Resolution of growth–defense conflict: mechanistic insights from jasmonate signaling

Stamp, 2003, Out of the quagmire of plant defense hypotheses, Q Rev Biol, 78, 23, 10.1086/367580 Herms, 1992, The dilemma of plants-to grow or defend, Q Rev Biol, 67, 283, 10.1086/417659 Heil, 2002, Fitness costs of induced resistance: emerging experimental support for a slippery concept, Trends Plant Sci, 7, 61, 10.1016/S1360-1385(01)02186-0 Zust, 2017, Trade-offs between plant growth and defense: an emerging mechnistic synthesis, Annu Rev Plant Biol, 68, 513, 10.1146/annurev-arplant-042916-040856 Huot, 2014, Growth-defense tradeoffs in plants: a balancing act to optimize fitness, Mol Plant, 7, 1267, 10.1093/mp/ssu049 Lozano-Duran, 2015, Trade-off between growth and immunity: role of brassinosteroids, Trends Plant Sci, 20, 12, 10.1016/j.tplants.2014.09.003 Havko, 2016, Control of carbon assimilation and partitioning by jasmonate: an accounting of growth-defense balance, Plants, 5, 7, 10.3390/plants5010007 Belkhadir, 2014, The growth-defense pivot: crisis management in plants mediated by LRR-RK surface receptors, Trends Biochem Sci, 39, 447, 10.1016/j.tibs.2014.06.006 Chae, 2016, Cooperation and conflict in the plant immune system, PLoS Pathog, 12, e1005452, 10.1371/journal.ppat.1005452 Geyter, 2012, Transcriptional machineries in jasmonate-elicited plant secondary metabolism, Trends Plant Sci, 17, 349, 10.1016/j.tplants.2012.03.001 Zhou, 2016, Jasmonate-responsive transcription factors regulating plant secondary metabolism, Biotechnol Adv, 34, 441, 10.1016/j.biotechadv.2016.02.004 D’Auria, 2005, The secondary metabolism of Arabidopsis thaliana: growing like a weed, Curr Opin Plant Biol, 8, 308, 10.1016/j.pbi.2005.03.012 Aharoni, 2011, Metabolic engineering of the plant primary–secondary metabolism interface, Curr Opin Biotechnol, 22, 239, 10.1016/j.copbio.2010.11.004 Schwachtje, 2008, Why does herbivore attack reconfigure primary metabolism?, Plant Physiol, 146, 845, 10.1104/pp.107.112490 Zhou, 2015, Alteration of plant primary metabolism in response to insect herbivory, Plant Physiol, 169, 1488 Papazian, 2016, Central metabolic responses to ozone and herbivory affect photosynthesis and stomatal closure, Plant Physiol, 172, 2057, 10.1104/pp.16.01318 Bilgin, 2010, Biotic stress globally downregulates photosynthesis genes, Plant Cell Environ, 33, 1597, 10.1111/j.1365-3040.2010.02167.x Attaran, 2014, Temporal dynamics of growth and photosynthesis suppression in response to jasmonate signaling, Plant Physiol, 165, 1302, 10.1104/pp.114.239004 Luo, 2009, Photosynthetic metabolism of C3 plants shows highly cooperative regulation under changing environments: a systems biological analysis, Proc Natl Acad Sci U S A, 106, 847, 10.1073/pnas.0810731105 Ishihara, 2017, Growth rate correlates negatively with protein turnover in Arabidopsis accessions, Plant J, 91, 416, 10.1111/tpj.13576 Xu, 2017, uORF-mediated translation allows engineered plant disease resistance without fitness costs, Nature, 545, 491, 10.1038/nature22372 Machado, 2013, Leaf-herbivore attack reduces carbon reserves and regrowth from the roots via jasmonate and auxin signaling, New Phytol, 200, 1234, 10.1111/nph.12438 Ullmann-Zeunert, 2013, Quantification of growth-defense trade-offs in a common currency: nitrogen required for phenolamide biosynthesis is not derived from ribulose-1,5-bisphosphate carboxylase/oxygenase