CoChat
Sign Up
Cited by 292Insect-Plant Interactions and ControlPlant-Microbe Interactions and ImmunityPlant biochemistry and biosynthesis

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

Open access
Guo, Qiang, Major, Ian T, Howe, Gregg A·2018·Current Opinion in Plant Biology
DOI 10.1016/j.pbi.2018.02.009
Open this paper in CoChat — free accountOpen PDF

Abstract

Induced plant resistance depends on the production of specialized metabolites that repel attack by biotic aggressors and is often associated with reduced growth of vegetative tissues. Despite progress in understanding the signal transduction networks that control growth-defense tradeoffs, much remains to be learned about how growth rate is coordinated with changes in metabolism during growth-to-defense transitions. Here, we highlight recent advances in jasmonate research to suggest how a major branch of plant immunity is dynamically regulated to calibrate growth-defense balance with shifts in carbon availability. We review evidence that diminished growth, as an integral facet of induced resistance, may optimize the temporal and spatial expression of defense compounds without compromising other critical roles of central metabolism. New insights into the evolution of jasmonate signaling further suggest that opposing selective pressures associated with too much or too little defense may have shaped the emergence of a modular jasmonate pathway that integrates primary and specialized metabolism through the control of repressor-transcription factor complexes. A better understanding of the mechanistic basis of growth-defense balance has important implications for boosting plant productivity, including insights into how these tradeoffs may be uncoupled for agricultural improvement.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1016/j.pbi.2018.02.009

Cites

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

No references could be resolved yet.

