Cytochrome P450 mono-oxygenase CYP703A2 plays a central role in sporopollenin formation and ms5ms6 fertility in cotton

J Integr Plant Biol. 2022 Oct;64(10):2009-2025. doi: 10.1111/jipb.13340. Epub 2022 Sep 15.

Abstract

The double-recessive genic male-sterile (ms) line ms5 ms6 has been used to develop cotton (Gossypium hirsutum) hybrids for many years, but its molecular-genetic basis has remained unclear. Here, we identified the Ms5 and Ms6 loci through map-based cloning and confirmed their function in male sterility through CRISPR/Cas9 gene editing. Ms5 and Ms6 are highly expressed in stages 7-9 anthers and encode the cytochrome P450 mono-oxygenases CYP703A2-A and CYP703A2-D. The ms5 mutant carries a single-nucleotide C-to-T nonsense mutation leading to premature chain termination at amino acid 312 (GhCYP703A2-A312aa ), and ms6 carries three nonsynonymous substitutions (D98E, E168K, and G198R) and a synonymous mutation (L11L). Enzyme assays showed that GhCYP703A2 proteins hydroxylate fatty acids, and the ms5 (GhCYP703A2-A312aa ) and ms6 (GhCYP703A2-DD98E,E168K,G198R ) mutant proteins have decreased enzyme activities. Biochemical and lipidomic analyses showed that in ms5 ms6 plants, C12-C18 free fatty acid and phospholipid levels are significantly elevated in stages 7-9 anthers, while stages 8-10 anthers lack sporopollenin fluorescence around the pollen, causing microspore degradation and male sterility. Overall, our characterization uncovered functions of GhCYP703A2 in sporopollenin formation and fertility, providing guidance for creating male-sterile lines to facilitate hybrid cotton production and therefore exploit heterosis for improvement of cotton.

Keywords: cotton; cytochrome P450 mono-oxygenase; double-recessive genic male sterility; sporopollenin formation.

MeSH terms

  • Amino Acids / metabolism
  • Codon, Nonsense / metabolism
  • Cytochrome P-450 Enzyme System / genetics
  • Cytochrome P-450 Enzyme System / metabolism
  • Fatty Acids, Nonesterified / metabolism
  • Fertility / genetics
  • Gene Expression Regulation, Plant / genetics
  • Gossypium* / genetics
  • Gossypium* / metabolism
  • Mutant Proteins / genetics
  • Mutant Proteins / metabolism
  • Nucleotides / metabolism
  • Phospholipids / metabolism
  • Plant Infertility* / genetics

Substances

  • Amino Acids
  • Codon, Nonsense
  • Cytochrome P-450 Enzyme System
  • Fatty Acids, Nonesterified
  • Mutant Proteins
  • Nucleotides
  • Phospholipids
  • sporopollenin