Herbivore induction of jasmonic acid and chemical defences reduce photosynthesis in Nicotiana attenuata

Journal of Experimental Botany

Volumn 64, Issue 2, 2013, Pages 685-694

  Nabity, Paul D ^a   Zavala, Jorge A ^b   Delucia, Evan H ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b Universidad de Buenos Aires   (Argentina)

Author keywords

chlorophyll fluorescence; defence; lipoxygenase; nicotine; plant insect interaction

Indexed keywords

CHLOROPHYLL; CYCLOPENTANE DERIVATIVE; JASMONIC ACID; LIPOXYGENASE; OXYLIPIN; VEGETABLE PROTEIN;

ANIMAL; ARTICLE; DOWN REGULATION; GENETICS; HERBIVORY; HOST PARASITE INTERACTION; MANDUCA; METABOLISM; PARASITOLOGY; PHOTOSYNTHESIS; PHYSIOLOGY; TOBACCO;

ANIMALS; CHLOROPHYLL; CYCLOPENTANES; DOWN-REGULATION; HERBIVORY; HOST-PARASITE INTERACTIONS; LIPOXYGENASE; MANDUCA; OXYLIPINS; PHOTOSYNTHESIS; PLANT PROTEINS; TOBACCO;

HEXAPODA; NICOTIANA ATTENUATA;

EID: 84872335945     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/ers364     Document Type: Article

References (45)