Research works printed but not linked: 65

  1. and recommended reading Papers of particular interest, published within the period of review, have been highlighted as: • of special interest •• of outstanding interest
  2. Stamp N: Out of the quagmire of plant defense hypotheses. Q Rev Biol 2003, 78:23- 55.
  3. Herms DA, Mattson WJ: The dilemma of plants-to grow or defend. Q Rev Biol 1992, 67:283-335.
  4. Heil M, Baldwin IT: Fitness costs of induced resistance: emerging experimental support for a slippery concept. Trends Plant Sci 2002, 7:61-67. •
  5. Zust T, Agrawal AA: Trade-offs between plant growth and defense: an emerging mechnistic synthesis. Annu Rev Plant Biol 2017, 68:513-534.
  6. A comprehensive review of growth-defense tradeoffs associated with plant herbivore interactions. The authors synthesize key concepts that have emerged from studies at the ecological, physiological, and molecular levels.
  7. Huot B, Yao J, Montgomery BL, He SY: Growth-defense tradeoffs in plants: a balancing act to optimize fitness. Mol Plant 2014, 7:1267-1287.
  8. Lozano-Duran R, Zipfel C: Trade-off between growth and immunity: role of brassinosteroids. Trends Plant Sci 2015, 20:12-19.
  9. Havko NE, Major IT, Jewell JB, Attaran E, Browse J, Howe GA: Control of carbon assimilation and partitioning by jasmonate: an accounting of growth-defense balance. Plants 2016, 5:7.
  10. Belkhadir Y, Yang L, Hetzel J, Dangl JL, Chory J: The growth-defense pivot: crisis management in plants mediated by LRR-RK surface receptors. Trends Biochem Sci 2014, 39:447-456.
  11. Chae E, Tran DT, Weigel D: Cooperation and conflict in the plant immune system. PLoS Pathog 2016, 12:e1005452.
  12. Geyter D, Gholami A, Goossens A: Transcriptional machineries in jasmonate- elicited plant secondary metabolism. Trends Plant Sci 2012, 17:349-359.
  13. Zhou M, Memelink J: Jasmonate-responsive transcription factors regulating plant secondary metabolism. Biotechnol Adv 2016, 34:441-449.
  14. D'Auria JC, Gershenzon J: The secondary metabolism of Arabidopsis thaliana: growing like a weed. Curr Opin Plant Biol 2005, 8:308-316.
  15. Aharoni A, Galili G: Metabolic engineering of the plant primary-secondary metabolism interface. Curr Opin Biotechnol 2011, 22:239-244.
  16. Schwachtje J, Baldwin IT: Why does herbivore attack reconfigure primary metabolism? Plant Physiol 2008, 146:845-851.
  17. Zhou SQ, Lou YR, Tzin V, Jander G: Alteration of plant primary metabolism in response to insect herbivory. Plant Physiol 2015, 169:1488-1498.
  18. Papazian S, Khaling E, Bonnet C, Lassueur S, Reymond P, Moritz T, Blande JD, Albrectsen BR: Central metabolic responses to ozone and herbivory affect photosynthesis and stomatal closure. Plant Physiol 2016, 172:2057-2078.
  19. Bilgin DD, Zavala JA, Zhu J, Clough SJ, Ort DR, DeLucia EH: Biotic stress globally downregulates photosynthesis genes. Plant Cell Environ 2010, 33:1597-1613.
  20. Attaran E, Major IT, Cruz JA, Rosa BA, Koo AJ, Chen J, Kramer DM, He SY, Howe GA: Temporal dynamics of growth and photosynthesis suppression in response to jasmonate signaling. Plant Physiol 2014, 165:1302-1314.
  21. Luo R, Wei H, Ye L, Wang K, Chen F, Luo L, Liu L, Li Y, Crabbe MJ, Jin L, et al.: Photosynthetic metabolism of C3 plants shows highly cooperative regulation under changing environments: a systems biological analysis. Proc Natl Acad Sci U S A 2009, 106:847-852.
  22. Ishihara H, Moraes TA, Pyl ET, Schulze WX, Obata T, Scheffel A, Fernie AR, Sulpice R, Stitt M: Growth rate correlates negatively with protein turnover in Arabidopsis accessions. Plant J 2017, 91:416-429. •
  23. Xu G, Yuan M, Ai C, Liu L, Zhuang E, Karapetyan S, Wang S, Dong X: uORF- mediated translation allows engineered plant disease resistance without fitness costs. Nature 2017, 545:491-494.
  24. Machado RA, Ferrieri AP, Robert CA, Glauser G, Kallenbach M, Baldwin IT, Erb M: Leaf-herbivore attack reduces carbon reserves and regrowth from the roots via jasmonate and auxin signaling. New Phytol 2013, 200:1234-1246. •
  25. Falk KL, Tokuhisa JG, Gershenzon J: The effect of sulfur nutrition on plant glucosinolate content: physiology and molecular mechanisms. Plant Biol (Stuttg) 2007, 9:573-581.
  26. Mugford SG, Yoshimoto N, Reichelt M, Wirtz M, Hill L, Mugford ST, Nakazato Y, Noji M, Takahashi H, Kramell R, et al.: Disruption of adenosine-5'- phosphosulfate kinase in Arabidopsis reduces levels of sulfated secondary metabolites. Plant Cell 2009, 21:910-927.
  27. Celenza JL, Quiel JA, Smolen GA, Merrikh H, Silvestro AR, Normanly J, Bender J: The Arabidopsis ATR1 Myb transcription factor controls indolic glucosinolate homeostasis. Plant Physiol 2005, 137:253-262.
  28. Gigolashvili T, Berger B, Mock HP, Muller C, Weisshaar B, Flugge UI: The transcription factor HIG1/MYB51 regulates indolic glucosinolate biosynthesis in Arabidopsis thaliana. Plant J 2007, 50:886-901.
  29. Yatusevich R, Mugford SG, Matthewman C, Gigolashvili T, Frerigmann H, Delaney S, Koprivova A, Flugge UI, Kopriva S: Genes of primary sulfate assimilation •39. Smith AM, Stitt M: Coordination of carbon supply and plant growth. Plant Cell Environ 2007, 30:1126-1149.
  30. A stimulating review that discusses how plant growth is regulated in response to acute and chronic changes in carbon availability. Although built largely on studies pertaining to diurnal changes in carbon status, the proposed acclimatory response hypothesis may also explain how stress-induced changes carbon availability affect growth.
  31. Machado RAR, Arce CCM, Ferrieri AP, Baldwin IT, Erb M: Jasmonate-dependent depletion of soluble sugars compromises plant resistance to Manduca sexta. New Phytol 2015, 207:91-105.
  32. Hanik N, Gomez S, Best M, Schueller M, Orians CM, Ferrieri RA: Partitioning of new carbon as 11 C in Nicotiana tabacum reveals insight into methyl jasmonate induced changes in metabolism. J Chem Ecol 2010, 36:1058-1067.
  33. Babst BA, Ferrieri RA, Gray DW, Lerdau M, Schlyer DJ, Schueller M, Thorpe MR, Orians CM: Jasmonic acid induces rapid changes in carbon transport and partitioning in Populus. New Phytol 2005, 167:63-72.
