Cell wall-bound invertase limits sucrose export and is involved in symptom development and inhibition of photosynthesis during compatible interaction between tomato and Xanthomonas campestris pv vesicatoria

Plant Physiol. 2008 Nov;148(3):1523-36. doi: 10.1104/pp.108.127977. Epub 2008 Sep 10.

Abstract

Cell wall-bound invertase (cw-Inv) plays an important role in carbohydrate partitioning and regulation of sink-source interaction. There is increasing evidence that pathogens interfere with sink-source interaction, and induction of cw-Inv activity has frequently been shown in response to pathogen infection. To investigate the role of cw-Inv, transgenic tomato (Solanum lycopersicum) plants silenced for the major leaf cw-Inv isoforms were generated and analyzed during normal growth and during the compatible interaction with Xanthomonas campestris pv vesicatoria. Under normal growth conditions, activities of sucrolytic enzymes as well as photosynthesis and respiration were unaltered in the transgenic plants compared with wild-type plants. However, starch levels of source leaves were strongly reduced, which was most likely caused by an enhanced sucrose exudation rate. Following X. campestris pv vesicatoria infection, cw-Inv-silenced plants showed an increased sucrose to hexose ratio in the apoplast of leaves. Symptom development, inhibition of photosynthesis, and expression of photosynthetic genes were clearly delayed in transgenic plants compared with wild-type plants. In addition, induction of senescence-associated and pathogenesis-related genes observed in infected wild-type plants was abolished in cw-Inv-silenced tomato lines. These changes were not associated with decreased bacterial growth. In conclusion, cw-Inv restricts carbon export from source leaves and regulates the sucrose to hexose ratio in the apoplast. Furthermore, an increased apoplastic hexose to sucrose ratio can be linked to inhibition of photosynthesis and induction of pathogenesis-related gene expression but does not significantly influence bacterial growth. Indirectly, bacteria may benefit from low invertase activity, since the longevity of host cells is raised and basal defense might be dampened.

MeSH terms

  • Cell Wall / enzymology*
  • Cell Wall / metabolism
  • Lycopersicon esculentum / metabolism
  • Lycopersicon esculentum / microbiology
  • Lycopersicon esculentum / physiology*
  • Molecular Sequence Data
  • Photosynthesis*
  • Plants, Genetically Modified
  • Sucrose / metabolism*
  • Xanthomonas campestris / growth & development
  • Xanthomonas campestris / physiology*
  • beta-Fructofuranosidase / metabolism*

Substances

  • Sucrose
  • beta-Fructofuranosidase

Associated data

  • GENBANK/AF506005
  • GENBANK/AF506007
  • GENBANK/AF527779
  • GENBANK/AY129402
  • GENBANK/DQ100158
  • GENBANK/U48695
  • GENBANK/X02353
  • GENBANK/X13934
  • GENBANK/X51576
  • GENBANK/X54456
  • GENBANK/X74905
  • GENBANK/X95932
  • GENBANK/Y14032