Journal
PLANT JOURNAL
Volume 109, Issue 3, Pages 675-692Publisher
WILEY
DOI: 10.1111/tpj.15586
Keywords
C-4 photosynthesis; Zea mays; bundle sheath; mesophyll; transcriptional regulation
Categories
Funding
- National Science Foundation of China [92035302, 31871313]
- Agricultural Science and Technology Innovation Program [CAASZDXT2019003]
- Hong Kong General Research Fund (GRF) [14104119, AoE/M-403/16]
- Natural Science Foundation of China (NSFC) [32100438]
- China Postdoctoral Science Foundation [2020M672858, 2021T140677]
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Through analyzing BS and M cells isolated from maize leaves using multiple techniques, it was found that chromatin accessibility coordinates with epigenetic features to regulate gene expression, and the preferential expression of genes in specific cell types is finely tuned by multiple chromatin features. This coordination is critical in ensuring the cell type-specific function of key C-4 genes.
C-4 plants partition photosynthesis enzymes between the bundle sheath (BS) and the mesophyll (M) cells for the better delivery of CO2 to RuBisCO and to reduce photorespiration. To better understand how C-4 photosynthesis is regulated at the transcriptional level, we performed RNA-seq, ATAC-seq, ChIP-seq and Bisulfite-seq (BS-seq) on BS and M cells isolated from maize leaves. By integrating differentially expressed genes with chromatin features, we found that chromatin accessibility coordinates with epigenetic features, especially H3K27me3 modification and CHH methylation, to regulate cell type-preferentially enriched gene expression. Not only the chromatin-accessible regions (ACRs) proximal to the genes (pACRs) but also the distal ACRs (dACRs) are determinants of cell type-preferentially enriched expression. We further identified cell type-preferentially enriched motifs, e.g. AAAG for BS cells and TGACC/T for M cells, and determined their corresponding transcription factors: DOFs and WRKYs. The complex interaction between cis and trans factors in the preferential expression of C-4 genes was also observed. Interestingly, cell type-preferentially enriched gene expression can be fine-tuned by the coordination of multiple chromatin features. Such coordination may be critical in ensuring the cell type-specific function of key C-4 genes. Based on the observed cell type-preferentially enriched expression pattern and coordinated chromatin features, we predicted a set of functionally unknown genes, e.g. Zm00001d042050 and Zm00001d040659, to be potential key C-4 genes. Our findings provide deep insight into the architectures associated with C-4 gene expression and could serve as a valuable resource to further identify the regulatory mechanisms present in C-4 species.
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