The OsBDR1-MPK3 Module Negatively Regulates Blast Resistance by Suppressing the Jasmonate Signaling and Terpenoid Biosynthesis Pathway

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2023 Mar 23

PMID 36952381

Authors

Lanlan Wang

Guojuan Xu

Lihua Li

Meiying Ruan

Anne Bennion

Guo-Liang Wang

Ran Li

Shaohong Qu

Affiliations

Soon will be listed here.

Abstract

Receptor-like kinases (RLKs) may initiate signaling pathways by perceiving and transmitting environmental signals to cellular machinery and play diverse roles in plant development and stress responses. The rice genome encodes more than one thousand RLKs, but only a small number have been characterized as receptors for phytohormones, polypeptides, elicitors, and effectors. Here, we screened the function of 11 RLKs in rice resistance to the blast fungus () and identified a negative regulator named BDR1 (Blast Disease Resistance 1). The expression of was rapidly increased under infection, while silencing or knockout of significantly enhanced resistance in two rice varieties. Protein interaction and kinase activity assays indicated that BDR1 directly interacted with and phosphorylated mitogen-activated kinase 3 (MPK3). Knockout of compromised -induced MPK3 phosphorylation levels. Moreover, transcriptome analysis revealed that -elicited jasmonate (JA) signaling and terpenoid biosynthesis pathway were negatively regulated by BDR1 and MPK3. Mutation of JA biosynthetic ( ()/signaling () genes decreased rice resistance to Besides diterpenoid, the monoterpene linalool and the sesquiterpene caryophyllene were identified as unique defensive compounds against , and their biosynthesis genes ( and ) were transcriptionally regulated by JA signaling and suppressed by BDR1 and MPK3. These findings demonstrate the existence of a BDR1-MPK3 cascade that negatively mediates rice blast resistance by affecting JA-related defense responses.

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References

Seo S, Katou S, Seto H, Gomi K, Ohashi Y . The mitogen-activated protein kinases WIPK and SIPK regulate the levels of jasmonic and salicylic acids in wounded tobacco plants. Plant J. 2007; 49(5):899-909. DOI: 10.1111/j.1365-313X.2006.03003.x. View

Yoshitomi K, Taniguchi S, Tanaka K, Uji Y, Akimitsu K, Gomi K . Rice terpene synthase 24 (OsTPS24) encodes a jasmonate-responsive monoterpene synthase that produces an antibacterial γ-terpinene against rice pathogen. J Plant Physiol. 2016; 191:120-6. DOI: 10.1016/j.jplph.2015.12.008. View

Nasir F, Tian L, Chang C, Li X, Gao Y, Tran L . Current understanding of pattern-triggered immunity and hormone-mediated defense in rice (Oryza sativa) in response to Magnaporthe oryzae infection. Semin Cell Dev Biol. 2017; 83:95-105. DOI: 10.1016/j.semcdb.2017.10.020. View

Shiu S, Karlowski W, Pan R, Tzeng Y, Mayer K, Li W . Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. Plant Cell. 2004; 16(5):1220-34. PMC: 423211. DOI: 10.1105/tpc.020834. View

Browse J . Jasmonate passes muster: a receptor and targets for the defense hormone. Annu Rev Plant Biol. 2008; 60:183-205. DOI: 10.1146/annurev.arplant.043008.092007. View

Zhou X, Liao H, Chern M, Yin J, Chen Y, Wang J . Loss of function of a rice TPR-domain RNA-binding protein confers broad-spectrum disease resistance. Proc Natl Acad Sci U S A. 2018; 115(12):3174-3179. PMC: 5866533. DOI: 10.1073/pnas.1705927115. View

Moon H, Lee B, Choi G, Shin D, Prasad D, Lee O . NDP kinase 2 interacts with two oxidative stress-activated MAPKs to regulate cellular redox state and enhances multiple stress tolerance in transgenic plants. Proc Natl Acad Sci U S A. 2002; 100(1):358-63. PMC: 140977. DOI: 10.1073/pnas.252641899. View

