Evolution of Rosaceae Plastomes Highlights Unique Cerasus Diversification and Independent Origins of Fruiting Cherry

Jing Zhang; Yan Wang; Tao Chen; Qing Chen; Lei Wang; Zhen-Shan Liu; Hao Wang; Rui Xie; Wen He; Ming Li; Cong-Li Liu; Shao-Feng Yang; Meng-Yao Li; Yuan-Xiu Lin; Yun-Ting Zhang; Yong Zhang; Ya Luo; Hao-Ru Tang; Li-Zhi Gao; Xiao-Rong Wang

doi:10.3389/fpls.2021.736053

Evolution of Rosaceae Plastomes Highlights Unique Cerasus Diversification and Independent Origins of Fruiting Cherry

Front Plant Sci. 2021 Nov 19:12:736053. doi: 10.3389/fpls.2021.736053. eCollection 2021.

Authors

Jing Zhang^{1

2}, Yan Wang^{1

2}, Tao Chen^{1

3}, Qing Chen¹, Lei Wang^{1

2}, Zhen-Shan Liu^{1

2}, Hao Wang^{1

2}, Rui Xie^{1

2}, Wen He^{1

2}, Ming Li⁴, Cong-Li Liu⁴, Shao-Feng Yang², Meng-Yao Li¹, Yuan-Xiu Lin^{1

2}, Yun-Ting Zhang^{1

2}, Yong Zhang¹, Ya Luo¹, Hao-Ru Tang^{1

2}, Li-Zhi Gao^{5

6}, Xiao-Rong Wang^{1

2}

Affiliations

¹ College of Horticulture, Sichuan Agricultural University, Chengdu, China.
² Institute of Pomology and Olericulture, Sichuan Agricultural University, Chengdu, China.
³ College of Life Science, Sichuan Agricultural University, Ya'an, China.
⁴ Zhengzhou Fruit Research Institute, Chinese Academy of Agricultural Sciences, Zhengzhou, China.
⁵ Institute of Genomics and Bioinformatics, South China Agricultural University, Guangzhou, China.
⁶ Plant Germplasm and Genomics Center, Germplasm Bank of Wild Species in Southwest China, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, China.

Abstract

Rosaceae comprises numerous types of economically important fruits, ornamentals, and timber. The lack of plastome characteristics has blocked our understanding of the evolution of plastome and plastid genes of Rosaceae crops. Using comparative genomics and phylogenomics, we analyzed 121 Rosaceae plastomes of 54 taxa from 13 genera, predominantly including Cerasus (true cherry) and its relatives. To our knowledge, we generated the first comprehensive map of genomic variation across Rosaceae plastomes. Contraction/expansion of inverted repeat regions and sequence losses of the two single-copy regions underlie large genomic variations in size among Rosaceae plastomes. Plastid protein-coding genes were characterized with a high proportion (over 50%) of synonymous variants and insertion-deletions with multiple triplets. Five photosynthesis-related genes were specially selected in perennial woody trees. Comparative genomic analyses implied divergent evolutionary patterns between pomaceous and drupaceous trees. Across all examined plastomes, unique and divergent evolution was detected in Cerasus plastomes. Phylogenomic analyses and molecular dating highlighted the relatively distant phylogenetic relationship between Cerasus and relatives (Microcerasus, Amygdalus, Prunus, and Armeniaca), which strongly supported treating the monophyletic true cherry group as a separate genus excluding dwarf cherry. High genetic differentiation and distinct phylogenetic relationships implied independent origins and domestication between fruiting cherries, particularly between Prunus pseudocerasus (Cerasus pseudocerasus) and P. avium (C. avium). Well-resolved maternal phylogeny suggested that cultivated P. pseudocerasus originated from Longmenshan Fault zone, the eastern edge of Himalaya-Hengduan Mountains, where it was subjected to frequent genomic introgression between its presumed wild ancestors and relatives.

Keywords: Cerasus; Rosaceae; evolutionary pattern; fruiting cherry; genomic variation; plastomes.