Arabidopsis MAPKKK δ-1 is Required for Full Immunity Against Bacterial and Fungal Infection

Overview

Journal J Exp Bot

Publisher Oxford University Press

Specialty Biology

Date 2019 Dec 18

PMID 31844896

Citations 13

Authors

Tomoya Asano

Thi Hang-Ni Nguyen

Michiko Yasuda

Yasir Sidiq

Kohji Nishimura

Hideo Nakashita

Takumi Nishiuchi

Affiliations

Soon will be listed here.

Abstract

The genome of Arabidopsis encodes more than 60 mitogen-activated protein kinase kinase (MAPKK) kinases (MAPKKKs); however, the functions of most MAPKKKs and their downstream MAPKKs are largely unknown. Here, MAPKKK δ-1 (MKD1), a novel Raf-like MAPKKK, was isolated from Arabidopsis as a subunit of a complex including the transcription factor AtNFXL1, which is involved in the trichothecene phytotoxin response and in disease resistance against the bacterial pathogen Pseudomonas syringae pv. tomato DC3000 (PstDC3000). A MKD1-dependent cascade positively regulates disease resistance against PstDC3000 and the trichothecene mycotoxin-producing fungal pathogen Fusarium sporotrichioides. MKD1 expression was induced by trichothecenes derived from Fusarium species. MKD1 directly interacted with MKK1 and MKK5 in vivo, and phosphorylated MKK1 and MKK5 in vitro. Correspondingly, mkk1 mutants and MKK5RNAi transgenic plants showed enhanced susceptibility to F. sporotrichioides. MKD1 was required for full activation of two MAPKs (MPK3 and MPK6) by the T-2 toxin and flg22. Finally, quantitative phosphoproteomics suggested that an MKD1-dependent cascade controlled phosphorylation of a disease resistance protein, SUMO, and a mycotoxin-detoxifying enzyme. Our findings suggest that the MKD1-MKK1/MKK5-MPK3/MPK6-dependent signaling cascade is involved in the full immune responses against both bacterial and fungal infection.

Citing Articles

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References

Doczi R, Brader G, Pettko-Szandtner A, Rajh I, Djamei A, Pitzschke A . The Arabidopsis mitogen-activated protein kinase kinase MKK3 is upstream of group C mitogen-activated protein kinases and participates in pathogen signaling. Plant Cell. 2007; 19(10):3266-79. PMC: 2174707. DOI: 10.1105/tpc.106.050039. View

Yasuda M, Nakashita H, Hasegawa S, Nishioka M, Arai Y, Uramoto M . N-cyanomethyl-2-chloroisonicotinamide induces systemic acquired resistance in arabidopsis without salicylic acid accumulation. Biosci Biotechnol Biochem. 2003; 67(2):322-8. DOI: 10.1271/bbb.67.322. View

Shilov I, Seymour S, Patel A, Loboda A, Tang W, Keating S . The Paragon Algorithm, a next generation search engine that uses sequence temperature values and feature probabilities to identify peptides from tandem mass spectra. Mol Cell Proteomics. 2007; 6(9):1638-55. DOI: 10.1074/mcp.T600050-MCP200. View

Rao K, Richa T, Kumar K, Raghuram B, Sinha A . In silico analysis reveals 75 members of mitogen-activated protein kinase kinase kinase gene family in rice. DNA Res. 2010; 17(3):139-53. PMC: 2885274. DOI: 10.1093/dnares/dsq011. View

Samaj J, Baluska F, Hirt H . From signal to cell polarity: mitogen-activated protein kinases as sensors and effectors of cytoskeleton dynamicity. J Exp Bot. 2003; 55(395):189-98. DOI: 10.1093/jxb/erh012. View

Mollapour M, Neckers L . Post-translational modifications of Hsp90 and their contributions to chaperone regulation. Biochim Biophys Acta. 2011; 1823(3):648-55. PMC: 3226900. DOI: 10.1016/j.bbamcr.2011.07.018. View

. Mitogen-activated protein kinase cascades in plants: a new nomenclature. Trends Plant Sci. 2002; 7(7):301-8. DOI: 10.1016/s1360-1385(02)02302-6. View