turnover, Plant J, 10.1111/tpj.12210 Falk, 2007, The effect of sulfur nutrition on plant glucosinolate content: physiology and molecular mechanisms, Plant Biol (Stuttg), 9, 573, 10.1055/s-2007-965431 Mugford, 2009, Disruption of adenosine-5’-phosphosulfate kinase in Arabidopsis reduces levels of sulfated secondary metabolites, Plant Cell, 21, 910, 10.1105/tpc.109.065581 Celenza, 2005, The Arabidopsis ATR1 Myb transcription factor controls indolic glucosinolate homeostasis, Plant Physiol, 137, 253, 10.1104/pp.104.054395 Gigolashvili, 2007, The transcription factor HIG1/MYB51 regulates indolic glucosinolate biosynthesis in Arabidopsis thaliana, Plant J, 50, 886, 10.1111/j.1365-313X.2007.03099.x Yatusevich, 2010, Genes of primary sulfate assimilation are part of the glucosinolate biosynthetic network in Arabidopsis thaliana, Plant J, 62, 1, 10.1111/j.1365-313X.2009.04118.x Gershenzon, 1994, Metabolic costs of terpenoid accumulation in higher-plants, J Chem Ecol, 20, 1281, 10.1007/BF02059810 Bekaert, 2012, Metabolic and evolutionary costs of herbivory defense: systems biology of glucosinolate synthesis, New Phytol, 196, 596, 10.1111/j.1469-8137.2012.04302.x Nour-Eldin, 2012, NRT/PTR transporters are essential for translocation of glucosinolate defence compounds to seeds, Nature, 488, 531, 10.1038/nature11285 Neilson, 2013, Plant chemical defense: at what cost?, Trends Plant Sci, 18, 250, 10.1016/j.tplants.2013.01.001 Kliebenstein, 2016, False idolatry of the mythical growth versus immunity tradeoff in molecular systems plant pathology, Physiol Mol Plant Pathol, 95, 55, 10.1016/j.pmpp.2016.02.004 Karasov, 2017, Mechanisms to mitigate the trade-off between growth and defense, Plant Cell, 29, 666, 10.1105/tpc.16.00931 Matin, 1991, The molecular-basis of carbon-starvation-induced general resistance in Escherichia coli, Mol Microbiol, 5, 3, 10.1111/j.1365-2958.1991.tb01819.x De Virgilio, 2012, The essence of yeast quiescence, Fems Microbiol Rev, 36, 306, 10.1111/j.1574-6976.2011.00287.x Campos, 2016, Rewiring of jasmonate and phytochrome B signalling uncouples plant growth-defense tradeoffs, Nat Commun, 7, 12570, 10.1038/ncomms12570 Machado, 2017, Herbivory-induced jasmonates constrain plant sugar accumulation and growth by antagonizing gibberellin signaling and not by promoting secondary metabolite production, New Phytol, 215, 803, 10.1111/nph.14597 Smith, 2007, Coordination of carbon supply and plant growth, Plant Cell Environ, 30, 1126, 10.1111/j.1365-3040.2007.01708.x Machado, 2015, Jasmonate-dependent depletion of soluble sugars compromises plant resistance to Manduca sexta, New Phytol, 207, 91, 10.1111/nph.13337 Hanik, 2010, Partitioning of new carbon as 11C in Nicotiana tabacum reveals insight into methyl jasmonate induced changes in metabolism, J Chem Ecol, 36, 1058, 10.1007/s10886-010-9835-x Babst, 2005, Jasmonic acid induces rapid changes in carbon transport and partitioning in Populus, New Phytol, 167, 63, 10.1111/j.1469-8137.2005.01388.x Schwachtje, 2006, SNF1-related kinases allow plants to tolerate herbivory by allocating carbon to roots, Proc Natl Acad Sci U S A, 103, 12935, 10.1073/pnas.0602316103 De Vleesschauwer, 2018, Target of rapamycin signaling orchestrates growth-defense trade-offs in plants, New Phytol, 217, 305, 10.1111/nph.14785 Liu, 2017, MdSnRK1.1 interacts with MdJAZ18 to regulate sucrose-induced anthocyanin and proanthocyanidin accumulation in apple, J