MAPK signaling: A key element in plant defense response to insects

Insect Science

Volumn 22, Issue 2, 2015, Pages 157-164

  Hettenhausen, Christian ^a   Schuman, Meredith C ^b   Wu, Jianqiang ^a  

^a KUNMING INSTITUTE OF BOTANY   (China)

^b MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

Author keywords

Defense; FAC; Insect; Jasmonate; Mitogen activated protein kinase (MAPK); Plant insect interaction

Indexed keywords

EUKARYOTA; HEXAPODA;

MITOGEN ACTIVATED PROTEIN KINASE; PHYTOHORMONE;

ANIMAL; HERBIVORY; HOST PARASITE INTERACTION; INSECT; METABOLISM; PARASITOLOGY; PHYSIOLOGY; PLANT; PLANT PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; HERBIVORY; HOST-PARASITE INTERACTIONS; INSECTS; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASES; PLANT GROWTH REGULATORS; PLANT PHYSIOLOGICAL PHENOMENA; PLANTS;

EID: 84925348180     PISSN: 16729609     EISSN: 17447917     Source Type: Journal    
DOI: 10.1111/1744-7917.12128     Document Type: Review

References (66)

1. Alborn, H.T., Hansen, T.V., Jones, T.H., Bennett, D.C., Tumlinson, J.H., Schmelz, E.A. and Teal, P.E. (2007) Disulfooxy fatty acids from the American bird grasshopper Schistocerca americana, elicitors of plant volatiles. Proceedings of National Academy of Sciences of the United States of America, 104, 12976-12981.
2. Alborn, T., Turlings, T.C.J., Jones, T.H., Stenhagen, G., Loughrin, J.H. and Tumlinson, J.H. (1997) An elicitor of plant volatiles from beet armyworm oral secretion. Science, 276, 945-949.
3. Andreasson, E., Jenkins, T., Brodersen, P., Thorgrimsen, S., Petersen, N.H., Zhu, S., Qiu, J.L., Micheelsen, P., Rocher, A., Petersen, M., Newman, M.A., Bjorn Nielsen, H., Hirt, H., Somssich, I., Mattsson, O. and Mundy, J. (2005) The MAP kinase substrate MKS1 is a regulator of plant defense responses. EMBO Journal, 24, 2579-2589.
4. Asai, T., Tena, G., Plotnikova, J., Willmann, M.R., Chiu, W.L., Gomez-Gomez, L., Boller, T., Ausubel, F.M. and Sheen, J. (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature, 415, 977-983.
5. Boller, T. and Felix, G. (2009) A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annual Review of Plant Biology, 60, 379-406.
6. Bonaventure, G., van Doorn, A. and Baldwin, I. T. (2011) Herbivore-associated elicitors: FAC signaling and metabolism. Trends in Plant Science, 16, 294-299.
7. Chang, L. and Karin, M. (2001) Mammalian MAP kinase signalling cascades. Nature, 410, 37-40.
8. Gao, M., Liu, J., Bi, D., Zhang, Z., Cheng, F., Chen, S. and Zhang, Y. (2008) MEKK1, MKK1/MKK2 and MPK4 function together in a mitogen-activated protein kinase cascade to regulate innate immunity in plants. Cell Research, 18, 1190-1198.
9. Gatehouse, J.A. (2002) Plant resistance towards insect herbivores: a dynamic interaction. New Phytologist, 156, 145-169.
10. Gilardoni, P.A., Hettenhausen, C., Baldwin, I.T. and Bonaventure, G. (2011) Nicotiana attenuata LECTIN RECEPTOR KINASE1 suppresses the insect-mediated inhibition of induced defense responses during Manduca sexta herbivory. Plant Cell, 23, 3512-3532.
11. Gomi, K., Ogawa, D., Katou, S., Kamada, H., Nakajima, N., Saji, H., Soyano, T., Sasabe, M., Machida, Y., Mitsuhara, I., Ohashi, Y. and Seo, S. (2005) A mitogen-activated protein kinase NtMPK4 activated by SIPKK is required for jasmonic acid signaling and involved in ozone tolerance via stomatal movement in tobacco. Plant Cell Physiology, 46, 1902-1914.
12. Green, T.R. and Ryan, C.A. (1972) Wound-induced proteinase inhibitor in plant leaves - possible defense mechanism against insects. Science, 175, 776-777.
13. Halitschke, R., Gase, K., Hui, D., Schmidt, D.D. and Baldwin, I.T. (2003) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. VI. Microarray analysis reveals that most herbivore-specific transcriptional changes are mediated by fatty acid-amino acid conjugates. Plant Physiology, 131, 1894-1902.
