Multiple highly expressed phospho enol pyruvate carboxylase genes have divergent enzyme kinetic properties in two C4 grasses

DiMario, Robert J.; Kophs, Ashley N.; Apalla, Anthony J. A.; Schnable, James N.; Cousins, Asaph B.

doi:10.1093/aob/mcad116

Title: Multiple highly expressed phospho enol pyruvate carboxylase genes have divergent enzyme kinetic properties in two C4 grasses

Journal Article · Thu Sep 07 00:00:00 EDT 2023 · Annals of Botany

DOI:https://doi.org/10.1093/aob/mcad116· OSTI ID:2217637

; Kophs, Ashley N.; Apalla, Anthony J. A.; Schnable, James N.;

Abstract Background and Aims Phosphoenolpyruvate (PEP) carboxylase (PEPC) catalyses the irreversible carboxylation of PEP with bicarbonate to produce oxaloacetate. This reaction powers the carbon-concentrating mechanism (CCM) in plants that perform C4 photosynthesis. This CCM is generally driven by a single PEPC gene product that is highly expressed in the cytosol of mesophyll cells. We found two C4 grasses, Panicum miliaceum and Echinochloa colona, that each have two highly expressed PEPC genes. We characterized the kinetic properties of the two most abundant PEPCs in E. colona and P. miliaceum to better understand how the enzyme’s amino acid structure influences its function. Methods Coding sequences of the two most abundant PEPC proteins in E. colona and P. miliaceum were synthesized by GenScript and were inserted into bacteria expression plasmids. Point mutations resulting in substitutions at conserved amino acid residues (e.g. N-terminal serine and residue 890) were created via site-directed PCR mutagenesis. The kinetic properties of semi-purified plant PEPCs from Escherichia coli were analysed using membrane-inlet mass spectrometry and a spectrophotometric enzyme-coupled reaction. Key Results The two most abundant P. miliaceum PEPCs (PmPPC1 and PmPPC2) have similar sequence identities (>95 %), and as a result had similar kinetic properties. The two most abundant E. colona PEPCs (EcPPC1 and EcPPC2) had identities of ~78 % and had significantly different kinetic properties. The PmPPCs and EcPPCs had different responses to allosteric inhibitors and activators, and substitutions at the conserved N-terminal serine and residue 890 resulted in significantly altered responses to allosteric regulators. Conclusions The two, significantly expressed C4Ppc genes in P. miliaceum were probably the result of genomes combining from two closely related C4Panicum species. We found natural variation in PEPC’s sensitivity to allosteric inhibition that seems to bypass the conserved 890 residue, suggesting alternative evolutionary pathways for increased malate tolerance and other kinetic properties.

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Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: SC0001685

OSTI ID:: 2217637

Alternate ID(s):: OSTI ID: 2000638

Journal Information:: Annals of Botany, Journal Name: Annals of Botany Vol. 132 Journal Issue: 3; ISSN 0305-7364

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United Kingdom

Language:: English

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