C<sub>4</sub> Phosphoenolpyruvate Carboxylase: Evolution and transcriptional regulation

Carvalho, Pedro; Gomes, Célia; Saibo, Nelson J.M.

doi:10.1590/1678-4685-GMB-2023-0190

Pedro Carvalho

conceived the review

wrote the manuscript

read and approved the final version

Universidade Nova de Lisboa, Instituto de Tecnologia Química e Biológica António Xavier, Oeiras, Portugal.

* These authors contributed equally to the article.

Célia Gomes

conceived the review

wrote the manuscript

read and approved the final version

Universidade Nova de Lisboa, Instituto de Tecnologia Química e Biológica António Xavier, Oeiras, Portugal.

* These authors contributed equally to the article.

Nelson J.M. Saibo

conceived the review

reviewed the manuscript

read and approved the final version

Universidade Nova de Lisboa, Instituto de Tecnologia Química e Biológica António Xavier, Oeiras, Portugal.

https://orcid.org/0000-0002-6679-3811

Send correspondence to
Nelson J.M. Saibo. Universidade NOVA de Lisboa, Instituto de Tecnologia Química e Biológica António Xavier, Avenida da República, 2780-157 Oeiras, Portugal. E-mail: saibo@itqb.unl.pt

Associate Editor:

Loreta Brandão de Freitas

*
These authors contributed equally to the article.

Conflict of Interests

The authors declare that there is no conflict of interest that could be perceived as prejudicial to the impartiality of the reported research.

Figures (3)
Tables (2)

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Figure 1 -
Simplified schematic representation of the role played by non-photosynthetic PEPC in the carbon-nitrogen balance. The carboxylation of phosphoenolpyruvate (PEP) is an important step to replenish carbon skeletons to the TCA cycle, re-routing carbon (glycolysis products) into the TCA cycle. The link between the TCA and GOGAT/GS cycles is important for the carbon-nitrogen balance, making PEPC an important regulator of carbon partitioning.

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Figure 2 -
Cladogram representing the amount of PEPC isoform present in plant genomes. Species are organised considering their phylogenetic relationships, with representatives of important evolutionary groups. Sequences were obtained from PLAZA and NCBI databases, using different PEPC protein sequences for BLASTp. Incomplete or unrelated sequences were removed by protein alignment and phylogenetic analysis. Red lines represent C₄ species, blue lines represent CAM species, and black lines represent C₃ species.

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Figure 3 -
Schematic representation of the different mechanisms proposed to regulate the transcription of C₄ ZmPEPC in an organ- and cell-specific way. (A) Regulation of C₄ ZmPEPC gene expression in M cells. The repressors ZmbHLH80 and ZmOrphan94 are less expressed than in BS cells, therefore there is a high gene expression activation by ZmbHLH90. (B) Regulation of C₄ ZmPEPC gene expression in BS cells. ZmbHLH80 and ZmOrphan94 are preferentially expressed in BS cells, working as repressors of ZmbHLH90, leading to a down-regulation of C₄ ZmPEPC expression. ZmbHLH80 and ZmOrphan94 can impair ZmbHLH90 function through heterodimerization or competitive binding for the same binding site. In addition, ZmOrphan94 may also impair ZmbHLH90 through its binding to CACA motifs, close to ZmbHLH90 binding site. In leaves, Dof1 is activated by light, allowing its binding and consequent activation of C₄ ZmPEPC gene expression (A and B). (C) Regulation of C₄ ZmPEPC in stems and roots by Dof1 and Dof2. These TFs are both expressed in these tissues, however, while Dof1 bind to the respective cis-elements in the C₄ ZmPEPC promoter to activate gene expression, Dof2 binds them to block Dof1 DNA-interaction, thus impairing C₄ ZmPEPC expression. The black arrows and the red lines represent activation and repression of gene expression, respectively. The thickness of the green arrow represents the expression levels of C₄ PEPC in each cell type. Activation and repression by the different TFs are represented as blue arrows and red lines, respectively. The different sizes of Dof1, ZmbHLH80 and ZmOrphan94, between A and B denote their gene expression levels in each cell type. The yellow rectangles represent the binding sites of Dof1 and Dof2 (Yanagisawa and Sheen, 1998Yanagisawa S and Sheen J (1998) Involvement of maize Dof zinc finger proteins in tissue-specific and light-regulated gene expression. Plant Cell 10:75-89.) and the green rectangles represent the ZmOrphan94 binding sites. The binding site of ZmbHLH80 and ZmbHLH90 (E-box) is represented by a white rectangle. Within this E-box, there is a CACA motif, which is represented by a green rectangle, similar to the other binding sites of ZmOrphan94. The orange lines underneath the promoter represent the CNSs identified by Gupta et al. (2020Gupta S das, Levey M, Schulze S, Karki S, Emmerling J, Streubel M, Gowik U, Paul Quick W and Westhoff P (2020) The C4Ppc promoters of many C4 grass species share a common regulatory mechanism for gene expression in the mesophyll cell. Plant J 101:204-216.).