14. Halitschke, R., Schittko, U., Pohnert, G., Boland, W. and Baldwin, I.T. (2001) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. III. Fatty acid-amino acid conjugates in herbivore oral secretions are necessary and sufficient for herbivore-specific plant responses. Plant Physiology, 125, 711-717.
15. Hamel, L.P., Nicole, M.C., Sritubtim, S., Morency, M.J., Ellis, M., Ehlting, J., Beaudoin, N., Barbazuk, B., Klessig, D., Lee, J., Martin, G., Mundy, J., Ohashi, Y., Scheel, D., Sheen, J., Xing, T., Zhang, S., Seguin, A. and Ellis, B.E. (2006) Ancient signals: comparative genomics of plant MAPK and MAPKK gene families. Trends in Plant Science, 11, 192-198.
16. Hanks, S.K., Quinn, A.M. and Hunter, T. (1988) The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science, 241, 42-52.
17. Hazzalin, C.A. and Mahadevan, L.C. (2002) MAPK-regulated transcription: a continuously variable gene switch? Nature Reviews Molecular Cell Biology, 3, 30-40.
18. Heinrich, M., Baldwin, I.T. and Wu, J. (2011a) Three MAPK kinases, MEK1, SIPKK, and NPK2, are not involved in activation of SIPK after wounding and herbivore feeding but important for accumulation of trypsin proteinase inhibitors. Plant Molecular Biology Reporter, 30, 731-740.
19. Heinrich, M., Baldwin, I.T. and Wu, J. (2011b) Two mitogen-activated protein kinase kinases, MKK1 and MEK2, are involved in wounding- and specialist lepidopteran herbivore Manduca sexta-induced responses in Nicotiana attenuata. Journal of Experimental Botany, 62, 4355-4365.
20. Herskowitz, I. (1995) MAP kinase pathways in yeast: for mating and more. Cell, 80, 187-197.
21. Hettenhausen, C., Baldwin, I. and Wu, J. (2012) Silencing MPK4 in Nicotiana attenuata enhances photosynthesis and seed production but compromises abscisic acid-induced stomatal closure and guard cell-mediated resistance to Pseudomonas syringae pv. tomato DC3000. Plant Physiology, 158, 759-776.
22. Hettenhausen, C., Baldwin, I.T. and Wu, J. (2013a) Nicotiana attenuata MPK4 suppresses a novel jasmonic acid (JA) signaling-independent defense pathway against the specialist insect Manduca sexta, but is not required for the resistance to the generalist Spodoptera littoralis. New Phytologist, 199, 787-799.
23. Hettenhausen, C., Yang, D.H., Baldwin, I.T. and Wu, J. (2013b) Calcium-dependent protein kinases, CDPK4 and CDPK5, affect early steps of jasmonic acid biosynthesis in Nicotiana attenuata. Plant Signaling & Behavior, 8: e22784.
24. Howe, G.A. and Jander, G. (2008) Plant immunity to insect herbivores. Annual Review of Plant Biology, 59, 41-66.
25. Ichimura, K., Mizoguchi, T., Yoshida, R., Yuasa, T. and Shinozaki, K. (2000) Various abiotic stresses rapidly activate Arabidopsis MAP kinases ATMPK4 and ATMPK6. Plant Journal, 24, 655-665.
26. Kallenbach, M., Alagna, F., Baldwin, I.T. and Bonaventure, G. (2010) Nicotiana attenuata SIPK, WIPK, NPR1, and fatty acid-amino acid conjugates participate in the induction of jasmonic acid biosynthesis by affecting early enzymatic steps in the pathway. Plant Physiology, 152, 96-106.
27. Kandoth, P.K., Ranf, S., Pancholi, S.S., Jayanty, S., Walla, M.D., Miller, W., Howe, G.A., Lincoln, D.E. and Stratmann, J.W. (2007) Tomato MAPKs LeMPK1, LeMPK2, and LeMPK3 function in the systemin-mediated defense response against herbivorous insects. Proceedings of National Academy Sciences of the United States of America, 104, 12205-12210.
28. Kiegerl, S., Cardinale, F., Siligan, C., Gross, A., Baudouin, E., Liwosz, A., Eklof, S., Till, S., Bogre, L., Hirt, H. and Meskiene, I. (2000) SIMKK, a mitogen-activated protein kinase (MAPK) kinase, is a specific activator of the salt stress-induced MAPK, SIMK. Plant Cell, 12, 2247-2258.
29. Kong, Q., Qu, N., Gao, M., Zhang, Z., Ding, X., Yang, F., Li, Y., Dong, O.X., Chen, S., Li, X. and Zhang, Y. (2012) The MEKK1-MKK1/MKK2-MPK4 kinase cascade negatively regulates immunity mediated by a mitogen-activated protein kinase kinase kinase in Arabidopsis. Plant Cell, 24, 2225-2236.