Exp Bot, 68, 2977, 10.1093/jxb/erx150 Song, 2017, The crosstalk between target of rapamycin (TOR) and jasmonic acid (JA) signaling existing in Arabidopsis and cotton, Sci Rep, 7, 45830, 10.1038/srep45830 Howe, 2018, Modularity in jasmonate signaling for multi-stress resilience, Annu Rev Plant Biol, 69, 10.1146/annurev-arplant-042817-040047 Chico, 2014, Repression of jasmonate-dependent defenses by shade involves differential regulation of protein stability of MYC transcription factors and their JAZ repressors in Arabidopsis, Plant Cell, 26, 1967, 10.1105/tpc.114.125047 Moreno, 2009, Ecological modulation of plant defense via phytochrome control of jasmonate sensitivity, Proc Natl Acad Sci U S A, 106, 4935, 10.1073/pnas.0900701106 Noir, 2013, Jasmonate controls leaf growth by repressing cell proliferation and the onset of endoreduplication while maintaining a potential stand-by mode, Plant Physiol, 161, 1930, 10.1104/pp.113.214908 Zhang, 2008, Wound-induced endogenous jasmonates stunt plant growth by inhibiting mitosis, PLoS One, e3699, 10.1371/journal.pone.0003699 Yan, 2007, A downstream mediator in the growth repression limb of the jasmonate pathway, Plant Cell, 19, 2470, 10.1105/tpc.107.050708 Hibara, 2016, Jasmonate regulates juvenile-to-adult phase transition in rice, Development, 143, 3407 Yang, 2012, Plant hormone jasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade, Proc Natl Acad Sci U S A, 109, 1192, 10.1073/pnas.1201616109 Major, 2017, Regulation of growth-defense balance by the JASMONATE ZIM-DOMAIN (JAZ)-MYC transcriptional module, New Phytol, 215, 1533, 10.1111/nph.14638 Gasperini, 2015, Multilayered organization of jasmonate signalling in the regulation of root growth, PLoS Genet, 11, e1005300, 10.1371/journal.pgen.1005300 Dubois, 2018, The pivotal role of ethylene in plant growth, Trends Plant Sci, 10.1016/j.tplants.2018.01.003 Chen, 2011, The basic helix–loop–helix transcription factor MYC2 directly represses PLETHORA expression during jasmonate-mediated modulation of the root stem cell niche in Arabidopsis, Plant Cell, 23, 3335, 10.1105/tpc.111.089870 Navarro, 2008, DELLAs control plant immune responses by modulating the balance of jasmonic acid and salicylic acid signaling, Curr Biol, 18, 650, 10.1016/j.cub.2008.03.060 Hou, 2010, DELLAs modulate jasmonate signaling via competitive binding to JAZs, Dev Cell, 19, 884, 10.1016/j.devcel.2010.10.024 Campos, 2014, Jasmonate-triggered plant immunity, J Chem Ecol, 40, 657, 10.1007/s10886-014-0468-3 Koo, 2012, Catabolism and deactivation of the lipid-derived hormone jasmonoyl-isoleucine, Front Plant Sci, 3, 19, 10.3389/fpls.2012.00019 Heitz, 2016, The rise and fall of jasmonate biological activities, Subcell Biochem, 86, 405, 10.1007/978-3-319-25979-6_16 Chung, 2010, Alternative splicing expands the repertoire of dominant JAZ repressors of jasmonate signaling, Plant J, 63, 613, 10.1111/j.1365-313X.2010.04265.x Thireault, 2015, Repression of jasmonate signaling by a non-TIFY JAZ protein in Arabidopsis, Plant J, 82, 669, 10.1111/tpj.12841 Shyu, 2012, JAZ8 lacks a canonical degron and has an EAR motif that mediates transcriptional repression of jasmonate responses in Arabidopsis, Plant Cell, 24, 536, 10.1105/tpc.111.093005 Moreno, 2013, Negative feedback control of jasmonate signaling by an alternative splice variant of JAZ10, Plant Physiol, 162, 1006, 10.1104/pp.113.218164 Zhang, 2017, Structural