The Essential Role of Jasmonic Acid in Plant–Herbivore Interactions – Using the Wild Tobacco Nicotiana attenuata as a Model

Lei Wang,
Jianqiang Wu^,

Key Laboratory of Economic Plants and Biotechnology, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China

More Information

Corresponding author: E-mail address: wujianqiang@mail.kib.ac.cn (Jianqiang Wu)

摘要

- /
- /
Abstract: The plant hormone jasmonic acid (JA) plays a central role in plant defense against herbivores. Herbivore damage elicits a rapid and transient JA burst in the wounded leaves and JA functions as a signal to mediate the accumulation of various secondary metabolites that confer resistance to herbivores. Nicotiana attenuata is a wild tobacco species that inhabits western North America. More than fifteen years of study and its unique interaction with the specialist herbivore insect Manduca sexta have made this plant one of the best models for studying plant–herbivore interactions. Here we review the recent progress in understanding the elicitation of JA accumulation by herbivore-specific elicitors, the regulation of JA biosynthesis, JA signaling, and the herbivore-defense traits in N. attenuata.
- Jasmonic acid /
- Defense /
- Plant–herbivore interaction

HTML全文

参考文献(120)

[1]	Aharoni, A., Jongsma, M.A., Bouwmeester, H.J. Volatile science? Metabolic engineering of terpenoids in plants Trends Plant Sci., 10 (2005),pp. 594-602
[2]	Alborn, H.T., Turlings, T.C.J., Jones, T.H. et al. An elicitor of plant volatiles from beet armyworm oral secretion Science, 276 (1997),pp. 945-949
[3]	Alborn, H.T., Hansen, T.V., Jones, T.H. et al. Proc. Natl. Acad. Sci. USA, 104 (2007),pp. 12976-12981
[4]	Allmann, S., Halitschke, R., Schuurink, R.C. et al. Plant Cell Environ., 33 (2010),pp. 2028-2040
[5]	Appel, H.M., Martin, M.M. Ecology, 73 (1992),pp. 216-228
[6]	Balandin, T., Vanderdoes, C., Albert, J.M.B. et al. Structure and induction-pattern of a novel proteinase-inhibitor class-II gene of tobacco Plant Mol. Biol., 27 (1995),pp. 1197-1204
[7]	Baldwin, I.T. Jasmonate-induced responses are costly but benefit plants under attack in native populations Proc. Natl. Acad. Sci. USA, 95 (1998),pp. 8113-8118
[8]	Baldwin, I.T. Novartis Found. Symp., 223 (1999),pp. 74-87
[9]	Baldwin, I.T., Halitschke, R., Paschold, A. et al. Volatile signaling in plant–plant interactions: “talking trees” in the genomics era Science, 311 (2006),pp. 812-815
[10]	Ballare, C.L. Jasmonate-induced defenses: a tale of intelligence, collaborators and rascals Trends Plant Sci., 16 (2011),pp. 249-257
[11]	Birkett, M.A., Campbell, C.A., Chamberlain, K. et al. Proc. Natl. Acad. Sci. USA, 97 (2000),pp. 9329-9334
[12]	Bishop, P.D., Makus, D.J., Pearce, G. et al. Proteinase inhibitor-inducing factor activity in tomato leaves resides in oligosaccharides enzymically released from cell walls Proc. Natl. Acad. Sci. USA, 78 (1981),pp. 3536-3540
[13]	Bode, W., Huber, R. Natural protein proteinase inhibitors and their interaction with proteinases Eur. J. Biochem., 204 (1992),pp. 433-451
[14]	Bonaventure, G. Plant Signal. Behav., 6 (2011),pp. 2060-2063
[15]	Bonaventure, G., Schuck, S., Baldwin, I.T. Plant Cell Environ., 34 (2011),pp. 1507-1520
[16]	Bonaventure, G., VanDoorn, A., Baldwin, I.T. Herbivore-associated elicitors: FAC signaling and metabolism Trends Plant Sci., 16 (2011),pp. 294-299
