RuBPCase activase (RCA) mediates growth–defense trade-offs: silencing RCA redirects jasmonic acid (JA) flux from JA-isoleucine to methyl jasmonate (MeJA) to attenuate induced defense responses in Nicotiana attenuata
Article first published online: 11 NOV 2013
© 2013 Max Planck Society. New Phytologist © 2013 New Phytologist Trust
Volume 201, Issue 4, pages 1385–1395, March 2014
How to Cite
Mitra, S. and Baldwin, I. T. (2014), RuBPCase activase (RCA) mediates growth–defense trade-offs: silencing RCA redirects jasmonic acid (JA) flux from JA-isoleucine to methyl jasmonate (MeJA) to attenuate induced defense responses in Nicotiana attenuata. New Phytologist, 201: 1385–1395. doi: 10.1111/nph.12591
- Issue published online: 3 FEB 2014
- Article first published online: 11 NOV 2013
- Manuscript Accepted: 3 OCT 2013
- Manuscript Received: 6 SEP 2013
- Max Planck Society. Grant Number: RGP0002/2012
- ClockworkGreen. Grant Number: 293926
- 2008. Proteomic identification and characterization of a novel peroxisomal adenine nucleotide transporter supplying ATP for fatty acid beta-oxidation in Soybean and Arabidopsis. Plant Cell 20: 3227–3240. , , .
- 1998. Jasmonate-induced responses are costly but benefit plants under attack in native populations. Proceedings of the National Academy of Sciences, USA 95: 8113–8118. .
- 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. , , .
- 2010. Biotic stress globally downregulates photosynthesis genes. Plant, Cell & Environment 33: 1597–1613. , , , , , .
- 2004. Is photosynthesis limited by decreased Rubisco activity and RuBP content under progressive water stress? New Phytologist 162: 671–681. , , .
- 2013. Herbivores can select for mixed defensive strategies in plants. New Phytologist 197: 576–585. , .
- 2008. Regulation and function of Arabidopsis JASMONATE ZIM-domain genes in response to wounding and herbivory. Plant Physiology 146: 952–964. , , , , , , .
- 1985. Resource availability and plant antiherbivore defense. Science 230: 895–899. , , .
- 1997. Oligosaccharins, brassinolides, and jasmonates: nontraditional regulators of plant growth, development, and gene expression. Plant Cell 9: 1211–1223. , .
- 1992. Jasmonic acid and methyl jasmonate accumulate in wounded Soybean hypocotyls and modulate wound gene-expression. Proceedings of the National Academy of Sciences, USA 89: 4938–4941. , , .
- 2004. Methyl jasmonate and cis-jasmone do not dispose of the herbivore-induced jasmonate burst in Nicotiana attenuata. Physiologia Plantarum 120: 474–481. , .
- 2005. Heat stress effects on ribulose-1,5-bisphosphate carboxylase/oxygenase, Rubisco binding protein and Rubisco activase in wheat leaves. Biologia Plantarum 49: 521–525. , , , .
- 1991. Source–sink carbon relations in 2 Panicum coloratum ecotypes in response to herbivory. Ecology 72: 1472–1483. , , , , , , .
- 1992. Octadecanoid precursors of jasmonic acid activate the synthesis of wound-inducible proteinase-inhibitors. Plant Cell 4: 129–134. , .
- 2009. (+)-7-iso-Jasmonoyl-L-isoleucine is the endogenous bioactive jasmonate. Nature Chemical Biology 5: 344–350. , , , , , , , , .
- 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. , , , , , , .
- 2003. Non-self recognition, transcriptional reprogramming, and secondary metabolite accumulation during plant/pathogen interactions. Proceedings of the National Academy of Sciences, USA 100: 14569–14576. , , , , , , , , , et al.
- 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. , , , , .
- 1997. Ribulose-1,5-bisphosphate carboxylase/oxygenase activase deficiency delays senescence of ribulose-1,5-bisphosphate carboxylase/oxygenase but progressively impairs its catalysis during tobacco leaf development. Plant Physiology 115: 1569–1580. , , , , , .
- 2002. Fitness costs of induced resistance: emerging experimental support for a slippery concept. Trends in Plant Science 7: 61–67. , .
