Nuclear phylotranscriptomics and phylogenomics support numerous polyploidization events and hypotheses for the evolution of rhizobial nitrogen-fixing symbiosis in Fabaceae.
Yiyong Zhao, Rong Zhang, Kai-Wen Jiang, Ji Qi, Yi Hu, Jing Guo, Renbin Zhu, Taikui Zhang, Ashley N Egan, Ting-Shuang Yi, Chien-Hsun Huang, Hong Ma
Author Information
Yiyong Zhao: State Key Laboratory of Genetic Engineering and Collaborative Innovation Center of Genetics and Development, Ministry of Education Key Laboratory of Biodiversity and Ecological Engineering, Institute of Plant Biology, Center of Evolutionary Biology, School of Life Sciences, Fudan University, 2005 Songhu Road, Shanghai 200433, China; Department of Biology, The Huck Institutes of the Life Sciences, The Pennsylvania State University, University Park, PA 16802, USA.
Rong Zhang: Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences, Lanhei Road, Kunming 650201, China.
Kai-Wen Jiang: Key Laboratory of Biodiversity Conservation in Southwest China, State Forestry Administration, Southwest Forestry University, Kunming 650224, PR China; Ningbo Botanical Garden Herbarium, Ningbo 315201, PR China.
Ji Qi: State Key Laboratory of Genetic Engineering and Collaborative Innovation Center of Genetics and Development, Ministry of Education Key Laboratory of Biodiversity and Ecological Engineering, Institute of Plant Biology, Center of Evolutionary Biology, School of Life Sciences, Fudan University, 2005 Songhu Road, Shanghai 200433, China.
Yi Hu: Department of Biology, The Huck Institutes of the Life Sciences, The Pennsylvania State University, University Park, PA 16802, USA.
Jing Guo: State Key Laboratory of Genetic Engineering and Collaborative Innovation Center of Genetics and Development, Ministry of Education Key Laboratory of Biodiversity and Ecological Engineering, Institute of Plant Biology, Center of Evolutionary Biology, School of Life Sciences, Fudan University, 2005 Songhu Road, Shanghai 200433, China.
Renbin Zhu: Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Menglun, Yunnan 666303, PR China.
Taikui Zhang: State Key Laboratory of Genetic Engineering and Collaborative Innovation Center of Genetics and Development, Ministry of Education Key Laboratory of Biodiversity and Ecological Engineering, Institute of Plant Biology, Center of Evolutionary Biology, School of Life Sciences, Fudan University, 2005 Songhu Road, Shanghai 200433, China.
Ashley N Egan: Department of Biology, Utah Valley University, Orem, UT 84058, USA.
Ting-Shuang Yi: Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences, Lanhei Road, Kunming 650201, China. Electronic address: tingshuangyi@mail.kib.ac.cn.
Chien-Hsun Huang: State Key Laboratory of Genetic Engineering and Collaborative Innovation Center of Genetics and Development, Ministry of Education Key Laboratory of Biodiversity and Ecological Engineering, Institute of Plant Biology, Center of Evolutionary Biology, School of Life Sciences, Fudan University, 2005 Songhu Road, Shanghai 200433, China. Electronic address: huang_ch@fudan.edu.cn.
Hong Ma: Department of Biology, The Huck Institutes of the Life Sciences, The Pennsylvania State University, University Park, PA 16802, USA. Electronic address: hxm16@psu.edu.
Fabaceae are the third largest angiosperm family, with 765 genera and ∼19 500 species. They are important both economically and ecologically, and global Fabaceae crops are intensively studied in part for their nitrogen-fixing ability. However, resolution of the intrasubfamilial Fabaceae phylogeny and divergence times has remained elusive, precluding a reconstruction of the evolutionary history of symbiotic nitrogen fixation in Fabaceae. Here, we report a highly resolved phylogeny using >1500 nuclear genes from newly sequenced transcriptomes and genomes of 391 species, along with other datasets, for a total of 463 legumes spanning all 6 subfamilies and 333 of 765 genera. The subfamilies are maximally supported as monophyletic. The clade comprising subfamilies Cercidoideae and Detarioideae is sister to the remaining legumes, and Duparquetioideae and Dialioideae are successive sisters to the clade of Papilionoideae and Caesalpinioideae. Molecular clock estimation revealed an early radiation of subfamilies near the K/Pg boundary, marked by mass extinction, and subsequent divergence of most tribe-level clades within ∼15 million years. Phylogenomic analyses of thousands of gene families support 28 proposed putative whole-genome duplication/whole-genome triplication events across Fabaceae, including those at the ancestors of Fabaceae and five of the subfamilies, and further analyses supported the Fabaceae ancestral polyploidy. The evolution of rhizobial nitrogen-fixing nodulation in Fabaceae was probed by ancestral character reconstruction and phylogenetic analyses of related gene families and the results support the hypotheses of one or two switch(es) to rhizobial nodulation followed by multiple losses. Collectively, these results provide a foundation for further morphological and functional evolutionary analyses across Fabaceae.