[17]	Broadway, R.M. Are insects resistant to plant proteinase-inhibitors? J. Insect Physiol., 41 (1995),pp. 107-116
[18]	Broadway, R.M., Duffey, S.S. The effect of plant protein-quality on insect digestive physiology and the toxicity of plant proteinase-inhibitors J. Insect Physiol., 34 (1988),pp. 1111-1117
[19]	Browse, J. Jasmonate passes muster: a receptor and targets for the defense hormone Annu. Rev. Plant Biol., 60 (2009),pp. 183-205
[20]	Cao, H., Bowling, S.A., Gordon, A.S. et al. Plant Cell, 6 (1994),pp. 1583-1592
[21]	Chen, H., Wilkerson, C.G., Kuchar, J.A. et al. Jasmonate-inducible plant enzymes degrade essential amino acids in the herbivore midgut Proc. Natl. Acad. Sci. USA, 102 (2005),pp. 19237-19242
[22]	Chini, A., Fonseca, S., Fernandez, G. et al. The JAZ family of repressors is the missing link in jasmonate signalling Nature, 448 (2007),pp. 666-671
[23]	Erb, M., Meldau, S., Howe, G.A. Role of phytohormones in insect-specific plant reactions Trends Plant Sci., 17 (2012),pp. 250-259
[24]	Farmer, E.E., Ryan, C.A. Interplant communication: airborne methyl jasmonate induces synthesis of proteinase inhibitors in plant leaves Proc. Natl. Acad. Sci. USA, 87 (1990),pp. 7713-7716
[25]	Farmer, E.E., Johnson, R.R., Ryan, C.A. Regulation of expression of proteinase-inhibitor genes by methyl jasmonate and jasmonic acid Plant Physiol., 98 (1992),pp. 995-1002
[26]	Felton, G.W., Tumlinson, J.H. Plant–insect dialogs: complex interactions at the plant–insect interface Curr. Opin. Plant Biol., 11 (2008),pp. 457-463
[27]	Gatehouse, J.A. Plant resistance towards insect herbivores: a dynamic interaction New Phytol., 156 (2002),pp. 145-169
[28]	Geoffroy, P., Legrand, M., Fritig, B. Isolation and characterization of a proteinaceous inhibitor of microbial proteinases induced during the hypersensitive reaction of tobacco to tobacco mosaic-virus Mol. Plant Microbe Interact., 3 (1990),pp. 327-333
[29]	Gidda, S.K., Miersch, O., Levitin, A. et al. J. Biol. Chem., 278 (2003),pp. 17895-17900
[30]	Glendinning, J.I. How do herbivorous insects cope with noxious secondary plant compounds in their diet? Entomol. Exp. Appl., 104 (2002),pp. 15-25
[31]	Green, E.S., Zangerl, A.R., Berenbaum, M.R. Effects of phytic acid and xanthotoxin on growth and detoxification in caterpillars J. Chem. Ecol., 27 (2001),pp. 1763-1773
[32]	Green, T.R., Ryan, C.A. Wound-induced proteinase inhibitor in plant leaves: a possible defense mechanism against insects Science, 175 (1972),pp. 776-777
[33]	Halitschke, R., Baldwin, I.T. Jasmonates and related compounds in plant–insect interactions J. Plant Growth Regul., 23 (2004),pp. 238-245
[34]	Halitschke, R., Kessler, A., Kahl, J. et al. Oecologia, 124 (2000),pp. 408-417
[35]	Halitschke, R., Schittko, U., Pohnert, G. et al. Plant Physiol., 125 (2001),pp. 711-717
[36]	Halitschke, R., Gase, K., Hui, D. et al. Plant Physiol., 131 (2003),pp. 1894-1902
[37]	Heath, R.L., Barton, P.A., Simpson, R.J. et al. Eur. J. Biochem., 230 (1995),pp. 250-257
[38]	Heiling, S., Schuman, M.C., Schoettner, M. et al. Plant Cell, 22 (2010),pp. 273-292
[39]	Heinrich, M., Hettenhausen, C., Lange, T. et al. Plant J., 73 (2013),pp. 591-606
[40]	Helder, H., Miersch, O., Vreugdenhil, D. et al. Physiol. Plant., 88 (1993),pp. 647-653
[41]	Hettenhausen, C., Baldwin, I.T., Wu, J. New Phytol., 199 (2013),pp. 787-799