Takahashi F, Yoshida R, Ichimura K, Mizoguchi T, Seo S, Yonezawa M . The mitogen-activated protein kinase cascade MKK3-MPK6 is an important part of the jasmonate signal transduction pathway in Arabidopsis. Plant Cell. 2007; 19(3):805-18. PMC: 1867372. DOI: 10.1105/tpc.106.046581. View

Wang C, Wang G, Zhang C, Zhu P, Dai H, Yu N . OsCERK1-Mediated Chitin Perception and Immune Signaling Requires Receptor-like Cytoplasmic Kinase 185 to Activate an MAPK Cascade in Rice. Mol Plant. 2017; 10(4):619-633. DOI: 10.1016/j.molp.2017.01.006. View

10.

Dangl J, Horvath D, Staskawicz B . Pivoting the plant immune system from dissection to deployment. Science. 2013; 341(6147):746-51. PMC: 3869199. DOI: 10.1126/science.1236011. View

11.

Inoue Y, Sakai M, Yao Q, Tanimoto Y, Toshima H, Hasegawa M . Identification of a novel casbane-type diterpene phytoalexin, ent-10-oxodepressin, from rice leaves. Biosci Biotechnol Biochem. 2013; 77(4):760-5. DOI: 10.1271/bbb.120891. View

12.

Taniguchi S, Miyoshi S, Tamaoki D, Yamada S, Tanaka K, Uji Y . Isolation of jasmonate-induced sesquiterpene synthase of rice: product of which has an antifungal activity against Magnaporthe oryzae. J Plant Physiol. 2014; 171(8):625-32. DOI: 10.1016/j.jplph.2014.01.007. View

13.

Liu W, Liu J, Ning Y, Ding B, Wang X, Wang Z . Recent progress in understanding PAMP- and effector-triggered immunity against the rice blast fungus Magnaporthe oryzae. Mol Plant. 2013; 6(3):605-20. DOI: 10.1093/mp/sst015. View

14.

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

15.

Li R, Wang M, Wang Y, Schuman M, Weinhold A, Schafer M . Flower-specific jasmonate signaling regulates constitutive floral defenses in wild tobacco. Proc Natl Acad Sci U S A. 2017; 114(34):E7205-E7214. PMC: 5576791. DOI: 10.1073/pnas.1703463114. View

16.

Huang M, Sanchez-Moreiras A, Abel C, Sohrabi R, Lee S, Gershenzon J . The major volatile organic compound emitted from Arabidopsis thaliana flowers, the sesquiterpene (E)-β-caryophyllene, is a defense against a bacterial pathogen. New Phytol. 2011; 193(4):997-1008. DOI: 10.1111/j.1469-8137.2011.04001.x. View

17.

Li C, Wang G, Zhao J, Zhang L, Ai L, Han Y . The Receptor-Like Kinase SIT1 Mediates Salt Sensitivity by Activating MAPK3/6 and Regulating Ethylene Homeostasis in Rice. Plant Cell. 2014; 26(6):2538-2553. PMC: 4114950. DOI: 10.1105/tpc.114.125187. View

18.

Fisher M, Henk D, Briggs C, Brownstein J, Madoff L, McCraw S . Emerging fungal threats to animal, plant and ecosystem health. Nature. 2012; 484(7393):186-94. PMC: 3821985. DOI: 10.1038/nature10947. View

19.

Taniguchi S, Hosokawa-Shinonaga Y, Tamaoki D, Yamada S, Akimitsu K, Gomi K . Jasmonate induction of the monoterpene linalool confers resistance to rice bacterial blight and its biosynthesis is regulated by JAZ protein in rice. Plant Cell Environ. 2013; 37(2):451-61. DOI: 10.1111/pce.12169. View

20.

Kaku H, Nishizawa Y, Ishii-Minami N, Akimoto-Tomiyama C, Dohmae N, Takio K . Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. Proc Natl Acad Sci U S A. 2006; 103(29):11086-91. PMC: 1636686. DOI: 10.1073/pnas.0508882103. View