Root exudation of phytochemicals in Arabidopsis follows specific patterns that are developmentally programmed and correlate with soil microbial functions.

Jacqueline M Chaparro,Jorge M Vivanco,Dayakar V Badri,Akifumi Sugiyama,Matthew G Bakker,Daniel K Manter,Keqiang Wu

doi:10.1371/journal.pone.0055731

Abstract

Plant roots constantly secrete compounds into the soil to interact with neighboring organisms presumably to gain certain functional advantages at different stages of development. Accordingly, it has been hypothesized that the phytochemical composition present in the root exudates changes over the course of the lifespan of a plant. Here, root exudates of in vitro grown Arabidopsis plants were collected at different developmental stages and analyzed using GC-MS. Principle component analysis revealed that the composition of root exudates varied at each developmental stage. Cumulative secretion levels of sugars and sugar alcohols were higher in early time points and decreased through development. In contrast, the cumulative secretion levels of amino acids and phenolics increased over time. The expression in roots of genes involved in biosynthesis and transportation of compounds represented in the root exudates were consistent with patterns of root exudation. Correlation analyses were performed of the in vitro root exudation patterns with the functional capacity of the rhizosphere microbiome to metabolize these compounds at different developmental stages of Arabidopsis grown in natural soils. Pyrosequencing of rhizosphere mRNA revealed strong correlations (p<0.05) between microbial functional genes involved in the metabolism of carbohydrates, amino acids and secondary metabolites with the corresponding compounds released by the roots at particular stages of plant development. In summary, our results suggest that the root exudation process of phytochemicals follows a developmental pattern that is genetically programmed.

Highlights

Plants use root exudates as chemical cues to monitor and interact with their surroundings [1,2]
The primary and secondary metabolites present in the root exudation profiles of in vitro grown wildtype Col-0 Arabidopsis through a developmental time series were analyzed by Gas Chromatography and Mass Spectrometry (GC-MS)
The identified compounds contributing most to component 2 were oxoproline, c-Aminobutyric acid (GABA), urea, isoleucine, galactose and tagatose. These data clearly indicate that the quantitative composition of Arabidopsis root exudates varies at each developmental stage

Summary

Introduction

Plants use root exudates as chemical cues to monitor and interact with their surroundings [1,2]. Zea mays releases 2,4dihydroxy-7-methoxy-1,4-benzoxazin-3-one that chemotactically attracts the beneficial rhizobacterium Pseudomonas putida KT2440 [9]. Besides such one-to-one interactions, multitrophic interactions occur in the rhizosphere. Medicago truncatula emits dimethyl sulfide that attracts Caenorhabditis elegans, which in turn transports rhizobia close to the legume roots to initiate symbiosis [10]. Evidence is mounting that the cross talk between plants and the soil microbes is largely orchestrated by root exudates, at the one compound-one microbe level, but at the community level. It has been reported that changes in root exudation due to mutation of an ABC transporter gene modulated the soil microbial community composition such that more beneficial microbes were cultured [11]. Micallef et al [12] showed that soil microbial communities are affected by plant age and genotype

Methods

Results

Conclusion