Molecular mechanisms underlying plant memory in JA-mediated defence responses

Plant, Cell and Environment

Volumn 32, Issue 6, 2009, Pages 617-627

  GÁlis, Ivan ^a   Gaquerel, Emmanuel ^a   Pandey, Shree P ^a,b   Baldwin, Ian T ^a  

^a MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

^b MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

Author keywords

Herbivory; Insect; Jasmonate (JA); JAZ repressors; Memory; Plant defence; Plant fitness; Priming; RNA interference (RNAi); Stress imprint; Tobacco

Indexed keywords

CYCLOPENTANE DERIVATIVE; JASMONIC ACID; OXYLIPIN; TRANSCRIPTION FACTOR;

FITNESS; HERBIVORY; HORMONE; INSECT; MOLECULAR ANALYSIS; PLANT DEFENSE; RNA; TOBACCO;

ADAPTATION; ANIMAL; ARTICLE; CELL WALL; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYSIOLOGICAL STRESS; PLANT; PLANT PHYSIOLOGY; TRANSCRIPTION INITIATION;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; CELL WALL; CYCLOPENTANES; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, PLANT; OXYLIPINS; PLANT PHYSIOLOGICAL PHENOMENA; PLANTS; STRESS, PHYSIOLOGICAL; TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION;

HEXAPODA; NICOTIANA TABACUM;

EID: 66149109676     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/j.1365-3040.2008.01862.x     Document Type: Article

References (103)

