Correlations between physical and chemical defences in plants: tradeoffs, syndromes, or just many different ways to skin a herbivorous cat?

Moles, Angela T.; Peco, Begoña; Wallis, Ian R.; Foley, William J.; Poore, Alistair G. B.; Seabloom, Eric W.; Vesk, Peter A.; Bisigato, Alejandro Jorge; Cella‐Pizarro, Lucrecia; Clark, Connie J.; Cohen, Philippe S.; Cornwell, William K.; Edwards, Will; Ejrnæs, Rasmus; Gonzales‐Ojeda, Therany; Graae, Bente Jessen; Hay, Gregory; Lumbwe, Fainess C.; Magaña‐Rodríguez, Benjamín; Moore, Ben D.; Peri, Pablo Luís; Poulsen, John R.; Stegen, James C.; Veldtman, Ruan; Zeipel, Hugo von; Andrew, Nigel R.; Boulter, Sarah; Borer, Elizabeth T.; Cornelissen, Johannes H. C.; Farji‐Brener, Alejandro G.; DeGabriel, Jane L.; Jurado, Enrique; Kyhn, Line A.; Low, Bill; Mulder, Christa P. H.; Reardon‐Smith, Kathryn; Rodríguez‐Velázquez, Jorge; Fortier, An De; Zhang, Zheng; Blendinger, Pedro G.; Enquist, Brian J.; Facelli, José M.; Knight, Tiffany M.; Majer, Jonathan; Martı́nez-Ramos, Miguel; McQuillan, PB; Hui, Francis K. C.

doi:10.1111/nph.12116

Cited by 132 publications

(169 citation statements)

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“…Hypotheses for the expression of multiple defensive v www.esajournals.org traits in a single species range from synergism or redundancy in their action, specificity of traits towards multiple attackers, to various nonadaptive explanations (Jones and Firn 1991, Berenbaum and Zangerl 1996, Agrawal 2011, Moles et al 2013). Yet, there are remarkably few tests of these hypotheses (e.g., Berenbaum et al 1991, Mü ller et al 2010.…”

Section: Introductionmentioning

confidence: 99%

Tests of the coupled expression of latex and cardenolide plant defense in common milkweed (Asclepias syriaca)

2014

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Abstract. The coexpression of plant resistance traits suggests the hypothesis that they may have complementary functions in defense against herbivory. To address the extent to which defensive traits are necessarily coupled in plants grown under various conditions, we focused on latex and cardenolides, two potent defenses of milkweeds. We measured defenses across ontogenetic stages, different biotic and abiotic environments, and across genetic families of the common milkweed Asclepias syriaca. We first addressed the extent to which foliar cardenolides are derived from latex because latex actively flows through canals in leaves. We rinsed latex out of shredded leaves, which had no impact on foliar cardenolides, suggesting cardenolides are allocated to leaves independently of latex. Accordingly, there is potential for independent expression of the two traits. We next followed a cohort of plants from germination over three years; expression of both latex exudation and cardenolides increased annually, with the exception of a second year dip in cardenolides. Damage by monarch caterpillars induced '50% increases of both latex and cardenolides, with the former occurring rapidly within a day and the latter taking five days of herbivory; these responses were preceded by an earlier peak of the signaling hormones jasmonic acid and abscisic acid. Endogenous jasmonic acid showed an instantaneous positive correlation with latex exudation and foliar cardenolides. Under drought stress, latex and cardenolide expression were reversed, with water stress suppressing latex exudation, but nearly doubling cardenolide concentrations. These drought effects were not driven by phytohormones in the expected manner, as jasmonic acid was unaffected, salicylic acid was strongly suppressed, and abscisic acid tripled in response to drought. Finally, a meta-analysis of four previously published field studies representing 85 genetic families of A. syriaca revealed no evidence for a genetic correlation between latex exudation and foliar cardenolide concentrations. The same lack of a correlation was observed across 22 populations of A. syriaca when grown in a common environment. Thus, the two most important defensive traits of milkweeds, although often coexpressed, can become uncoupled during some ontogenetic stages, under some biotic and abiotic conditions, and there is no evidence that they evolve together.

