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The roots of plant defenses: integrative multivariate analyses uncover dynamic behaviors of gene and metabolic networks of roots elicited by leaf herbivory.

ABSTRACT: High-throughput analyses have frequently been used to characterize herbivory-induced reconfigurations in plant primary and secondary metabolism in above- and below-ground tissues, but the conclusions drawn from these analyses are often limited by the univariate methods used to analyze the data. Here we use our previously described multivariate time-series data analysis to evaluate leaf herbivory-elicited transcriptional and metabolic dynamics in the roots of Nicotiana attenuata. We observed large, but transient, systemic responses in the roots that contrasted with the pattern of co-linearity observed in the up- and downregulation of genes and metabolites across the entire time series in treated and systemic leaves. Using this newly developed approach for the analysis of whole-plant molecular responses in a time-course multivariate data set, we simultaneously analyzed stress responses in leaves and roots in response to the elicitation of a leaf. We found that transient systemic responses in roots resolved into two principal trends characterized by: (i) an inversion of root-specific semi-diurnal (12 h) transcript oscillations and (ii) transcriptional changes with major amplitude effects that translated into a distinct suite of root-specific secondary metabolites (e.g. alkaloids synthesized in the roots of N. attenuata). These findings underscore the importance of understanding tissue-specific stress responses in the correct day-night phase context and provide a holistic framework for the important role played by roots in above-ground stress responses.

SUBMITTER: Gulati J

PROVIDER: S-EPMC4190575 | biostudies-literature | 2014 Mar

REPOSITORIES: biostudies-literature

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The roots of plant defenses: integrative multivariate analyses uncover dynamic behaviors of gene and metabolic networks of roots elicited by leaf herbivory.

Gulati Jyotasana J Baldwin Ian T IT Gaquerel Emmanuel E

The Plant journal : for cell and molecular biology 20140308 6

High-throughput analyses have frequently been used to characterize herbivory-induced reconfigurations in plant primary and secondary metabolism in above- and below-ground tissues, but the conclusions drawn from these analyses are often limited by the univariate methods used to analyze the data. Here we use our previously described multivariate time-series data analysis to evaluate leaf herbivory-elicited transcriptional and metabolic dynamics in the roots of Nicotiana attenuata. We observed larg ...[more]

PMID: 24456376

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Project description:There is conclusive evidence that there are fitness costs of plant defense and that herbivores can drive selection for defense. However, most work has focused on above-ground interactions, even though belowground herbivory may have greater impacts on individual plants than above-ground herbivory. Given the role of belowground plant structures in resource acquisition and storage, research on belowground herbivores has much to contribute to theories on the evolution of plant defense. Pocket gophers (Geomyidae) provide an excellent opportunity to study root herbivory. These subterranean rodents spend their entire lives belowground and specialize on consuming belowground plant parts.We compared the root defenses of native forbs from mainland populations (with a history of gopher herbivory) to island populations (free from gophers for up to 500,000 years). Defense includes both resistance against herbivores and tolerance of herbivore damage. We used three approaches to compare these traits in island and mainland populations of two native California forbs: 1) Eschscholzia californica populations were assayed to compare alkaloid deterrents, 2) captive gophers were used to test the palatability of E. californica roots and 3) simulated root herbivory assessed tolerance to root damage in Deinandra fasciculata and E. californica. Mainland forms of E. californica contained 2.5 times greater concentration of alkaloids and were less palatable to gophers than island forms. Mainland forms of D. fasciculata and, to a lesser extent, E. californica were also more tolerant of root damage than island conspecifics. Interestingly, undamaged island individuals of D. fasciculata produced significantly more fruit than either damaged or undamaged mainland individuals.These results suggest that mainland plants are effective at deterring and tolerating pocket gopher herbivory. Results also suggest that both forms of defense are costly to fitness and thus reduced in the absence of the putative target herbivore.

Dataset Information

The roots of plant defenses: integrative multivariate analyses uncover dynamic behaviors of gene and metabolic networks of roots elicited by leaf herbivory.

Publications

The roots of plant defenses: integrative multivariate analyses uncover dynamic behaviors of gene and metabolic networks of roots elicited by leaf herbivory.

Similar Datasets

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