The Arabidopsis microRNA396-GRF1/GRF3 regulatory module acts as a developmental regulator in the reprogramming of root cells during cyst nematode infection

Plant Physiol. 2012 May;159(1):321-35. doi: 10.1104/pp.112.193649. Epub 2012 Mar 14.

Abstract

The syncytium is a unique plant root organ whose differentiation is induced by plant-parasitic cyst nematodes to create a source of nourishment. Syncytium formation involves the redifferentiation and fusion of hundreds of root cells. The underlying regulatory networks that control this unique change of plant cell fate are not understood. Here, we report that a strong down-regulation of Arabidopsis (Arabidopsis thaliana) microRNA396 (miR396) in cells giving rise to the syncytium coincides with the initiation of the syncytial induction/formation phase and that specific miR396 up-regulation in the developed syncytium marks the beginning of the maintenance phase, when no new cells are incorporated into the syncytium. In addition, our results show that miR396 in fact has a role in the transition from one phase to the other. Expression modulations of miR396 and its Growth-Regulating Factor (GRF) target genes resulted in reduced syncytium size and arrested nematode development. Furthermore, genome-wide expression profiling revealed that the miR396-GRF regulatory system can alter the expression of 44% of the more than 7,000 genes reported to change expression in the Arabidopsis syncytium. Thus, miR396 represents a key regulator for the reprogramming of root cells. As such, this regulatory unit represents a powerful molecular target for the parasitic animal to modulate plant cells and force them into novel developmental pathways.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Arabidopsis / genetics
  • Arabidopsis / immunology
  • Arabidopsis / metabolism
  • Arabidopsis / parasitology*
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / immunology
  • Arabidopsis Proteins / metabolism
  • Disease Resistance
  • Gene Expression Profiling
  • Gene Expression Regulation, Plant
  • Genes, Plant
  • Giant Cells / metabolism
  • Giant Cells / pathology
  • MicroRNAs / genetics
  • MicroRNAs / metabolism*
  • Nematoda / growth & development
  • Nematoda / pathogenicity*
  • Plant Cells / metabolism
  • Plant Cells / parasitology
  • Plant Diseases / immunology
  • Plant Diseases / parasitology
  • Plant Roots / genetics
  • Plant Roots / metabolism*
  • Plant Roots / parasitology
  • Plants, Genetically Modified / genetics
  • Plants, Genetically Modified / metabolism
  • Plants, Genetically Modified / parasitology
  • Plasmids / genetics
  • Plasmids / metabolism
  • RNA, Plant / genetics
  • RNA, Plant / metabolism
  • Transgenes

Substances

  • Arabidopsis Proteins
  • MIRN396 microRNA, Arabidopsis
  • MicroRNAs
  • RNA, Plant

Associated data

  • GEO/GSE31593