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Table 1 -
Histone modifications found in C₄ PEPC gene promoter and regulated processes.

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Table 2 -
Summary of the abiotic stress effects in C₄ PEPC levels.

Figure 3 - Schematic representation of the different mechanisms proposed to regulate the transcription of C₄ ZmPEPC in an organ- and cell-specific way. (A) Regulation of C₄ ZmPEPC gene expression in M cells. The repressors ZmbHLH80 and ZmOrphan94 are less expressed than in BS cells, therefore there is a high gene expression activation by ZmbHLH90. (B) Regulation of C₄ ZmPEPC gene expression in BS cells. ZmbHLH80 and ZmOrphan94 are preferentially expressed in BS cells, working as repressors of ZmbHLH90, leading to a down-regulation of C₄ ZmPEPC expression. ZmbHLH80 and ZmOrphan94 can impair ZmbHLH90 function through heterodimerization or competitive binding for the same binding site. In addition, ZmOrphan94 may also impair ZmbHLH90 through its binding to CACA motifs, close to ZmbHLH90 binding site. In leaves, Dof1 is activated by light, allowing its binding and consequent activation of C₄ ZmPEPC gene expression (A and B). (C) Regulation of C₄ ZmPEPC in stems and roots by Dof1 and Dof2. These TFs are both expressed in these tissues, however, while Dof1 bind to the respective cis-elements in the C₄ ZmPEPC promoter to activate gene expression, Dof2 binds them to block Dof1 DNA-interaction, thus impairing C₄ ZmPEPC expression. The black arrows and the red lines represent activation and repression of gene expression, respectively. The thickness of the green arrow represents the expression levels of C₄ PEPC in each cell type. Activation and repression by the different TFs are represented as blue arrows and red lines, respectively. The different sizes of Dof1, ZmbHLH80 and ZmOrphan94, between A and B denote their gene expression levels in each cell type. The yellow rectangles represent the binding sites of Dof1 and Dof2 (Yanagisawa and Sheen, 1998Yanagisawa S and Sheen J (1998) Involvement of maize Dof zinc finger proteins in tissue-specific and light-regulated gene expression. Plant Cell 10:75-89.) and the green rectangles represent the ZmOrphan94 binding sites. The binding site of ZmbHLH80 and ZmbHLH90 (E-box) is represented by a white rectangle. Within this E-box, there is a CACA motif, which is represented by a green rectangle, similar to the other binding sites of ZmOrphan94. The orange lines underneath the promoter represent the CNSs identified by Gupta et al. (2020Gupta S das, Levey M, Schulze S, Karki S, Emmerling J, Streubel M, Gowik U, Paul Quick W and Westhoff P (2020) The C4Ppc promoters of many C4 grass species share a common regulatory mechanism for gene expression in the mesophyll cell. Plant J 101:204-216.).

