Tissue specific diurnal rhythms of metabolites and their regulation during herbivore attack in a native Tobacco, Nicotiana attenuata

PLoS ONE

Volumn 6, Issue 10, 2011, Pages

  Kim, Sang Gyu ^a   Yon, Felipe ^a   Gaquerel, Emmanuel ^a   Gulati, Jyotasana ^a   Baldwin, Ian T ^a  

^a MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

12 OXOPHYTODIENOIC ACID; COUMAROYL TYRAMINE; DISACCHARIDE; JASMONIC ACID; LYCIUMOSIDE 1; PHENYLALANINE; TYROSINE; UNCLASSIFIED DRUG; 12-OXOPHYTODIENOIC ACID; CYCLOPENTANE DERIVATIVE; GLYCOSIDE; MESSENGER RNA; OXYLIPIN; POLYAMINE; UNSATURATED FATTY ACID;

ALGORITHM; ARTICLE; BIOSYNTHESIS; CIRCADIAN RHYTHM; CONTROLLED STUDY; GENETIC TRANSCRIPTION; HERBIVORE; LIQUID CHROMATOGRAPHY; MANDUCA SEXTA; MASS SPECTROMETRY; METABOLIC REGULATION; NICOTINA ATTENUTA; NONHUMAN; OSCILLATION; PLANT LEAF; PLANT ROOT; TISSUE SPECIFICITY; TOBACCO; ANIMAL; ANTIBODY SPECIFICITY; DRUG EFFECT; GENETICS; HERBIVORY; LARVA; LEPIDOPTERA; MECHANICS; METABOLISM; PHYSIOLOGY; PLANT GENE;

HEXAPODA; MANDUCA SEXTA; NICOTIANA ATTENUATA; NICOTIANA TABACUM;

ANIMALS; CIRCADIAN RHYTHM; CYCLOPENTANES; DISACCHARIDES; FATTY ACIDS, UNSATURATED; GENES, PLANT; GLYCOSIDES; HERBIVORY; LARVA; MANDUCA; MECHANICAL PROCESSES; ORGAN SPECIFICITY; OXYLIPINS; PHENYLALANINE; PLANT LEAVES; PLANT ROOTS; POLYAMINES; RNA, MESSENGER; TOBACCO; TYROSINE;

EID: 80054755079     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0026214     Document Type: Article

References (60)

