Plants Know Where It Hurts: Root and Shoot Jasmonic Acid Induction Elicit Differential Responses in Brassica oleracea

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Tytgat, Tom O G ^a   Verhoeven, Koen J F ^b   Jansen, Jeroen J ^a   Raaijmakers, Ciska E ^b   Bakx Schotman, Tanja ^b   McIntyre, Lauren M ^c   van der Putten, Wim H ^b,d   Biere, Arjen ^b   van Dam, Nicole M ^a  

^a RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^b NETHERLANDS INSTITUTE OF ECOLOGY NIOO KNAW   (Netherlands)

^c UNIVERSITY OF FLORIDA   (United States)

^d WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

JASMONIC ACID;

ARTICLE; BIOCHEMISTRY; BRASSICA OLERACEA; GENE EXPRESSION; MOLECULAR MECHANICS; NONHUMAN; NUCLEOTIDE SEQUENCE; PLANT DAMAGE; PLANT DEFENSE; PLANT DEVELOPMENT; PLANT GENE; PLANT HERBIVORE INTERACTION; PLANT METABOLISM; PLANT ROOT; QUALITATIVE ANALYSIS; SHOOT; SIGNAL TRANSDUCTION; TISSUE SPECIFICITY;

BRASSICA; CYCLOPENTANES; OXYLIPINS; PLANT GROWTH REGULATORS; PLANT ROOTS; PLANT SHOOTS;

BRASSICA OLERACEA;

EID: 84878914445     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0065502     Document Type: Article

References (66)