30. Kosetsu, K., Matsunaga, S., Nakagami, H., Colcombet, J., Sasabe, M., Soyano, T., Takahashi, Y., Hirt, H. and Machida, Y. (2010) The MAP kinase MPK4 is required for cytokinesis in Arabidopsis thaliana. Plant Cell, 22, 3778-3790.
31. Lee, S., Hirt, H. and Lee, Y. (2001) Phosphatidic acid activates a wound-activated MAPK in Glycine max. Plant Journal, 26, 479-486.
32. Li, Q., Xie, Q.G., Smith-Becker, J., Navarre, D.A. and Kaloshian, I. (2006) Mi-1-mediated aphid resistance involves salicylic acid and mitogen-activated protein kinase signaling cascades. Molecular Plant-Microbe Interactions, 19, 655-664.
33. Liu, J.Z., Horstman, H.D., Braun, E., Graham, M.A., Zhang, C., Navarre, D., Qiu, W.L., Lee, Y., Nettleton, D., Hill, J.H. and Whitham, S.A. (2011) Soybean homologs of MPK4 negatively regulate defense responses and positively regulate growth and development. Plant Physiology, 157, 1363-1378.
34. Liu, Y., Schiff, M. and Dinesh-Kumar, S.P. (2004) Involvement of MEK1 MAPKK, NTF6 MAPK, WRKY/MYB transcription factors, COI1 and CTR1 in N-mediated resistance to tobacco mosaic virus. Plant Journal, 38, 800-809.
35. Liu, Y. and Zhang, S. (2004) Phosphorylation of 1-aminocyclopropane-1-carboxylic acid synthase by MPK6, a stress-responsive mitogen-activated protein kinase, induces ethylene biosynthesis in Arabidopsis. Plant Cell, 16, 3386-3399.
36. Maffei, M., Bossi, S., Spiteller, D., Mithofer, A. and Boland, W. (2004) Effects of feeding Spodoptera littoralis on lima bean leaves. I. Membrane potentials, intracellular calcium variations, oral secretions, and regurgitate components. Plant Physiology, 134, 1752-1762.
37. MAPK Group (2002) Mitogen-activated protein kinase cascades in plants: A new nomenclature. Trends in Plant Science, 7, 301-308
38. Mattiacci, L., Dicke, M. and Posthumus, M.A. (1995) beta-Glucosidase: an elicitor of herbivore-induced plant odor that attracts host-searching parasitic wasps. Proceedings of National Academy of Sciences of the United States of America, 92, 2036-2040.
39. Meldau, S., Wu, J. and Baldwin, I.T. (2009) Silencing two herbivory-activated MAP kinases, SIPK and WIPK, does not increase Nicotiana attenuata's susceptibility to herbivores in the glasshouse and in nature. New Phytology, 181, 161-173.
40. Mithöfer, A. and Boland, W. (2008) Recognition of herbivory-associated molecular patterns. Plant Physiology, 146, 825-831.
41. Mithöfer, A. and Boland, W. (2012) Plant defense against herbivores: chemical aspects. Annual Review of Plant Biology, 63, 431-450.
42. Mousavi, S.A., Chauvin, A., Pascaud, F., Kellenberger, S. and Farmer, E.E. (2013) GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling. Nature, 500, 422-426.
43. Musser, R.O., Cipollini, D.F., Hum-Musser, S.M., Williams, S.A., Brown, J.K. and Felton, G.W. (2005) Evidence that the caterpillar salivary enzyme glucose oxidase provides herbivore offense in solanaceous plants. Archive of Insect Biochemistry and Physiology, 58, 128-137.
44. O'donnell, P.J., Calvert, C., Atzorn, R., Wasternack, C., Leyser, H.M.O. and Bowles, D.J. (1996) Ethylene as a signal mediating the wound response of tomato plants. Science, 274, 1914-1917.
45. Paschold, A., Halitschke, R. and Baldwin, I.T. (2007) Co(i)-ordinating defenses: NaCOI1 mediates herbivore- induced resistance in Nicotiana attenuata and reveals the role of herbivore movement in avoiding defenses. Plant Journal, 51, 79-91.
46. Petersen, M., Brodersen, P., Naested, H., Andreasson, E., Lindhart, U., Johansen, B., Nielsen, H.B., Lacy, M., Austin, M.J., Parker, J.E., Sharma, S.B., Klessig, D.F., Martienssen, R., Mattsson, O., Jensen, A.B. and Mundy, J. (2000) Arabidopsis map kinase 4 negatively regulates systemic acquired resistance. Cell, 103, 1111-1120.
47. Pohnert, G., Jung, V., Haukioja, E., Lempa, K. and Boland, W. (1999) New fatty acid amides from regurgitant of lepidopteran (Noctuidae, Geometridae) caterpillars. Tetrahedron, 55, 11275-11280.
