Integration of the SMXL/D53 strigolactone signalling repressors in the model of shoot branching regulation in Pisum sativum

Plant J. 2021 Sep;107(6):1756-1770. doi: 10.1111/tpj.15415. Epub 2021 Aug 13.

Abstract

DWARF53 (D53) in rice (Oryza sativa) and its homologs in Arabidopsis (Arabidopsis thaliana), SUPPRESSOR OF MAX2-LIKE 6 (SMXL6), SMXL7 and SMXL8, are well established negative regulators of strigolactone (SL) signalling in shoot branching regulation. Little is known of pea (Pisum sativum) homologs and whether D53 and related SMXLs are specific to SL signalling pathways. Here, we identify two allelic pea mutants, dormant3 (dor3), and demonstrate through gene mapping and sequencing that DOR3 corresponds to a homolog of D53 and SMXL6/SMXL7, designated PsSMXL7. Phenotype analysis, gene expression, protein and hormone quantification assays were performed to determine the role of PsSMXL7 in regulation of bud outgrowth and the role of PsSMXL7 and D53 in integrating SL and cytokinin (CK) responses. Like D53 and related SMXLs, we show that PsSMXL7 can be degraded by SL and induces feedback upregulation of PsSMXL7 transcript. Here we reveal a system conserved in pea and rice, whereby CK also upregulates PsSMXL7/D53 transcripts, providing a clear mechanism for SL and CK cross-talk in the regulation of branching. To further deepen our understanding of the branching network in pea, we provide evidence that SL acts via PsSMXL7 to modulate auxin content via PsAFB5, which itself regulates expression of SL biosynthesis genes. We therefore show that PsSMXL7 is key to a triple hormone network involving an auxin-SL feedback mechanism and SL-CK cross-talk.

Keywords: D53; Pisum sativum (garden pea); SMXL; auxin; cytokinin; feedback regulation; strigolactone.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis / genetics
  • Arabidopsis / metabolism
  • Co-Repressor Proteins / genetics
  • Co-Repressor Proteins / metabolism
  • Cytokinins / metabolism
  • Feedback, Physiological
  • Gene Expression Regulation, Plant
  • Heterocyclic Compounds, 3-Ring / metabolism*
  • Indoleacetic Acids / metabolism
  • Lactones / metabolism*
  • Loss of Function Mutation
  • Oryza
  • Phylogeny
  • Pisum sativum / genetics
  • Pisum sativum / growth & development*
  • Pisum sativum / metabolism
  • Plant Proteins / genetics*
  • Plant Proteins / metabolism
  • Plants, Genetically Modified
  • Signal Transduction / genetics

Substances

  • Co-Repressor Proteins
  • Cytokinins
  • GR24 strigolactone
  • Heterocyclic Compounds, 3-Ring
  • Indoleacetic Acids
  • Lactones
  • Plant Proteins
  • indoleacetic acid