J Integr Plant Biol ›› 2024, Vol. 66 ›› Issue (11): 2505-2527.DOI: 10.1111/jipb.13765  cstr: 32098.14.jipb.13765

所属专题： Photosynthesis

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  • 收稿日期:2024-04-15 接受日期:2024-07-25 出版日期:2024-11-01 发布日期:2024-11-25

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

Hongbing Liu1†, Hang Zhao2,3†, Yanwen Zhang1,4,5†, Xiuli Li1†, Yi Zuo6†, Zhen Wu1, Kaining Jin2,7, Wenfei Xian1, Wenzheng Wang2, Weidong Ning1, Zijian Liu1,3, Xiaoxiao Zhao1, Lei Wang6, Rowan F. Sage8, Tiegang Lu2, Matt Stata9,10* and Shifeng Cheng1*   

  1. 1. 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
    2. Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, Beijing 100081, China
    3. Gembloux Agro‐Bio Tech, TERRA Teaching and Research Centre, University of Liège, Gembloux 4000, Belgium
    4. State Key Laboratory of Crop Stress Adaptation and Improvement, School of Life Sciences, Henan University, Kaifeng 475004, China
    5. Shenzhen Research Institute of Henan university, Shenzhen 518000, China
    6. Key Laboratory of Plant Molecular Physiology, Institute of Botany, China National Botanical Garden, Chinese Academy of Science, Beijing 100093, China
    7. Department of Plant Sciences, Centre for Crop Systems Analysis, Wageningen University & Research, Wageningen 6708 WB, The Netherlands
    8. Department of Ecology and Evolutionary Biology, The University of Toronto, Toronto, ON M5S 3B2, Canada
    9. Plant Resilience Institute, Michigan State University, East Lansing, MI 48824, USA
    10. Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, MI 48824, USA
    †These authors contributed equally to this article.
    *Correspondences: Matt Stata (statamat@msu.edu); Shifeng Cheng (chengshifeng@caas.cn, Dr. Cheng is fully responsible for the distributions of all materials associated with this article)
  • Received:2024-04-15 Accepted:2024-07-25 Online:2024-11-01 Published:2024-11-25
  • Supported by:
    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, “Zhu Jiang Talent Innovation” project (2019ZT08N628), and the Special Funds for Science Technology Innovation and Industrial Development of Shenzhen Dapeng New District (PT202101‐01).

Abstract: 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.

Key words: C4 photosynthesis, Cyperaceae, Eleocharis vivipara, evolution

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