Adaptive evolution of chloroplast division mechanisms during plant terrestrialization

被引:10
作者
Liu, Moyang [1 ,2 ]
Yu, Jing [1 ,2 ]
Yang, Ming [1 ,2 ]
Cao, Lingyan [3 ]
Chen, Cheng [1 ,2 ]
机构
[1] Shanghai Jiao Tong Univ, Shanghai Collaborat Innovat Ctr Agriseeds, Sch Agr & Biol, Shanghai 200240, Peoples R China
[2] Shanghai Jiao Tong Univ, Sch Agr & Biol, Joint Ctr Single Cell Biol, Shanghai 200240, Peoples R China
[3] Shanghai Jiao Tong Univ, Sch Life Sci & Biotechnol, Joint Int Res Lab Metab & Dev Sci, State Key Lab Hybrid Rice, Shanghai 200240, Peoples R China
基金
中国国家自然科学基金;
关键词
PLASTID DIVISION; DUPLICATE GENES; PHOTOSYNTHETIC EUKARYOTES; FTSZ-RING; PROTEIN; ARABIDOPSIS; CELL; EXPRESSION; BACTERIAL; DIVERGENCE;
D O I
10.1016/j.celrep.2024.113950
中图分类号
Q2 [细胞生物学];
学科分类号
071009 ; 090102 ;
摘要
Despite extensive research, the origin and evolution of the chloroplast division machinery remain unclear. Here, we employ recently sequenced genomes and transcriptomes of Archaeplastida clades to identify the core components of chloroplast division and reconstruct their evolutionary histories, respectively. Our findings show that complete division ring structures emerged in Charophytes. We find that Glaucophytes experienced strong selection pressure, generating diverse variants adapted to the changing terrestrial environments. By integrating the functions of chloroplast division genes ( CDG s) annotated in a workflow developed using large-scale multiomics data, we further show that dispersed duplications acquire more species -specific functions under stronger selection pressures. Notably, PARC6 , a dispersed duplicate CDG , regulates leaf color and plant growth in Solanum lycopersicum , demonstrating neofunctionalization. Our findings provide an integrated perspective on the functional evolution of chloroplast division machinery and highlight the potential of dispersed duplicate genes as the primary source of adaptive evolution of chloroplast division.
引用
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页数:18
相关论文
共 105 条
[1]   Polyploidy and genome evolution in plants [J].
Adams, KL ;
Wendel, JF .
CURRENT OPINION IN PLANT BIOLOGY, 2005, 8 (02) :135-141
[2]   The plastid division protein AtMinD1 is a Ca2+-ATPase stimulated by AtMinE1 [J].
Aldridge, C ;
Moller, SG .
JOURNAL OF BIOLOGICAL CHEMISTRY, 2005, 280 (36) :31673-31678
[3]   Mapping genome-wide transcription-factor binding sites using DAP-seq [J].
Bartlett, Anna ;
O'Malley, Ronan C. ;
Huang, Shao-shan Carol ;
Galli, Mary ;
Nery, Joseph R. ;
Gallavotti, Andrea ;
Ecker, Joseph R. .
NATURE PROTOCOLS, 2017, 12 (08) :1659-1672
[4]   The gene balance hypothesis: From classical genetics to modern genomics [J].
Birchler, James A. ;
Veitia, Reiner A. .
PLANT CELL, 2007, 19 (02) :395-402
[5]   Treadmilling by FtsZ filaments drives peptidoglycan synthesis and bacterial cell division [J].
Bisson-Filho, Alexandre W. ;
Hsu, Yen-Pang ;
Squyres, Georgia R. ;
Kuru, Erkin ;
Wu, Fabai ;
Jukes, Calum ;
Sun, Yingjie ;
Dekker, Cees ;
Holden, Seamus ;
VanNieuwenhze, Michael S. ;
Brun, Yves V. ;
Garner, Ethan C. .
SCIENCE, 2017, 355 (6326) :739-743
[6]   Functional divergence of duplicated genes formed by polyploidy during Arabidopsis evolution [J].
Blanc, G ;
Wolfe, KH .
PLANT CELL, 2004, 16 (07) :1679-1691
[7]   Insights into Land Plant Evolution Garnered from the Marchantia polymorpha Genome [J].
Bowman, John L. ;
Kohchi, Takayuki ;
Yamato, Katsuyuki T. ;
Jenkins, Jerry ;
Shu, Shengqiang ;
Ishizaki, Kimitsune ;
Yamaoka, Shohei ;
Nishihama, Ryuichi ;
Nakamura, Yasukazu ;
Berger, Frederic ;
Adam, Catherine ;
Aki, Shiori Sugamata ;
Althoff, Felix ;
Araki, Takashi ;
Arteaga-Vazquez, Mario A. ;
Balasubrmanian, Sureshkumar ;
Barry, Kerrie ;
Bauer, Diane ;
Boehm, Christian R. ;
Briginshaw, Liam ;
Caballero-Perez, Juan ;
Catarino, Bruno ;
Chen, Feng ;
Chiyoda, Shota ;
Chovatia, Mansi ;
Davies, Kevin M. ;
Delmans, Mihails ;
Demura, Taku ;
Dierschke, Tom ;
Dolan, Liam ;
Dorantes-Acosta, Ana E. ;
Eklund, D. Magnus ;
Florent, Stevie N. ;
Flores-Sandoval, Eduardo ;
Fujiyama, Asao ;
Fukuzawa, Hideya ;
Galik, Bence ;
Grimanelli, Daniel ;
Grimwood, Jane ;
Grossniklaus, Ueli ;
Hamada, Takahiro ;
Haseloff, Jim ;
Hetherington, Alexander J. ;
Higo, Asuka ;
Hirakawa, Yuki ;
Hundley, Hope N. ;
Ikeda, Yoko ;
Inoue, Keisuke ;
Inoue, Shin-Ichiro ;
Ishida, Sakiko .
CELL, 2017, 171 (02) :287-+
[8]   Chloroplast import motor subunits FtsHi1 and FtsHi2 are located on opposite sides of the inner envelope membrane [J].
Chang, Chia-Yun ;
Chen, Lih-Jen ;
Li, Hsou-Min .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2023, 120 (37)
[9]   The peptidoglycan synthase PBP interacts with PLASTID DIVISION2 to promote chloroplast division in Physcomitrium patens [J].
Chang, Ying ;
Tang, Ning ;
Zhang, Min .
NEW PHYTOLOGIST, 2024, 241 (03) :1115-1129
[10]   ARC3 Activation by PARC6 Promotes FtsZ-Ring Remodeling at the Chloroplast Division Site [J].
Chen, Cheng ;
Cao, Lingyan ;
Yang, Yue ;
Porter, Katie J. ;
Osteryoung, Katherine W. .
PLANT CELL, 2019, 31 (04) :862-885