Matsuoka D, Nanmori T, Sato K, Fukami Y, Kikkawa U, Yasuda T . Activation of AtMEK1, an Arabidopsis mitogen-activated protein kinase kinase, in vitro and in vivo: analysis of active mutants expressed in E. coli and generation of the active form in stress response in seedlings. Plant J. 2002; 29(5):637-47. DOI: 10.1046/j.0960-7412.2001.01246.x. View

Gu Y, Innes R . The KEEP ON GOING protein of Arabidopsis recruits the ENHANCED DISEASE RESISTANCE1 protein to trans-Golgi network/early endosome vesicles. Plant Physiol. 2011; 155(4):1827-38. PMC: 3091131. DOI: 10.1104/pp.110.171785. View

10.

Meszaros T, Helfer A, Hatzimasoura E, Magyar Z, Serazetdinova L, Rios G . The Arabidopsis MAP kinase kinase MKK1 participates in defence responses to the bacterial elicitor flagellin. Plant J. 2006; 48(4):485-98. DOI: 10.1111/j.1365-313X.2006.02888.x. View

11.

Choi H, Lee D, Hwang B . The pepper calmodulin gene CaCaM1 is involved in reactive oxygen species and nitric oxide generation required for cell death and the defense response. Mol Plant Microbe Interact. 2009; 22(11):1389-400. DOI: 10.1094/MPMI-22-11-1389. View

12.

Kieber J, Rothenberg M, Roman G, Feldmann K, Ecker J . CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the raf family of protein kinases. Cell. 1993; 72(3):427-41. DOI: 10.1016/0092-8674(93)90119-b. View

13.

Koizumi K, Sugiyama M, Fukuda H . A series of novel mutants of Arabidopsis thaliana that are defective in the formation of continuous vascular network: calling the auxin signal flow canalization hypothesis into question. Development. 2000; 127(15):3197-204. DOI: 10.1242/dev.127.15.3197. View

14.

Gardiner S, Boddu J, Berthiller F, Hametner C, Stupar R, Adam G . Transcriptome analysis of the barley-deoxynivalenol interaction: evidence for a role of glutathione in deoxynivalenol detoxification. Mol Plant Microbe Interact. 2010; 23(7):962-76. DOI: 10.1094/MPMI-23-7-0962. View

15.

Penninckx I, Thomma B, Buchala A, Metraux J, Broekaert W . Concomitant activation of jasmonate and ethylene response pathways is required for induction of a plant defensin gene in Arabidopsis. Plant Cell. 1998; 10(12):2103-13. PMC: 143966. DOI: 10.1105/tpc.10.12.2103. View

16.

Frye C, Innes R . An Arabidopsis mutant with enhanced resistance to powdery mildew. Plant Cell. 1998; 10(6):947-56. PMC: 144036. DOI: 10.1105/tpc.10.6.947. View

17.

Kawasaki T, Yamada K, Yoshimura S, Yamaguchi K . Chitin receptor-mediated activation of MAP kinases and ROS production in rice and Arabidopsis. Plant Signal Behav. 2017; 12(9):e1361076. PMC: 5640189. DOI: 10.1080/15592324.2017.1361076. View

18.

Frye C, Tang D, Innes R . Negative regulation of defense responses in plants by a conserved MAPKK kinase. Proc Natl Acad Sci U S A. 2000; 98(1):373-8. PMC: 14597. DOI: 10.1073/pnas.98.1.373. View

19.

Hanano S, Goto K . Arabidopsis TERMINAL FLOWER1 is involved in the regulation of flowering time and inflorescence development through transcriptional repression. Plant Cell. 2011; 23(9):3172-84. PMC: 3203435. DOI: 10.1105/tpc.111.088641. View

20.

Menke F, van Pelt J, Pieterse C, Klessig D . Silencing of the mitogen-activated protein kinase MPK6 compromises disease resistance in Arabidopsis. Plant Cell. 2004; 16(4):897-907. PMC: 412864. DOI: 10.1105/tpc.015552. View