The REL3-mediated TAS3 ta-siRNA pathway integrates auxin and ethylene signaling to regulate nodulation in Lotus japonicus

New Phytol. 2014 Jan;201(2):531-544. doi: 10.1111/nph.12550. Epub 2013 Oct 25.

Abstract

The ta-siRNA pathway is required for lateral organ development, including leaf patterning, flower differentiation and lateral root growth. Legumes can develop novel lateral root organs--nodules--resulting from symbiotic interactions with rhizobia. However, ta-siRNA regulation in nodule formation remains unknown. To explore ta-siRNA regulation in nodule formation, we investigated the roles of REL3, a key component of TAS3 ta-siRNA biogenesis, during nodulation in Lotus japonicus. We characterized the symbiotic phenotypes of the TAS3 ta-siRNA defective rel3 mutant, and analyzed the responses of the rel3 mutant to auxin and ethylene in order to gain insight into TAS3 ta-siRNA regulation of nodulation. The rel3 mutant produced fewer pink nitrogen-fixing nodules, with substantially decreased infection frequency and nodule initiation. Moreover, the rel3 mutant was more resistant than wild-type to 1-naphthaleneacetic acid (NAA) and N-1-naphthylphthalamic acid (NPA) in root growth, and exhibited insensitivity to auxins but greater sensitivity to auxin transport inhibitors during nodulation. Furthermore, the rel3 mutant has enhanced root-specific ethylene sensitivity and altered responses to ethylene during nodulation; the low-nodulating phenotype of the rel3 mutant can be restored by ethylene synthesis inhibitor L-α-(2-aminoethoxyvinyl)-glycine (AVG) or action inhibitor Ag(+). The REL3-mediated TAS3 ta-siRNA pathway regulates nodulation by integrating ethylene and auxin signaling.

Keywords: TAS3 ta-siRNA biogenesis; auxin; auxin response regulator (ARF); ethylene; nodulation; rel3 mutant.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Ethylenes / metabolism*
  • Indoleacetic Acids / metabolism*
  • Lotus / metabolism*
  • Mesorhizobium / physiology
  • Phenotype
  • Plant Proteins / genetics
  • Plant Proteins / metabolism
  • Plant Proteins / physiology*
  • Plant Root Nodulation / genetics*
  • RNA Interference
  • RNA, Small Interfering / genetics
  • RNA, Small Interfering / metabolism
  • RNA, Small Interfering / physiology*
  • Signal Transduction
  • Symbiosis / genetics

Substances

  • Ethylenes
  • Indoleacetic Acids
  • Plant Proteins
  • RNA, Small Interfering
  • ethylene