1. Aldea M, Hamilton JG, Resti JP, Zangerl AR, Berenbaum MR, DeLucia EH. 2005. Indirect effects of insect herbivory on leaf gas exchange in soybean. Plant, Cell and Environment 28, 402-411.
2. Aldea M, Hamilton, JG, Resti JP, Zangerl AR, Berenbaum MR, Frank TD, DeLucia EH. 2006. Comparison of photosynthetic damage from arthropod herbivory and pathogen infection in understory hardwood samplings. Oecologia 149, 221-232.
3. Baker NR. 2008. Chlorophyll fluorescence: A probe of photosynthesis in vivo. Annual Review of Plant Biology 59, 89-113.
4. Baker NR, Harbinson J, Kramer DM. 2007. Determining the limitations and regulation of photosynthetic energy transduction in leaves. Plant, Cell & Environment 30, 1107-1125.
5. Baldwin IT, Callahan P. 1993. Autotoxicity and chemical defense: Nicotine accumulation and carbon gain in solanaceous plants. Oecologia 94, 534-541.
6. Barron-Gafford GA, Rasher U, Bronstein JL, Davidowitz G, Chaszar B, Huxman TE. 2012. Herbivory of wild Manduca sexta causes fast down-regulation of photosynthetic efficiency in Datura wrightii: An early signaling cascade visualized by chlorophyll fluorescence. Photosynthesis Research 113, 249-260.
7. Berger S, Benediktyova Z, Matous K, Bonfig K, Mueller MJ, Nedbal L, Roitsch T. 2007. Visualization of dynamics of plant-pathogen interaction by novel combination of chlorophyll fluorescence imaging and statistical analysis: Differential effects of virulent and avirulent strains of P. syringae and of oxylipins on A. thaliana. Journal of Experimental Botany 58, 797-806.
8. Bilgin DD, Zavala JA, Zhu J, Clough SJ, Ort DR, DeLucia EH. 2010. Biotic stress globally down-regulates photosynthesis genes. Plant, Cell & Environment 33, 1597-1613.
9. Chen Y, Pang Q, Dai S, Wang Y, Chen S, Yan X. 2011. Proteomic identification of differentially expressed proteins in Arabidopsis in response to methyl jasmonate. Journal of Plant Physiology 168, 995-1008.
10. Cipollini D. 2007. Consequences of the overproduction of methyl jasmonate on seed production, tolerance to defoliation, and competitive effect and response of Arabidopsis thaliana. New Phytologist 173, 146-153.
11. Donovan MP, Nabity PD, DeLucia EH. 2012. Salicylic acidmediated reductions in yield in Nicotiana attenuata challenged by aphid herbivory. Arthropod-Plant Interactions doi: 10.1007/ s11829-012-9220-5.
12. Frenkel M, Kulheim C, Jankanpaa HJ, Skogstrom O, Dall'Osto L, Agren J, Bassi R, Moritz T, Moen J, Jansson S. 2009. Improper excess light energy dissipation in Arabidopsis results in a metabolic reprogramming. BMC Plant Biology 9, 12.
13. Gao Z, Meng C, Zhang X, Xu D, Zhao Y, Wang Y, Lv H, Yang L, Chen L, Ye N. 2012. Differential expression of carotenogenic genes, associated changes on astaxanthin production, and photosynthesis features induce by JA in H. pluvialis. PLoS One 7, e42243.
14. Gfeller A, Dubugnon L, Liechti R, Farmer EE. 2010. Jasmonate biochemical pathway. Science Signaling 3, cm3.
15. Giri AP, Wunsche H, Mitra S, Zavala SJA, Muck A, Svatos A, Baldwin IT. 2006. Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera: sphingidae) and its natural host Nicotiana attenuata. VII. Changes in the plant's proteome. Plant Physiology 142, 1621-1641.
16. Gog L, Berenbaum MR, DeLucia EH, Zangerl AR. 2005. Autotoxic effects of essential oils on photosynthesis in parsley, parsnip, and rough lemon. Chemoecology 15, 115-119.
17. Halitschke R, Baldwin IT. 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.
18. Halitschke R, Hamilton JG, Kessler A. 2011. Herbivore-specific elicitation of photosynthesis by mirid bug salivary secretions in the wild tobacco Nicotiana attenuata. New Phytologist 191, 528-535.
19. Heidel AJ, Baldwin IT. 2004. Microarray analysis of salicylic acidand jasmonic acid-signaling in responses of Nicotiana attenuata to attack by insects from multiple feeding guilds. Plant, Cell & Environment 27, 1362-1373.
20. Keinanen 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 Agriculture and Food Chemistry 49, 3553-3558.
21. Kessler A, Halitschke R, Baldwin IT. 2004. Silencing the jasmonate cascade: Induced plant defenses and insect populations. Science 305, 665-668.
22. Kessler A, Halitschke R, Poveda K. 2011. Herbivory-mediated pollinator limitation: Negative impacts of induced volatiles on plant-pollinator interactions. Ecology 92, 1769-1780.
23. Kim EH, Kim YS, Park SH, Koo YJ, Choi YD, Chung YY, Lee IJ, Kim JK. 2009. Methyl jasmonate reduces grain yield by mediating stress signals to alter spikelet development in rice. Plant Physiology 149, 1751-1760.
24. Krugel 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.
25. Longstaff BJ, Kildea T, Runcie JW, Cheshire A, Dennison WC, Hurd C, Kana T, Raven JA, Larkum AW. 2002. An in situ study of photosynthetic oxygen exchange and electron transport rate in the marine macroalga Ulva lactuca (Chlorophyta). Photosynthesis Research 74, 281-293.
26. Maserti BE, Del Carratore R, Della Croce CM, et al. 2010. Comparative analysis of proteome changes induced by the twospotted spider mite Tetranychus urticae and methyl jasmonate in citrus leaves. Journal of Plant Physiology 168, 392-402.
27. McKey D. 1974. Adaptive patterns in alkaloid physiology. American Naturalist 108, 305-320.
28. Nabity PD, Zavala JA, DeLucia EH. 2009. Indirect suppression of photosynthesis on individual leaves by arthropod herbivory. Annals of Botany 103, 655-663.
29. Nabity PD, Hillstrom ML, Lindroth RL, DeLucia EH. 2012. Elevated CO2 interacts with herbivory to alter chlorophyll fluorescence and leaf temperature in Betula papyrifera and Populus tremuloides. Oecologia 169, 905-913.
30. Sack L, Holbrook NM. 2006. Leaf hydraulics. Annual Review of Plant Biology 57, 361-381.
31. Shi Q, Li C, Zhang F. 2006. Nicotine synthesis in Nicotiana tabacum L. induced by mechanical wounding is regulated by auxin. Journal of Experimental Botany 57, 2899-2907.
32. Steppuhn A, Gase K, Krock B, Halitschke R, Baldwin IT. 2004. Nicotine's defensive function in nature. PLoS Biology 2, 1074-1080.
33. Tang JY, Zielinski RE, Zangerl AR, Crofts AR, Berenbaum MR, DeLucia EH. 2006. The differential effects of herbivory by first and fourth instars of Trichoplusia ni (Lepidoptera: noctuidae) on photosynthesis in Arabidopsis thaliana. Journal of Experimental Botany 57, 527-536.
34. Tang JY, Zielinski R, Aldea M, DeLucia EH. 2009. Spatial association of photosynthesis and chemical defense in Arabidopsis thaliana following herbivory by Trichoplusia ni. Physiologia Plantarum 137, 115-124.
35. Thivierge K, Prado A, Driscoll BT, Bonneil E, Thibault P, Bede JC. 2010. Caterpillar and salivary specific modification of plant proteins. Journal of Proteome Research 9, 5887-5895.
36. Van Dam NM, Horn M, Mares M, Baldwin IT. 2001. Ontogeny constrains systemic protease inhibitor response in Nicotiana attenuata. Journal of Chemical Ecology 27, 547-568.
37. Voelckel C, Baldwin IT. 2004. Herbivore-induced plant vaccination. Part II. Array studies reveal the transience of herbivorespecific transcriptional imprints and a distinct imprint from stress combinations. The Plant Journal 38, 650-663.
38. Walling LL. 2000. The myriad plant responses to herbivores. Journal of Plant Growth and Regulation 19, 195-216.
39. Wang L, Halitschke R, Kang J, Berg A, Harnish F, Baldwin IT. 2007. Independently silencing two members of JAR family impairs trypsin protease inhibitors activities but not nicotine accumulations. Planta 226, 159-167.
40. 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.
41. Welter SC. 1989. Arthropod impact on plant gas exchange. In Bernays EA, ed. Insect-plant interactions. CRC Press, Boca Raton, FL, 135-151.
42. Zangerl AR, Arntz AM, Berenbaum MR. 1997. Physiological price of an induced chemical defense: Photosynthesis, respiration, biosynthesis, and growth. Oecologia 109, 433-441.
43. Zangerl AR, Hamilton JG, Miller TJ, Crofts AR, Oxborough K, Berenbaum MR, DeLucia EH. 2002. Impact of folivory on photosynthesis is greater than the sum of its holes. Proceedings of the National Academy of Sciences USA 99, 1088-1091.
44. Zavala JA, Baldwin IT. 2004. Fitness benefits of trypsin proteinase inhibitor expression in Nicotiana attenuata are greater than their costs when plants are attacked. BMC Ecology 4, 11.
45. Zavala JA, Patankar AG, Gase K, Baldwin IT. 2004. Constitutive and inducible trypsin proteinase inhibitor production incurs large fitness costs in Nicotiana attenuata. Proceedings of the National Academy of Sciences USA 101, 1607-1612.