- 1992. The dilemma of plants – to grow or defend. Quarterly Review of Biology 67: 478–478. , .
- 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. , , .
- 1996. Herbivore-induced changes in plant carbon allocation: assessment of below-ground C fluxes using carbon-14. Oecologia 107: 87–94. , , .
- 2002. Oxylipin metabolism in response to stress. Current Opinion in Plant Biology 5: 230–236. , .
- 2005. Integrated expressional analysis: application to the drug discovery process. Methods 37: 280–288. , , , , , , , , , et al.
- 2010. Nicotiana attenuata SIPK, WIPK, NPR1, and fatty acid-amino acid conjugates participate in the induction of jasmonic acid biosynthesis by affecting early enzymatic steps in the pathway. Plant Physiology 152: 96–106. , , , .
- 2006. Silencing threonine deaminase and JAR4 in Nicotiana attenuata impairs jasmonic acid-isoleucine-mediated defenses against Manduca sexta. Plant Cell 18: 3303–3320. , , , .
- 2001. Defensive function of herbivore-induced plant volatile emissions in nature. Science 291: 2141–2144. , .
- 1996. Carbohydrate-modulated gene expression in plants. Annual Review of Plant Physiology and Plant Molecular Biology 47: 509–540. .
- 2011. Cytochrome P450 CYP94B3 mediates catabolism and inactivation of the plant hormone jasmonoyl-L-isoleucine. Proceedings of the National Academy of Sciences, USA 108: 9298–9303. , , .
- 2002. Agrobacterium-mediated transformation of Nicotiana attenuata, a model ecological expression system. Chemoecology 12: 177–183. , , , , .
- 2006. A meta-analysis of tradeoffs between plant tolerance and resistance to herbivores: combining the evidence from ecological and agricultural studies. Oikos 112: 1–9. , .
- 2002. Identification of ultraviolet-B responsive genes in the pea, Pisum sativum L. Plant Cell Reports 20: 1067–1074. , , .
- 2013. Leaf-herbivore attack reduces carbon reserves and regrowth from the roots via jasmonate and auxin signaling. New Phytologist 200: 1234–1246. , , , , , .
- 1998. Growth of tobacco in short-day conditions leads to high starch, low sugars, altered diurnal changes in the Nia transcript and low nitrate reductase activity, and inhibition of amino acid synthesis. Planta 207: 27–41. , , , , .
- 1974. Adaptive patterns in alkaloid physiology. American Naturalist 108: 305–320. .
- 1979. The distribution of secondary compounds within plants. New York, NY, USA: Academic Press. .
- 2009. Regulation of gene expression by jasmonate hormones. Phytochemistry 70: 1560–1570. .
- 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. , , , , .
- 2008. Independently silencing two photosynthetic proteins in Nicotiana attenuata has different effects on herbivore resistance. Plant Physiology 148: 1128–1138. , .
- 2013. Herbivore induction of jasmonic acid and chemical defences reduce photosynthesis in Nicotiana attenuata. Journal of Experimental Botany 64: 685–694. , , .
- 2001. AAA(+) superfamily ATPases: common structure–diverse function. Genes to Cells 6: 575–597. , .
- 2008. Jasmonate perception regulates jasmonate biosynthesis and JA-Ile metabolism: the case of COI1 in Nicotiana attenuata. Plant and Cell Physiology 49: 1165–1175. , , , .
- 2007. Co(i)-ordinating defenses: NaCOI1 mediates herbivore-induced resistance in Nicotiana attenuata and reveals the role of herbivore movement in avoiding defenses. Plant Journal 51: 79–91. , , .
- 2001. Changes in Rubisco and Rubisco activase gene expression and polypeptide content in Pinus halepensis M. subjected to ozone and drought. Plant, Cell & Environment 24: 123–131. , , , , .
- 2003. Rubisco activase – Rubisco's catalytic chaperone. Photosynthesis Research 75: 11–27. .
- 2005. An indole-3-acetic acid carboxyl methyltransferase regulates Arabidopsis leaf development. Plant Cell 17: 2693–2704. , , , , , , , , , et al.
- 2001. Fitness costs of jasmonic acid-induced defense in tomato, Lycopersicon esculentum. Oecologia 126: 380–385. , , .