1. Pruneda-Paz JL, Kay SA, (2010) An expanding universe of circadian networks in higher plants. Trends in Plant Science 15: 259-265.
2. Espinoza C, Degenkolbe T, Caldana C, Zuther E, Leisse A, et al. (2010) Interaction with diurnal and circadian regulation results in dynamic metabolic and transcriptional changes during cold acclimation in Arabidopsis. PLoS One 5: e14101.
3. Kolosova N, Gorenstein N, Kish CM, Dudareva N, (2001) Regulation of circadian methyl benzoate emission in diurnally and nocturnally emitting plants. The Plant Cell 13: 2333-2347.
4. Wang W, Barnaby JY, Tada Y, Li H, Tor M, et al. (2011) Timing of plant immune responses by a central circadian regulator. Nature 470: 110-114.
5. Doherty C, Kay S, (2010) Circadian control of global gene expression patterns. Annual Review of Genetics 44: 419-444.
6. Covington MF, Maloof JN, Straume M, Kay SA, Harmer SL, (2008) Global transcriptome analysis reveals circadian regulation of key pathways in plant growth and development. Genome Biology 9: R130.
7. Dodd AN, Salathia N, Hall A, Kévei E, Tóth R, et al. (2005) Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science 309: 630-633.
8. Michael TP, Salomé PA, Yu HJ, Spencer TR, Sharp EL, et al. (2003) Enhanced fitness conferred by naturally occurring variation in the circadian clock. Science 302: 1049-1053.
9. Gibon Y, Usadel B, Blaesing OE, Kamlage B, Hoehne M, et al. (2006) Integration of metabolite with transcript and enzyme activity profiling during diurnal cycles in Arabidopsis rosettes. Genome Biology 7: R76.
10. James AB, Monreal JA, Nimmo GA, Kelly CL, Herzyk P, et al. (2008) The circadian clock in Arabidopsis roots is a simplified slave version of the clock in shoots. Science 322: 1832-1835.
11. Moreno-Risueno MA, Van Norman JM, Moreno A, Zhang J, Ahnert SE, et al. (2010) Oscillating gene expression determines competence for periodic Arabidopsis root branching. Science 329: 1306-1311.
12. Takase T, Ishikawa H, Murakami H, Kikuchi J, Sato-Nara K, et al. (2011) The circadian clock modulates water dynamics and aquaporin expression in Arabidopsis roots. Plant and Cell Physiology 52: 373-383.
13. Kessler D, Baldwin IT, (2007) Making sense of nectar scents: the effects of nectar secondary metabolites on floral visitors of Nicotiana attenuata. The Plant Journal 49: 840-854.
14. Kessler D, Diezel C, Baldwin IT, (2010) Changing pollinators as a means of escaping herbivores. Current Biology 20: 237-242.
15. Allmann S, Halitschke R, Schuurink RC, Baldwin IT, (2010) Oxylipin channelling in Nicotiana attenuata: lipoxygenase 2 supplies substrates for green leaf volatile production. Plant Cell and Environment 33: 2028-2040.
16. Halitschke R, Schittko U, Pohnert G, Boland W, Baldwin IT, (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.
17. Gaquerel E, Heiling S, Schoettner M, Zurek G, Baldwin IT, (2010) Development and validation of a liquid chromatography-electrospray ionization-time-of-flight mass spectrometry method for induced changes in Nicotiana attenuata leaves during simulated herbivory. Journal of Agricultural and Food Chemistry 58: 9418-9427.
18. Keinänen M, Oldham NJ, Baldwin IT, (2001) Rapid HPLC screening of jasmonate-induced increases in tobacco alkaloids, phenolics, and diterpene glycosides in Nicotiana attenuata. Journal of Agricultural and Food Chemistry 49: 3553-3558.
19. Smith CA, Want EJ, O'Maille G, Abagyan R, Siuzdak G, (2006) XCMS: Processing mass spectrometry data for metabolite profiling using nonlinear peak alignment, matching, and identification. Analytical Chemistry 78: 779-787.
20. Michael TP, Mockler TC, Breton G, McEntee C, Byer A, et al. (2008) Network discovery pipeline elucidates conserved time-of-day-specific cis-regulatory modules. PLoS Genetics 4: e14.
21. Schwachtje J, Baldwin IT, (2008) Why does herbivore attack reconfigure primary metabolism? Plant Physiology 146: 845-851.
22. Harmer SL, Hogenesch JB, Straume M, Chang HS, Han B, et al. (2000) Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science 290: 2110-2113.