1. Alpi A., Amrhein N., Bertl A., et al 2007) Plant neurobiology: no brain, no gain? Trends in Plant Science 12, 135 136.
2. Baldwin I.T. Schmelz E.A. (1996) Immunological 'memory' in the induced accumulation of nicotine in wild tobacco. Ecology 77, 236 246.
3. Bartel D.P. (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281 297.
4. Beckers G.J. Conrath U. (2007) Priming for stress resistance: from the lab to the field. Current Opinion in Plant Biology 10, 425 431.
5. Bernays E.A. Woods H.A. (2000) Foraging in nature by larvae of Manduca sexta- influenced by an endogenous oscillation. Journal of Insect Physiology 46, 825 836.
6. Bernays E.A., Singer M.S. Rodrigues D. (2004) Foraging in nature: foraging efficiency and attentiveness in caterpillars with different diet breadths. Ecological Entomology 29, 389 397.
7. Bonaventure G., Gfeller A., Proebsting W.M., Hortensteiner S., Chetelat A., Martinoia E. Farmer E.E. (2007) A gain-of-function allele of TPC1 activates oxylipin biogenesis after leaf wounding in Arabidopsis. The Plant Journal 49, 889 898.
8. Boyko A. Kovalchuk I. (2008) Epigenetic control of plant stress response. Environmental and Molecular Mutagenesis 49, 61 72.
9. Brenner E.D., Stahlberg R., Mancuso S., Baluska F. Van Volkenburgh E. (2007) Response to Alpi et al.: Plant neurobiology: the gain is more than the name. Trends in Plant Science 12, 285 286.
10. Bronner C., Chataigneau T., Schini-Kerth V.B. Landry Y. (2007) The 'epigenetic, code replication machinery', ECREM: a promising druggable target of the epigenetic cell memory. Current Medicinal Chemistry 14, 2629 2641.
11. Browse J. Howe G.A. (2008) New weapons and a rapid response against insect attack. Plant Physiology 146, 832 838.
12. Bruce T.J.A., Matthes M.C., Napier J.A. Pickett J.A. (2007) Stressful 'memories' of plants: evidence and possible mechanisms. Plant Science 173, 603 608.
13. Buseman C.M., Tamura P., Sparks A.A., et al 2006) Wounding stimulates the accumulation of glycerolipids containing oxophytodienoic acid and dinoroxophytodienoic acid in Arabidopsis leaves. Plant Physiology 142, 28 39.
14. Chapman E.J. Carrington J.C. (2007) Specialization and evolution of endogenous small RNA pathways. Nature Reviews Genetics 8, 884 896.
15. Chen M.H. Citovsky V. (2003) Systemic movement of a tobamovirus requires host cell pectin methylesterase. The Plant Journal 35, 386 392.
16. Chini A., Fonseca S., Fernandez G., et al 2007) The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448, 666 671.
17. Chong J., Pierrel M.A., Atanassova R., Werck-Reithhart D., Fritig B. Saindrenan P. (2001) Free and conjugated benzoic acid in tobacco plants and cell cultures. Induced accumulation upon elicitation of defense responses and role as salicylic acid precursors. Plant Physiology 125, 318 328.
18. Chung H.S., Koo A.J.K., Gao X., Jayanty S., Thines B., Jones A.D. Howe G.A. (2008) Regulation and function of Arabidopsis JASMONATE ZIM-domain genes in response to wounding and herbivory. Plant Physiology 146, 952 964.
19. Conrath U., Thulke O., Katz V., Schwindling S. Kohler A. (2001) Priming as a mechanism in induced systemic resistance of plants. European Journal of Plant Pathology 107, 113 119.
20. Conrath U., Beckers G.J.M., Flors V., et al 2006) Priming: getting ready for battle. Molecular Plant-Microbe Interactions 19, 1062 1071.
21. De Vos M., Van Zaanen W., Koornneef A., Korzelius J.P., Dicke M., Van Loon L.C. Pieterse C.M.J. (2006) Herbivore-induced resistance against microbial pathogens in Arabidopsis. Plant Physiology 142, 352 363.
22. Demongeot J., Thomas R. Thellier M. (2000) A mathematical model for storage and recall functions in plants. Comptes Rendus De L Academie Des Sciences Serie III-Sciences De La Vie-Life Sciences 323, 93 97.
23. Demongeot J., Thellier M. Thomas R. (2006) Storage and recall of environmental signals in a plant: modelling by use of a differential (continuous) formulation. Comptes Rendus Biologies 329, 971 978.
24. Desbiez M.O., Kergosien Y., Champagnat P. Thellier M. (1984) Memorization and delayed expression of regulatory messages in plants. Planta 160, 392 399.
25. Dharmasiri N., Dharmasiri S. Estelle M. (2005) The F-box protein TIR1 is an auxin receptor. Nature 435, 441 445.
26. Dombrecht B., Xue G.P., Sprague S.J., et al. (2007) MYC2 differentially modulates diverse jasmonate-dependent functions in Arabidopsis. The Plant Cell 19, 2225 2245.
27. Dorokhov Y.L. (2007) Gene silencing in plants. Molecular Biology 41, 519 530.
28. Dorokhov Y.L., Frolova O.Y., Skurat E.V., et al 2006) A novel function for a ubiquitous plant enzyme pectin methylesterase: the enhancer of RNA silencing. FEBS Letters 580, 3872 3878.
