Abstract
Self-incompatibility (SI) is found in approximately 40% of flowering plant species and at least 100 families. Although orchids belong to the largest angiosperm family, only 10% of orchid species present SI and have gametophytic SI (GSI). Furthermore, a majority (72%) of Dendrobium species, which constitute one of the largest Orchidaceae genera, show SI and have GSI. However, nothing is known about the molecular mechanism of GSI. The S-determinants of GSI have been well characterized at the molecular level in Solanaceae, Rosaceae, and Plantaginaceae, which use an S-ribonuclease (S-RNase)-based system. Here, we investigate the hypothesis that Orchidaceae uses a similar S-RNase to those described in Rosaceae, Solanaceae, and Plantaginaceae SI species. In this study, two SI species (Dendrobium longicornu and D. chrysanthum) were identified using fluorescence microscopy. Then, the S-RNase- and SLF-interacting SKP1-like1 (SSK1)-like genes present in their transcriptomes and the genomes of Phalaenopsis equestris, D. catenatum, Vanilla shenzhenica, and Apostasia shenzhenica were investigated. Sequence, phylogenetic, and tissue-specific expression analyses revealed that none of the genes identified was an S-determinant, suggesting that Orchidaceae might have a novel SI mechanism. The results also suggested that RNase-based GSI might have evolved after the split of monocotyledons (monocots) and dicotyledons (dicots) but before the split of Asteridae and Rosidae. This is also the first study to investigate S-RNase-based GSI in monocots. However, studies on gene identification, differential expression, and segregation analyses in controlled crosses are needed to further evaluate the genes with high expression levels in GSI tissues.
Highlights
Orchidaceae, which represents approximately 8% of all vascular plant species and contains five subfamilies (Apostasioideae, Vanilloideae, Cypripedioideae, Orchidoideae, and Epidendroideae), is one of the largest plant families and includes more than 25,000 species that are known for their diverse specialized reproductive and ecological strategies (Givnish et al, 2015)
At 3 DAP, when the pollen tubes started to grow into the style, the cross-pollination pollen tubes were longer than the selfpollination pollen tubes; approximately 4 DAP, the self-pollination pollen tubes stopped growing at the top of the style
Phylogenetic analysis based on the RNase-T2 genes from four Orchidaceae genomes; the pollen, style, and leaf transcriptomes of D. chrysanthum; and the pollen, self-pollination style, and cross-pollination style transcriptomes of D. longicornu, which represent SC, partial SI, and SI species, respectively, suggested that these genes were not phylogenetically related to S-RNases and were clustered with Class-I and Class-II RNase-T2s from other species
Summary
Orchidaceae, which represents approximately 8% of all vascular plant species and contains five subfamilies (Apostasioideae, Vanilloideae, Cypripedioideae, Orchidoideae, and Epidendroideae), is one of the largest plant families and includes more than 25,000 species that are known for their diverse specialized reproductive and ecological strategies (Givnish et al, 2015). Self-incompatibility (SI) is estimated to occur in 10% of orchid species; a majority (72%) of the 61 Dendrobium species that are self-pollinated show self-sterility (Johansen, 1990). Nearly one-half of orchid SI species are from Dendrobium. As one of the largest Orchidaceae genera, the high SI rate in Dendrobium species might contribute to their high levels of species diversity
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