Ectopic expression of Kip-related proteins restrains root-knot nematode-feeding site expansion

New Phytol. 2013 Jul;199(2):505-519. doi: 10.1111/nph.12255. Epub 2013 Apr 10.

Abstract

The development of nematode feeding sites induced by root-knot nematodes involves the synchronized activation of cell cycle processes such as acytokinetic mitoses and DNA amplification. A number of key cell cycle genes are reported to be critical for nematode feeding site development. However, it remains unknown whether plant cyclin-dependent kinase (CDK) inhibitors such as the Arabidopsis interactor/inhibitor of CDK (ICK)/Kip-related protein (KRP) family are involved in nematode feeding site development. This study demonstrates the involvement of Arabidopsis ICK2/KRP2 and ICK1/KRP1 in the control of mitosis to endoreduplication in galls induced by the root-knot nematode Meloidogyne incognita. Using ICK/KRP promoter-GUS fusions and mRNA in situ hybridizations, we showed that ICK2/KRP2, ICK3/KRP5 and ICK4/KRP6 are expressed in galls after nematode infection. Loss-of-function mutants have minor effects on gall development and nematode reproduction. Conversely, overexpression of both ICK1/KRP1 and ICK2/KRP2 impaired mitosis in giant cells and blocked neighboring cell proliferation, resulting in a drastic reduction of gall size. Studying the dynamics of protein expression demonstrated that protein levels of ICK2/KRP2 are tightly regulated during giant cell development and reliant on the presence of the nematode. This work demonstrates that impeding cell cycle progression by means of ICK1/KRP1 and ICK2/KRP2 overexpression severely restricts gall development, leading to a marked limitation of root-knot nematode development and reduced numbers of offspring.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Arabidopsis / cytology
  • Arabidopsis / genetics
  • Arabidopsis / metabolism*
  • Arabidopsis / parasitology*
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism*
  • Cell Cycle Proteins / genetics
  • Cell Cycle Proteins / metabolism*
  • Cell Nucleus / metabolism
  • Cyclin-Dependent Kinase Inhibitor Proteins / genetics
  • Cyclin-Dependent Kinase Inhibitor Proteins / metabolism*
  • Feeding Behavior*
  • Gene Expression Regulation, Plant
  • Genes, Plant / genetics
  • Giant Cells / cytology
  • Giant Cells / metabolism
  • Mitosis
  • Organelle Size
  • Plant Roots / genetics
  • Plant Roots / parasitology*
  • Plant Tumors / genetics
  • Plant Tumors / parasitology
  • Plants, Genetically Modified
  • Ploidies
  • Protein Transport / genetics
  • Tylenchoidea / growth & development
  • Tylenchoidea / metabolism
  • Tylenchoidea / physiology*

Substances

  • Arabidopsis Proteins
  • Cell Cycle Proteins
  • Cyclin-Dependent Kinase Inhibitor Proteins
  • ICK1 protein, Arabidopsis
  • ICK2 protein, Arabidopsis