Trichoderma atroviride-emitted volatiles improve growth of Arabidopsis seedlings through modulation of sucrose transport and metabolism

Plant Cell Environ. 2021 Jun;44(6):1961-1976. doi: 10.1111/pce.14014. Epub 2021 Feb 16.

Abstract

Plants host a diverse microbiome and differentially react to the fungal species living as endophytes or around their roots through emission of volatiles. Here, using divided Petri plates for Arabidopsis-T. atroviride co-cultivation, we show that fungal volatiles increase endogenous sugar levels in shoots, roots and root exudates, which improve Arabidopsis root growth and branching and strengthen the symbiosis. Tissue-specific expression of three sucrose phosphate synthase-encoding genes (AtSPS1F, AtSPS2F and AtSPS3F), and AtSUC2 and SWEET transporters revealed that the gene expression signatures differ from those of the fungal pathogens Fusarium oxysporum and Alternaria alternata and that AtSUC2 is largely repressed either by increasing carbon availability or by perception of the fungal volatile 6-pentyl-2H-pyran-2-one. Our data point to Trichoderma volatiles as chemical signatures for sugar biosynthesis and exudation and unveil specific modulation of a critical, long-distance sucrose transporter in the plant.

Keywords: Arabidopsis; Trichoderma; root exudates; sucrose; sugar transporters; volatile compounds.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis / drug effects
  • Arabidopsis / genetics
  • Arabidopsis / growth & development*
  • Arabidopsis / metabolism
  • Biological Transport
  • Gene Expression Regulation, Plant / drug effects
  • Glucose / metabolism
  • Glucosyltransferases / genetics
  • Hypocreales / chemistry*
  • Membrane Transport Proteins / genetics
  • Membrane Transport Proteins / metabolism
  • Plant Exudates / metabolism
  • Plant Leaves / metabolism
  • Plant Proteins / genetics
  • Plant Proteins / metabolism
  • Plant Roots / growth & development
  • Plants, Genetically Modified
  • Pyrones / pharmacology
  • Seedlings / growth & development
  • Seedlings / metabolism
  • Sucrose / metabolism*
  • Sucrose / pharmacology
  • Volatile Organic Compounds / pharmacology*

Substances

  • 6-pentylpyrone
  • Membrane Transport Proteins
  • Plant Exudates
  • Plant Proteins
  • Pyrones
  • Volatile Organic Compounds
  • sucrose transport protein, plant
  • Sucrose
  • Glucosyltransferases
  • sucrose-phosphate synthase
  • Glucose

Supplementary concepts

  • Trichoderma atroviride