29. Engelberth J., Alborn H.T., Schmelz E.A. Tumlinson J.H. (2004) Airborne signals prime plants against insect herbivore attack. Proceedings of the National Academy of Sciences of the United States of America 101, 1781 1785.
30. Engelberth J., Seidl-Adams I., Schultz J.C. Tumlinson J.H. (2007) Insect elicitors and exposure to green leafy volatiles differentially upregulate major octadecanoids and transcripts of 12-oxo phytodienoic acid reductases in Zea mays. Molecular Plant-Microbe Interactions 20, 707 716.
31. Filipowicz W., Bhattacharyya S.N. Sonenberg N. (2008) Mechanisms of posttranscriptional regulation by microRNAs: are the answers in sight? Nature Reviews Genetics 9, 102 114.
32. Foster T.M., Lough T.J., Emerson S.J., Lee R.H., Bowman J.L., Forster R.L.S. Lucas W.J. (2002) A surveillance system regulates selective entry of RNA into the shoot apex. The Plant Cell 14, 1497 1508.
33. Frost C.J., Appel M., Carlson J.E., De Moraes C.M., Mescher M.C. Schultz J.C. (2007) Within-plant signalling via volatiles overcomes vascular constraints on systemic signalling and primes responses against herbivores. Ecology Letters 10, 490 498.
34. Frost C.J., Mescher M.C., Carlson J.E. De Moraes C.M. (2008) Plant defense priming against herbivores: getting ready for a different battle. Plant Physiology 146, 818 824.
35. Halitschke R. Baldwin I.T. (2003) Antisense LOX expression increases herbivore performance by decreasing defense responses and inhibiting growth-related transcriptional reorganization in Nicotiana attenuata. The Plant Journal 36, 794 807.
36. Halitschke R., Schittko U., Pohnert G., Boland W. 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.
37. Heil M. Baldwin I.T. (2002) Fitness costs of induced resistance: emerging experimental support for a slippery concept. Trends in Plant Science 7, 61 67.
38. Hermsmeier D., Schittko U. Baldwin I.T. (2001) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. I. Large-scale changes in the accumulation of growth- and defense-related plant mRNAs. Plant Physiology 125, 683 700.
39. Hui D.Q., Iqbal J., Lehmann K., Gase K., Saluz H.P. Baldwin I.T. (2003) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata: V. Microarray analysis and further characterization of large-scale changes in herbivore-induced mRNAs. Plant Physiology 131, 1877 1893.
40. Hyun Y., Choi S., Hwang H.J., et al 2008) Cooperation and functional diversification of two closely related galactolipase genes for jasmonate biosynthesis. Developmental Cell 14, 183 192.
41. Iriti M., Mapelli S. Faoro F. (2007) Chemical-induced resistance against post-harvest infection enhances tomato nutritional traits. Food Chemistry 105, 1040 1046.
42. Ishiguro S., Kawai-Oda A., Ueda J., Nishida I. Okada K. (2001) The DEFECTIVE IN ANTHER DEHISCENCE1 gene encodes a novel phospholipase A1 catalyzing the initial step of jasmonic acid biosynthesis, which synchronizes pollen maturation, anther dehiscence, and flower opening in Arabidopsis. The Plant Cell 13, 2191 2209.
43. Jones G.D., Russell L., DarleyUsmar V.M., Stone D. Wilson M.T. (1996) Role of lipid hydroperoxides in the activation of 15-lipoxygenase. Biochemistry 35, 7197 7203.
44. Kalantidis K., Schurnacher H.T., Alexiadis T. Helm J.M. (2008) RNA silencing movement in plants. Biology of the Cell 100, 13 26.
45. Kang J.H., Wang L., Giri A. Baldwin I.T. (2006) Silencing threonine deaminase and JAR4 in Nicotiana attenuata impairs jasmonic acid-isoleucine- mediated defenses against Manduca sexta. The Plant Cell 18, 3303 3320.
46. Karban R., Baldwin I.T., Baxter K.J., Laue G. Felton G.W. (2000) Communication between plants: induced resistance in wild tobacco plants following clipping of neighboring sagebrush. Oecologia 125, 66 71.
47. Karban R., Maron J., Felton G.W., Ervin G. Eichenseer H. (2003) Herbivore damage to sagebrush induces resistance in wild tobacco: evidence for eavesdropping between plants. Oikos 100, 325 332.
48. Katsir L., Schilmiller A.L., Staswick P.E., He S.Y. Howe G.A. (2008) COI1 is a critical component of a receptor for jasmonate and the bacterial virulence factor coronatine. Proceedings of the National Academy of Sciences of the United States of America 105, 7100 7105.
49. Kessler A. Baldwin I.T. (2004) Herbivore-induced plant vaccination. Part I. The orchestration of plant defenses in nature and their fitness consequences in the wild tobacco Nicotiana attenuata. The Plant Journal 38, 639 649.
50. Kikuta Y., Kusunose E. Kusunose M. (2002) Prostaglandin and leukotriene omega-hydroxylases. Prostaglandins & Other Lipid Mediators 68-9, 345 362.
51. Koch T., Bandemer K. Boland W. (1997) Biosynthesis of cis-jasmone: a pathway for the inactivation and the disposal of the plant stress hormone jasmonic acid to the gas phase? Helvetica Chimica Acta 80, 838 850.
