Self-incompatibility (SI) is an important mechanism that prevents self-fertilization and inbreeding in flowering plants. The most widespread SI system utilizes S ribonucleases (S-RNases) and S-locus F-boxes (SLFs) as S determinants. In citrus, SI is ancestral, and Citrus maxima (pummelo) is self-incompatible, while Citrus reticulata (mandarin) and its hybrids are self-compatible (SC). Here, we identify nine highly polymorphic pistil-specific, developmentally expressed S-RNases from pummelo that segregate with S haplotypes in a gametophytic manner and cluster with authentic S-RNases. We provide evidence that these S-RNases function as the female S determinants in citrus. Moreover, we show that each S-RNase is linked to approximately nine SLFs. In an analysis of 117 citrus SLF and SFL-like (SLFL) genes, we reveal that they cluster into 12 types and that the S-RNases and intra-haplotypic SLF and SLFL genes co-evolved. Our data support the notion that citrus have a S locus comprising a S-RNase and several SLFs that fit the non-self-recognition model. We identify a predominant single nucleotide mutation, Sm-RNase, in SC citrus, which provides a 'natural' loss of function. We show that SI-SC transitions due to the Sm-RNase initially arose in mandarin, spreading to its hybrids and became fixed. Identification of an evolutionarily distant new genus utilizing the S-RNase-based SI system, >100 million years separated from the nearest S-RNase family, is a milestone for evolutionary comparative studies.
Bibliographical noteFunding Information:
We are grateful to J. Wu from Nanjing Agricultural University for providing the sample of Pyrus bretschneideri. This research was financially supported by the National Key Research and Development Programme of China (grant no. 2018YFD1000107), the National Natural Science Foundation of China (grant nos. 31772259, 31630065 and 31521092), the Fundamental Research Funds for the Central Universities (grant no. 2662019PY044) and the China Agriculture Research System (grant no. CARS-27). The Biotechnology and Biological Sciences Research Council (BBSRC) funds research in the laboratories of M.B. and V.E.F.-T. (grant no. BB/P005489/1). We would like to thank T. Li (China Agricultural University) and C. Franklin (School of Biosciences, University of Birmingham, UK) for their valuable suggestions.
© 2020, The Author(s), under exclusive licence to Springer Nature Limited.
ASJC Scopus subject areas
- Plant Science