Cited by 89Plant-Microbe Interactions and ImmunityInsect-Plant Interactions and ControlImmune Response and Inflammation

The DOI matches its Crossref record.

False idolatry of the mythical growth versus immunity tradeoff in molecular systems plant pathology

Open access
Kliebenstein, Daniel J.·2016·Physiological and Molecular Plant Pathology

Abstract

Systems studies of signal transduction pathways that modulate plant growth and immunity are rapidly identifying a large number of interactions within these pathways. These interactions are frequently presented as mechanisms allowing a plant to make proper decisions with regards to how to partition energy and resources in a proposed growth versus immunity tradeoff. This is a reinterpretation of the classical costs of resistance theory that has a long history in the ecology research community. While the ecology community is reinterpreting this theory, the reinterpretation has not been introduced into the molecular systems biology community that is studying the intersection of regulatory pathways. In this article, I describe evidence against a simple growth versus immunity tradeoff concept and propose an alternative wherein the intersection of these regulatory pathways is instead designed to coordinate these pathways, and not simply link them in mutual antagonism, to optimize fitness in complex environments where resistance/immunity and growth do not have simple linear relationships with fitness.

Overview

Integrity signals

Registry

Crossref · 10.1016/j.pmpp.2016.02.004

Cites

Statistics

Recomputing p-values needs the paper’s full text.

Verification

Claims the paper makes

We couldn’t retrieve this paper’s full text, so its claims and self-check weren’t run. The registry and citation checks still apply.

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?

Citations

Cites

No references could be resolved yet.

