The Compact Root Architecture 2 systemic pathway is required for the repression of cytokinins and miR399 accumulation in Medicago truncatula N-limited plants

J Exp Bot. 2024 Sep 27;75(18):5667-5680. doi: 10.1093/jxb/erae281.

Abstract

Legume plants can acquire mineral nitrogen (N) either through their roots or via a symbiotic interaction with N-fixing rhizobia bacteria housed in root nodules. To identify shoot-to-root systemic signals acting in Medicago truncatula plants at N deficit or N satiety, plants were grown in a split-root experimental design in which either high or low N was provided to half of the root system, allowing the analysis of systemic pathways independently of any local N response. Among the plant hormone families analyzed, the cytokinin trans-zeatin accumulated in plants at N satiety. Cytokinin application by petiole feeding led to inhibition of both root growth and nodulation. In addition, an exhaustive analysis of miRNAs revealed that miR2111 accumulates systemically under N deficit in both shoots and non-treated distant roots, whereas a miRNA related to inorganic phosphate (Pi) acquisition, miR399, accumulates in plants grown under N satiety. These two accumulation patterns are dependent on Compact Root Architecture 2 (CRA2), a receptor required for C-terminally Encoded Peptide (CEP) signaling. Constitutive ectopic expression of miR399 reduced nodule numbers and root biomass depending on Pi availability, suggesting that the miR399-dependent Pi-acquisition regulatory module controlled by N availability affects the development of the whole legume plant root system.

Keywords: CEP peptide; CLE peptide; CRA2 receptor; cytokinin; legume; miR399; microRNA; nitrogen-fixing symbiotic root nodulation; phosphate.

MeSH terms

  • Cytokinins* / metabolism
  • Gene Expression Regulation, Plant
  • Medicago truncatula* / genetics
  • Medicago truncatula* / growth & development
  • Medicago truncatula* / metabolism
  • MicroRNAs* / genetics
  • MicroRNAs* / metabolism
  • Nitrogen* / metabolism
  • Plant Growth Regulators / metabolism
  • Plant Proteins / genetics
  • Plant Proteins / metabolism
  • Plant Roots* / genetics
  • Plant Roots* / growth & development
  • Plant Roots* / metabolism
  • RNA, Plant / genetics
  • RNA, Plant / metabolism
  • Signal Transduction

Substances

  • MicroRNAs
  • Cytokinins
  • Nitrogen
  • Plant Proteins
  • RNA, Plant
  • Plant Growth Regulators