1. Kaplan I, Halitschke R, Kessler A, Sardanelli S, Denno RF, (2008) Constitutive and induced defenses to herbivory in above- and belowground plant tissues. Ecol 89: 392-406.
2. van Dam NM, Witjes L, Svatos A, (2004) Interactions between aboveground and belowground induction of glucosinolates in two wild Brassica species. New Phytol 161: 801-810.
3. Karban R, Baldwin IT (1997) Induced Responses to Herbivory. Chicago, Illinois, USA: University of Chicago Press. 0-226 p.
4. Erb M, Meldau S, Howe GA, (2012) Role of phytohormones in insect-specific plant reactions. Trends Plant Sci 17: 250-259.
5. Dicke M, Baldwin IT, (2010) The evolutionary context for herbivore-induced plant volatiles: beyond the 'cry for help'. Trends Plant Sci 15: 167-175.
6. Balbi V, Devoto A, (2008) Jasmonate signalling network in Arabidopsis thaliana: crucial regulatory nodes and new physiological scenarios. New Phytol 177: 301-318.
7. Ballare CL, (2011) Jasmonate-induced defenses: a tale of intelligence, collaborators and rascals. Trends Plant Sci 16: 249-257.
8. Wasternack C, Kombrink E, (2010) Jasmonates: Structural Requirements for Lipid-Derived Signals Active in Plant Stress Responses and Development. Acs Chemical Biology 5: 63-77.
9. Chini A, Fonseca S, Fernandez G, Adie B, Chico JM, et al. (2007) The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448: 666-671.
10. De Vos M, Van Oosten VR, Van Poecke RMP, Van Pelt JA, Pozo MJ, et al. (2005) Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Mol Plant-Microbe Interact 18: 923-937.
11. Glauser G, Grata E, Dubugnon L, Rudaz S, Farmer EE, et al. (2008) Spatial and temporal dynamics of jasmonate synthesis and accumulation in Arabidopsis in response to wounding. J Biol Chem 283: 16400-16407.
12. Pauwels L, Inze D, Goossens A, (2009) Jasmonate-inducible gene: what does it mean? Trends Plant Sci 14: 87-91.
13. Chung HS, Howe GA, (2009) A Critical Role for the TIFY Motif in Repression of Jasmonate Signaling by a Stabilized Splice Variant of the JASMONATE ZIM-Domain Protein JAZ10 in Arabidopsis. Plant Cell 21: 131-145.
14. Bezemer TM, van Dam NM, (2005) Linking aboveground and belowground interactions via induced plant defenses. Trends Ecol Evol 20: 617-624.
15. Erb M, Lenk C, Degenhardt J, Turlings TCJ, (2009) The underestimated role of roots in defense against leaf attackers. Trends Plant Sci 14: 653-659.
16. Rasmann S, Turlings TCJ, (2007) Simultaneous feeding by aboveground and belowground herbivores attenuates plant-mediated attraction of their respective natural enemies. Ecol Lett 10: 926-936.
17. Van der Putten WH, Vet LEM, Harvey JA, Wackers FL, (2001) Linking above- and belowground multitrophic interactions of plants, herbivores, pathogens, and their antagonists. Trends Ecol Evol 16: 547-554.
18. van Dam NM, Heil M, (2011) Multitrophic interactions below and above ground: en route to the next level. J Ecol 99: 77-88.
19. Gomez S, Ferrieri RA, Schueller M, Orians CM, (2010) Methyl jasmonate elicits rapid changes in carbon and nitrogen dynamics in tomato. New Phytol 188: 835-844.
20. Henkes GJ, Thorpe MR, Minchin PEH, Schurr U, Röse USR, (2008) Jasmonic acid treatment to part of the root system is consistent with simulated leaf herbivory, diverting recently assimilated carbon towards untreated roots within an hour. Plant Cell Environ 31: 1229-1236.
21. Schwachtje J, Minchin PEH, Jahnke S, van Dongen JT, Schittko U, et al. (2006) SNF1-related kinases allow plants to tolerate herbivory by allocating carbon to roots. Proc Natl Acad Sci U S A 103: 12935-12940.
22. Strauss SY, Agrawal AA, (1999) The ecology and evolution of plant tolerance to herbivory. Trends Ecol Evol 14: 179-185.
23. van Dam NM, van der Meijden E (2011) A role for metabolomics in plant ecology. In: Hall RD, editor. Biology of Plant Metabolomics. Chichester, West Sussex, UK: Wiley-Blackwell. 87-107.
24. Rasmann S, Agrawal AA, (2008) In defense of roots: A research agenda for studying plant resistance to belowground herbivory. Plant Physiol 146: 875-880.
25. Jansen JJ, Allwood JW, Marsden-Edwards E, van der Putten WH, Goodacre R, et al. (2009) Metabolomic analysis of the interaction between plants and herbivores. Metabolomics 5: 150-161.
26. Pierre PS, Jansen JJ, Hordijk CA, van Dam NM, Cortesero A-M, et al. (2011) Differences in Volatile Profiles of Turnip Plants Subjected to Single and Dual Herbivory Above- and Belowground. J Chem Ecol 37: 368-377.
27. van Dam NM, Qiu B-L, Hordijk CA, Vet LEM, Jansen JJ, (2010) Identification of Biologically Relevant Compounds in Aboveground and Belowground Induced Volatile Blends. J Chem Ecol 36: 1006-1016.
28. Soler R, Harvey JA, Kamp AFD, Vet LEM, Van der Putten WH, et al. (2007) Root herbivores influence the behaviour of an aboveground parasitoid through changes in plant-volatile signals. Oikos 116: 367-376.
29. Lee HS, Wang JL, Tian L, Jiang HM, Black MA, et al. (2004) Sensitivity of 70-mer oligonucleotides and cDNAs for microarray analysis of gene expression in Arabidopsis and its related species. Plant Biotechnol J 2: 45-57.
30. Broekgaarden C, Poelman EH, Steenhuis G, Voorrips RE, Dicke M, et al. (2007) Genotypic variation in genome-wide transcription profiles induced by insect feeding: Brassica oleracea-Pieris rapae interactions. BMC Genomics 8: 239.
31. Broekgaarden C, Poelman EH, Steenhuis G, Voorrips RE, Dicke M, et al. (2008) Responses of Brassica oleracea cultivars to infestation by the aphid Brevicoryne brassicae: an ecological and molecular approach. Plant Cell Environ 31: 1592-1605.
32. Baldwin IT, (1996) Methyl jasmonate-induced nicotine production in Nicotiana attenuata: Inducing defenses in the field without wounding. Entomol Exp Appl 80: 213-220.
33. Bruinsma M, Ijdema H, van Loon JJA, Dicke M, (2008) Differential effects of jasmonic acid treatment of Brassica nigra on the attraction of pollinators, parasitoids, and butterflies. Entomol Exp Appl 128: 109-116.
