An ATPase Promotes Autophosphorylation of the Pattern Recognition Receptor XA21 and Inhibits XA21-mediated Immunity

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2010 Apr 14

PMID 20385831

Citations 46

Authors

Xuewei Chen

Mawsheng Chern

Patrick E Canlas

Deling Ruan

Caiying Jiang

Pamela C Ronald

Affiliations

Soon will be listed here.

Abstract

Cell-surface pattern recognition receptors (PRRs) are key components of the innate immune response in animals and plants. These receptors typically carry or associate with non-RD kinases to control early events of innate immunity signaling. Despite their importance, the mode of regulation of PRRs is largely unknown. Here we show that the rice PRR, XA21, interacts with XA21 binding protein 24 (XB24), a previously undescribed ATPase. XB24 promotes autophosphorylation of XA21 through its ATPase activity. Rice lines silenced for Xb24 display enhanced XA21-mediated immunity, whereas rice lines overexpressing XB24 are compromised for immunity. XB24 ATPase enzyme activity is required for XB24 function. XA21 is degraded in the presence of the pathogen-associated molecular pattern Ax21 when XB24 is overexpressed. These results demonstrate a function for this large class of broadly conserved ATPases in PRR-mediated immunity.

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References

Xu W, Wang Y, Liu G, Chen X, Tinjuangjun P, Pi L . The autophosphorylated Ser686, Thr688, and Ser689 residues in the intracellular juxtamembrane domain of XA21 are implicated in stability control of rice receptor-like kinase. Plant J. 2006; 45(5):740-51. DOI: 10.1111/j.1365-313X.2005.02638.x. View

Dardick C, Ronald P . Plant and animal pathogen recognition receptors signal through non-RD kinases. PLoS Pathog. 2006; 2(1):e2. PMC: 1331981. DOI: 10.1371/journal.ppat.0020002. View

Park C, Bart R, Chern M, Canlas P, Bai W, Ronald P . Overexpression of the endoplasmic reticulum chaperone BiP3 regulates XA21-mediated innate immunity in rice. PLoS One. 2010; 5(2):e9262. PMC: 2822859. DOI: 10.1371/journal.pone.0009262. View

Gomez-Gomez L, Boller T . FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol Cell. 2000; 5(6):1003-11. DOI: 10.1016/s1097-2765(00)80265-8. View

Vivanco I, Sawyers C . The phosphatidylinositol 3-Kinase AKT pathway in human cancer. Nat Rev Cancer. 2002; 2(7):489-501. DOI: 10.1038/nrc839. View

Bross P, Naundrup S, Hansen J, Nielsen M, Christensen J, Kruhoffer M . The Hsp60-(p.V98I) mutation associated with hereditary spastic paraplegia SPG13 compromises chaperonin function both in vitro and in vivo. J Biol Chem. 2008; 283(23):15694-700. PMC: 3259655. DOI: 10.1074/jbc.M800548200. View

Peng Y, Bartley L, Chen X, Dardick C, Chern M, Ruan R . OsWRKY62 is a negative regulator of basal and Xa21-mediated defense against Xanthomonas oryzae pv. oryzae in rice. Mol Plant. 2009; 1(3):446-58. DOI: 10.1093/mp/ssn024. View

Wang Y, Pi L, Chen X, Chakrabarty P, Jiang J, De Leon A . Rice XA21 binding protein 3 is a ubiquitin ligase required for full Xa21-mediated disease resistance. Plant Cell. 2006; 18(12):3635-46. PMC: 1785399. DOI: 10.1105/tpc.106.046730. View

Fire A, Xu S, Montgomery M, Kostas S, Driver S, Mello C . Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature. 1998; 391(6669):806-11. DOI: 10.1038/35888. View

10.

Zipfel C, Kunze G, Chinchilla D, Caniard A, Jones J, Boller T . Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell. 2006; 125(4):749-60. DOI: 10.1016/j.cell.2006.03.037. View

11.

Towb P, Sun H, Wasserman S . Tube Is an IRAK-4 homolog in a Toll pathway adapted for development and immunity. J Innate Immun. 2009; 1(4):309-21. PMC: 2690232. DOI: 10.1159/000200773. View

12.

Song W, Wang G, Chen L, Kim H, PI L, Holsten T . A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science. 1995; 270(5243):1804-6. DOI: 10.1126/science.270.5243.1804. View

13.

Jones J, Dangl J . The plant immune system. Nature. 2006; 444(7117):323-9. DOI: 10.1038/nature05286. View

14.

Zhai P, Stanworth C, Liu S, Silberg J . The human escort protein Hep binds to the ATPase domain of mitochondrial hsp70 and regulates ATP hydrolysis. J Biol Chem. 2008; 283(38):26098-106. PMC: 3258852. DOI: 10.1074/jbc.M803475200. View

15.

Ausubel F . Are innate immune signaling pathways in plants and animals conserved?. Nat Immunol. 2005; 6(10):973-9. DOI: 10.1038/ni1253. View

16.

Sun X, Cao Y, Yang Z, Xu C, Li X, Wang S . Xa26, a gene conferring resistance to Xanthomonas oryzae pv. oryzae in rice, encodes an LRR receptor kinase-like protein. Plant J. 2004; 37(4):517-27. DOI: 10.1046/j.1365-313x.2003.01976.x. View

17.

Robatzek S, Chinchilla D, Boller T . Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis. Genes Dev. 2006; 20(5):537-42. PMC: 1410809. DOI: 10.1101/gad.366506. View

18.

da Silva F, Shen Y, Dardick C, Burdman S, Yadav R, Lopez de Leon A . Bacterial genes involved in type I secretion and sulfation are required to elicit the rice Xa21-mediated innate immune response. Mol Plant Microbe Interact. 2004; 17(6):593-601. DOI: 10.1094/MPMI.2004.17.6.593. View

19.

Century K, Lagman R, Adkisson M, Morlan J, Tobias R, Schwartz K . Short communication: developmental control of Xa21-mediated disease resistance in rice. Plant J. 1999; 20(2):231-6. DOI: 10.1046/j.1365-313x.1999.00589.x. View

20.

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