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The genome of Eleocharis vivipara elucidates the genetics of C3-C4 photosynthetic plasticity and karyotype evolution in the Cyperaceae

文献类型: 外文期刊

作者: Liu, Hongbing 1 ; Zhao, Hang 2 ; Zhang, Yanwen 1 ; Li, Xiuli 1 ; Zuo, Yi 6 ; Wu, Zhen 1 ; Jin, Kaining 2 ; Xian, Wenfei 1 ; Wang, Wenzheng 2 ; Ning, Weidong 1 ; Liu, Zijian 1 ; Zhao, Xiaoxiao 1 ; Wang, Lei 6 ; Sage, Rowan F. 8 ; Lu, Tiegang 2 ; Stata, Matt 9 ; Cheng, Shifeng 1 ;

作者机构: 1.Chinese Acad Agr Sci, Shenzhen Branch,Agr Genom Inst Shenzhen, Guangdong Lab Lingnan Modern Agr, Genome Anal Lab,Minist Agr & Rural Affairs, Shenzhen 518120, Peoples R China

2.Chinese Acad Agr Sci, Biotechnol Res Inst, Beijing 100081, Peoples R China

3.Univ Liege, TERRA Teaching & Res Ctr, Gembloux Agrobio Tech, B-4000 Gembloux, Belgium

4.Henan Univ, Sch Life Sci, State Key Lab Crop Stress Adaptat & Improvement, Kaifeng 475004, Peoples R China

5.Henan Univ, Shenzhen Res Inst, Shenzhen 518000, Peoples R China

6.Chinese Acad Sci, Inst Bot, Key Lab Plant Mol Physiol, China Natl Bot Garden, Beijing 100093, Peoples R China

7.Wageningen Univ & Res, Ctr Crop Syst Anal, Dept Plant Sci, NL-6708 WB Wageningen, Netherlands

8.Univ Toronto, Dept Ecol & Evolutionary Biol, Toronto, ON M5S 3B2, Canada

9.Michigan State Univ, Plant Resilience Inst, E Lansing, MI 48824 USA

10.Michigan State Univ, Dept Biochem & Mol Biol, E Lansing, MI 48824 USA

关键词: C-4 photosynthesis; Cyperaceae; Eleocharis vivipara; evolution

期刊名称:JOURNAL OF INTEGRATIVE PLANT BIOLOGY ( 影响因子:9.3; 五年影响因子:9.3 )

ISSN: 1672-9072

年卷期: 2024 年

页码:

收录情况: SCI

摘要: Eleocharis vivipara, an amphibious sedge in the Cyperaceae family, has several remarkable properties, most notably its alternate use of C-3 photosynthesis underwater and C-4 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 C-4 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 C-4 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 C-4 photosynthesis in E. vivipara, and hypothesize that the evolution of C-4 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 C-3 and C-4 photosynthesis, offering promising avenues for crop improvement and breeding.

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