Evolutionary history of two pollen self-incompatibility factors reveals alternate routes to self-compatibility within Solanum

• Published in: American journal of botany 2017-12, Vol.104 (12), p.1904-1919
• Main Authors: Markova, Dragomira N., Petersen, Jennifer J., Yam, Sarah E., Corral, Adryanna, Valle, Matthew J., Li, Wentao, Chetelat, Roger T.
• Format: Article
• Language: English
• Subjects: Biological Evolution; Compatibility; Complementation; Cullin1; Demography; Fertilization; Flowers & plants; Gene sequencing; Inbreeding; Incompatibility; Mating; mating system transitions; Mutation; Phylogeny; Pistils; Pollen; Pollen - genetics; Pollen - physiology; Pollination - genetics; Pollination - physiology; Proteins; RESEARCH ARTICLE; Ribonuclease S; Self-fertilization; Self-incompatibility; Solanaceae; Solanum; Solanum - genetics; Solanum - physiology; Solanum arcanum; Solanum chmielewskii; Solanum neorickii; Studies; S‐locus F‐box protein; S‐RNase; tomato; Tomatoes; unilateral incompatibility
• ISSN: 0002-9122; 1537-2197
• DOI: 10.3732/ajb.1700196

PREMISE OF THE STUDY: Self‐incompatibility (SI) prevents self‐fertilization and reduces inbreeding. While SI is common in plants, transitions to self‐compatibility (SC) occur frequently. Little is known about the genetic changes and evolutionary steps underlying these shifts. METHODS: In the Solanaceae, SI is gametophytic, with specificity determined by S‐RNases in the pistil and S‐locus F‐box proteins (SLFs) in pollen. We examined the role of two pollen factors, Cullin1 (CUL1) and SLF‐23, in SI → SC transitions in wild tomato species from the Arcanum species group (Solanum arcanum, S. neorickii, and S. chmielewskii). Pollen compatibility was assessed on tester lines that reject pollen lacking functional SLF‐23 or CUL1. Complementation tests, gene sequencing, and phylogenetic analyses were used to characterize both functional and nonfunctional alleles. KEY RESULTS: We found evidence for multiple independent SI → SC transitions. In S. arcanum and S. chmielewskii, SC is caused by loss of pistil S‐RNase activity, while in S. neorickii SC is associated with expression of a functional SLF‐23 that recognizes the S9 type S‐RNase expressed in its pistils. Interestingly, we found identical deletion mutations in CUL1 exon 7 of S. chmielewskii as previously seen in S. habrochaites. CONCLUSIONS: Mating system transitions in the Arcanum group have occurred via both pistil loss‐of‐function and pollen gain‐of‐function SC mutations. Mutations common to S. chmielewskii and S. habrochaites must have arisen in a common ancestor, possibly to the entire tomato clade, then became fixed in different lineages after loss of pistil‐side SI function.