  34. Schwachtje J, Minchin PE, Jahnke S, van Dongen JT, Schittko U, Baldwin IT: SNF1- related kinases allow plants to tolerate herbivory by allocating carbon to roots. Proc Natl Acad Sci U S A 2006, 103:12935-12940.
  35. De Vleesschauwer D, Filipe O, Hoffman G, Seifi HS, Haeck A, Canlas P, Van Bockhaven J, De Waele E, Demeestere K, Ronald P, et al.: Target of rapamycin signaling orchestrates growth-defense trade-offs in plants. New Phytol 2018, 217:305-319.
  36. Liu XJ, An XH, Liu X, Hu DG, Wang XF, You CX, Hao YJ: MdSnRK1.1 interacts with MdJAZ18 to regulate sucrose-induced anthocyanin and proanthocyanidin accumulation in apple. J Exp Bot 2017, 68:2977-2990.
  37. Song Y, Zhao G, Zhang X, Li L, Xiong F, Zhuo F, Zhang C, Yang Z, Datla R, Ren M, et al.: The crosstalk between target of rapamycin (TOR) and jasmonic acid (JA) signaling existing in Arabidopsis and cotton. Sci Rep 2017, 7:45830.
  38. Howe GA, Major IT, Koo AJK: Modularity in jasmonate signaling for multi- stress resilience. Annu Rev Plant Biol 2018, 69, in press.
  39. Chico JM, Fernandez-Barbero G, Chini A, Fernandez-Calvo P, Diez-Diaz M, Solano R: 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 2014, 26:1967-1980.
  40. Moreno JE, Tao Y, Chory J, Ballare CL: Ecological modulation of plant defense via phytochrome control of jasmonate sensitivity. Proc Natl Acad Sci U S A 2009, 106:4935-4940.
  41. Noir S, Bomer M, Takahashi N, Ishida T, Tsui TL, Balbi V, Shanahan H, Sugimoto K, Devoto A: Jasmonate controls leaf growth by repressing cell proliferation and the onset of endoreduplication while maintaining a potential stand-by mode. Plant Physiol 2013, 161:1930-1951.
  42. Yan Y, Stolz S, Chetelat A, Reymond P, Pagni M, Dubugnon L, Farmer EE: A downstream mediator in the growth repression limb of the jasmonate pathway. Plant Cell 2007, 19:2470-2483.
  43. Hibara K, Isono M, Mimura M, Sentoku N, Kojima M, Sakakibara H, Kitomi Y, Yoshikawa T, Itoh J, Nagato Y: Jasmonate regulates juvenile-to-adult phase transition in rice. Development 2016, 143:3407-3416.
  44. Yang DL, Yao J, Mei CS, Tong XH, Zeng LJ, Li Q, Xiao LT, Sun TP, Li JG, Deng XW, et al.: Plant hormone jasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade. Proc Natl Acad Sci U S A 2012, 109:1192-1200. •
  45. Major IT, Yoshida Y, Campos ML, Kapali G, Xin XF, Sugimoto K, de Oliveira Ferreira D, He SY, Howe GA: Regulation of growth-defense balance by the JASMONATE ZIM-DOMAIN (JAZ)-MYC transcriptional module. New Phytol 2017, 215:1533-1547.
  46. Gasperini D, Chetelat A, Acosta IF, Goossens J, Pauwels L, Goossens A, Dreos R, Alfonso E, Farmer EE: Multilayered organization of jasmonate signalling in the regulation of root growth. PLoS Genet 2015, 11:e1005300.
  47. Chen Q, Sun JQ, Zhai QZ, Zhou WK, Qi LL, Xu L, Wang B, Chen R, Jiang HL, Qi J, et al.: 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 2011, 23:3335-3352.
  48. Navarro L, Bari R, Achard P, Lison P, Nemri A, Harberd NP, Jones JD: DELLAs control plant immune responses by modulating the balance of jasmonic acid and salicylic acid signaling. Curr Biol 2008, 18:650-655.
  49. Hou X, Lee LY, Xia K, Yan Y, Yu H: DELLAs modulate jasmonate signaling via competitive binding to JAZs. Dev Cell 2010, 19:884-894.
  50. Campos ML, Kang JH, Howe GA: Jasmonate-triggered plant immunity. J Chem Ecol 2014, 40:657-675.
  51. Koo AJ, Howe GA: Catabolism and deactivation of the lipid-derived hormone jasmonoyl-isoleucine. Front Plant Sci 2012, 3:19.
  52. Heitz T, Smirnova E, Widemann E, Aubert Y, Pinot F, Menard R: The rise and fall of jasmonate biological activities. Subcell Biochem 2016, 86:405-426.
  53. Chung HS, Cooke TF, Depew CL, Patel LC, Ogawa N, Kobayashi Y, Howe GA: Alternative splicing expands the repertoire of dominant JAZ repressors of jasmonate signaling. Plant J 2010, 63:613-622.
  54. Thireault C, Shyu C, Yoshida Y, St Aubin B, Campos ML, Howe GA: Repression of jasmonate signaling by a non-TIFY JAZ protein in Arabidopsis. Plant J 2015, 82:669-679.
  55. Shyu C, Figueroa P, DePew CL, Cooke TF, Sheard LB, Moreno JE, Katsir L, Zheng N, Browse J, Howe GA: JAZ8 lacks a canonical degron and has an EAR motif that mediates transcriptional repression of jasmonate responses in Arabidopsis. Plant Cell 2012, 24:536-550.
  56. Moreno JE, Shyu C, Campos ML, Patel LC, Chung HS, Yao J, He SY, Howe GA: Negative feedback control of jasmonate signaling by an alternative splice variant of JAZ10. Plant Physiol 2013, 162:1006-1017.
  57. Zhang F, Ke J, Zhang L, Chen R, Sugimoto K, Howe GA, Xu HE, Zhou M, He SY, Melcher K: Structural insights into alternative splicing-mediated desensitization of jasmonate signaling. Proc Natl Acad Sci U S A 2017, 114:1720-1725.
  58. Nakata M, Mitsuda N, Herde M, Koo AJ, Moreno JE, Suzuki K, Howe GA, Ohme- Takagi M: 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 2013, 25:1641-1656.
  59. Mao YB, Liu YQ, Chen DY, Chen FY, Fang X, Hong GJ, Wang LJ, Wang JW, Chen XY: Jasmonate response decay and defense metabolite accumulation contributes to age-regulated dynamics of plant insect resistance. Nat Commun 2017, 8:13925.
  60. Ueda J, Kato J: Isolation and identification of a senescence-promoting substance from wormwood (Artemisia absinthium L.). Plant Physiol 1980, 66:246-249.
  61. Zhang L, Xing D: Methyl jasmonate induces production of reactive oxygen species and alterations in mitochondrial dynamics that precede photosynthetic dysfunction and subsequent cell death. Plant Cell Physiol 2008, 49:1092-1111.
  62. Koo AJK, Howe GA: The wound hormone jasmonate. Phytochemistry 2009, 70:1571-1580.
  63. Thaler JS, Humphrey PT, Whiteman NK: Evolution of jasmonate and salicylate signal crosstalk. Trends Plant Sci 2012, 17:260-270.
  64. Howe G, Jander G: Plant immunity to insect herbivores. Annu Rev Plant Biol 2008, 59:41-66.
  65. Pratiwi P, Tanaka G, Takahashi T, Xie X, Yoneyama K, Matsuura H, Takahashi K: Identification of jasmonic acid and jasmonoyl-isoleucine, and characterization of AOS, AOC, OPR and JAR1 in the model lycophyte Selaginella moellendorffii. Plant Cell Physiol 2017, 58:789-801.

