A rice fungal MAMP‐responsive MAPK cascade regulates metabolic flow to antimicrobial metabolite synthesis

Abstract

Summary Plants recognize potential microbial pathogens through microbial‐associated molecular patterns (MAMPs) and activate a series of defense responses, including cell death and the production of reactive oxygen species (ROS) and diverse anti‐microbial secondary metabolites. Mitogen‐activated protein kinase (MAPK) cascades are known to play a pivotal role in mediating MAMP signals; however, the signaling pathway from a MAPK cascade to the activation of defense responses is poorly understood. Here, we found in rice that the chitin elicitor, a fungal MAMP, activates two rice MAPKs (OsMPK3 and OsMPK6) and one MAPK kinase (OsMKK4). OsMPK6 was essential for the chitin elicitor‐induced biosynthesis of diterpenoid phytoalexins. Conditional expression of the active form of OsMKK4 (OsMKK4 DD ) induced extensive alterations in gene expression, which implied dynamic changes of metabolic flow from glycolysis to secondary metabolite biosynthesis while suppressing basic cellular activities such as translation and cell division. OsMKK4 DD also induced various defense responses, such as cell death, biosynthesis of diterpenoid phytoalexins and lignin but not generation of extracellular ROS. OsMKK4 DD ‐induced cell death and expression of diterpenoid phytoalexin pathway genes, but not that of phenylpropanoid pathway genes, were dependent on OsMPK6. Collectively, the OsMKK4–OsMPK6 cascade plays a crucial role in reprogramming plant metabolism during MAMP‐triggered defense responses.

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References 70

1. 1.

   Andreasson E, Jenkins T, Brodersen P, et al. The MAP kinase substrate MKS1 is a regulator of plant defense responses. EMBO J. 2005;24:2579-2589.

   Not in our library10.1038/sj.emboj.7600737

2. 2.

   Asai T, Tena G, Plotnikova J, Willmann MR, Chiu WL, Gomez-Gomez L, Boller T, Ausubel FM, Sheen J. MAP kinase signalling cascade in Arabidopsis innate immunity. Nature. 2002;415:977-983.

   Not in our library10.1038/415977a

3. 3.

   Asai S, Ohta K, Yoshioka H. MAPK signaling regulates nitric oxide and NADPH oxidase-dependent oxidative bursts in Nicotiana benthamiana. Plant Cell. 2008;20:1390-1406.

   Not in our library10.1105/tpc.107.055855

4. 4.

   Ausubel FM. Are innate immune signaling pathways in plants and animals conserved? Nat. Immunol. 2005;6:973-979.

   Not in our library10.1038/ni1253

5. 5.

   Berger S, Papadopoulos M, Schreiber U, Kaiser W, Roitsch T. Complex regulation of gene expression, photosynthesis and sugar levels by pathogen infection in tomato. Physiol Plant. 2004;122:419-428.

   Not in our library

6. 6.

   Cai K, Gao D, Luo S, Zeng R, Yang J, Zhu X. Physiological and cytological mechanisms of silicon-induced resistance in rice against blast disease. Physiol Plant. 2008;134:324-333.

   Not in our library10.1111/j.1399-3054.2008.01140.x

7. 7.

   Campbell MM, Ellis BE. Fungal elicitor-mediated responses in pine cell cultures. I. Induction of phenylpropanoid metabolism. Planta. 1992;186:409-417.

   Not in our library10.1007/bf00195322

8. 8.

   Cartwright DW, Langcake P, Pryce RJ, Leworthy DP, Ride JP. Isolation and characterization of two phytoalexins from rice as momilactones A and B. Phytochemistry. 1981;20:535-537.

   Not in our library

9. 9.

   Chisholm ST, Coaker G, Day B, Staskawicz BJ. Host-microbe interactions: shaping the evolution of the plant immune response. Cell. 2006;124:803-814.

   Not in our library10.1016/j.cell.2006.02.008

10. 10.

    Desaki Y, Miya A, Venkatesh B, Tsuyumu S, Yamane H, Kaku H, Minami E, Shibuya N. Bacterial lipopolysaccharides induce defense responses associated with programmed cell death in rice cells. Plant Cell Physiol. 2006;47:1530-1540.

    Not in our library10.1093/pcp/pcl019

11. 11.

    Dixon RA. Natural products and plant disease resistance. Nature. 2001;411:843-847.

