Single-cell multi-omics reveals distinct regulatory architectures coordinating carbon assimilation and cyclic electron flow in maize C₄ photosynthesis.

Authors

Chuanshun Li, You Zhang, Kande Lin, Xiaojian Liu, Hanxiao Zhang, Jianzhao Yang, Caiyao Zhao, Leyi Yang, Zhengbiao Long, Yangmeihui Li, Qilin Deng, Bin Ma, Tong Wei, Silin Zhong, Xinguang Zhu, Pinghua Li, Xiaoyong Pan, Xiaoyu Tu

Published in

Molecular plant. Oct 26, 2026. Epub Oct 26, 2026.

Abstract

C₄ photosynthesis arose repeatedly through redeployment of pre-existing regulatory circuitry, yet how a shared regulatory system coordinates its interdependent photosynthetic functions remains unresolved. Here we integrate single-nucleus RNA-seq and sci-ATAC-seq with bulk histone profiles from mesophyll- and bundle sheath-enriched fractions and transcription factor binding profiles obtained in protoplasts. We compare the C₄ shuttle and Calvin-Benson-Bassham cycle with NDH-mediated cyclic electron flow in bundle sheath cells. Selected carbon assimilation loci were associated with differential H3K27me3, whereas the NDH-associated branch showed regulatory inputs linked to DNA binding with one finger (DOF) transcription factors. Dissection of the ZmNdhU promoter identifies a 49 bp DOF-responsive cis element whose activity is sensitive to local sequence context and insertion position in the promoter constructs tested and that supports vascular bundle-associated reporter expression in a heterologous promoter context. Bundle sheath-enriched expression of ZmDOF30 increases NDH-associated expression, cyclic electron flow, leaf ATP content and photosynthetic performance. In a field trial, the transgenic lines showed increased growth and biomass. Comparative analyses revealed lineage-associated variation in predicted promoter-proximal DOF-binding potential within a broader H3K27me3-associated transcription factor background. These findings distinguish regulatory configurations among maize photosynthetic modules and identify DOF-NDH regulation as a candidate route for improving photosynthetic performance in maize, with broader relevance to NADP-ME grasses.

PMID:
42935097
Bibliographic data and abstract were imported from PubMed on 27 Oct 2026.

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