TREHALOSE PHOSPHATE SYNTHASE11-dependent trehalose metabolism promotes Arabidopsis thaliana defense against the phloem-feeding insect Myzus persicae

Plant J. 2011 Jul;67(1):94-104. doi: 10.1111/j.1365-313X.2011.04583.x. Epub 2011 Apr 26.

Abstract

Agricultural productivity is limited by the removal of sap, alterations in source-sink patterns, and viral diseases vectored by aphids, which are phloem-feeding pests. Here we show that TREHALOSE PHOSPHATE SYNTHASE11 (TPS11) gene-dependent trehalose metabolism regulates Arabidopsis thaliana defense against Myzus persicae (Sülzer), commonly known as the green peach aphid (GPA). GPA infestation of Arabidopsis resulted in a transient increase in trehalose and expression of the TPS11 gene, which encodes a trehalose-6-phosphate synthase/phosphatase. Knockout of TPS11 function abolished trehalose increases in GPA-infested leaves of the tps11 mutant plant and attenuated defense against GPA. Trehalose application restored resistance in the tps11 mutant, confirming that the lack of trehalose accumulation is associated with the inability of the tps11 mutant to control GPA infestation. Resistance against GPA was also higher in the trehalose hyper-accumulating tre1 mutant and in bacterial otsB gene-expressing plants, further supporting the conclusion that trehalose plays a role in Arabidopsis defense against GPA. Evidence presented here indicates that TPS11-dependent trehalose regulates expression of the PHYTOALEXIN DEFICIENT4 gene, which is a key modulator of defenses against GPA. TPS11 also promotes the re-allocation of carbon into starch at the expense of sucrose, the primary plant-derived carbon and energy source for the insect. Our results provide a framework for the signaling function of TPS11-dependent trehalose in plant stress responses, and also reveal an important contribution of starch in controlling the severity of aphid infestation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antibiosis
  • Aphids / immunology
  • Aphids / physiology*
  • Arabidopsis / genetics
  • Arabidopsis / immunology
  • Arabidopsis / metabolism
  • Arabidopsis / physiology*
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism*
  • Carboxylic Ester Hydrolases / genetics
  • Carboxylic Ester Hydrolases / metabolism*
  • Gene Expression Regulation, Plant
  • Glucosyltransferases / genetics
  • Glucosyltransferases / metabolism*
  • Phosphoric Monoester Hydrolases / genetics
  • Phosphoric Monoester Hydrolases / metabolism*
  • Plant Diseases / immunology
  • Plant Immunity
  • Plant Leaves / genetics
  • Plant Leaves / immunology
  • Plant Leaves / metabolism
  • Sequence Deletion
  • Signal Transduction
  • Starch / metabolism
  • Stress, Physiological
  • Sucrose / metabolism
  • Trehalose / metabolism*
  • Trehalose / pharmacology

Substances

  • Arabidopsis Proteins
  • Sucrose
  • Starch
  • Trehalose
  • Glucosyltransferases
  • trehalose-6-phosphate synthase
  • Carboxylic Ester Hydrolases
  • PAD4 protein, Arabidopsis
  • trehalose-phosphatase
  • Phosphoric Monoester Hydrolases