[42]	Howe, G.A., Jander, G. Plant immunity to insect herbivores Annu. Rev. Plant Biol., 59 (2008),pp. 41-66
[43]	Jackson, D.M., Johnson, A.W., Stephenson, M.G. J. Econ. Entomol., 95 (2002),pp. 1294-1302
[44]	Jassbi, A.R., Gase, K., Hettenhausen, C. et al. Plant Physiol., 146 (2008),pp. 974-986
[45]	Johnson, R., Narvaez, J., An, G. et al. Proc. Natl. Acad. Sci. USA, 86 (1989),pp. 9871-9875
[46]	Kallenbach, M., Alagna, F., Baldwin, I.T. et al. Plant Physiol., 152 (2010),pp. 96-106
[47]	Kang, J.H., Wang, L., Giri, A. et al. Plant Cell, 18 (2006),pp. 3303-3320
[48]	Karban, R., Baldwin, I.T., Baxter, K.J. et al. Communication between plants: induced resistance in wild tobacco plants following clipping of neighboring sagebrush Oecologia, 125 (2000),pp. 66-71
[49]	Katsir, L., Schilmiller, A.L., Staswick, P.E. et al. COI1 is a critical component of a receptor for jasmonate and the bacterial virulence factor coronatine Proc. Natl. Acad. Sci. USA, 105 (2008),pp. 7100-7105
[50]	Keinanen, M., Oldham, N.J., Baldwin, I.T. J. Agric. Food Chem., 49 (2001),pp. 3553-3558
[51]	Kessler, A., Baldwin, I.T. Defensive function of herbivore-induced plant volatile emissions in nature Science, 291 (2001),pp. 2141-2144
[52]	Kessler, A., Baldwin, I.T. Plant responses to insect herbivory: the emerging molecular analysis Annu. Rev. Plant Biol., 53 (2002),pp. 299-328
[53]	Kessler, A., Halitschke, R., Diezel, C. et al. Oecologia, 148 (2006),pp. 280-292
[54]	Koiwa, H., Bressan, R.A., Hasegawa, P.M. Regulation of protease inhibitors and plant defense Trends Plant Sci., 2 (1997),pp. 379-384
[55]	Konno, K., Hirayama, C., Nakamura, M. et al. Papain protects papaya trees from herbivorous insects: role of cysteine proteases in latex Plant J., 37 (2004),pp. 370-378
[56]	Koo, A.J., Gao, X., Jones, A.D. et al. Plant J., 59 (2009),pp. 974-986
[57]	Lawrence, S.D., Novak, N.G. Expression of poplar chitinase in tomato leads to inhibition of development in colorado potato beetle Biotechnol. Lett., 28 (2006),pp. 593-599
[58]	Li, C., Schilmiller, A.L., Liu, G. et al. Role of beta-oxidation in jasmonate biosynthesis and systemic wound signaling in tomato Plant Cell, 17 (2005),pp. 971-986
[59]	Li, L., Li, C., Lee, G.I. et al. Distinct roles for jasmonate synthesis and action in the systemic wound response of tomato Proc. Natl. Acad. Sci. USA, 99 (2002),pp. 6416-6421
[60]	Maffei, M., Bossi, S., Spiteller, D. et al. Plant Physiol., 134 (2004),pp. 1752-1762
[61]	Maffei, M.E., Mithofer, A., Arimura, G. et al. Plant Physiol., 140 (2006),pp. 1022-1035
[62]	Mattiacci, L., Dicke, M., Posthumus, M.A. beta-Glucosidase: an elicitor of herbivore-induced plant odor that attracts host-searching parasitic wasps Proc. Natl. Acad. Sci. USA, 92 (1995),pp. 2036-2040
[63]	McConn, M., Creelman, R.A., Bell, E. et al. Proc. Natl. Acad. Sci. USA, 94 (1997),pp. 5473-5477
[64]	Mcmanus, M.T., White, D.W.R., Mcgregor, P.G. Accumulation of a chymotrypsin inhibitor in transgenic tobacco can affect the growth of insect pests Transgenic Res., 3 (1994),pp. 50-58
[65]	Meldau, S., Baldwin, I.T., Wu, J. New Phytol., 189 (2011),pp. 1143-1156
[66]	Meldau, S., Baldwin, I.T., Wu, J. For security and stability: SGT1 in plant defense and development Plant Signal. Behav., 6 (2011),pp. 1479-1482
