A Legume TOR Protein Kinase Regulates Rhizobium Symbiosis and Is Essential for Infection and Nodule Development

Plant Physiol. 2016 Nov;172(3):2002-2020. doi: 10.1104/pp.16.00844. Epub 2016 Oct 3.

Abstract

The target of rapamycin (TOR) protein kinase regulates metabolism, growth, and life span in yeast, animals, and plants in coordination with nutrient status and environmental conditions. The nutrient-dependent nature of TOR functionality makes this kinase a putative regulator of symbiotic associations involving nutrient acquisition. However, TOR's role in these processes remains to be understood. Here, we uncovered the role of TOR during the bean (Phaseolus vulgaris)-Rhizobium tropici (Rhizobium) symbiotic interaction. TOR was expressed in all tested bean tissues, with higher transcript levels in the root meristems and senesced nodules. We showed TOR promoter expression along the progressing infection thread and in the infected cells of mature nodules. Posttranscriptional gene silencing of TOR using RNA interference (RNAi) showed that this gene is involved in lateral root elongation and root cell organization and also alters the density, size, and number of root hairs. The suppression of TOR transcripts also affected infection thread progression and associated cortical cell divisions, resulting in a drastic reduction of nodule numbers. TOR-RNAi resulted in reduced reactive oxygen species accumulation and altered CyclinD1 and CyclinD3 expression, which are crucial factors for infection thread progression and nodule organogenesis. Enhanced expression of TOR-regulated ATG genes in TOR-RNAi roots suggested that TOR plays a role in the recognition of Rhizobium as a symbiont. Together, these data suggest that TOR plays a vital role in the establishment of root nodule symbiosis in the common bean.

MeSH terms

  • Amino Acid Sequence
  • Autophagy / genetics
  • Cell Wall / genetics
  • Down-Regulation / genetics
  • Gene Expression Profiling
  • Gene Expression Regulation, Plant
  • Genes, Plant
  • Phagosomes / metabolism
  • Phagosomes / ultrastructure
  • Phaseolus / enzymology*
  • Phaseolus / genetics
  • Phaseolus / microbiology*
  • Phaseolus / ultrastructure
  • Phenotype
  • Phylogeny
  • Plant Proteins / chemistry
  • Plant Proteins / metabolism*
  • Plant Root Nodulation / genetics
  • Plants, Genetically Modified
  • Promoter Regions, Genetic / genetics
  • RNA Interference
  • Reactive Oxygen Species / metabolism
  • Rhizobium / physiology*
  • Root Nodules, Plant / genetics
  • Root Nodules, Plant / microbiology*
  • Root Nodules, Plant / ultrastructure
  • Sequence Analysis, DNA
  • Symbiosis / genetics*
  • TOR Serine-Threonine Kinases / chemistry
  • TOR Serine-Threonine Kinases / metabolism*
  • Up-Regulation / genetics

Substances

  • Plant Proteins
  • Reactive Oxygen Species
  • TOR Serine-Threonine Kinases