Abstract
Integrated metabolomics and transcriptomics of Medicago truncatula seedling border cells and root tips revealed substantial metabolic differences between these distinct and spatially segregated root regions. Large differential increases in oxylipin-pathway lipoxygenases and auxin-responsive transcript levels in border cells corresponded to differences in phytohormone and volatile levels compared with adjacent root tips. Morphological examinations of border cells revealed the presence of significant starch deposits that serve as critical energy and carbon reserves, as documented through increased β-amylase transcript levels and associated starch hydrolysis metabolites. A substantial proportion of primary metabolism transcripts were decreased in border cells, while many flavonoid- and triterpenoid-related metabolite and transcript levels were increased dramatically. The cumulative data provide compounding evidence that primary and secondary metabolism are differentially programmed in border cells relative to root tips. Metabolic resources normally destined for growth and development are redirected toward elevated accumulation of specialized metabolites in border cells, resulting in constitutively elevated defense and signaling compounds needed to protect the delicate root cap and signal motile rhizobia required for symbiotic nitrogen fixation. Elevated levels of 7,4'-dihydroxyflavone were further increased in border cells of roots exposed to cotton root rot (Phymatotrichopsis omnivora), and the value of 7,4'-dihydroxyflavone as an antimicrobial compound was demonstrated using in vitro growth inhibition assays. The cumulative and pathway-specific data provide key insights into the metabolic programming of border cells that strongly implicate a more prominent mechanistic role for border cells in plant-microbe signaling, defense, and interactions than envisioned previously.
Highlights
Integrated metabolomics and transcriptomics of Medicago truncatula seedling border cells and root tips revealed substantial metabolic differences between these distinct and spatially segregated root regions
The differentiation of border cells begins with important developmental cues and heightened hormonal activity, resulting in substantial differences in primary and secondary metabolism fueled through intracellular starch-based energy production (Fig. 6)
Discussions follow that provide detailed gene expression and metabolomics data supporting our conclusion that border cells are differentially programmed with enhanced secondary metabolism
Summary
Integrated metabolomics and transcriptomics of Medicago truncatula seedling border cells and root tips revealed substantial metabolic differences between these distinct and spatially segregated root regions. The cumulative data provide compounding evidence that primary and secondary metabolism are differentially programmed in border cells relative to root tips. The root cap of many species produces thousands of differentiated cells that separate from the root but remain appressed to it in a water-soluble polysaccharide matrix, or mucilage, until released by exposure to water. Two landmark publications that characterized root development in Arabidopsis (Arabidopsis thaliana) were based on comparisons of anatomically distinct cell types over a developmental time series using microarray gene expression data (Birnbaum et al, 2003; Brady et al, 2007) These studies provided a model for understanding root architecture and its relationship to root development in both space and time. Legume roots produce numerous border cells that are viable even after release from the root (Hawes et al, 1998)
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