Research works printed but not linked: 73

  1. Strauss, 1999, The ecology and evolution of plant tolerance to herbivory, Trends Ecol. Evol., 14, 179, 10.1016/S0169-5347(98)01576-6 · DOI
  2. Agrawal, 1999, Costs of induced responses and tolerance to herbivory in male and female fitness components of wild radish, Evolution, 53, 1093, 10.1111/j.1558-5646.1999.tb04524.x · DOI
  3. Agrawal, 2011, Current trends in the evolutionary ecology of plant defence, Funct. Ecol., 25, 420, 10.1111/j.1365-2435.2010.01796.x · DOI
  4. Agrawal, 2011, New synthesis-trade-offs in chemical ecology, J. Chem. Ecol., 37, 230, 10.1007/s10886-011-9930-7 · DOI
  5. Lin, 2013, Inverse modulation of plant immune and brassinosteroid signaling pathways by the receptor-like cytoplasmic kinase BIK1, Proc. Natl. Acad. Sci. U. S. A., 110, 12114, 10.1073/pnas.1302154110 · DOI
  6. Lozano-Duran, 2013, The transcriptional regulator BZR1 mediates trade-off between plant innate immunity and growth, Elife, 2
  7. Chandran, 2014, Atypical E2F transcriptional repressor DEL1 acts at the intersection of plant growth and immunity by controlling the hormone salicylic acid, Cell Host Microbe, 15, 506, 10.1016/j.chom.2014.03.007 · DOI
  8. Fan, 2014, The bHLH transcription factor HBI1 mediates the trade-off between growth and pathogen-associated molecular pattern-triggered immunity in Arabidopsis, Plant Cell, 26, 828, 10.1105/tpc.113.121111 · DOI
  9. Malinovsky, 2014, Antagonistic regulation of growth and immunity by the Arabidopsis basic helix-loop-helix transcription factor homolog of brassinosteroid enhanced expression2 interacting with increased leaf inclination1 binding bHLH1, Plant physiol., 164, 1443, 10.1104/pp.113.234625 · DOI
  10. Wang, 2014, At the intersection of plant growth and immunity, Cell Host Microbe, 15, 401, 10.1016/j.chom.2014.03.014 · DOI
  11. Lozano-Duran, 2015, Trade-off between growth and immunity: role of brassinosteroids, Trends Plant Sci., 20, 12, 10.1016/j.tplants.2014.09.003 · DOI
  12. Herms, 1992, The dilemma of plants – to grow or defend, Q. Rev. Biol., 67, 283, 10.1086/417659 · DOI
  13. Pieterse CMJ, Van der Does D, Zamioudis C, Leon-Reyes A, Van Wees SCM. Hormonal modulation of plant immunity. In: Schekman R, editor. Annual Review of Cell and Developmental Biology, vol. 282012. p. 489–521. · DOI
  14. Wierzba, 2015, An allelic series of bak1 mutations differentially alter bir1 cell-death, immune response, growth, and root development phenotypes in Arabidopsis thaliana, Genetics
  15. Navarro, 2006, A plant miRNA contributes to antibacterial resistance by repressing auxin signaling, Science, 312, 436, 10.1126/science.1126088 · DOI
  16. Navarro, 2008, DELLAs control plant immune responses by modulating the balance and salicylic acid signaling, Curr. Biol., 18, 650, 10.1016/j.cub.2008.03.060 · DOI
  17. Yang, 2012, Plant hormone jasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade, Proc. Natl. Acad. Sci. U. S. A., 109, E1192, 10.1073/pnas.1201616109 · DOI
  18. Attaran, 2014, Temporal dynamics of growth and photosynthesis suppression in response to jasmonate signaling, Plant Physiol., 165, 1302, 10.1104/pp.114.239004 · DOI
  19. 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 · DOI
  20. Zhang, 2013, Crosstalk between the circadian clock and innate immunity in Arabidopsis, Plos Pathog., 9
  21. Wang, 2011, Timing of plant immune responses by a central circadian regulator, Nature, 470, 110, 10.1038/nature09766 · DOI
  22. Fay, 2015, Grassland productivity limited by multiple nutrients, Nat. Plants, 1, 15080, 10.1038/nplants.2015.80 · DOI
  23. 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 · DOI
  24. Halkier, 2006, Biology and biochemistry of glucosinolates, Annu. Rev. Plant Biol., 57, 303, 10.1146/annurev.arplant.57.032905.105228 · DOI
  25. Glazebrook, 2005, Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens, Annu. Rev. Phytopathol., 43, 205, 10.1146/annurev.phyto.43.040204.135923 · DOI
  26. Rate, 1999, The gain-of-function Arabidopsis acd6 mutant reveals novel regulation and function of the salicylic acid signaling pathway in controlling cell death, defenses, and cell growth, Plant Cell., 11, 1695, 10.1105/tpc.11.9.1695 · DOI
  27. Song, 2004, A key role for ALD1 in activation of local and systemic defenses in Arabidopsis, Plant J., 40, 200, 10.1111/j.1365-313X.2004.02200.x · DOI
  28. Ellis, 2001, The Arabidopsis mutant cev1 has constitutively active jasmonate and ethylene signal pathways and enhanced resistance to pathogens, Plant Cell., 13, 1025, 10.1105/tpc.13.5.1025 · DOI
  29. Lu, 2009, Genetic analysis of acd6-1 reveals complex defense networks and leads to identification of novel defense genes in Arabidopsis, Plant J., 58, 401, 10.1111/j.1365-313X.2009.03791.x · DOI
  30. Todesco, 2010, Natural allelic variation underlying a major fitness trade-off in Arabidopsis thaliana, Nature, 465, 10.1038/nature09083 · DOI
  31. Ng, 2011, Genetic dissection of salicylic acid-mediated defense signaling networks in Arabidopsis, Genetics, 189, 10.1534/genetics.111.132332 · DOI
  32. Hemm, 2003, The Arabidopsis ref2 mutant is defective in the gene encoding CYP83A1 and shows both phenylpropanoid and glucosinolate phenotypes, Plant Cell., 15, 179, 10.1105/tpc.006544 · DOI · Paper page
  33. Humphreys, 2002, Rewriting the lignin roadmap, Curr. Opin. Plant Biol., 5, 224, 10.1016/S1369-5266(02)00257-1 · DOI
  34. Kim, 2014, Chemically induced conditional rescue of the reduced epidermal fluorescence8 mutant of Arabidopsis reveals rapid restoration of growth and selective turnover of secondary metabolite pools, Plant Physiol., 164, 584, 10.1104/pp.113.229393 · DOI
  35. Landry, 1995, Arabidopsis mutants lacking phenolic sunscreens exhibit enhanced ultraviolet-B injury and oxidative damage, Plant Physiol., 109, 1159, 10.1104/pp.109.4.1159 · DOI
  36. Bonawitz, 2012, REF4 and RFR1, subunits of the transcriptional coregulatory complex mediator, are required for phenylpropanoid homeostasis in Arabidopsis, J. Biol. Chem., 287, 5434, 10.1074/jbc.M111.312298 · DOI
  37. Bonawitz, 2014, Disruption of mediator rescues the stunted growth of a lignin-deficient Arabidopsis mutant, Nature, 509, 10.1038/nature13084 · DOI