    Not in our library10.1038/35081178

12. 12.

    Ehness R, Ecker M, Godt DE, Roitsch T. Glucose and stress independently regulate source and sink metabolism and defense mechanisms via signal transduction pathways involving protein phosphorylation. Plant Cell. 1997;9:1825-1841.

    Not in our library10.1105/tpc.9.10.1825

13. 13.

    Essmann J, Schmitz-Thom I, Schon H, Sonnewald S, Weis E, Scharte J. RNA interference-mediated repression of cell wall invertase impairs defense in source leaves of tobacco. Plant Physiol. 2008;147:1288-1299.

    Not in our library10.1104/pp.108.121418

14. 14.

    Feilner T, Hultschig C, Lee J, et al. High throughput identification of potential Arabidopsis mitogen-activated protein kinases substrates. Mol. Cell Proteomics. 2005;4:1558-1568.

    Not in our library10.1074/mcp.m500007-mcp200

15. 15.

    Franke R, Hemm MR, Denault JW, Ruegger MO, Humphreys JM, Chapple C. Changes in secondary metabolism and deposition of an unusual lignin in the ref8 mutant of Arabidopsis. Plant J. 2002;30:47-59.

    Not in our library10.1046/j.1365-313x.2002.01267.x

16. 16.

    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;5:1003-1011.

    Not in our library10.1016/s1097-2765(00)80265-8

17. 17.

    Hamel LP, Nicole MC, Sritubtim S, et al. Ancient signals: comparative genomics of plant MAPK and MAPKK gene families. Trends Plant Sci. 2006;11:192-198.

    Not in our library10.1016/j.tplants.2006.02.007

18. 18.

    Hammerschmidt R. Phytoalexins: what have we learned after 60 years? Annu Rev Phytopathol. 1999;37:285-306.

    Not in our library10.1146/annurev.phyto.37.1.285

19. 19.

    Hano C, Addi M, Bensaddek L, et al. Differential accumulation of monolignol-derived compounds in elicited flax (Linum usitatissimum) cell suspension cultures. Planta. 2006;223:975-989.

    Not in our library10.1007/s00425-005-0156-1

20. 20.

    Ichimura K, Shinozaki K, Tena G, et al. Mitogen-activated protein kinase cascades in plants: a new nomenclature. Trends Plant Sci. 2002;7:301-308.

    Not in our library10.1016/s1360-1385(02)02302-6

21. 21.

    Ichinose Y, Andi S, Doi R, Tanaka R, Taguchi F, Sasabe M, Toyoda K, Shiraishi T, Yamada T. Generation of hydrogen peroxide is not required for harpin-induced apoptotic cell death in tobacco BY-2 cell suspension culture. Plant Physiol Biochem. 2001;39:771-776.

    Not in our library

22. 22.

    Ishihara A, Hashimoto Y, Tanaka C, Dubouzet JG, Nakao T, Matsuda F, Nishioka T, Miyagawa H, Wakasa K. The tryptophan pathway is involved in the defense responses of rice against pathogenic infection via serotonin production. Plant J. 2008;54:481-495.

    Not in our library10.1111/j.1365-313x.2008.03441.x

23. 23.

    Jones JD, Dangl JL. The plant immune system. Nature. 2006;444:323-329.

    Not in our library10.1038/nature05286

24. 24.

    Kaku H, Nishizawa Y, Ishii-Minami N, Akimoto-Tomiyama C, Dohmae N, Takio K, Minami E, Shibuya N. Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. Proc. Natl. Acad. Sci. USA. 2006;103:11086-11091.

    Not in our library10.1073/pnas.0508882103

25. 25.

    Kaneda T, Taga Y, Takai R, Iwano M, Matsui H, Takayama S, Isogai A, Che FS. The transcription factor OsNAC4 is a key positive regulator of plant hypersensitive cell death. EMBO J. 2009;28:926-936.

    Not in our library10.1038/emboj.2009.39

26. 26.

    Kanzaki H, Saitoh H, Takahashi Y, Berberich T, Ito A, Kamoun S, Terauchi R. NbLRK1, a lectin-like receptor kinase protein of Nicotiana benthamiana, interacts with Phytophthora infestans INF1 elicitin and mediates INF1-induced cell death. Planta. 2008;228:977-987.

    Not in our library10.1007/s00425-008-0797-y

27. 27.

