Comparative plastomes of Carya species provide new insights into the plastomes evolution and maternal phylogeny of the genus

Authors: XI, JIANWEI - Zhejiang A & F University; LV, SAIBIN - Zhejiang A & F University; ZHANG, WEIPING - Beijing Normal University; ZHANG, JINGBO - St John'S University; WANG, KETAO - Zhejiang A & F University; GUO, HAOBING - Bgi Shenzhen; HU, JIE - Bgi Shenzhen; YANG, YANG - Beijing Normal University; WANG, JIANHUA - Zhejiang A & F University; XIA, GUOHUA - Zhejiang A & F University; FAN, GUANGYI - Bgi Shenzhen; Wang, Xinwang; XIAO, LIHONG - Zhejiang A & F University

Submitted to: Frontiers in Plant Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/21/2022
Publication Date: 10/13/2022
Citation: Xi, J., Lv, S., Zhang, W., Zhang, J., Wang, K., Guo, H., Hu, J., Yang, Y., Wang, J., Xia, G., Fan, G., Wang, X., Xiao, L. 2022. Comparative plastomes of the critically endangered Carya poilanei and other Carya species provide new insights into the maternal relationship and phylogeny of the genus. Frontiers in Plant Science. 13. Article 990064. https://doi.org/10.3389/fpls.2022.
DOI: https://doi.org/10.3389/fpls.2022.990064

Interpretive Summary: Like many other trees, pecans inherit their chloroplasts from their female parent. Chloroplasts are important organs (organelles) in the cell that capture light and conduct photosynthesis, and are involved in the plant's immune response. The relationships between some Carya species have not been fully characterized using molecular tools. In this work, we sequenced the chloroplast genomes of 19 different Carya species. The variation of these chloroplast genomes was clustered in a phylogenetic tree. A maternal relationship between an endangered Carya species with others was determined and is in agreement with our previous findings. This work advances ongoing efforts to improve pecans as a successful crop for U.S. farmers and those in other nations as well.

Technical Abstract: Genus Carya in Juglandiodeae family belongs a temperate-subtropical forest tree representing the typical intercontinental disjunction between eastern Asia (EA) and North America (NA). Although previous efforts based on multiple molecular markers or genome-wide SNPs supported the monophyly of Carya and its two major subclades, the phylogenetic relationships, especially at the subclade level, still need to be comprehensively evaluated. The variation of Carya plastome has not been thoroughly characterized. Here, the plastomes of 19 congeneric Carya species, including the critically endangered C. poilanei, were de novo assembled. The overall assessment of plastomes revealed a high conservatism in the general genome features of Carya. However, remarkable differences presented among species, such as the IR-SC junction, SSR numbers, codon numbers, paired nucleotide variation, etc., which are consistent with the EA-NA disjunction. The IR-SC junction patterns indicated the relative diverse matrilineal sources among EA Carya in comparison with NA Carya. We reconstructed seven phylogenetic trees of Carya based on different plastome regions and the full-length plastome dataset. Six of the phylogenies strongly supported the previously reported relationships among genera of Juglandoideae and the two subclades of EA and NA Carya. However, the phylogenies based on different plastome datasets indicated significant differences between species within the EA and NA subclades, indicating the diverse selection and evolution trajectories of these plastome regions. The phylogenetic tree based on the full-length plastomes displayed the optimal topology. In which, the material relationship of several controversial species, C. dabieshanensis, C. sinensis, C. glabra, and C. ovata were further determined. Our findings suggested the full-length plastome is an ideal tool to explore maternal relationships among the subclades of Carya and potentially in the other outcrossing perennial woody plants. In addition, the plastome SSR markers provide variable tools for identifying and protecting the endangered species C. poilanei.