Abstract

The majority of plants use C3 photosynthesis, but over 60 independent lineages of angiosperms have evolved the C4 pathway. In most C4 species, photosynthesis gene expression is compartmented between mesophyll and bundle-sheath cells. We performed DNaseI sequencing to identify genome-wide profiles of transcription factor binding in leaves of the C4 grasses Zea mays, Sorghum bicolor, and Setaria italica as well as C3 Brachypodium distachyon In C4 species, while bundle-sheath strands and whole leaves shared similarity in the broad regions of DNA accessible to transcription factors, the short sequences bound varied. Transcription factor binding was prevalent in gene bodies as well as promoters, and many of these sites could represent duons that influence gene regulation in addition to amino acid sequence. Although globally there was little correlation between any individual DNaseI footprint and cell-specific gene expression, within individual species transcription factor binding to the same motifs in multiple genes provided evidence for shared mechanisms governing C4 photosynthesis gene expression. Furthermore, interspecific comparisons identified a small number of highly conserved transcription factor binding sites associated with leaves from species that diverged around 60 million years ago. These data therefore provide insight into the architecture associated with C4 photosynthesis gene expression in particular and characteristics of transcription factor binding in cereal crops in general.

Highlights

  • Most photosynthetic organisms, including crops of global importance such as wheat, rice and potato use the C3 photosynthesis pathway in which Ribulose-BisphosphateCarboxylase Oxygenase (RuBisCO) catalyses the primary fixation of CO2

  • Only 6-20% of the narrower Digital Genomic Footprints (DGF) found in the bundle sheath were identified in whole leaves (Supplemental Table 7). These findings indicate that specific cell types of cereal leaves share similarity in the broad regions of DNA that are accessible to transcription factors (DHS), but that the short sequences bound by transcription factors (DGF) vary dramatically

  • Thaliana (Sullivan et al, 2014) to metazoans (Natarajan et al, 2012; Stergachis et al, 2013, 2014), the majority of DGF detected in the four grasses were centred around annotated transcription start sites

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Summary

Introduction

Most photosynthetic organisms, including crops of global importance such as wheat, rice and potato use the C3 photosynthesis pathway in which Ribulose-BisphosphateCarboxylase Oxygenase (RuBisCO) catalyses the primary fixation of CO2. Carboxylation by RuBisCO is competitively inhibited by oxygen binding the active site (Bowes et al, 1971). This oxygenation reaction generates toxic waste-products that are recycled by an energy-demanding series of metabolic reactions known as photorespiration (Bauwe et al, 2010; Tolbert, 1971). The ratio of oxygenation to carboxylation increases with temperature (Jordan and Ogren, 1984; Sharwood et al, 2016) and so losses from photorespiration are high in the tropics. Multiple plant lineages have evolved mechanisms that suppress oxygenation by concentrating CO2 around RuBisCO. One such strategy is known as C4 photosynthesis

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