Investigating the cis- regulatory basis of C3 and C4 photosynthesis in grasses at single- cell resolution

• 成果类型: Article
• 署名作者: Mendieta, John Pablo; Tu, Xiaoyu; Jiang, Daiquan; Yan, Haidong; Zhang, Xuan; Marand, Alexandre P.; Zhong, Silin; Schmitz, Robert J.
• 署名单位: University of Michigan System; University of Michigan; University System of Georgia; University of Georgia; Shanghai Jiao Tong University; Chinese University of Hong Kong
• 刊物名称: PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
• ISSN/ISSBN: 0027-12065
• DOI: 10.1073/pnas.2402781121
• 发表日期: 2024-10-01
• 关键词: aspartate-aminotransferase isozymes; panicum-miliaceum l; phosphoenolpyruvate carboxylase; orthophosphate dikinase; transcription factors; expression; maize; plant; gene; promoter

摘要

While considerable knowledge exists about the enzymes pivotal for C4 photosynthesis, much less is known about the cis- regulation important for specifying their expression in distinct cell types. Here, we use single- cell- indexed ATAC-seq to identify cell- type- specific accessible chromatin regions (ACRs) associated with C4 enzymes for five different grass species. This study spans four C4 species, covering three distinct photosynthetic subtypes: Zea mays and Sorghum bicolor (NADP- dependent malic enzyme), Panicum miliaceum (NAD- dependent malic enzyme), Urochloa fusca (phosphoenolpyruvate carboxykinase), along with the C3 outgroup Oryza sativa. We studied the cis- regulatory landscape of enzymes essential across all C4 species and those unique to C4 subtypes, measuring cell- type- specific biases for C4 enzymes using chromatin accessibility data. Integrating these data with phylogenetics revealed diverse co- option of gene family members between species, showcasing the various paths of C4 evolution. Besides promoter proximal ACRs, we found that, on average, C4 genes have two to three distal cell- type- specific ACRs, highlighting the complexity and divergent nature of C4 evolution. Examining the evolutionary history of these cell- type- specific ACRs revealed a spectrum of conserved and novel ACRs, even among closely related species, indicating ongoing evolution of cis- regulation at these C4 loci. This study illuminates the dynamic and complex nature of cis- regulatory elements evolution in C4 photosynthesis, particularly highlighting the intricate cis- regulatory evolution of key loci. Our findings offer a valuable resource for future investigations, potentially aiding in the optimization of C3 crop performance under changing climatic conditions.