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.
Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, Beijing, 100081, China.
J Integr Plant Biol. 2024 Nov;66(11):2505-2527. doi: 10.1111/jipb.13765. Epub 2024 Aug 23.
Eleocharis vivipara, an amphibious sedge in the Cyperaceae family, has several remarkable properties, most notably its alternate use of C photosynthesis underwater and C 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 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 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 photosynthesis in E. vivipara, and hypothesize that the evolution of C 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 and C photosynthesis, offering promising avenues for crop improvement and breeding.
荸荠（Eleocharis vivipara），莎草科荸荠属的两栖植物，具有多项显著特性，最值得注意的是其在水下和陆地上分别采用 C3 和 C4 光合作用。然而，由于缺乏基因组数据，限制了其在进化和遗传研究中的应用。本研究提供了一个高质量的荸荠基因组，这是荸荠属的首个染色体水平基因组，大小约为 965.22 Mb，主要分布在 10 条染色体上。其 Hi-C 图谱、染色体聚类结果和两个亚组之间的一对一基因组同线性表明，其具有 2n = 4x = 20 的四倍体结构。系统发育分析表明，荸荠与食用莎草（Cyperus esculentus）大约在 3296 万年前（Mya）分化，并在大约 350 万年前经历了一次全基因组加倍（WGD）。在荸荠及其近亲的染色体之间鉴定到了大量的融合和裂变事件。本研究表明，荸荠具有全着丝粒，这一染色体特征可以维持这种染色体重排的稳定性。实验移植和横切研究表明，其陆生茎秆发育出 C3 Kranz 解剖结构，束鞘（BS）细胞中的叶绿体数量增加。基因表达和加权基因共表达网络分析（WGCNA）表明，与 C 途径相关的核心基因的整体表达水平升高，与改良茎秆解剖结构和光合作用效率相关的基因显著富集。本研究在荸荠中发现了混合烟酰胺腺嘌呤二核苷酸-苹果酸酶和磷酸烯醇式丙酮酸羧激酶型 C4 光合作用的证据，并假设 C4 光合作用的进化先于 WGD 事件。这种混合类型主要由亚基因组 A 主导，亚基因组 B 为辅。总的来说，本研究结果不仅阐明了荸荠和莎草科内的进化和核型演变，还为 C3 和 C4 光合作用之间的转变提供了有价值的见解，为作物改良和育种提供了有前景的途径。