34. Koornneef A, Leon-Reyes A, Ritsema T, Verhage A, Den Otter FC, et al. (2008) Kinetics of salicylate-mediated suppression of jasmonate signaling reveal a role for redox modulation. Plant Physiol 147: 1358-1368.
35. Abdel-Farid IB, Jahangir M, Mustafa NR, van Dam NM, van den Hondel C, et al. (2010) Glucosinolate profiling of Brassica rapa cultivars after infection by Leptosphaeria maculans and Fusarium oxysporum. Biochem Syst Ecol 38: 612-620.
36. van Dam NM, Oomen WAT, (2008) Root and shoot jasmonic acid applications differentially affect leaf chemistry and herbivore growth Plant Signal Behav. 3: 91-98.
37. Verhoeven KJF, Simonsen KL, McIntyre LM, (2005) Implementing false discovery rate control: increasing your power. Oikos 108: 643-647.
38. Saeed AI, Sharov V, White J, Li J, Liang W, et al. (2003) TM4: A free, open-source system for microarray data management and analysis. Biotechniques 34: 374-378.
39. Usadel B, Nagel A, Steinhauser D, Gibon Y, Blasing OE, et al. (2006) PageMan: An interactive ontology tool to generate, display, and annotate overview graphs for profiling experiments. BMC Bioinformatics 7: 535.
40. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, et al. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3: research0034.1-research0034.11.
41. Muller PY, Janovjak H, Miserez AR, Dobbie Z, (2002) Processing of gene expression data generated by quantitative real-time RT-PCR. Biotechniques 32: 1372-1379.
42. Chung KM, Igari K, Uchida N, Tasaka M, (2008) New perspectives on plant defense responses through modulation of developmental pathways. Mol Cells 26: 107-112.
43. Soppe WJJ, Bentsink L, Koornneef M, (1999) The early-flowering mutant efs is involved in the autonomous promotion pathway of Arabidopsis thaliana. Development 126: 4763-4770.
44. Grini PE, Thorstensen T, Alm V, Vizcay-Barrena G, Windju SS, et al. (2009) The ASH1 HOMOLOG 2 (ASHH2) Histone H3 Methyltransferase Is Required for Ovule and Anther Development in Arabidopsis. PloS One 4: e7817.
45. Ishikawa M, Kiba T, Chua NH, (2006) The Arabidopsis SPA1 gene is required for circadian clock function and photoperiodic flowering. Plant J 46: 736-746.
46. van Dam NM, Tytgat TOG, Kirkegaard JA, (2009) Root and shoot glucosinolates: a comparison of their diversity, function and interactions in natural and managed ecosystems. Phytochem Rev 8: 171-186.
47. Karban R, Agrawal AA, Thaler JS, Adler LS, (1999) Induced plant responses and information content about risk of herbivory. Trends Ecol Evol 14: 443-447.
48. Qiu BL, Harvey JA, Raaijmakers CE, Vet LEM, van Dam NM, (2009) Nonlinear effects of plant root and shoot jasmonic acid application on the performance of Pieris brassicae and its parasitoid Cotesia glomerata. Funct Ecol 23: 496-505.
49. Jansen JJ, van Dam NM, Hoefsloot HCJ, Smilde AK, (2009) Crossfit analysis: a novel method to characterize the dynamics of induced plant responses. BMC Bioinformatics 10: 425.
50. Dicke M, van Loon JJA, Soler R, (2009) Chemical complexity of volatiles from plants induced by multiple attack. Nat Chem Biol 5: 317-324.
51. Arimura G-i, Matsui K, Takabayashi J, (2009) Chemical and Molecular Ecology of Herbivore-Induced Plant Volatiles: Proximate Factors and Their Ultimate Functions. Plant Cell Physiol 50: 911-923.
52. Hasegawa S, Sogabe Y, Asano T, Nakagawa T, Nakamura H, et al. (2011) Gene expression analysis of wounding-induced root-to-shoot communication in Arabidopsis thaliana. Plant Cell Environ 34: 705-716.
53. Zhou LC, Franck C, Yang K, Pilot G, Heath LS, et al. (2012) Mining for Meaning: Visualization Approaches to Deciphering Arabidopsis Stress Responses in Roots and Shoots. Omics 16: 208-228.
54. Taki N, Sasaki-Sekimoto Y, Obayashi T, Kikuta A, Kobayashi K, et al. (2005) 12-oxo-phytodienoic acid triggers expression of a distinct set of genes and plays a role in wound-induced gene expression in Arabidopsis. Plant Physiol 139: 1268-1283.
55. Bottcher C, Pollmann S, (2009) Plant oxylipins: Plant responses to 12-oxo-phytodienoic acid are governed by its specific structural and functional properties. Febs J 276: 4693-4704.
56. Stintzi A, Weber H, Reymond P, Browse J, Farmer EE, (2001) Plant defense in the absence of jasmonic acid: The role of cyclopentenones. Proc Natl Acad Sci U S A 98: 12837-12842.
57. Chico JM, Chini A, Fonseca S, Solano R, (2008) JAZ repressors set the rhythm in jasmonate signaling. Curr Opin Plant Biol 11: 486-494.
58. Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, et al. (2007) JAZ repressor proteins are targets of the SCFCO11 complex during jasmonate signalling. Nature 448: 661-665.
59. Sheard LB, Tan X, Mao HB, Withers J, Ben-Nissan G, et al. (2010) Jasmonate perception by inositol-phosphate-potentiated COI1-JAZ co-receptor. Nature 468: 400-405.
60. Kazan K, Manners JM, (2012) JAZ repressors and the orchestration of phytohormone crosstalk. Trends Plant Sci 17: 22-31.
61. Chung HS, Niu YJ, Browse J, Howe GA, (2009) Top hits in contemporary JAZ: An update on jasmonate signaling. Phytochemistry 70: 1547-1559.
62. Chung HS, Cooke TF, DePew CL, Patel LC, Ogawa N, et al. (2010) Alternative splicing expands the repertoire of dominant JAZ repressors of jasmonate signaling. Plant J 63: 613-622.
63. Schilmiller AL, Howe GA, (2005) Systemic signaling in the wound response. Curr Opin Plant Biol 8: 369-377.
64. Niu Y, Figueroa P, Browse J, (2011) Characterization of JAZ-interacting bHLH transcription factors that regulate jasmonate responses in Arabidopsis. J Exp Bot 62: 2143-2154.
65. Cheng Z, Sun L, Qi T, Zhang B, Peng W, et al. (2011) The bHLH Transcription Factor MYC3 Interacts with the Jasmonate ZIM-Domain Proteins to Mediate Jasmonate Response in Arabidopsis. Mol Plant 4: 279-288.
66. Matsuura H, Takeishi S, Kiatoka N, Sato C, Sueda K, et al. (2012) Transportation of de novo synthesized jasmonoyl isoleucine in tomato. Phytochemistry 83: 25-33.