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While considerable knowledge exists about the enzymes pivotal for C₄photosynthesis, much less is known about thecis-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 C₄enzymes for five different grass species. This study spans four C₄species, covering three distinct photosynthetic subtypes:Zea maysandSorghum bicolor(NADP-dependent malic enzyme),Panicum miliaceum(NAD-dependent malic enzyme),Urochloa fusca(phosphoenolpyruvate carboxykinase), along with the C₃outgroupOryza sativa. We studied thecis-regulatory landscape of enzymes essential across all C₄species and those unique to C₄subtypes, measuring cell-type-specific biases for C₄enzymes using chromatin accessibility data. Integrating these data with phylogenetics revealed diverse co-option of gene family members between species, showcasing the various paths of C₄evolution. Besides promoter proximal ACRs, we found that, on average, C₄genes have two to three distal cell-type-specific ACRs, highlighting the complexity and divergent nature of C₄evolution. 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 ofcis-regulation at these C₄loci. This study illuminates the dynamic and complex nature ofcis-regulatory elements evolution in C₄photosynthesis, particularly highlighting the intricatecis-regulatory evolution of key loci. Our findings offer a valuable resource for future investigations, potentially aiding in the optimization of C₃crop performance under changing climatic conditions. 

Abstract Research in Arabidopsis thaliana has a powerful influence on our understanding of gene functions and pathways. However, not everything translates from Arabidopsis to crops and other plants. Here, a group of experts consider instances where translation has been lost and why such translation is not possible or is challenging. First, despite great efforts, floral dip transformation has not succeeded in other species outside Brassicaceae. Second, due to gene duplications and losses throughout evolution, it can be complex to establish which genes are orthologs of Arabidopsis genes. Third, during evolution Arabidopsis has lost arbuscular mycorrhizal symbiosis. Fourth, other plants have evolved specialized cell types that are not present in Arabidopsis. Fifth, similarly, C4 photosynthesis cannot be studied in Arabidopsis, which is a C3 plant. Sixth, many other plant species have larger genomes, which has given rise to innovations in transcriptional regulation that are not present in Arabidopsis. Seventh, phenotypes such as acclimation to water stress can be challenging to translate due to different measurement strategies. And eighth, while the circadian oscillator is conserved, there are important nuances in the roles of circadian regulators in crop plants. A key theme emerging across these vignettes is that even when translation is lost, insights can still be gained through comparison with Arabidopsis. 

Abstract Cis-regulatory elements (CREs) are essential for regulating gene expression, yet their evolutionary dynamics in plants remain elusive. Here we constructed a single-cell chromatin accessibility atlas forOryza sativafrom 103,911 nuclei representing 126 cell states across nine organs. Comparative genomics betweenO. sativaand 57,552 nuclei from four additional grass species (Zea mays,Sorghum bicolor,Panicum miliaceumandUrochloa fusca) revealed that chromatin accessibility conservation varies with cell-type specificity. Epidermal accessible chromatin regions in the leaf were less conserved compared to other cell types, indicating accelerated regulatory evolution in the L1-derived epidermal layer ofO. sativarelative to other species. Conserved accessible chromatin regions overlapping the repressive histone modification H3K27me3 were identified as potentially silencer-like CREs, as deleting these regions led to up-regulation of gene expression. This study provides a comprehensive epigenomic resource for the rice community, demonstrating the utility of a comparative genomics approach that highlights the dynamics of plant cell-type-specific CRE evolution.