Integrated Metabolomics and Transcriptomics Reveal Enhanced Specialized Metabolism in Medicago truncatula Root Border Cells  

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 b-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 7,49-dihydroxyflavone were further increased in border cells of roots exposed to cotton root rot (Phymatotrichopsis omnivora), and the value of 7,49-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.

Root exudate ofSolanum tuberosumis enriched in galactose-containing molecules and impacts the growth ofPectobacterium atrosepticum

“…border cells were found to be highly enriched in large starch granules. It was speculated that starch provides an energy and carbon source for root border cells of Medicago truncatula (Watson et al, 2015). It is likely that starch also plays an important role in the survival of potato root border cells after their release within the rhizosphere.…”

The Transcription Factor NIN-LIKE PROTEIN7 Controls Border-Like Cell Release

“…For example, border cells in pea protect the root tip from infection by the pathogenic fungus Nectria hematococca (Gunawardena and Hawes, 2002), while those of maize (Zea mays) exude a compound that promotes branching in the arbuscular mycorrhizal fungus Gigaspora gigantea (Nagahashi and Douds, 2004). In Medicago truncatula, border cells have elevated levels of defense compounds (Watson et al, 2015). In Arabidopsis, BLCs perceive and activate defense signaling in response to microbe-associated molecular patterns, such as flagellin22 and peptidoglycan (Plancot et al, 2013).…”

“…Border cells and BLCs are known for their protective roles in plant defense (Hawes et al, 2000;Watson et al, 2015). For example, border cells in pea protect the root tip from infection by the pathogenic fungus Nectria hematococca (Gunawardena and Hawes, 2002), while those of maize (Zea mays) exude a compound that promotes branching in the arbuscular mycorrhizal fungus Gigaspora gigantea (Nagahashi and Douds, 2004).…”

“…Border cells and BLCs secrete root exudates including antimicrobial compounds and are an important part of the root's defense against both biotic and abiotic rhizosphere stresses (Hawes et al, 1998(Hawes et al, , 2000Vicré et al, 2005;Driouich et al, 2013;Plancot et al, 2013;Watson et al, 2015). Both border cell and BLC release require cell wall-degrading enzymes (Hawes and Lin, 1990;Wen et al, 1999;Vicré et al, 2005;Durand et al, 2009).…”

“…This tissue is critical to plant health as it protects the delicate root meristem (Barlow, 2003), senses gravity (Blancaflor et al, 1998(Blancaflor et al, , 1999 and water (Eapen et al, 2005), and secretes antimicrobial compounds and secondary metabolites that defend the root against soilborne pathogens and abiotic stress (Hawes et al, 1998(Hawes et al, , 2000Vicré et al, 2005;Driouich et al, 2013;Watson et al, 2015). The root cap is composed of two cell types that surround the meristem: the lateral root cap, which flanks the meristem, and the columella root cap located at the root tip (Fig.…”