  38. Kim, 2015, Indole glucosinolate biosynthesis limits phenylpropanoid accumulation in Arabidopsis thaliana, Plant Cell, 27, 1529, 10.1105/tpc.15.00127 · DOI · Paper page
  39. Cipollini, 2010, Constitutive expression of methyl jasmonate-inducible responses delays reproduction and constrains fitness responses to nutrients in Arabidopsis thaliana, Evol. Ecol., 24, 59, 10.1007/s10682-008-9290-0 · DOI
  40. Paul-Victor, 2010, A new method for measuring relative growth rate can uncover the costs of defensive compounds in Arabidopsis thaliana, New Phytol., 187, 1102, 10.1111/j.1469-8137.2010.03325.x · DOI
  41. Züst, 2011, Using knockout mutants to reveal the growth costs of defensive traits, Proc. R. Soc. B-Biol. Sci., 278, 2598, 10.1098/rspb.2010.2475 · DOI
  42. Joseph, 2013, Hierarchical nuclear and cytoplasmic genetic architectures for plant growth and defense within Arabidopsis, Plant Cell, 25, 1929, 10.1105/tpc.113.112615 · DOI
  43. Lankau, 2009, Competition, herbivory and genetics interact to determine the accumulation and fitness consequences of a defence metabolite, J. Ecol., 97, 78
  44. Lankau, 2007, Mutual feedbacks maintain both genetic and species diversity in a plant community, Science, 317, 1561, 10.1126/science.1147455 · DOI
  45. Lankau, 2008, Community complexity drives patterns of natural selection on a chemical defense of Brassica nigra, Am. Nat., 171, 150, 10.1086/524959 · DOI
  46. Mauricio, 2003, Natural selection for polymorphism in the disease resistance gene Rps2 of Arabidopsis thaliana, Genetics, 163, 735, 10.1093/genetics/163.2.735 · DOI
  47. Tian, 2003, Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana, Nature, 423, 74, 10.1038/nature01588 · DOI
  48. Korves, 2004, A novel cost of R gene resistance in the presence of disease, Am. Nat., 163, 489, 10.1086/382552 · DOI
  49. Kliebenstein, 2008, Ecological costs of biotrophic versus necrotrophic pathogen resistance, the hypersensitive response and signal transduction, Plant Sci., 174, 551, 10.1016/j.plantsci.2008.03.005 · DOI
  50. Lankau, 2007, Specialist and generalist herbivores exert opposing selection on a chemical defense, New Phytol., 175, 176, 10.1111/j.1469-8137.2007.02090.x · DOI
  51. Kniskern, 2007, Salicylic acid and jasmonic acid signaling defense pathways reduce natural bacterial diversity on Arabidopsis thaliana, Mol. Plant-Microbe Interact., 20, 1512, 10.1094/MPMI-20-12-1512 · DOI
  52. Lebeis, 2015, Salicylic acid modulates colonization of the root microbiome by specific bacterial taxa, Science, 349, 860, 10.1126/science.aaa8764 · DOI
  53. Lorang, 2004, Identification and characterization of victorin sensitivity in Arabidopsis thaliana, Mol. Plant-Microbe Interact., 17, 577, 10.1094/MPMI.2004.17.6.577 · DOI
  54. Lorang, 2007, Plant disease susceptibility conferred by a “resistance” gene, Proc. Natl. Acad. Sci. U. S. A., 104, 14861, 10.1073/pnas.0702572104 · DOI
  55. Sweat, 2007, Thioredoxin h5 is required for victorin sensitivity mediated by a CC-NBS-LRR gene in Arabidopsis, Plant Cell, 19, 673, 10.1105/tpc.106.047563 · DOI
  56. Sweat, 2008, Characterization of natural and induced variation in the LOV1 gene, a CC-NB-LRR gene conferring victorin sensitivity and disease susceptibility in Arabidopsis, Mol. Plant-Microbe Interact., 21, 7, 10.1094/MPMI-21-1-0007 · DOI
  57. Lorang, 2012, Tricking the guard: exploiting plant defense for disease susceptibility, Science, 338, 659, 10.1126/science.1226743 · DOI
  58. Mauricio, 1997, Experimental manipulation of putative selective agents provides evidence for the role of natural enemies in the evolution of plant defense, Evolution, 51, 1435, 10.1111/j.1558-5646.1997.tb01467.x · DOI
  59. Bidart-Bouzat, 2008, Differential levels of insect herbivory in the field associated with genotypic variation in glucosinolates in Arabidopsis thaliana, J. Chem. Ecol., 34, 1026, 10.1007/s10886-008-9498-z · DOI
  60. Siemens, 2013, Plant chemical defense allocation constrains evolution of tolerance to community change across a range boundary, Ecol. Evol., 3, 4339, 10.1002/ece3.657 · DOI
  61. Kessler, 2011, Herbivory-mediated pollinator limitation: negative impacts of induced volatiles on plant-pollinator interactions, Ecology, 92, 1769, 10.1890/10-1945.1 · DOI
  62. Kerwin, 2015, Natural genetic variation in Arabidopsis thaliana defense metabolism genes modulates field fitness, Elife, 4
  63. Mauricio, 1997, Variation in the defense strategies of plants: Are resistance and tolerance mutually exclusive?, Ecology, 78, 1301, 10.1890/0012-9658(1997)078[1301:VITDSO]2.0.CO;2 · DOI
  64. Agrawal, 2000, Overcompensation of plants in response to herbivory and the by-product benefits of mutualism, Trends plant Sci., 5, 309, 10.1016/S1360-1385(00)01679-4 · DOI
  65. Paige, 1992, Overcompensation in response to mammallian herbivory – from mutualistic to antagonistic interactions, Ecology, 73, 2076, 10.2307/1941456 · DOI
  66. Kliebenstein, 2013, Making new molecules – evolution of structures for novel metabolites in plants, Curr. Opin. Plant Biol., 16, 112, 10.1016/j.pbi.2012.12.004 · DOI
  67. Zhao, 2008, Functional proteomics of Arabidopsis thaliana guard cells uncovers new stomatal signaling pathways, Plant Cell., 20, 3210, 10.1105/tpc.108.063263 · DOI
  68. Melotto, 2008, Role of stomata in plant innate immunity and foliar bacterial diseases, Annu. Rev. Phytopathol., 46, 101, 10.1146/annurev.phyto.121107.104959 · DOI
  69. Shroff, 2008, Nonuniform distribution of glucosinolates in Arabidopsis thaliana leaves has important consequences for plant defense, Proc. Natl. Acad. Sci. U. S. A., 105, 6196, 10.1073/pnas.0711730105 · DOI
  70. Hoelscher, 2009, Matrix-free UV-laser desorption/ionization (LDI) mass spectrometric imaging at the single-cell level: distribution of secondary metabolites of Arabidopsis thaliana and Hypericum species, Plant J., 60, 907, 10.1111/j.1365-313X.2009.04012.x · DOI
  71. Gols, 2008, Genetic variation in defense chemistry in wild cabbages affects herbivores and their endoparasitoids, Ecology, 89, 1616, 10.1890/07-0873.1 · DOI
  72. Shelton, 2004, Variation in chemical defences of plants may improve the effectiveness of defence, Evol. Ecol. Res., 6, 709
  73. Shelton, 2005, Within-plant variation in glucosinolate concentrations of Raphanus sativus across multiple scales, J. Chem. Ecol., 31, 1711, 10.1007/s10886-005-5922-9 · DOI