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Section: Introductionmentioning

confidence: 99%

Tests of the coupled expression of latex and cardenolide plant defense in common milkweed (Asclepias syriaca)

2014

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“…Consequently, the allocation of resources to defences is hypothesized to be subjected to trade-offs such that high investment in one defence type should reduce investment in others with similar effectiveness [30], [31], [32]. However, most studies that have explored trade-offs in plant defences have focused on the leaves of seedlings and adult plants (e.g., [30], [31], [32], [33], and it remains unclear whether a trade-off exists between physical and chemical defensive traits in seeds.…”

Section: Introductionmentioning

confidence: 99%

Investment in Seed Physical Defence Is Associated with Species' Light Requirement for Regeneration and Seed Persistence: Evidence from Macaranga Species in Borneo

et al. 2014

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The seed stage is often critical in determining the regeneration success of plants. Seeds must survive an array of seed predators and pathogens and germinate under conditions favourable for seedling establishment. To maximise recruitment success plants protect seeds using a diverse set of chemical and physical defences. However, the relationship between these defence classes, and their association with other life history traits, is not well understood. Data on seed coat thickness and fracture resistance, and the abundance and diversity of potential defensive compounds were collected for 10 tree species of Macaranga from Borneo. The data were used to test whether there is a trade-off in physical versus chemical defence investment, and to determine how investment varies with seed mass, and light requirement for regeneration. Across species there was no correlation between seed coat thickness and abundance of potential defensive compounds, indicating the absence of a direct trade-off between defence classes. While chemical defences were not correlated to other traits, physical defences were positively correlated with light requirement for regeneration. For a subset of five Macaranga species we evaluated the relative investment in chemical and physical defence to seed persistence in the soil, measured as the time to half initial seed viability (seed half-life). Half-life was negatively related to the ratio of potential defensive compound abundance to seed coat thickness, suggesting that species with long persistence invested in physical defence more than stored chemical defences. These results indicate that investment in seed defences are associated with species' light requirements for regeneration, rather than scaling positively with seed mass. Furthermore, chemical defences, although highly variable among species, do not appear to be critical to long term persistence of Macaranga seeds, and may be important in defending seeds from natural enemies distinct from those found in the soil.

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“…There is an intricate inter-trophic chemical interaction between plants, herbivores, and herbivores' natural enemies as they have been coevolving for over 400 million years [47,48]. As a result, plants have evolved highly sophisticated ways of defending themselves from herbivorous insects such as, through emission of volatile semiochemicals.…”

Section: Discussionmentioning

confidence: 99%

Volatile Semiochemical Mediated Plant Defense in Cereals: A Novel Strategy for Crop Protection

Tamiru

2017

Agronomy

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Plants have evolved highly intriguing ways of defending themselves against insect attacks, including through emission of defense volatiles. These volatiles serve the plant's defense by directly repelling phytophagous insects and/or indirectly through attracting natural enemies antagonistic to the herbivores. Several laboratory studies established the potential of improving plant resistance against insect attacks by manipulating the plant-derived volatile semiochemicals emissions. Yet, more efforts need to be conducted to translate the promising laboratory studies to fight economically-important crop pests under real field conditions. This is needed to address an increasing demand for alternative pest control options driven by ecological and environmental costs associated with the use of broad-spectrum insecticides. The practical examples discussed in this review paper demonstrate the real prospect of exploiting an inducible and constitutive plant volatile semiochemicals for developing novel and ecologically-sustainable pest management strategies to protect cereal crops from damaging insect pests.

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Correlations between physical and chemical defences in plants: tradeoffs, syndromes, or just many different ways to skin a herbivorous cat?

Cited by 132 publications

References 92 publications

Tests of the coupled expression of latex and cardenolide plant defense in common milkweed (Asclepias syriaca)

Tests of the coupled expression of latex and cardenolide plant defense in common milkweed (Asclepias syriaca)

Investment in Seed Physical Defence Is Associated with Species' Light Requirement for Regeneration and Seed Persistence: Evidence from Macaranga Species in Borneo

Volatile Semiochemical Mediated Plant Defense in Cereals: A Novel Strategy for Crop Protection

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