Cited by

Sorted by citations

Authors
Guo, Q., Major, I. T., & Howe, G. A.
Affiliations
Michigan State University (US)
Corresponding author
Howe, Gregg A
ORCID
Venue
Current Opinion in Plant Biology
Publisher
Elsevier BV
Published
2018-08
Volume
44
Pages
72-81
ISSN
1369-5266 (ISSN-L)
DOI
10.1016/j.pbi.2018.02.009
OpenAlex
W2792116459
Cited by
292
References
0
Citations by year
2026: 17 · 2025: 36 · 2024: 20 · 2023: 30 · 2022: 49 · 2021: 45 · 2020: 48 · 2019: 33 · 2018: 14
FWCI
4.27
Type
journal article
Language
en
Open access
Licence
Locations
  • Current Opinion in Plant Biology (acceptedVersion)
  • PubMed (publishedVersion)
Funders
Chemical Sciences, Geosciences and Biosciences Division, Office of Basic Energy Sciences, Office of Science, US Department of Energy (DE-FG02-91ER20021)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Insect Science › Insect-Plant Interactions and Control
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant-Microbe Interactions and Immunity
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Plant biochemistry and biosynthesis
Keywords
growth-defense trade-off, jasmonic acid signaling, induced plant resistance, plant immunity, secondary metabolites, carbon availability, primary metabolism, plant productivity, plant defense regulation
MeSH terms
Cyclopentanes, Signal Transduction, Gene Expression Regulation, Plant, Oxylipins, Plant Immunity

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review