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Cited by 103Insect-Plant Interactions and ControlPlant biochemistry and biosynthesisPlant-Microbe Interactions and Immunity

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Herbivory‐induced jasmonates constrain plant sugar accumulation and growth by antagonizing gibberellin signaling and not by promoting secondary metabolite production

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Machado, Ricardo A. R., Baldwin, Ian T., Erb, Matthias·2017·New Phytologist
DOI 10.1111/nph.14597
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Abstract

Summary: Plants respond to herbivory by reconfiguring hormonal networks, increasing secondary metabolite production and decreasing growth. Furthermore, some plants display a decrease in leaf energy reserves in the form of soluble sugars and starch, leading to the hypothesis that herbivory‐induced secondary metabolite production and growth reduction may be linked through a carbohydrate‐based resource trade‐off. In order to test the above hypothesis, we measured leaf carbohydrates and plant growth in seven genetically engineered Nicotiana attenuata genotypes that are deficient in one or several major herbivore‐induced, jasmonate‐dependent defensive secondary metabolites and proteins. Furthermore, we manipulated gibberellin and jasmonate signaling, and quantified the impact of these phytohormones on secondary metabolite production, sugar accumulation and growth. Simulated herbivore attack by Manduca sexta specifically reduced leaf sugar concentrations and growth in a jasmonate‐dependent manner. These effects were similar or even stronger in defenseless genotypes with intact jasmonate signaling. Gibberellin complementation rescued carbohydrate accumulation and growth in induced plants without impairing the induction of defensive secondary metabolites. These results are consistent with a hormonal antagonism model rather than a resource–cost model to explain the negative relationship between herbivory‐induced defenses, leaf energy reserves and growth.

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  • 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 Machado et al., 2017

    The article title reproduced in Supporting Information Table S1 (p. 1) states that herbivory-induced jasmonates constrain plant growth, supporting the herbivore-related part of the claim. The passages available from our copy do not address pathogen attack or establish that plants often reduce growth investment after either kind of attack. (LLM, conf=0.72)

    Experimental — accuracy not yet measured

  • 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 Machado et al., 2017

    The article title reproduced in Supporting Information Table S1 (p. 1) attributes constrained growth to antagonism of gibberellin signaling, supporting the signaling part of the claim. The table reports carbohydrate and growth comparisons, but neither it nor the title establishes that growth reduction is largely due to signaling rather than a lack of resources. (LLM, conf=0.72)

    Experimental — accuracy not yet measured

  • Costs of secondary metabolite production are not always evident and may mostly occur under specific environmental conditions such as strong competition and nutrient limitation.

    “These costs are not always evident (Züst et al., 2011;Machado et al., 2017), and may mostly occur under specific environmental conditions such as strong competition and nutrient limitation (Cipollini et al., 2018).”

    From Plant Secondary Metabolites as Defenses, Regulators, and Primary Metabolites: The Blurred Functional Trichotomy (2020) · cites this paper as Machado et al., 2017

    Machado et al. is cited for the claim that costs are not always evident; the environmental-conditions clause is attributed to Cipollini et al. Our accessible copy of Machado et al. contains Supporting Information Table S1 (p. 1), which compares growth across genotypes but does not establish whether secondary-metabolite production has an evident cost. Searches for that claim returned no decisive passage. (LLM, conf=0.70)

    Experimental — accuracy not yet measured

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Metadata

Authors
Machado, R. A. R., Baldwin, I. T., & Erb, M.
Affiliations
  • University of Bern (CH)
  • Max Planck Institute for Chemical Ecology (DE)
Corresponding author
  • Machado, Ricardo A. R.
  • Baldwin, Ian T.
  • Erb, Matthias
ORCID
Venue
New Phytologist
Publisher
Wiley
Published
2017-05-18
Volume
215
Issue
2
Pages
803-812
ISSN
  • 0028-646X (ISSN-L)
  • 1469-8137
DOI
10.1111/nph.14597
OpenAlex
W2616286676
Cited by
103
References
0
Citations by year
2026: 7 · 2025: 11 · 2024: 11 · 2023: 8 · 2022: 11 · 2021: 18 · 2020: 13 · 2019: 10 · 2018: 13 · 2017: 1
FWCI
9.39
Type
journal article
Language
en
Open access
Licence
Locations
  • New Phytologist (publishedVersion)
  • PubMed (publishedVersion)
  • MPG.PuRe (Max Planck Society) (submittedVersion, other-oa)
  • BORIS (University Library Bern) (submittedVersion)
Funders
  • European Research Council (293926)
  • SNF early post doc fellowship (134930)
  • Marie Curie Intra European Fellowship (273107)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Insect Science › Insect-Plant Interactions and Control
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Plant biochemistry and biosynthesis
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant-Microbe Interactions and Immunity
Keywords
herbivory, jasmonic acid signaling, gibberellin signaling, plant growth, carbohydrate reserves, resource allocation trade-offs, secondary metabolite production, Manduca sexta, Nicotiana attenuata, plant defense
MeSH terms
Acetates, Animals, Carbon, Cyclopentanes, Gibberellins, Plant Proteins, Nicotiana, Signal Transduction, Manduca, Plant Leaves, Plant Shoots, Plants, Genetically Modified, Carbohydrate Metabolism, Oxylipins, Herbivory, Secondary Metabolism

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