AUTHOR=Yamamoto Naoki , Tong Wurina , Lv Bingbing , Peng Zhengsong , Yang Zaijun 

TITLE=The Original Form of C4-Photosynthetic Phosphoenolpyruvate Carboxylase Is Retained in Pooids but Lost in Rice

JOURNAL=Frontiers in Plant Science

VOLUME=13

YEAR=2022

URL=https://www.frontiersin.org/journals/plant-science/articles/10.3389/fpls.2022.905894

DOI=10.3389/fpls.2022.905894

ISSN=1664-462X

ABSTRACT=<p>Poaceae is the most prominent monocot family that contains the primary cereal crops wheat, rice, and maize. These cereal species exhibit physiological diversity, such as different photosynthetic systems and environmental stress tolerance. Phospho<italic>enol</italic>pyruvate carboxylase (PEPC) in Poaceae is encoded by a small multigene family and plays a central role in C<sub>4</sub>-photosynthesis and dicarboxylic acid metabolism. Here, to better understand the molecular basis of the cereal species diversity, we analyzed the <italic>PEPC</italic> gene family in wheat together with other grass species. We could designate seven plant-type and one bacterial-type grass <italic>PEPC groups</italic>, ppc1a, ppc1b, ppc2a, ppc2b, ppc3, ppc4, ppcC<sub>4</sub>, and ppc-b, respectively, among which ppc1b is an uncharacterized type of <italic>PEPC</italic>. Evolutionary inference revealed that these <italic>PEPCs</italic> were derived from five types of ancient <italic>PEPCs</italic> (<italic>ppc1</italic>, <italic>ppc2</italic>, <italic>ppc3</italic>, <italic>ppc4</italic>, and <italic>ppc-b</italic>) in three chromosomal blocks of the ancestral Poaceae genome. C<sub>4</sub>-photosynthetic <italic>PEPC</italic> (<italic>ppcC<sub>4</sub></italic>) had evolved from <italic>ppc1b</italic>, which seemed to be arisen by a chromosomal duplication event. We observed that <italic>ppc1b</italic> was lost in many <italic>Oryza</italic> species but preserved in Pooideae after natural selection. <italic>In silico</italic> analysis of cereal RNA-Seq data highlighted the preferential expression of <italic>ppc1b</italic> in upper ground organs, selective up-regulation of <italic>ppc1b</italic> under osmotic stress conditions, and nitrogen response of <italic>ppc1b</italic>. Characterization of wheat <italic>ppc1b</italic> showed high levels of gene expression in young leaves, transcriptional responses under nitrogen and abiotic stress, and the presence of a Dof1 binding site, similar to <italic>ppcC<sub>4</sub></italic> in maize. Our results indicate the evolving status of Poaceae PEPCs and suggest the functional association of <italic>ppc1</italic>-derivatives with adaptation to environmental changes.</p>