Nuclear phylogeny and insights into whole-genome duplications and reproductive development of Solanaceae plants

Jie Huang; Weibin Xu; Junwen Zhai; Yi Hu; Jing Guo; Caifei Zhang; Yiyong Zhao; Lin Zhang; Christopher Martine; Hong Ma; Chien-Hsun Huang

doi:10.1016/j.xplc.2023.100595

Nuclear phylogeny and insights into whole-genome duplications and reproductive development of Solanaceae plants

Plant Commun. 2023 Jul 10;4(4):100595. doi: 10.1016/j.xplc.2023.100595. Epub 2023 Mar 25.

Authors

Jie Huang¹, Weibin Xu², Junwen Zhai³, Yi Hu⁴, Jing Guo⁵, Caifei Zhang⁵, Yiyong Zhao⁵, Lin Zhang⁵, Christopher Martine⁶, Hong Ma⁷, Chien-Hsun Huang⁸

Affiliations

¹ 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, Shanghai 200438, China; Guangxi Key Laboratory of Plant Conservation and Restoration Ecology in Karst Terrain, Guangxi Institute of Botany, Guangxi Zhuangzu Autonomous Region and Chinese Academy of Sciences, Guilin 541006, China.
² Guangxi Key Laboratory of Plant Conservation and Restoration Ecology in Karst Terrain, Guangxi Institute of Botany, Guangxi Zhuangzu Autonomous Region and Chinese Academy of Sciences, Guilin 541006, China.
³ Key Laboratory of National Forestry and Grassland Administration for Orchid Conservation and Utilization, Fujian Agriculture and Forestry University, Fuzhou 350002, China.
⁴ Department of Biology, the Huck Institutes of Life Sciences, the Pennsylvania State University, University Park, State College, PA 16802, USA.
⁵ 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, Shanghai 200438, China.
⁶ Department of Biology, Bucknell University, Lewisburg, PA 17837, USA.
⁷ Department of Biology, the Huck Institutes of Life Sciences, the Pennsylvania State University, University Park, State College, PA 16802, USA. Electronic address: hxm16@psu.edu.
⁸ 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, Shanghai 200438, China. Electronic address: huang_ch@fudan.edu.cn.

Abstract

Solanaceae, the nightshade family, have ∼2700 species, including the important crops potato and tomato, ornamentals, and medicinal plants. Several sequenced Solanaceae genomes show evidence for whole-genome duplication (WGD), providing an excellent opportunity to investigate WGD and its impacts. Here, we generated 93 transcriptomes/genomes and combined them with 87 public datasets, for a total of 180 Solanaceae species representing all four subfamilies and 14 of 15 tribes. Nearly 1700 nuclear genes from these transcriptomic/genomic datasets were used to reconstruct a highly resolved Solanaceae phylogenetic tree with six major clades. The Solanaceae tree supports four previously recognized subfamilies (Goetzeioideae, Cestroideae, Nicotianoideae, and Solanoideae) and the designation of three other subfamilies (Schizanthoideae, Schwenckioideae, and Petunioideae), with the placement of several previously unassigned genera. We placed a Solanaceae-specific whole-genome triplication (WGT1) at ∼81 million years ago (mya), before the divergence of Schizanthoideae from other Solanaceae subfamilies at ∼73 mya. In addition, we detected two gene duplication bursts (GDBs) supporting proposed WGD events and four other GDBs. An investigation of the evolutionary histories of homologs of carpel and fruit developmental genes in 14 gene (sub)families revealed that 21 gene clades have retained gene duplicates. These were likely generated by the Solanaceae WGT1 and may have promoted fleshy fruit development. This study presents a well-resolved Solanaceae phylogeny and a new perspective on retained gene duplicates and carpel/fruit development, providing an improved understanding of Solanaceae evolution.

Keywords: Solanaceae; carpel and fruit development; phylogeny; transcriptome; whole-genome duplication.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Evolution, Molecular
Gene Duplication*
Phylogeny
Plants / genetics
Solanaceae* / genetics