A disulfide bond A-like oxidoreductase is a strong candidate gene for self-incompatibility in apricot (Prunus armeniaca) pollen

J Exp Bot. 2017 Nov 2;68(18):5069-5078. doi: 10.1093/jxb/erx336.

Abstract

S-RNase based gametophytic self-incompatibility (SI) is a widespread prezygotic reproductive barrier in flowering plants. In the Solanaceae, Plantaginaceae and Rosaceae gametophytic SI is controlled by the pistil-specific S-RNases and the pollen S-locus F-box proteins but non-S-specific factors, namely modifiers, are also required. In apricot, Prunus armeniaca (Rosaceae), we previously mapped two pollen-part mutations that confer self-compatibility in cultivars Canino and Katy at the distal end of chromosome 3 (M-locus) unlinked to the S-locus. Here, we used high-resolution mapping to identify the M-locus with an ~134 kb segment containing ParM-1-16 genes. Gene expression analysis identified four genes preferentially expressed in anthers as modifier gene candidates, ParM-6, -7, -9 and -14. Variant calling of WGS Illumina data from Canino, Katy, and 10 self-incompatible cultivars detected a 358 bp miniature inverted-repeat transposable element (MITE) insertion in ParM-7 shared only by self-compatible apricots, supporting ParM-7 as strong candidate gene required for SI. ParM-7 encodes a disulfide bond A-like oxidoreductase protein, which we named ParMDO. The MITE insertion truncates the ParMDO ORF and produces a loss of SI function, suggesting that pollen rejection in Prunus is dependent on redox regulation. Based on phylogentic analyses we also suggest that ParMDO may have originated from a tandem duplication followed by subfunctionalization and pollen-specific expression.

Keywords: DsbA oxidoreductase; M-locus; Prunus; gametophytic self-incompatibility; modifier; pollen-part mutation.

MeSH terms

  • Disulfides
  • Genetic Loci / genetics
  • Genotype
  • High-Throughput Nucleotide Sequencing
  • Loss of Function Mutation
  • Oxidoreductases / genetics
  • Oxidoreductases / metabolism*
  • Plant Proteins / genetics
  • Plant Proteins / metabolism
  • Pollen / enzymology*
  • Pollen / genetics
  • Pollen / physiology
  • Prunus armeniaca / enzymology*
  • Prunus armeniaca / genetics
  • Prunus armeniaca / physiology
  • Self-Incompatibility in Flowering Plants / genetics*
  • Sequence Analysis, DNA

Substances

  • Disulfides
  • Plant Proteins
  • Oxidoreductases