[67]	Miersch, O., Neumerkel, J., Dippe, M. et al. Hydroxylated jasmonates are commonly occurring metabolites of jasmonic acid and contribute to a partial switch-off in jasmonate signaling New Phytol., 177 (2008),pp. 114-127
[68]	Mithofer, A., Boland, W. Plant defense against herbivores: chemical aspects Annu. Rev. Plant Biol., 63 (2012),pp. 431-450
[69]	Mousavi, S.A., Chauvin, A., Pascaud, F. et al. GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling Nature, 500 (2013),pp. 422-426
[70]	Musser, R.O., Hum-Musser, S.M., Eichenseer, H. et al. Herbivory: caterpillar saliva beats plant defences Nature, 416 (2002),pp. 599-600
[71]	Nombela, G., Williamson, V.M., Muniz, M. Mol. Plant Microbe Interact., 16 (2003),pp. 645-649
[72]	Paschold, A., Halitschke, R., Baldwin, I.T. Plant J., 51 (2007),pp. 79-91
[73]	Paschold, A., Bonaventure, G., Kant, M.R. et al. Plant Cell Physiol., 49 (2008),pp. 1165-1175
[74]	Pauchet, Y., Wilkinson, P., Vogel, H. et al. Insect Mol. Biol., 19 (2010),pp. 61-75
[75]	Pauwels, L., Barbero, G.F., Geerinck, J. et al. NINJA connects the co-repressor TOPLESS to jasmonate signalling Nature, 464 (2010),pp. 788-791
[76]	Penacortes, H., Sanchezserrano, J., Rochasosa, M. et al. Systemic induction of proteinase-inhibitor-II gene-expression in potato plants by wounding Planta, 174 (1988),pp. 84-89
[77]	Pohlon, E., Baldwin, I.T. Artificial diets ‘capture’ the dynamics of jasmonate-induced defenses in plants Entomol. Exp. Appl., 100 (2001),pp. 127-130
[78]	Rayapuram, C., Baldwin, I.T. Plant J., 52 (2007),pp. 700-715
[79]	Romero-Puertas, M.C., Campostrini, N., Matte, A. et al. Proteomics, 8 (2008),pp. 1459-1469
[80]	Ryan, C.A. Protease inhibitors in plants – genes for improving defenses against insects and pathogens Annu. Rev. Phytopathol., 28 (1990),pp. 425-449
[81]	Ryan, C.A., Pearce, G. Systemin: a polypeptide signal for plant defensive genes Annu. Rev. Cell Dev. Biol., 14 (1998),pp. 1-17
[82]	Schaller, A., Stintzi, A. Enzymes in jasmonate biosynthesis – structure, function, regulation Phytochemistry, 70 (2009),pp. 1532-1538
[83]	Schilmiller, A.L., Howe, G.A. Systemic signaling in the wound response Curr. Opin. Plant Biol., 8 (2005),pp. 369-377
[84]	Schmelz, E.A., Engelberth, J., Alborn, H.T. et al. Phytohormone-based activity mapping of insect herbivore-produced elicitors Proc. Natl. Acad. Sci. USA, 106 (2009),pp. 653-657
[85]	Schmelz, E.A., Carroll, M.J., LeClere, S. et al. Fragments of ATP synthase mediate plant perception of insect attack Proc. Natl. Acad. Sci. USA, 103 (2006),pp. 8894-8899
[86]	Sembdner, G., Parthier, B. The biochemistry and the physiological and molecular actions of jasmonates Annu. Rev. Plant Physiol. Plant Mol. Biol., 44 (1993),pp. 569-589
[87]	Seo, H.S., Song, J.T., Cheong, J.J. et al. Jasmonic acid carboxyl methyltransferase: a key enzyme for jasmonate-regulated plant responses Proc. Natl. Acad. Sci. USA, 98 (2001),pp. 4788-4793
[88]	Snook, M.E., Johnson, A.W., Severson, R.F. et al. J. Agric. Food Chem., 45 (1997),pp. 2299-2308
[89]	Staswick, P.E., Tiryaki, I. Plant Cell, 16 (2004),pp. 2117-2127
[90]	Steppuhn, A., Gase, K., Krock, B. et al. Nicotine's defensive function in nature PLoS Biol., 2 (2004),p. E217
[91]	Stitz, M., Baldwin, I.T., Gaquerel, E. PLoS ONE, 6 (2011),p. e25925
[92]	Stitz, M., Gase, K., Baldwin, I.T. et al. Plant Physiol., 157 (2011),pp. 341-354