- 1979. Evolution of plant chemical defense against herbivores. New York, NY, USA: Academic Press. .
- 2009. Enzymes in jasmonate biosynthesis – structure, function, regulation. Phytochemistry 70: 1532–1538. , .
- 2008. Why does herbivore attack reconfigure primary metabolism? Plant Physiology 146: 845–851. , .
- 2008. Reverse genetics in ecological research. PLoS ONE 3: e1543. , , .
- 2006. SNF1-related kinases allow plants to tolerate herbivory by allocating carbon to roots. Proceedings of the National Academy of Sciences, USA 103: 12935–12940. , , , , , .
- 2001. Jasmonic acid carboxyl methyltransferase: a key enzyme for jasmonate-regulated plant responses. Proceedings of the National Academy of Sciences, USA 98: 4788–4793. , , , , , , , .
- 2011. The role of Arabidopsis Rubisco activase in jasmonate-induced leaf senescence. Plant Physiology 155: 751–764. , , , , , .
- 2008. Induced plant defenses in the natural environment: Nicotiana attenuata WRKY3 and WRKY6 coordinate responses to herbivory. Plant Cell 20: 1984–2000. , , , .
- 2007. Coordination of carbon supply and plant growth. Plant, Cell & Environment 30: 1126–1149. , .
- 2006. Quantification of starch in plant tissues. Nature Protocols 1: 1342–1345. , .
- 2002. Jasmonate response locus JAR1 and several related Arabidopsis genes encode enzymes of the firefly luciferase superfamily that show activity on jasmonic, salicylic, and indole-3-acetic acids in an assay for adenylation. Plant Cell 14: 1405–1415. , , .
- 2004. Nicotine's defensive function in nature. Plos Biology 2: 1074–1080. , , , , .
- 2011a. Diverting the flux of the JA pathway in Nicotiana attenuata compromises the plant's defense metabolism and fitness in nature and glasshouse. PLoS ONE 6: e25925. , , .
- 2011b. Ectopic expression of AtJMT in Nicotiana attenuata: creating a metabolic sink has tissue-specific consequences for the jasmonate metabolic network and silences downstream gene expression. Plant Physiology 157: 341–354. , , , .
- 2002. Purification and partial amino acid sequences of an esterase from tomato. Phytochemistry 60: 233–240. , , .
- 2004. Cloning and expression of a tomato cDNA encoding a methyl jasmonate cleaving esterase. European Journal of Biochemistry 271: 2976–2983. , , .
- 2007. JAZ repressor proteins are targets of the SCFCO11 complex during jasmonate signalling. Nature 448: 661–665. , , , , , , , , , .
- 2010. Functional analysis of a tomato salicylic acid methyl transferase and its role in synthesis of the flavor volatile methyl salicylate. Plant Journal 62: 113–123. , , , , , , .
- 2007. Methylation of gibberellins by Arabidopsis GAMT1 and GAMT2. Plant Cell 19: 32–45. , , , , , , , , , et al.
- 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. , , , .
- 2007. Independently silencing two JAR family members impairs levels of trypsin proteinase inhibitors but not nicotine. Planta 226: 159–167. , , , , , .
- 2002. Jasmonates and octadecanoids: signals in plant stress responses and development. Progress in Nucleic Acid Research and Molecular Biology 72: 165–221. , .
- 2013. Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Annals of Botany 111: 1021–1058. , .
- 2012. Jasmonoyl-l-isoleucine hydrolase 1 (JIH1) regulates jasmonoyl-l-isoleucine levels and attenuates plant defenses against herbivores. Plant Journal 72: 758–767. , , , .
- 2008. Methyl jasmonate-elicited herbivore resistance: does MeJA function as a signal without being hydrolyzed to JA? Planta 227: 1161–1168. , , .
- 2012. Plant hormone jasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade. Proceedings of the National Academy of Sciences, USA 109: E1192–E1200. , , , , , , , , , et al.
- 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. , , , , , , .
- 2004. Manipulation of endogenous trypsin proteinase inhibitor production in Nicotiana attenuata demonstrates their function as antiherbivore defenses. Plant Physiology 134: 1181–1190. , , , , .