The Andromonoecious Sex Determination Gene Predates the Separation of Cucumis and Citrullus Genera

PLoS One. 2016 May 12;11(5):e0155444. doi: 10.1371/journal.pone.0155444. eCollection 2016.

Abstract

Understanding the evolution of sex determination in plants requires the cloning and the characterization of sex determination genes. Monoecy is characterized by the presence of both male and female flowers on the same plant. Andromonoecy is characterized by plants carrying both male and bisexual flowers. In watermelon, the transition between these two sexual forms is controlled by the identity of the alleles at the A locus. We previously showed, in two Cucumis species, melon and cucumber, that the transition from monoecy to andromonoecy results from mutations in 1-aminocyclopropane-1-carboxylic acid synthase (ACS) gene, ACS-7/ACS2. To test whether the ACS-7/ACS2 function is conserved in cucurbits, we cloned and characterized ClACS7 in watermelon. We demonstrated co-segregation of ClACS7, the homolog of CmACS-7/CsACS2, with the A locus. Sequence analysis of ClACS7 in watermelon accessions identified three ClACS7 isoforms, two in andromonoecious and one in monoecious lines. To determine whether the andromonoecious phenotype is due to a loss of ACS enzymatic activity, we expressed and assayed the activity of the three protein isoforms. Like in melon and cucumber, the isoforms from the andromonoecious lines showed reduced to no enzymatic activity and the isoform from the monoecious line was active. Consistent with this, the mutations leading andromonoecy were clustered in the active site of the enzyme. Based on this, we concluded that active ClACS7 enzyme leads to the development of female flowers in monoecious lines, whereas a reduction of enzymatic activity yields hermaphrodite flowers. ClACS7, like CmACS-7/CsACS2 in melon and cucumber, is highly expressed in carpel primordia of buds determined to develop carpels and not in male flowers. Based on this finding and previous investigations, we concluded that the monoecy gene, ACS7, likely predated the separation of the Cucumis and Citrullus genera.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alleles
  • Base Sequence
  • Biological Evolution*
  • Chromosome Segregation / genetics
  • Citrullus / genetics*
  • Citrullus / physiology*
  • Cucumis sativus / genetics*
  • Cucumis sativus / physiology*
  • Ecotype
  • Flowers / genetics
  • Gene Expression Regulation, Plant
  • Genes, Plant*
  • Genetic Loci
  • Genetic Variation
  • Kinetics
  • Multigene Family
  • Phylogeny
  • Plant Proteins / genetics
  • Plant Proteins / metabolism
  • Protein Isoforms / genetics
  • Protein Isoforms / metabolism
  • Sequence Homology, Nucleic Acid
  • Synteny / genetics

Substances

  • Plant Proteins
  • Protein Isoforms

Grants and funding

This work was supported by BAP department in INRA, the grant Program Saclay Plant Sciences (SPS, ANR-10-LABX-40) for ABo and ABe, the Agence Nationale de la Recherche grant MELODY (ANR-11-BSV7-0024) for ABo, ABe and CD and the European Research Council grant (ERC-SEXYPARTH) for ABe. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.