Altered sucrose synthase and invertase expression affects the local and systemic sugar metabolism of nematode-infected Arabidopsis thaliana plants

J Exp Bot. 2014 Jan;65(1):201-12. doi: 10.1093/jxb/ert359. Epub 2013 Nov 1.

Abstract

Sedentary endoparasitic nematodes of plants induce highly specific feeding cells in the root central cylinder. From these, the obligate parasites withdraw all required nutrients. The feeding cells were described as sink tissues in the plant's circulation system that are supplied with phloem-derived solutes such as sugars. Currently, there are several publications describing mechanisms of sugar import into the feeding cells. However, sugar processing has not been studied so far. Thus, in the present work, the roles of the sucrose-cleaving enzymes sucrose synthases (SUS) and invertases (INV) in the development of Heterodera schachtii were studied. Gene expression analyses indicate that both enzymes are regulated transcriptionally. Nematode development was enhanced on multiple INV and SUS mutants. Syncytia of these mutants were characterized by altered enzyme activity and changing sugar pool sizes. Further, the analyses revealed systemically affected sugar levels and enzyme activities in the shoots of the tested mutants, suggesting changes in the source-sink relationship. Finally, the development of the root-knot nematode Meloidogyne javanica was studied in different INV and SUS mutants and wild-type Arabidopsis plants. Similar effects on the development of both sedentary endoparasitic nematode species (root-knot and cyst nematode) were observed, suggesting a more general role of sucrose-degrading enzymes during plant-nematode interactions.

Keywords: Cytosolic invertase; Heterodera schachtii; Meloidogyne javanica; enzyme activity; nematode; neutral invertase; plant pathogen; sucrose synthase..

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Arabidopsis / enzymology*
  • Arabidopsis / genetics
  • Arabidopsis / parasitology
  • Arabidopsis Proteins / genetics*
  • Arabidopsis Proteins / metabolism
  • Gene Expression Regulation, Plant*
  • Glucosyltransferases / genetics*
  • Glucosyltransferases / metabolism
  • Host-Parasite Interactions
  • Mutagenesis, Insertional
  • Phloem / enzymology
  • Phloem / genetics
  • Phloem / parasitology
  • Plant Diseases / parasitology
  • Plant Roots / enzymology
  • Plant Roots / genetics
  • Plant Roots / parasitology
  • Plant Shoots
  • Plants, Genetically Modified
  • Sucrose / metabolism
  • Tylenchoidea / physiology*
  • beta-Fructofuranosidase / genetics*
  • beta-Fructofuranosidase / metabolism

Substances

  • Arabidopsis Proteins
  • Sucrose
  • Glucosyltransferases
  • sucrose synthase
  • beta-Fructofuranosidase