23. Chen LQ, Hou BH, Lalonde S, Takanaga H, Hartung ML, et al. (2010) Sugar transporters for intercellular exchange and nutrition of pathogens. Nature 468: 527-532.
24. Schwachtje J, Minchin PE, Jahnke S, van Dongen JT, Schittko U, et al. (2006) SNF1-related kinases allow plants to tolerate herbivory by allocating carbon to roots. Proceedings of the National Academy of Sciences of the United States of America 103: 12935-12940.
25. Stitt M, Lunn J, Usadel B, (2010) Arabidopsis and primary photosynthetic metabolism- more than the icing on the cake. The Plant Journal 61: 1067-1091.
26. Lu Y, Gehan JP, Sharkey TD, (2005) Daylength and circadian effects on starch degradation and maltose metabolism. Plant Physiology 138: 2280-2291.
27. Graf A, Schlereth A, Stitt M, Smith AM, (2010) Circadian control of carbohydrate availability for growth in Arabidopsis plants at night. Proceedings of the National Academy of Sciences of the United States of America 107: 9458-9463.
28. Bläsing OE, Gibon Y, Günther M, Höhne M, Morcuende R, et al. (2005) Sugars and circadian regulation make major contributions to the global regulation of diurnal gene expression in Arabidopsis. The Plant Cell 17: 3257-3281.
29. Heil M, Baldwin IT, (2002) Fitness costs of induced resistance: emerging experimental support for a slippery concept. Trends in Plant Science 7: 61-67.
30. Kaplan I, Halitschke R, Kessler A, Rehill BJ, Sardanelli S, et al. (2008) Physiological integration of roots and shoots in plant defense strategies links above- and belowground herbivory. Ecology Letters 11: 841-851.
31. Heiling S, Schuman MC, Schoettner M, Mukerjee P, Berger B, et al. (2010) Jasmonate and ppHsystemin regulate key malonylation steps in the biosynthesis of 17-hydroxygeranyllinalool diterpene glycosides, an abundant and effective direct defense against herbivores in Nicotiana attenuata. The Plant Cell 22: 273-292.
32. Schittko U, Hermsmeier D, Baldwin IT, (2001) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. II. Accumulation of plant mRNAs in response to insect-derived cues. Plant Physiology 125: 701-710.
33. Vogt T, (2010) Phenylpropanoid biosynthesis. Molecular Plant 3: 2-20.
34. Gattolin S, Newbury HJ, Bale JS, Tseng HM, Barrett DA, et al. (2008) A diurnal component to the variation in sieve tube amino acid content in wheat. Plant Physiology 147: 912-921.
35. Hunt E, Gattolin S, Newbury HJ, Bale JS, Tseng HM, et al. (2010) A mutation in amino acid permease AAP6 reduces the amino acid content of the Arabidopsis sieve elements but leaves aphid herbivores unaffected. Journal of Experimental Botany 61: 55-64.
36. Turgeon R, Wolf S, (2009) Phloem transport: cellular pathways and molecular trafficking. Annual Review of Plant Biology 60: 207-221.
37. Abe I, Takahashi Y, Morita H, Noguchi H, (2001) Benzalacetone synthase. European Journal of Biochemistry 268: 3354-3359.
38. Euler M, Baldwin IT, (1996) The chemistry of defense and apparency in the corollas of Nicotiana attenuata. Oecologia 107: 102-112.
39. Hagel JM, Facchini PJ, (2005) Elevated tyrosine decarboxylase and tyramine hydroxycinnamoyltransferase levels increase wound-induced tyramine-derived hydroxycinnamic acid amide accumulation in transgenic tobacco leaves. Planta 221: 904-914.
40. Louis V, Negrel J, (1991) Tyramine hydroxycinnamoyl transferase in the roots of wheat and barley seedlings. Phytochemistry 30: 2519-2522.
41. Muroi A, Ishihara A, Tanaka C, Ishizuka A, Takabayashi J, et al. (2009) Accumulation of hydroxycinnamic acid amides induced by pathogen infection and identification of agmatine coumaroyltransferase in Arabidopsis thaliana. Planta 230: 517-527.
42. Newman MA, von Roepenack-Lahaye E, Parr A, Daniels MJ, Dow JM, (2001) Induction of hydroxycinnamoyl-tyramine conjugates in pepper by Xanthomonas campestris, a plant defense response activated by hrp gene-dependent and hrp gene-independent mechanisms. Molecular Plant-Microbe Interactions 14: 785-792.
