Article (Scientific journals)
The genome of Eleocharis vivipara elucidates the genetics of C3-C4 photosynthetic plasticity and karyotype evolution in the Cyperaceae.
Liu, Hongbing; Zhao, Hang; Zhang, Yanwen et al.
2024In Journal of Integrative Plant Biology, 66 (11), p. 2505 - 2527
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Keywords :
C4 photosynthesis; Cyperaceae; Eleocharis vivipara; evolution; Chromosomes, Plant/genetics; Eleocharis/genetics; Evolution, Molecular; Synteny/genetics; Photosynthesis/genetics; Genome, Plant/genetics; Phylogeny; Karyotype; Chromosomes, Plant; Eleocharis; Genome, Plant; Photosynthesis; Synteny; Biochemistry; Biochemistry, Genetics and Molecular Biology (all); Plant Science
Abstract :
[en] Eleocharis vivipara, an amphibious sedge in the Cyperaceae family, has several remarkable properties, most notably its alternate use of C3 photosynthesis underwater and C4 photosynthesis on land. However, the absence of genomic data has hindered its utility for evolutionary and genetic research. Here, we present a high-quality genome for E. vivipara, representing the first chromosome-level genome for the Eleocharis genus, with an approximate size of 965.22 Mb mainly distributed across 10 chromosomes. Its Hi-C pattern, chromosome clustering results, and one-to-one genome synteny across two subgroups indicates a tetraploid structure with chromosome count 2n = 4x = 20. Phylogenetic analysis suggests that E. vivipara diverged from Cyperus esculentus approximately 32.96 million years ago (Mya), and underwent a whole-genome duplication (WGD) about 3.5 Mya. Numerous fusion and fission events were identified between the chromosomes of E. vivipara and its close relatives. We demonstrate that E. vivipara has holocentromeres, a chromosomal feature which can maintain the stability of such chromosomal rearrangements. Experimental transplantation and cross-section studies showed its terrestrial culms developed C4 Kranz anatomy with increased number of chloroplasts in the bundle sheath (BS) cells. Gene expression and weighted gene co-expression network analysis (WGCNA) showed overall elevated expression of core genes associated with the C4 pathway, and significant enrichment of genes related to modified culm anatomy and photosynthesis efficiency. We found evidence of mixed nicotinamide adenine dinucleotide - malic enzyme and phosphoenolpyruvate carboxykinase type C4 photosynthesis in E. vivipara, and hypothesize that the evolution of C4 photosynthesis predates the WGD event. The mixed type is dominated by subgenome A and supplemented by subgenome B. Collectively, our findings not only shed light on the evolution of E. vivipara and karyotype within the Cyperaceae family, but also provide valuable insights into the transition between C3 and C4 photosynthesis, offering promising avenues for crop improvement and breeding.
Disciplines :
Agriculture & agronomy
Author, co-author :
Liu, Hongbing  ;  Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Genome Analysis Laboratory of the Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, 518120, China
Zhao, Hang   ;  Université de Liège - ULiège > TERRA Research Centre ; Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, Beijing, 100081, China
Zhang, Yanwen  ;  Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Genome Analysis Laboratory of the Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, 518120, China ; State Key Laboratory of Crop Stress Adaptation and Improvement, School of Life Sciences, Henan University, Kaifeng, 475004, China ; Shenzhen Research Institute of Henan university, Shenzhen, 518000, China
Li, Xiuli  ;  Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Genome Analysis Laboratory of the Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, 518120, China
Zuo, Yi  ;  Key Laboratory of Plant Molecular Physiology, Institute of Botany, China National Botanical Garden, Chinese Academy of Science, Beijing, 100093, China
Wu, Zhen ;  Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Genome Analysis Laboratory of the Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, 518120, China
Jin, Kaining ;  Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, Beijing, 100081, China ; Department of Plant Sciences, Centre for Crop Systems Analysis, Wageningen University & Research, Wageningen, 6708 WB, The Netherlands
Xian, Wenfei ;  Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Genome Analysis Laboratory of the Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, 518120, China
Wang, Wenzheng ;  Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, Beijing, 100081, China
Ning, Weidong ;  Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Genome Analysis Laboratory of the Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, 518120, China
Liu, Zijian  ;  Université de Liège - ULiège > TERRA Research Centre ; Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Genome Analysis Laboratory of the Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, 518120, China
Zhao, Xiaoxiao ;  Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Genome Analysis Laboratory of the Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, 518120, China
Wang, Lei ;  Key Laboratory of Plant Molecular Physiology, Institute of Botany, China National Botanical Garden, Chinese Academy of Science, Beijing, 100093, China
Sage, Rowan F ;  Department of Ecology and Evolutionary Biology, The University of Toronto, Toronto, M5S 3B2, ON, Canada
Lu, Tiegang ;  Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, Beijing, 100081, China
Stata, Matt  ;  Plant Resilience Institute, Michigan State University, East Lansing, 48824, MI, USA ; Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, 48824, MI, USA
Cheng, Shifeng  ;  Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Genome Analysis Laboratory of the Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, 518120, China
More authors (7 more) Less
 These authors have contributed equally to this work.
Language :
English
Title :
The genome of Eleocharis vivipara elucidates the genetics of C3-C4 photosynthetic plasticity and karyotype evolution in the Cyperaceae.
Publication date :
November 2024
Journal title :
Journal of Integrative Plant Biology
ISSN :
1672-9072
eISSN :
1744-7909
Publisher :
John Wiley and Sons Inc, China republic 1949
Volume :
66
Issue :
11
Pages :
2505 - 2527
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
NSCF - National Natural Science Foundation of China
Funding text :
This research was funded by the National Natural Science Foundation of China (32300217), the National Key R&D Program of China (2023YFA0914600), the Guangdong Basic and Applied Basic Research Foundation (2022A1515110358), the Guangdong Science and Technology Foundation, \u201CZhu Jiang Talent Innovation\u201D project (2019ZT08N628), and the Special Funds for Science Technology Innovation and Industrial Development of Shenzhen Dapeng New District (PT202101\u201001).
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