Evolution of self-compatibility by a mutant Sm-RNase in citrus

Mei Liang, Zonghong Cao, Andan Zhu, Yuanlong Liu, Mengqin Tao, Huayan Yang, Qiang Xu (Jr.), Shaohua Wang, Junjie Liu, Yongping Li, Chuanwu Chen, Zongzhou Xie, Chongling Deng, Junli Ye, Wenwu Guo, Qiang Xu, Rui Xia, Robert Larkin, Xiuxin Deng, Maurice BoschVernonica E. Franklin-Tong, Lijun Chai

Research output: Contribution to journalArticlepeer-review

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Abstract

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.
Original languageEnglish
Pages (from-to)131-142
Number of pages12
JournalNature Plants
Volume6
Issue number2
DOIs
Publication statusPublished - 13 Feb 2020

Keywords

  • Biological Evolution
  • Citrus/enzymology
  • Mutation
  • Plant Proteins/genetics
  • Reproduction
  • Ribonucleases/genetics

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