43. Wu J, Baldwin IT, (2010) New insights into plant responses to the attack from insect herbivores. Annual Review of Genetics 44: 1-24.
44. Bonaventure G, Vandoorn A, Baldwin IT, (2011) Herbivore-associated elicitors: FAC signaling and metabolism. Trends in Plant Science 16: 294-299.
45. Abdala G, Miersch O, Kramell R, Vigliocco A, Agostini E, et al. (2003) Jasmonate and octadecanoid occurrence in tomato hairy roots. Endogenous level changes in response to NaCl. Plant Growth Regulation 40: 21-27.
46. Baldwin IT, Schmelz EA, Ohnmeiss TE, (1994) Wound-induced changes in root and shoot jasmonic acid pools correlate with induced nicotine synthesis in Nicotiana sylvestris spegazzini and comes. Journal of Chemical Ecology 20: 2139-2157.
47. Bonaventure G, Schuck S, Baldwin IT, (2011) Revealing complexity and specificity in the activation of lipase-mediated oxylipin biosynthesis: A specific role of the Nicotiana attenuata GLA1 lipase in the activation of JA biosynthesis in leaves and roots. Plant Cell & Environment 34: 1507-1520.
48. Gao X, Starr J, Göbel C, Engelberth J, Feussner I, et al. (2008) Maize 9-lipoxygenase ZmLOX3 controls development, root-specific expression of defense genes, and resistance to root-knot nematodes. Molecular Plant-Microbe Interactions 21: 98-109.
49. Wang L, Allmann S, Wu J, Baldwin IT, (2008) Comparisons of LIPOXYGENASE3- and JASMONATE-RESISTANT4/6-silenced plants reveal that jasmonic acid and jasmonic acid-amino acid conjugates play different roles in herbivore resistance of Nicotiana attenuata. Plant Physiology 146: 904-915.
50. O'Connor TR, Dyreson C, Wyrick JJ, (2005) Athena: a resource for rapid visualization and systematic analysis of Arabidopsis promoter sequences. Bioinformatics 21: 4411-4413.
51. Pan Y, Michael TP, Hudson ME, Kay SA, Chory J, et al. (2009) Cytochrome P450 Monooxygenases as Reporters for Circadian-Regulated Pathways. Plant Physiology 150: 858-878.
52. Robson F, Okamoto H, Patrick E, Harris SR, Wasternack C, et al. (2010) Jasmonate and phytochrome A signaling in Arabidopsis wound and shade responses are integrated through JAZ1 stability. The Plant Cell 22: 1143-1160.
53. Radhika V, Kost C, Mithofer A, Boland W, (2010) Regulation of extrafloral nectar secretion by jasmonates in lima bean is light dependent. Proceedings of the National Academy of Sciences of the United States of America 107: 17228-17233.
54. Kerwin RE, Jimenez-Gomez JM, Fulop D, Harmer SL, Maloof JN, et al. (2011) Network quantitative trait loci mapping of circadian clock outputs identifies metabolic pathway-to-clock linkages in Arabidopsis. The Plant Cell 23: 471-485.
55. Ueda HR, Chen W, Minami Y, Honma S, Honma K, et al. (2004) Molecular-timetable methods for detection of body time and rhythm disorders from single-time-point genome-wide expression profiles. Proceedings of the National Academy of Sciences of the United States of America 101: 11227-11232.
56. Gaquerel E, Weinhold A, Baldwin IT, (2009) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphigidae) and its natural host Nicotiana attenuata. VIII. An unbiased GCxGC-ToFMS analysis of the plant's elicited volatile emissions. Plant Physiology 149: 1408-1423.
57. Kaur H, Heinzel N, Schöttner M, Baldwin IT, Gális I, (2010) R2R3-NaMYB8 regulates the accumulation of phenylpropanoid-polyamine conjugates, which are essential for local and systemic defense against insect herbivores in Nicotiana attenuata. Plant Physiology 152: 1731-1747.
58. Krügel T, Lim M, Gase K, Halitschke R, Baldwin IT, (2002) Agrobacterium-mediated transformation of Nicotiana attenuata, a model ecological expression system. Chemoecology 12: 177-183.
59. Guillet G, De Luca V, (2005) Wound-inducible biosynthesis of phytoalexin hydroxycinnamic acid amides of tyramine in tryptophan and tyrosine decarboxylase transgenic tobacco lines. Plant Physiology 137: 692-699.
60. Pearce G, Marchand PA, Griswold J, Lewis NG, Ryan CA, (1998) Accumulation of feruloyltyramine and p-coumaroyltyramine in tomato leaves in response to wounding. Phytochemistry 47: 659-664.