Abstract
C4 photosynthesis is characterized by the compartmentalization of the processes of atmospheric uptake of CO2 and its conversion into carbohydrate between mesophyll and bundle-sheath cells. As a result, most of the enzymes participating in the Calvin-Benson-Bassham (CBB) cycle, including RubisCO, are highly expressed in bundle-sheath cells. There is evidence that changes in the regulatory sequences of RubisCO contribute to its bundle-sheath-specific expression, however, little is known about how the spatial-expression pattern of other CBB cycle enzymes is regulated. In this study, we use a computational approach to scan for transcription factor binding sites in the regulatory regions of the genes encoding CBB cycle enzymes, SBPase, FBPase, PRK, and GAPDH-B, of C3 and C4 grasses. We identified potential cis-regulatory elements present in each of the genes studied here, regardless of the photosynthetic path used by the plant. The trans-acting factors that bind these elements have been validated in A. thaliana and might regulate the expression of the genes encoding CBB cycle enzymes. In addition, we also found C4-specific transcription factor binding sites in the genes encoding CBB cycle enzymes that could potentially contribute to the pathway-specific regulation of gene expression. These results provide a foundation for the functional analysis of the differences in regulation of genes encoding CBB cycle enzymes between C3 and C4 grasses.
Highlights
C4 plants achieve higher photosynthetic efficiency by concentrating CO2 around RubisCO
To account for the numerous independent origins of C4 photosynthesis, we focus on a small subset of eight grasses: Oryza sativa, Hordeum vulgare, Brachypodium distachyon, Dichanthelium oligosanthes, Zea mays, Sorghum bicolor, Panicum virgatum, and Setaria viridis
For SBPase, we identified one coding Sequences (CNS) located at the last intron of most orthologs (Figures 1A,C), and two CNSs found only in SBPase orthologous genes from PACMAD species (C4 species + D. oligosanthes; Figure 1C)
Summary
C4 plants achieve higher photosynthetic efficiency by concentrating CO2 around RubisCO. A number of regulatory elements conferring a M or BS specific expression pattern have been identified in the CBB Genes in CC4 Grasses regulatory sequences of the genes encoding PEPC, Ppdk; or NADP-ME, NAD-ME, and RubisCO (Nomura et al, 2000; Berry et al, 2011; Williams et al, 2016; Reyna-Llorens et al, 2018) To further interrogate those regulatory elements, a combination of comparative transcriptomics to identify differential expression of genes (Bräutigam et al, 2011; Aubry et al, 2014; Xu et al, 2016) and DNAse-seq to map differences in open chromatin regions between M and BS cells (Burgess et al, 2019) have been used. These studies have led to the identification of putative cisregulatory elements and the trans-acting transcription factors binding to those elements, and have shown that the motifs conferring differences in expression in the C4 species have been recruited from pre-existing sequences in C3 species, rather than being generated de novo during the evolution of the C4 condition (Niklaus and Kelly, 2019)
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