Cited by

Sorted by citations

Metadata

Authors
Kliebenstein, D. J.
Affiliations
University of Copenhagen (DK)
Corresponding author
Kliebenstein, Daniel J.
Venue
Physiological and Molecular Plant Pathology
Publisher
Elsevier BV
Published
2016-07
Volume
95
Pages
55-59
ISSN
0885-5765 (ISSN-L)
OpenAlex
W2266514286
Cited by
89
References
0
Citations by year
2026: 7 · 2025: 6 · 2024: 12 · 2023: 4 · 2022: 10 · 2021: 12 · 2020: 10 · 2019: 7 · 2018: 7 · 2017: 10 · 2016: 3
FWCI
10.54
Type
journal article
Language
en
Open access
Locations
  • Physiological and Molecular Plant Pathology (acceptedVersion)
  • eScholarship (California Digital Library) (submittedVersion)
  • Research at the University of Copenhagen (University of Copenhagen) (submittedVersion)
Funders
  • National Science Foundation (IOS 1339125, MCB 1330337)
  • Danmarks Grundforskningsfond (DNRF99)
  • National Institute of Food and Agriculture (CA-D-PLS-7033-H)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant-Microbe Interactions and Immunity
  • Life Sciences › Agricultural and Biological Sciences › Insect Science › Insect-Plant Interactions and Control
  • Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
Keywords
fitness cost of resistance, plant signaling, plant immunity, plant growth, resource allocation, systems biology, plant-pathogen interaction, fitness maximization

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