[93]	Takahashi, F., Yoshida, R., Ichimura, K. et al. Plant Cell, 19 (2007),pp. 805-818
[94]	Thines, B., Katsir, L., Melotto, M. et al. JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling Nature, 448 (2007),pp. 661-665
[95]	Truitt, C.L., Pare, P.W. Planta, 218 (2004),pp. 999-1007
[96]	van Dam, N.M., Horn, M., Mares, M. et al. J. Chem. Ecol., 27 (2001),pp. 547-568
[97]	VanDoorn, A., Baldwin, I.T., Bonaventure, G. Lipoxygenase-mediated modification of insect elicitors: generating chemical diversity on the leaf wound surface Plant Signal. Behav., 5 (2010),pp. 1674-1676
[98]	VanDoorn, A., Kallenbach, M., Borquez, A.A. et al. BMC Plant Biol., 10 (2010),p. 164
[99]	Verhage, A., van Wees, S.C., Pieterse, C.M. Plant immunity: it's the hormones talking, but what do they say? Plant Physiol., 154 (2010),pp. 536-540
[100]	Von Dahl, C.C., Baldwin, I.T. Physiol. Plant., 120 (2004),pp. 474-481
[101]	Wang, L., Allmann, S., Wu, J. et al. Plant Physiol., 146 (2008),pp. 904-915
[102]	Wasternack, C. Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development Ann. Bot., 100 (2007),pp. 681-697
[103]	Wasternack, C., Stenzel, I., Hause, B. et al. The wound response in tomato – role of jasmonic acid J. Plant Physiol., 163 (2006),pp. 297-306
[104]	Wu, J., Baldwin, I.T. Herbivory-induced signalling in plants: perception and action Plant Cell Environ., 32 (2009),pp. 1161-1174
[105]	Wu, J., Baldwin, I.T. New insights into plant responses to the attack from insect herbivores Annu. Rev. Genet., 44 (2010),pp. 1-24
[106]	Wu, J., Wang, L., Baldwin, I.T. Methyl jasmonate-elicited herbivore resistance: does MeJA function as a signal without being hydrolyzed to JA? Planta, 227 (2008),pp. 1161-1168
[107]	Wu, J., Hettenhausen, C., Meldau, S. et al. Plant Cell, 19 (2007),pp. 1096-1122
[108]	Wunsche, H., Baldwin, I.T., Wu, J. J. Integr. Plant Biol., 53 (2011),pp. 619-631
[109]	Wunsche, H., Baldwin, I.T., Wu, J. J. Exp. Bot., 62 (2011),pp. 4605-4616
[110]	Xie, D.X., Feys, B.F., James, S. et al. Science, 280 (1998),pp. 1091-1094
[111]	Xu, L., Liu, F., Lechner, E. et al. The SCF(COI1) ubiquitin-ligase complexes are required for jasmonate response in Arabidopsis Plant Cell, 14 (2002),pp. 1919-1935
[112]	Yan, J., Zhang, C., Gu, M. et al. Plant Cell, 21 (2009),pp. 2220-2236
[113]	Yang, D.H., Hettenhausen, C., Baldwin, I.T. et al. J. Exp. Bot., 62 (2011),pp. 641-652
[114]	Yang, D.H., Hettenhausen, C., Baldwin, I.T. et al. The multifaceted function of BAK1/SERK3: plant immunity to pathogens and responses to insect herbivores Plant Signal. Behav., 6 (2011),pp. 1322-1324
[115]	Yang, D.H., Hettenhausen, C., Baldwin, I.T. et al. Plant Physiol., 159 (2012),pp. 1591-1607
[116]	Yoshinaga, N., Aboshi, T., Abe, H. et al. Proc. Natl. Acad. Sci. USA, 105 (2008),pp. 18058-18063
[117]	Yoshinaga, N., Alborn, H.T., Nakanishi, T. et al. Fatty acid-amino acid conjugates diversification in lepidopteran caterpillars J. Chem. Ecol., 36 (2010),pp. 319-325
[118]	Zavala, J.A., Patankar, A.G., Gase, K. et al. Proc. Natl. Acad. Sci. USA, 101 (2004),pp. 1607-1612
[119]	Zavala, J.A., Patankar, A.G., Gase, K. et al. Plant Physiol., 134 (2004),pp. 1181-1190
[120]	Zimmermann, M.R., Maischak, H., Mithofer, A. et al. System potentials, a novel electrical long-distance apoplastic signal in plants, induced by wounding Plant Physiol., 149 (2009),pp. 1593-1600