48. Schäfer, M., Fischer, C., Meldau, S., Seebald, E., Oelmuller, R. and Baldwin, I.T. (2011) Lipase activity in insect oral secretions mediates defense responses in Arabidopsis. Plant Physiology, 156, 1520-1534.
49. Schmelz, E.A., Carroll, M.J., Leclere, S., Phipps, S.M., Meredith, J., Chourey, P.S., Alborn, H.T. and Teal, P.E. (2006) Fragments of ATP synthase mediate plant perception of insect attack. Proceedings of National Academy of Sciences of the United States of America, 103, 8894-8899.
50. Schmelz, E.A., Engelberth, J., Alborn, H.T., Tumlinson, J.H. and Teal, P.E.A. (2009) Phytohormone-based activity mapping of insect herbivore-produced elicitors. Proceedings of National Academy of Sciences of the United States of America, 106, 653-657.
51. Seo, S., Okamoto, M., Seto, H., Ishizuka, K., Sano, H. and Ohashi, Y. (1995) Tobacco MAP kinase: a possible mediator in wound signal transduction pathways. Science, 270, 1988-1992.
52. Seo, S., Sano, H. and Ohashi, Y. (1999) Jasmonate-based wound signal transduction requires activation of WIPK, a tobacco mitogen-activated protein kinase. Plant Cell, 11, 289-298.
53. Spiteller, D. and Boland, W. (2003) N-(15, 16-Dihydroxy-linoleoyl)-glutamine and N-(15, 16-epoxylinoleoyl)-gluta-mine isolated from oral secretions of lepidopteran larvae. Tetrahedron, 59, 135-139.
54. Stratmann, J.W. and Ryan, C.A. (1997) Myelin basic protein kinase activity in tomato leaves is induced systemically by wounding and increases in response to systemin and oligosaccharide elicitors. Proceedings of National Academy of Sciences of the United States of America, 94, 11085-11089.
55. Steppuhn, A. and Baldwin, I.T. (2007) Resistance management in a native plant: nicotine prevents herbivores from compensating for plant protease inhibitors. Ecological Letters, 10, 499-511.
56. Von Dahl, C.C., Winz, R.A., Halitschke, R., Kuhnemann, F., Gase, K. and Baldwin, I.T. (2007) Tuning the herbivore-induced ethylene burst: the role of transcript accumulation and ethylene perception in Nicotiana attenuata. Plant Journal, 51, 293-307.
57. Wasternack, C. (2007) Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Annals of Botany (Lond), 100, 681-697.
58. Wu, J. and Baldwin, I.T. (2009) Herbivory-induced signalling in plants: perception and action. Plant, Cell & Environment, 32, 1161-1174.
59. Wu, J. and Baldwin, I.T. (2010) New insights into plant responses to the attack from insect herbivores. Annual Review of Genomics, 44, 1-24.
60. Wu, J., Hettenhausen, C., Meldau, S. and Baldwin, I.T. (2007) Herbivory rapidly activates MAPK signaling in attacked and unattacked leaf regions but not between leaves of Nicotiana attenuata. Plant Cell, 19, 1096-1122.
61. Xie, D.X., Feys, B.F., James, S., Nieto-Rostro, M. and Turner, J.G. (1998) COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility. Science, 280, 1091-1094.
62. Yang, D.H., Hettenhausen, C., Baldwin, I.T. and Wu, J. (2011) BAK1 regulates the accumulation of jasmonic acid and the levels of trypsin proteinase inhibitors in Nicotiana attenuata's responses to herbivory. Journal of Experimental Botany, 62, 641-652.
63. Yang, D.H., Hettenhausen, C., Baldwin, I.T. and Wu, J. (2012) Silencing Nicotiana attenuata calcium-dependent protein kinases, CDPK4 and CDPK5, strongly up-regulates wound- and herbivory-induced jasmonic acid accumulations. Plant Physiology, 159, 1591-1607.
64. Yang, K.Y., Liu, Y. and Zhang, S. (2001) Activation of a mitogen-activated protein kinase pathway is involved in disease resistance in tobacco. Proceedings of National Academy of Sciences of the United States of America, 98, 741-746.
65. Zimmermann, M.R., Maischak, H., Mithofer, A., Boland, W. and Felle, H.H. (2009) System potentials, a novel electrical long-distance apoplastic signal in plants, induced by wounding. Plant Physiology, 149, 1593-1600.
66. Zolnierowicz, S. and Bollen, M. (2000) Protein phosphorylation and protein phosphatases. De Panne, Belgium, September 19-24, 1999. EMBO Journal, 19, 483-488.