insights into alternative splicing-mediated desensitization of jasmonate signaling, Proc Natl Acad Sci U S A, 114, 1720, 10.1073/pnas.1616938114 Nakata, 2013, A bHLH-type transcription factor, ABA-INDUCIBLE BHLH-TYPE TRANSCRIPTION FACTOR/JA-ASSOCIATED MYC2-LIKE1, acts as a repressor to negatively regulate jasmonate signaling in Arabidopsis, Plant Cell, 25, 1641, 10.1105/tpc.113.111112 Fonseca, 2014, bHLH003, bHLH013 and bHLH017 are new targets of JAZ repressors negatively regulating JA responses, PLoS One, 9, 10.1371/journal.pone.0086182 Song, 2013, The bHLH subgroup IIId factors negatively regulate jasmonate-mediated plant defense and development, PLoS Genet, 9, 10.1371/journal.pgen.1003653 Mao, 2017, Jasmonate response decay and defense metabolite accumulation contributes to age-regulated dynamics of plant insect resistance, Nat Commun, 8, 13925, 10.1038/ncomms13925 Zhou, 2016, Evolution of herbivore-induced early defense signaling was shaped by genome-wide duplications in Nicotiana, Elife, 5, 10.7554/eLife.19531 Ueda, 1980, Isolation and identification of a senescence-promoting substance from wormwood (Artemisia absinthium L.), Plant Physiol, 66, 246, 10.1104/pp.66.2.246 Zhang, 2008, Methyl jasmonate induces production of reactive oxygen species and alterations in mitochondrial dynamics that precede photosynthetic dysfunction and subsequent cell death, Plant Cell Physiol, 49, 1092, 10.1093/pcp/pcn086 Koo, 2009, The wound hormone jasmonate, Phytochemistry, 70, 1571, 10.1016/j.phytochem.2009.07.018 Thaler, 2012, Evolution of jasmonate and salicylate signal crosstalk, Trends Plant Sci, 17, 260, 10.1016/j.tplants.2012.02.010 Howe, 2008, Plant immunity to insect herbivores, Annu Rev Plant Biol, 59, 41, 10.1146/annurev.arplant.59.032607.092825 Pratiwi, 2017, Identification of jasmonic acid and jasmonoyl-isoleucine, and characterization of AOS, AOC, OPR and JAR1 in the model lycophyte Selaginella moellendorffii, Plant Cell Physiol, 58, 789, 10.1093/pcp/pcx031 Bowman, 2017, Insights into land plant evolution garnered from the Marchantia polymorpha genome, Cell, 171, 10.1016/j.cell.2017.09.030 Shoval, 2012, Evolutionary trade-offs, Pareto optimality, and the geometry of phenotype space, Science, 336, 1157, 10.1126/science.1217405 Chen, 2006, Constitutive activation of the jasmonate signaling pathway enhances the production of secondary metabolites in tomato, FEBS Lett, 580, 2540, 10.1016/j.febslet.2006.03.070 Smirnova, 2017, Jasmonic Acid Oxidase 2 (JAO2) hydroxylates jasmonic acid and represses basal defense and resistance responses against Botrytis cinerea infection, Mol Plant, 10, 1159, 10.1016/j.molp.2017.07.010 Hu, 2013, JAV1 controls jasmonate-regulated plant defense, Mol Cell, 50, 504, 10.1016/j.molcel.2013.04.027 Jimenez-Aleman, 2017, JA-Ile-macrolactones uncouple growth and defense in wild tobacco, Org Biomol Chem, 15, 3391, 10.1039/C7OB00249A Brown, 2002, Yield penalties of disease resistance in crops, Curr Opin Plant Biol, 5, 339, 10.1016/S1369-5266(02)00270-4 Ning, 2017, Balancing immunity and yield in crop plants, Trends Plant Sci, 22, 1069, 10.1016/j.tplants.2017.09.010 Deng, 2017, Epigenetic regulation of antagonistic receptors confers rice blast resistance with yield balance, Science, 355, 962, 10.1126/science.aai8898 Li, 2017, A natural allele of a transcription factor in rice confers broad-spectrum blast resistance, Cell, 170, 10.1016/j.cell.2017.06.008