52. Kvaalen H. Johnsen O. (2008) Timing of bud set in Picea abies is regulated by a memory of temperature during zygotic and somatic embryogenesis. New Phytologist 177, 49 59.
53. Leavitt S.W. (1994) Major wet interval in White Mountains medieval warm period evidenced in delta-C-13 of bristlecone-pine tree-rings. Climatic Change 26, 299 307.
54. Lee R.C., Feinbaum R.L. Ambros V. (1993) The C. elegans heterochronic gene Lin-4 encodes small RNAs with antisense complementarity to Lin-14. Cell 75, 843 854.
55. Li L.C., Okino S.T., Zhao H., Pookot D., Place R.P., Urakami S., Enokida H. Dahiya R. (2006) Small dsRNAs induce transcriptional activation in human cells. Proceedings of the National Academy of Sciences of the United States of America 103, 17337 17342.
56. Lloyd C. Buschmann H. (2007) Plant division: remembering where to build the wall. Current Biology, 17, R1053 R1055.
57. Mathieu O., Reinders J., Caikovski M., Smathajitt C. Paszkowski J. (2007) Transgenerational stability of the Arabidopsis epigenome is coordinated by CG methylation. Cell 130, 851 862.
58. Mehler M.F. Mattick J.S. (2007) Noncoding RNAs and RNA editing in brain development, functional diversification, and neurological disease. Physiological Reviews 87, 799 823.
59. Michaels S.D. Amasino R.M. (2000) Memories of winter: vernalization and the competence to flower. Plant Cell and Environment 23, 1145 1153.
60. Micheli F. (2001) Pectin methylesterases: cell wall enzymes with important roles in plant physiology. Trends in Plant Science 6, 414 419.
61. Miersch O., Neumerkel J., Dippe M., Stenzel I. Wasternack C. (2008) Hydroxylated jasmonates are commonly occurring metabolites of jasmonic acid and contribute to a partial switch-off in jasmonate signaling. New Phytologist 177, 114 127.
62. Molinier J., Ries G., Zipfel C. Hohn B. (2006) Transgeneration memory of stress in plants. Nature 442, 1046 1049.
63. Oldham M.L., Brash A.R. Newcomer M.E. (2005) Insights from the X-ray crystal structure of coral 8R-lipoxygenase - calcium activation via a C2-like domain and a structural basis of product chirality. Journal of Biological Chemistry 280, 39545 39552.
64. Pandey S.P. Baldwin I.T. (2007) RNA-directed RNA polymerase 1 (RdR1) mediates the resistance of Nicotiana attenuata to herbivore attack in nature. The Plant Journal 50, 40 53.
65. Pandey S.P. Baldwin I.T. (2008) Silencing RNA-directed RNA polymerase 2 increases the susceptibility of Nicotiana attenuata to UV in the field and in the glasshouse. The Plant Journal 845 862.
66. Pandey S.P., Shahi P., Gase K. Baldwin I.T. (2008) Herbivory-induced changes in the small-RNA transcriptome and phytohormone signaling in Nicotiana attenuata. Proceedings of the National Academy of Sciences of the United States of America 105, 4559 4564.
67. Paschold A., Halitschke R. 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. The Plant Journal 51, 79 91.
68. Pickford A.S. Cogoni C. (2003) RNA-mediated gene silencing. Cellular and Molecular Life Sciences 60, 871 882.
69. Rogelj B. Giese K.P. (2004) Expression and function of brain specific small RNAs. Reviews in the Neurosciences 15, 185 198.
70. Schwach F., Vaistij F.E., Jones L. Baulcombe D.C. (2005) An RNA-dependent RNA polymerase prevents meristem invasion by potato virus X and is required for the activity but not the production of a systemic silencing signal. Plant Physiology 138, 1842 1852.
71. Sembdner G. Parthier B. (1993) The biochemistry and the physiological and molecular actions of jasmonates. Annual Review of Plant Physiology and Plant Molecular Biology 44, 569 589.
72. Seo H.S., Song J.T., Cheong J.J., Lee Y.H., Lee Y.W., Hwang I., Lee J.S. Choi Y.D. (2001) Jasmonic acid carboxyl methyltransferase: a key enzyme for jasmonate regulated plant responses. Proceedings of the National Academy of Sciences of the United States of America 98, 4788 4793.
73. Seo S., Katou S., Seto H., Gomi K. Ohashi Y. (2007) The mitogen-activated protein kinases WIPK and SIPK regulate the levels of jasmonic and salicylic acids in wounded tobacco plants. The Plant Journal 49, 899 909.
74. Shimmen T. (2001) Involvement of receptor potentials and action potentials in mechano-perception in plants. Australian Journal of Plant Physiology 28, 567 576.
75. Skibbe M., Qu N., Galis I. Baldwin I.T. (2008) Induced plant defenses in the natural environment: Nicotiana attenuata's WRKY3 and WRKY6 coordinate responses to herbivory. The Plant Cell.
76. Stenzel I., Hause B., Miersch O., Kurz T., Maucher H., Weichert H., Ziegler J., Feussner I. Wasternack C. (2003) Jasmonate biosynthesis and the allene oxide cyclase family of Arabidopsis thaliana. Plant Molecular Biology 51, 895 911.
