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Contingency rules for pathogen competition and antagonism in a genetically based, plant defense hierarchy.

ABSTRACT: Plant defense against pathogens includes a range of mechanisms, including, but not limited to, genetic resistance, pathogen-antagonizing endophytes, and pathogen competitors. The relative importance of each mechanism can be expressed in a hierarchical view of defense. Several recent studies have shown that pathogen antagonism is inconsistently expressed within the plant defense hierarchy. Our hypothesis is that the hierarchy is governed by contingency rules that determine when and where antagonists reduce plant disease severity.Here, we investigated whether pathogen competition influences pathogen antagonism using Populus as a model system. In three independent field experiments, we asked whether competition for leaf mesophyll cells between a Melampsora rust pathogen and a microscopic, eriophyid mite affects rust pathogen antagonism by fungal leaf endophytes. The rust pathogen has an annual, phenological disadvantage in competition with the mite because the rust pathogen must infect its secondary host in spring before infecting Populus. We varied mite-rust competition by utilizing Populus genotypes characterized by differential genetic resistance to the two organisms. We inoculated plants with endophytes and allowed mites and rust to infect plants naturally.Two contingency rules emerged from the three field experiments: (a) Pathogen antagonism by endophytes can be preempted by host genes for resistance that suppress pathogen development, and (b) pathogen antagonism by endophytes can secondarily be preempted by competitive exclusion of the rust by the mite. Synthesis: Our results point to a Populus defense hierarchy with resistance genes on top, followed by pathogen competition, and finally pathogen antagonism by endophytes. We expect these rules will help to explain the variation in pathogen antagonism that is currently attributed to context dependency.

SUBMITTER: Busby PE

PROVIDER: S-EPMC6662256 | biostudies-literature | 2019 Jun

REPOSITORIES: biostudies-literature

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Contingency rules for pathogen competition and antagonism in a genetically based, plant defense hierarchy.

Busby Posy E PE Crutsinger Gregory G Barbour Matthew M Newcombe George G

Ecology and evolution 20190523 12

Plant defense against pathogens includes a range of mechanisms, including, but not limited to, genetic resistance, pathogen-antagonizing endophytes, and pathogen competitors. The relative importance of each mechanism can be expressed in a hierarchical view of defense. Several recent studies have shown that pathogen antagonism is inconsistently expressed within the plant defense hierarchy. Our hypothesis is that the hierarchy is governed by contingency rules that determine when and where antagoni ...[more]

PMID: 31380021

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Project description:The relative importance of different community assembly mechanisms varies depending on the environment. According to the stress-dominance hypothesis (SDH), assembly mechanisms range from strong abiotic filtering to competition as the environment becomes more favourable. Most evidence for the SDH comes from studies in gradients of conditions (i.e. abiotic environmental factors that influence the functioning of organisms but are not consumed by them). However, we hypothesized that in resource gradients, competition increases as abiotic filtering becomes stronger. To test our hypothesis, we set up eight plots at different sites along an abiotic severity gradient in the Brazilian semi-arid region (BSAR). In each plot, we identified and measured each woody plant species found, and we recorded 11 functional traits of the main species, dividing the traits into alpha (competition effects) and beta (abiotic filtering effects). We investigated the presence of phylogenetic signal in the traits, the community phylogenetic and phenotypic patterns, and associated the variation in these patterns with the availability of water and soil nutrients. We found phylogenetic signal for most (91%) of the traits analysed. The phylogenetic patterns varied from clustered in stressful sites to random or overdispersed in favourable sites, and we concluded that these phylogenetic patterns were the result of historical processes influencing community assembly in different environments in the BSAR. In general, the phenotypic patterns varied from clustered at the most stressful end to random at less stressful sites. Our results show that in resource gradients, any restriction of the resource (hydric or edaphic) intensifies abiotic filtering and, at the same time, increases the competitive hierarchy among species. On the other hand, stochastic processes seem to have a stronger influence under more favourable abiotic conditions, where abiotic filtering and competition are weaker. Thus, we conclude that the SDH is not supported in resource gradients.

Dataset Information

Contingency rules for pathogen competition and antagonism in a genetically based, plant defense hierarchy.

Publications

Contingency rules for pathogen competition and antagonism in a genetically based, plant defense hierarchy.

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