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Functional variation in a key defense gene structures herbivore communities and alters plant performance.

ABSTRACT: Plant genetic diversity structures animal communities and affects plant population productivity. However, few studies have investigated which traits are involved and the mechanisms mediating these effects. We studied the consequences of varying the expression of a single biosynthetic gene in jasmonate (JA) defense hormones, which are essential for defense against herbivores but constrain plant growth, in experimental mesocosm populations of wild tobacco (Nicotiana attenuata) plants under attack from three native herbivores. Empoasca leafhoppers preferentially attack JA-deficient N. attenuata plants in nature, and the specialist Tupiocoris notatus mirids avoid Empoasca-damaged plants. However, in experimental mesocosm populations having equal numbers of wild-type (WT) and JA-deficient plants that are silenced in the expression of the biosynthetic gene lipoxygenase 3 (LOX3), Empoasca sp. attacked both genotypes. Empoasca sp. damage, rather than JA, determined T. notatus damage, which was reduced in mixed populations. The growth of specialist Manduca sexta larvae was reduced on WT vs. asLOX3 monocultures, but differed in mixtures depending on caterpillar density. However, seed capsule number remained similar for WT and asLOX3 plants in mixtures, not in monocultures, in two experimental scenarios reflecting high and low caterpillar attack. At high caterpillar density, WT plants growing in mixtures produced more seed capsules than those growing in monocultures while seed production of asLOX3 plants did not differ by population type. However, at low caterpillar density, asLOX3 plants growing in mixed populations produced more seed capsules than those growing in monoculture, while seed capsule production did not differ for WT by population type. Thus, mixed populations had a more stable output of seed capsules under the two scenarios. This may result from a balance between JA-mediated herbivore defense and plant competitive ability in mixed populations.

SUBMITTER: Adam N

PROVIDER: S-EPMC5991399 | biostudies-literature | 2018

REPOSITORIES: biostudies-literature

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Functional variation in a key defense gene structures herbivore communities and alters plant performance.

Adam Nora N Kallenbach Mario M Meldau Stefan S Veit Daniel D van Dam Nicole M NM Baldwin Ian T IT Schuman Meredith C MC

PloS one 20180606 6

Plant genetic diversity structures animal communities and affects plant population productivity. However, few studies have investigated which traits are involved and the mechanisms mediating these effects. We studied the consequences of varying the expression of a single biosynthetic gene in jasmonate (JA) defense hormones, which are essential for defense against herbivores but constrain plant growth, in experimental mesocosm populations of wild tobacco (Nicotiana attenuata) plants under attack ...[more]

PMID: 29874269

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Project description:BackgroundShrub cover in arctic and alpine ecosystems has increased in recent decades, and is predicted to further increase with climate change. Changes in shrub abundance may alter ecosystem carbon (C) sequestration and storage, with potential positive feedback on global C cycling. Small and large herbivores may reduce shrub expansion and thereby counteract the positive feedback on C cycling, but herbivore pressures have also changed in the alpine-arctic tundra; the increased shrub cover together with changes in herbivore pressure is leading to unpredictable changes in carbon sequestration and storage. In this study we investigate the importance of herbivory and shrub introduction for carbon sequestration in the short term. We measured standing biomass and daytime mid-growing season carbon fluxes in plots in a full factorial design where we excluded small and large mammalian herbivores and introduced Salix by planting Salix transplants. We used three study sites: one Empetrum-dominated heath, one herb- and cryptogam-dominated meadow, and one Salix-dominated shrub community in the low-alpine zone of the Dovre Mountains, Central Norway.ResultsAfter 2 years, significant treatment effects were recorded in the heath community, but not in the meadow and shrub communities. In the heath community cessation of herbivory increased standing biomass due to increased biomass of dwarf shrubs. Cessation of herbivory also reduced biomass of bryophytes and ecosystem respiration (ER). Except for an increase in biomass of deciduous shrubs caused by the Salix introduction, the only effect of Salix introduction was an increase in biomass of graminoids in the heath.ConclusionsOur short-term study demonstrated that herbivore exclusion had small but still significant effects on heath vegetation, whereas such effects were not apparent in the herb-and cryptogam-dominated meadow and the Salix-dominated shrub community. Following the treatments over more years is needed to estimate the long-term effects on community structure and the consequences for C sequestration in the three plant communities. Such data are important for predicting the impact of shrub expansion on C budgets from alpine regions.

Project description:Resistance to herbivores and pathogens is considered a key plant trait with strong adaptive value in trees, usually involving high concentrations of a diverse array of plant secondary metabolites (PSM). Intraspecific genetic variation and plasticity of PSM are widely known. However, their ecology and evolution are unclear, and even the implication of PSM as traits that provide direct effective resistance against herbivores is currently questioned. We used control and methyl jasmonate (MJ) induced clonal copies of genotypes within families from ten populations of the main distribution range of maritime pine to exhaustively characterize the constitutive and induced profile and concentration of PSM in the stem phloem, and to measure insect herbivory damage as a proxy of resistance. Then, we explored whether genetic variation in resistance to herbivory may be predicted by the constitutive concentration of PSM, and the role of its inducibility to predict the increase in resistance once the plant is induced. We found large and structured genetic variation among populations but not between families within populations in resistance to herbivory. The MJ-induction treatment strongly increased resistance to the weevil in the species, and the genetic variation in the inducibility of resistance was significantly structured among populations, with greater inducibility in the Atlantic populations. Genetic variation in resistance was largely explained by the multivariate concentration and profile of PSM at the genotypic level, rather than by bivariate correlations with individual PSM, after accounting for genetic relatedness among genotypes. While the constitutive concentration of the PSM blend did not show a clear pattern of resistance to herbivory, specific changes in the chemical profile and the increase in concentration of the PSM blend after MJ induction were related to increased resistance. To date, this is the first example of a comprehensive and rigorous approach in which inducibility of PSM in trees and its implication in resistance was analyzed excluding spurious associations due to genetic relatedness, often overlooked in intraspecific studies. Here we provide evidences that multivariate analyses of PSM, rather than bivariate correlations, provide more realistic information about the potentially causal relationships between PSM and resistance to herbivory in pine trees.

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Functional variation in a key defense gene structures herbivore communities and alters plant performance.

Publications

Functional variation in a key defense gene structures herbivore communities and alters plant performance.

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