77. Struik P.C., Yin X. Meinke H. (2008) Plant neurobiology and green plant intelligence: science, metaphors and nonsense. Journal of the Science of Food and Agriculture 88, 363 370.
78. Sunkar R. Zhu J.K. (2007) Micro RNAs and short-interfering RNAs in plants. Journal of Integrative Plant Biology 49, 817 826.
79. Sunkar R., Chinnusamy V., Zhu J.H. Zhu J.K. (2007) Small RNAs as big players in plant abiotic stress responses and nutrient deprivation. Trends in Plant Science 12, 301 309.
80. Swiatek A., Van Dongen W., Esmans E.L. Van Onckelen H. (2004) Metabolic fate of jasmonates in tobacco Bright Yellow-2 cells. Plant Physiology 135, 161 172.
81. Takahashi F., Yoshida R., Ichimura K., Mizoguchi T., Seo S., Yonezawa M., Maruyama K., Yamaguchi-Shinozaki K. Shinozaki K. (2007) The mitogen-activated protein kinase cascade MKK3-MPK6 is an important part of the jasmonate signal transduction pathway in Arabidopsis. The Plant Cell 19, 805 818.
82. Thellier M., Le Sceller L., Norris V., Verdus M.C. Ripoll C. (2000) Long-distance transport, storage and recall of morphogenetic information in plants. The existence of a sort of primitive plant 'memory'. Comptes Rendus De L Academie Des Sciences Serie III-Sciences De La Vie-Life Sciences 323, 81 91.
83. Thellier M., Demongeot J., Norris V., Guespin J., Ripoll C. Thomas R. (2004) A logical (discrete) formulation for the storage and recall of environmental signals in plants. Plant Biology 6, 590 597.
84. Thines B., Katsir L., Melotto M., Niu Y., Mandaokar A., Liu G.H., Nomura K., He S.Y., Howe G.A. Browse J. (2007) JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling. Nature 448, 661 662.
85. Tiryaki I. Staswick P.E. (2002) An Arabidopsis mutant defective in jasmonate response is allelic to the auxin-signaling mutant axr1. Plant Physiology 130, 887 894.
86. Ton J., D'Alessandro M., Jourdie V., Jakab G., Karlen D., Held M., Mauch-Mani B. Turlings T.C.J. (2007) Priming by airborne signals boosts direct and indirect resistance in maize. The Plant Journal 49, 16 26.
87. Tournier B., Tabler M. Kalantidis K. (2006) Phloem flow strongly influences the systemic spread of silencing in GFP Nicotiana benthamiana plants. The Plant Journal 47, 383 394.
88. Trewavas A. (2003) Aspects of plant intelligence. Annals of Botany 92, 1 20.
89. Trewavas A. (2004) Aspects of plant intelligence: an answer to Firn. Annals of Botany 93, 353 357.
90. Trewavas A. (2005) Green plants as intelligent organisms. Trends in Plant Science 10, 413 419.
91. Trewavas A. (2007) Response to Alpi et al.: Plant neurobiology - all metaphors have value. Trends in Plant Science 12, 231 233.
92. Tulving E. (1985) How many memory systems are there? American Psychologist 40, 385 398.
93. Van Bentem S.D. Hirt H. (2007) Using phosphoproteomics to reveal signalling dynamics in plants. Trends in Plant Science 12, 404 411.
94. Voelckel C. Baldwin I.T. (2004) Herbivore-induced plant vaccination. Part II. Array-studies reveal the transience of herbivore-specific transcriptional imprints and a distinct imprint from stress combinations. The Plant Journal 38, 650 663.
95. Von Dahl C.C., Havecker M., Schlogl R. Baldwin I.T. (2006) Caterpillar-elicited methanol emission: a new signal in plant-herbivore interactions? The Plant Journal 46, 948 960.
96. Von Dahl C.C., Winz R.A., Halitschke R., Kuhnemann F., Gase K. Baldwin I.T. (2007) Tuning the herbivore-induced ethylene burst: the role of transcript accumulation and ethylene perception in Nicotiana attenuata. The Plant Journal 51, 293 307.
97. Wassenegger M. Krczal G. (2006) Nomenclature and functions of RNA-directed RNA polymerases. Trends in Plant Science 11, 142 151.
98. Wasternack C. (2007) Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Annals of Botany 100, 681 697.
99. Wu J.Q., Hettenhausen C., Meldau S. Baldwin I.T. (2007) Herbivory rapidly activates MAPK signaling in attacked and unattacked leaf regions but not between leaves of Nicotiana attenuata. The Plant Cell 19, 1096 1122.
100. Xie D.X., Feys B.F., James S., Nieto-Rostro M. Turner J.G. (1998) COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility. Science 280, 1091 1094.
101. Yang W.Y., Devaiah S.P., Pan X.Q., Isaac G., Welti R. Wang X.M. (2007) AtPLAI is an acyl hydrolase involved in basal jasmonic acid production and Arabidopsis resistance to Botrytis cinerea. Journal of Biological Chemistry 282, 18116 18128.
102. Zhang S.Q. Klessig D.F. (2001) MAPK cascades in plant defense signaling. Trends in Plant Science 6, 520 527.
103. Ziegler J., Keinänen M. Baldwin I.T. (2001) Herbivore-induced allene oxide synthase transcripts and jasmonic acid in Nicotiana attenuata. Phytochemistry 58, 729 738.