rice similar to the NPR1-mediated signaling pathway in Arabidopsis. Plant J. 2001; 27(2):101-13. DOI: 10.1046/j.1365-313x.2001.01070.x. View

13.

Chern M, Canlas P, Fitzgerald H, Ronald P . Rice NRR, a negative regulator of disease resistance, interacts with Arabidopsis NPR1 and rice NH1. Plant J. 2005; 43(5):623-35. DOI: 10.1111/j.1365-313X.2005.02485.x. View

14.

Chisholm S, Coaker G, Day B, Staskawicz B . Host-microbe interactions: shaping the evolution of the plant immune response. Cell. 2006; 124(4):803-14. DOI: 10.1016/j.cell.2006.02.008. View

15.

Choi H, Kim D, Kim N, Jung H, Ham J, Hwang B . Xanthomonas filamentous hemagglutinin-like protein Fha1 interacts with pepper hypersensitive-induced reaction protein CaHIR1 and functions as a virulence factor in host plants. Mol Plant Microbe Interact. 2013; 26(12):1441-54. DOI: 10.1094/MPMI-07-13-0204-R. View

16.

Collier S, Moffett P . NB-LRRs work a "bait and switch" on pathogens. Trends Plant Sci. 2009; 14(10):521-9. DOI: 10.1016/j.tplants.2009.08.001. View

17.

Derevnina L, Contreras M, Adachi H, Upson J, Cruces A, Xie R . Plant pathogens convergently evolved to counteract redundant nodes of an NLR immune receptor network. PLoS Biol. 2021; 19(8):e3001136. PMC: 8412950. DOI: 10.1371/journal.pbio.3001136. View

18.

Ding P, Ngou B, Furzer O, Sakai T, Shrestha R, MacLean D . High-resolution expression profiling of selected gene sets during plant immune activation. Plant Biotechnol J. 2020; 18(7):1610-1619. PMC: 7292544. DOI: 10.1111/pbi.13327. View

19.

Ding P, Sakai T, Shrestha R, Manosalva Perez N, Guo W, Ngou B . Chromatin accessibility landscapes activated by cell-surface and intracellular immune receptors. J Exp Bot. 2021; 72(22):7927-7941. DOI: 10.1093/jxb/erab373. View

20.

Du X, Miao M, Ma X, Liu Y, Kuhl J, Martin G . Plant programmed cell death caused by an autoactive form of Prf is suppressed by co-expression of the Prf LRR domain. Mol Plant. 2012; 5(5):1058-67. DOI: 10.1093/mp/sss014. View