The DOI matches its Crossref record.
False idolatry of the mythical growth versus immunity tradeoff in molecular systems plant pathology
Open accessAbstract
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
Cites
Statistics
Verification
Claims the paper makes
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?
Plants often reduce growth investment upon herbivore- or pathogen attack.
“Plants regulate their growth dynamically and often reduce their investment into growth and development upon herbivore-or pathogen attack.”
From Plant Secondary Metabolites as Defenses, Regulators, and Primary Metabolites: The Blurred Functional Trichotomy (2020) · cites this paper as Kliebenstein, 2016
This reduction in growth is thought to be largely due to reconfiguration of a plant's signaling network rather than a lack of resources.
“This reduction in growth is thought to be largely due to the reconfiguration of a plant's signaling network rather than a lack of resources (Kliebenstein, 2016;Machado et al., 2017;Guo et al., 2018).”
From Plant Secondary Metabolites as Defenses, Regulators, and Primary Metabolites: The Blurred Functional Trichotomy (2020) · cites this paper as Kliebenstein, 2016
Citations
Cites
No references could be resolved yet.
Research works printed but not linked: 73
- Strauss, 1999, The ecology and evolution of plant tolerance to herbivory, Trends Ecol. Evol., 14, 179, 10.1016/S0169-5347(98)01576-6 · DOI
- 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
- Agrawal, 2011, Current trends in the evolutionary ecology of plant defence, Funct. Ecol., 25, 420, 10.1111/j.1365-2435.2010.01796.x · DOI
- Agrawal, 2011, New synthesis-trade-offs in chemical ecology, J. Chem. Ecol., 37, 230, 10.1007/s10886-011-9930-7 · DOI
- 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
- Lozano-Duran, 2013, The transcriptional regulator BZR1 mediates trade-off between plant innate immunity and growth, Elife, 2
- 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
- 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
- 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
- Wang, 2014, At the intersection of plant growth and immunity, Cell Host Microbe, 15, 401, 10.1016/j.chom.2014.03.014 · DOI
- 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
- Herms, 1992, The dilemma of plants – to grow or defend, Q. Rev. Biol., 67, 283, 10.1086/417659 · DOI
- 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
- Wierzba, 2015, An allelic series of bak1 mutations differentially alter bir1 cell-death, immune response, growth, and root development phenotypes in Arabidopsis thaliana, Genetics
- Navarro, 2006, A plant miRNA contributes to antibacterial resistance by repressing auxin signaling, Science, 312, 436, 10.1126/science.1126088 · DOI
- 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
- 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
- Attaran, 2014, Temporal dynamics of growth and photosynthesis suppression in response to jasmonate signaling, Plant Physiol., 165, 1302, 10.1104/pp.114.239004 · DOI
- 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
- Zhang, 2013, Crosstalk between the circadian clock and innate immunity in Arabidopsis, Plos Pathog., 9
- Wang, 2011, Timing of plant immune responses by a central circadian regulator, Nature, 470, 110, 10.1038/nature09766 · DOI
- Fay, 2015, Grassland productivity limited by multiple nutrients, Nat. Plants, 1, 15080, 10.1038/nplants.2015.80 · DOI
- 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
- Halkier, 2006, Biology and biochemistry of glucosinolates, Annu. Rev. Plant Biol., 57, 303, 10.1146/annurev.arplant.57.032905.105228 · DOI
- Glazebrook, 2005, Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens, Annu. Rev. Phytopathol., 43, 205, 10.1146/annurev.phyto.43.040204.135923 · DOI
- 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
- 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
- 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
- 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
- Todesco, 2010, Natural allelic variation underlying a major fitness trade-off in Arabidopsis thaliana, Nature, 465, 10.1038/nature09083 · DOI
- Ng, 2011, Genetic dissection of salicylic acid-mediated defense signaling networks in Arabidopsis, Genetics, 189, 10.1534/genetics.111.132332 · DOI
- 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
- Humphreys, 2002, Rewriting the lignin roadmap, Curr. Opin. Plant Biol., 5, 224, 10.1016/S1369-5266(02)00257-1 · DOI
- 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
- 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
- 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
- Bonawitz, 2014, Disruption of mediator rescues the stunted growth of a lignin-deficient Arabidopsis mutant, Nature, 509, 10.1038/nature13084 · DOI
- Kim, 2015, Indole glucosinolate biosynthesis limits phenylpropanoid accumulation in Arabidopsis thaliana, Plant Cell, 27, 1529, 10.1105/tpc.15.00127 · DOI · Paper page
- 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
- 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
- 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
- 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
- Lankau, 2009, Competition, herbivory and genetics interact to determine the accumulation and fitness consequences of a defence metabolite, J. Ecol., 97, 78
- Lankau, 2007, Mutual feedbacks maintain both genetic and species diversity in a plant community, Science, 317, 1561, 10.1126/science.1147455 · DOI
- Lankau, 2008, Community complexity drives patterns of natural selection on a chemical defense of Brassica nigra, Am. Nat., 171, 150, 10.1086/524959 · DOI
- 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
- Tian, 2003, Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana, Nature, 423, 74, 10.1038/nature01588 · DOI
- Korves, 2004, A novel cost of R gene resistance in the presence of disease, Am. Nat., 163, 489, 10.1086/382552 · DOI
- 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
- 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
- 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
- Lebeis, 2015, Salicylic acid modulates colonization of the root microbiome by specific bacterial taxa, Science, 349, 860, 10.1126/science.aaa8764 · DOI
- 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
- Lorang, 2007, Plant disease susceptibility conferred by a “resistance” gene, Proc. Natl. Acad. Sci. U. S. A., 104, 14861, 10.1073/pnas.0702572104 · DOI
- 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
- 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
- Lorang, 2012, Tricking the guard: exploiting plant defense for disease susceptibility, Science, 338, 659, 10.1126/science.1226743 · DOI
- 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
- 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
- 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
- Kessler, 2011, Herbivory-mediated pollinator limitation: negative impacts of induced volatiles on plant-pollinator interactions, Ecology, 92, 1769, 10.1890/10-1945.1 · DOI
- Kerwin, 2015, Natural genetic variation in Arabidopsis thaliana defense metabolism genes modulates field fitness, Elife, 4
- 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
- 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
- Paige, 1992, Overcompensation in response to mammallian herbivory – from mutualistic to antagonistic interactions, Ecology, 73, 2076, 10.2307/1941456 · DOI
- 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
- Zhao, 2008, Functional proteomics of Arabidopsis thaliana guard cells uncovers new stomatal signaling pathways, Plant Cell., 20, 3210, 10.1105/tpc.108.063263 · DOI
- 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
- 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
- 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
- Gols, 2008, Genetic variation in defense chemistry in wild cabbages affects herbivores and their endoparasitoids, Ecology, 89, 1616, 10.1890/07-0873.1 · DOI
- Shelton, 2004, Variation in chemical defences of plants may improve the effectiveness of defence, Evol. Ecol. Res., 6, 709
- 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
Erb, M., & Kliebenstein, D. J. (2020) · Plant Physiology · doi:10.1104/pp.20.00433 · Cited by 1,333
Self-citation
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
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (am, 335 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- 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