The genotype of barley cultivars influences multiple aspects of their associated microbiota via differential root exudate secretion

PLoS Biol. 2024 Apr 25;22(4):e3002232. doi: 10.1371/journal.pbio.3002232. eCollection 2024 Apr.

Abstract

Plant-associated microbes play vital roles in promoting plant growth and health, with plants secreting root exudates into the rhizosphere to attract beneficial microbes. Exudate composition defines the nature of microbial recruitment, with different plant species attracting distinct microbiota to enable optimal adaptation to the soil environment. To more closely examine the relationship between plant genotype and microbial recruitment, we analysed the rhizosphere microbiomes of landrace (Chevallier) and modern (NFC Tipple) barley (Hordeum vulgare) cultivars. Distinct differences were observed between the plant-associated microbiomes of the 2 cultivars, with the plant-growth promoting rhizobacterial genus Pseudomonas substantially more abundant in the Tipple rhizosphere. Striking differences were also observed between the phenotypes of recruited Pseudomonas populations, alongside distinct genotypic clustering by cultivar. Cultivar-driven Pseudomonas selection was driven by root exudate composition, with the greater abundance of hexose sugars secreted from Tipple roots attracting microbes better adapted to growth on these metabolites and vice versa. Cultivar-driven selection also operates at the molecular level, with both gene expression and the abundance of ecologically relevant loci differing between Tipple and Chevallier Pseudomonas isolates. Finally, cultivar-driven selection is important for plant health, with both cultivars showing a distinct preference for microbes selected by their genetic siblings in rhizosphere transplantation assays.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Genotype*
  • Hordeum* / genetics
  • Hordeum* / metabolism
  • Hordeum* / microbiology
  • Microbiota* / genetics
  • Microbiota* / physiology
  • Plant Exudates / metabolism
  • Plant Roots* / metabolism
  • Plant Roots* / microbiology
  • Pseudomonas* / genetics
  • Pseudomonas* / metabolism
  • Pseudomonas* / physiology
  • Rhizosphere*
  • Soil Microbiology

Substances

  • Plant Exudates

Grants and funding

APM was funded by UKRI-BBSRC DTP Studentship Award (BB/M011216/1) to the Norwich Research Park. ABG was supported by a John Innes Foundation Rotation PhD Studentship. GC, PB, JD, OT, JKMB, PN, CR and JGM were supported by BBSRC Institute Strategic Programme Grant BBS/E/J/000PR9797 to the John Innes Centre. PP and VR were supported by UKRI-BBSRC Responsive mode Grant BB/T001801/1 to PP. CR and SD were supported by UKRI-BBSRC Responsive mode Grant BB/K02003X/1 to CR. The funders played no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.