    Kawasaki T, Koita H, Nakatsubo T, Hasegawa K, Wakabayashi K, Takahashi H, Umemura K, Umezawa T, Shimamoto K. Cinnamoyl-CoA reductase, a key enzyme in lignin biosynthesis, is an effector of small GTPase Rac in defense signaling in rice. Proc. Natl. Acad. Sci. USA. 2006;103:230-235.

    Not in our library10.1073/pnas.0509875103

28. 28.

    Kuchitsu K, Hosaka H, shiga T, Shibuya N. EPR evidence for generation of hydroxyl radical triggered byN-acetylchitooligosaccharide elicitor and a protein phosphatase inhibitor in suspension-cultured rice cells. Protoplasma. 1995;188:138-142.

    Not in our library

29. 29.

    Kurusu T, Yagala T, Miyao A, Hirochika H, Kuchitsu K. Identification of a putative voltage-gated Ca2+ channel as a key regulator of elicitor-induced hypersensitive cell death and mitogen-activated protein kinase activation in rice. Plant J. 2005;42:798-809.

    Not in our library10.1111/j.1365-313x.2005.02415.x

30. 30.

    Lamb C, Dixon RA. The oxidative burst in plant disease resistance. Annu Rev Plant Physiol Plant Mol Biol. 1997;48:251-275.

    Not in our library10.1146/annurev.arplant.48.1.251

31. 31.

    Lampard GR, Macalister CA, Bergmann DC. Arabidopsis stomatal initiation is controlled by MAPK-mediated regulation of the bHLH SPEECHLESS. Science. 2008;322:1113-1116.

    Not in our library10.1126/science.1162263

32. 32.

    Lange BM, Lapierre C, Sandermann H. Elicitor-induced spruce stress lignin (structural similarity to early developmental lignins). Plant Physiol. 1995;108:1277-1287.

    Not in our library10.1104/pp.108.3.1277

33. 33.

    Lichtenthaler HK, Schwender J, Disch A, Rohmer M. Biosynthesis of isoprenoids in higher plant chloroplasts proceeds via a mevalonate-independent pathway. FEBS Lett. 1997;400:271-274.

    Not in our library10.1016/s0014-5793(96)01404-4

34. 34.

    Lieberherr D, Thao NP, Nakashima A, Umemura K, Kawasaki T, Shimamoto K. A sphingolipid elicitor-inducible mitogen-activated protein kinase is regulated by the small GTPase OsRac1 and heterotrimeric G-protein in rice 1[w]. Plant Physiol. 2005;138:1644-1652.

    Not in our library10.1104/pp.104.057414

35. 35.

    Liu Y, Jin H, Yang KY, Kim CY, Baker B, Zhang S. Interaction between two mitogen-activated protein kinases during tobacco defense signaling. Plant J. 2003;34:149-160.

    Not in our library10.1046/j.1365-313x.2003.01709.x

36. 36.

    Liu Y, Ren D, Pike S, Pallardy S, Gassmann W, Zhang S. Chloroplast-generated reactive oxygen species are involved in hypersensitive response-like cell death mediated by a mitogen-activated protein kinase cascade. Plant J. 2007;51:941-954.

    Not in our library10.1111/j.1365-313x.2007.03191.x

37. 37.

    Menden B, Kohlhoff M, Moerschbacher BM. Wheat cells accumulate a syringyl-rich lignin during the hypersensitive resistance response. Phytochemistry. 2007;68:513-520.

    Not in our library10.1016/j.phytochem.2006.11.011

38. 38.

    Menke FL, Kang HG, Chen Z, Park JM, Kumar D, Klessig DF. Tobacco transcription factor WRKY1 is phosphorylated by the MAP kinase SIPK and mediates HR-like cell death in tobacco. Mol. Plant Microbe Interact. 2005;18:1027-1034.

    Not in our library10.1094/mpmi-18-1027

39. 39.

    Miya A, Albert P, Shinya T, Desaki Y, Ichimura K, Shirasu K, Narusaka Y, Kawakami N, Kaku H, Shibuya N. CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc. Natl. Acad. Sci. USA. 2007;104:19613-19618.

    Not in our library10.1073/pnas.0705147104

40. 40.

    Moerschbacher BM, Noll U, Gorrichon L, Reisener HJ. Specific inhibition of lignification breaks hypersensitive resistance of wheat to stem rust. Plant Physiol. 1990;93:465-470.

    Not in our library10.1104/pp.93.2.465

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