Associated process	Modification	PEPC promoter region	Specie	Reference
Cell-specificity	H3K4me3 H3K4me2	Proximal	Zea mays	Danker et al., 2008Danker T, Dreesen B, Offermann S, Horst I and Peterhänsel C (2008) Developmental information but not promoter activity controls the methylation state of histone H3 lysine 4 on two photosynthetic genes in maize. Plant J 53:465-474.
Circadian regulation	H3K9ac	Distal	Zea mays	Horst et al., 2009Horst I, Offermann S, Dreesen B, Niessen M and Peterhansel C (2009) Core promoter acetylation is not required for high transcription from the phosphoenolpyruvate carboxylase promoter in maize. Epigenetics Chromatin 2:17.
Light regulation	H3K9ac	Proximal	Zea mays Setaria italica	Offermann et al., 2008Offermann S, Dreesen B, Horst I, Danker T, Jaskiewicz M and Peterhansel C (2008) Developmental and environmental signals induce distinct histone acetylation profiles on distal and proximal promoter elements of the C4-Pepc gene in maize. Genetics 179:1891-1901.; Horst et al., 2009Horst I, Offermann S, Dreesen B, Niessen M and Peterhansel C (2009) Core promoter acetylation is not required for high transcription from the phosphoenolpyruvate carboxylase promoter in maize. Epigenetics Chromatin 2:17.; Heimann et al., 2013Heimann L, Horst I, Perduns R, Dreesen B, Offermann S and Peterhansel C (2013) A common histone modification code on C4 genes in maize and its conservation in sorghum and Setaria italica. Plant Physiol 162:456-69.
	H3K9ac	Distal	Zea mays Sorghum bicolor
	H4K5ac	Proximal	Zea mays Setaria italica	Offermann et al., 2008Offermann S, Dreesen B, Horst I, Danker T, Jaskiewicz M and Peterhansel C (2008) Developmental and environmental signals induce distinct histone acetylation profiles on distal and proximal promoter elements of the C4-Pepc gene in maize. Genetics 179:1891-1901.; Horst et al., 2009Horst I, Offermann S, Dreesen B, Niessen M and Peterhansel C (2009) Core promoter acetylation is not required for high transcription from the phosphoenolpyruvate carboxylase promoter in maize. Epigenetics Chromatin 2:17.; Heimann et al., 2013Heimann L, Horst I, Perduns R, Dreesen B, Offermann S and Peterhansel C (2013) A common histone modification code on C4 genes in maize and its conservation in sorghum and Setaria italica. Plant Physiol 162:456-69.
	H4K5ac	Distal	Zea mays Sorghum bicolor
	H4K16Ac	Proximal and Distal	Zea mays	Horst et al., 2009Horst I, Offermann S, Dreesen B, Niessen M and Peterhansel C (2009) Core promoter acetylation is not required for high transcription from the phosphoenolpyruvate carboxylase promoter in maize. Epigenetics Chromatin 2:17.
	H3K23Ac	Proximal and Distal	Zea mays	Horst et al., 2009Horst I, Offermann S, Dreesen B, Niessen M and Peterhansel C (2009) Core promoter acetylation is not required for high transcription from the phosphoenolpyruvate carboxylase promoter in maize. Epigenetics Chromatin 2:17.

Stress condition	Species	Regulatory effect	Reference
Osmotic stress	Zea mays	Decrease transcipt	Pelleschi et al., 1997Pelleschi S, Rocher JP and Prioul JL (1997) Effect of water restriction on carbohydrate metabolism and photosynthesis in mature maize leaves. Plant Cell Environ 20:493-503.; Foyer et al., 1998Foyer CH, Kingston-Smith A, Pastori G and Harbinson J (1998) Photosynthesis and antioxidant metabolism in maize leaves subjected to low temperatures. In: Garab G (ed) Photosynthesis: Mechanisms and effects. , Springer, Dordrecht, pp 2425-2431.
	Zea mays	Increase activity	Ghannoum, 2009Ghannoum O (2009) C4 photosynthesis and water stress. Ann Bot 103:635-644.
	Sorghum bicolor	Decrease transcript	Buchanan et al., 2005Buchanan CD, Lim S, Salzman RA, Kagiampakis I, Morishige DT, Weers BD, Klein RR, Pratt LH, Cordonnier-Pratt MM, Klein PE et al. (2005) Sorghum bicolor’s transcriptome response to dehydration, high salinity and ABA. Plant Mol Biol 58:699-720.
Salt stress	Zea mays	Increase activity	Hatzig et al., 2010Hatzig S, Kumar A, Neubert A and Schubert S (2010) PEP-carboxylase activity: A comparison of its role in a C4 and a C3 species under salt stress. J Agron Crop Sci 196:185-192.)
Salt stress	Sorghum bicolor	Increase transcript	Buchanan et al., 2005Buchanan CD, Lim S, Salzman RA, Kagiampakis I, Morishige DT, Weers BD, Klein RR, Pratt LH, Cordonnier-Pratt MM, Klein PE et al. (2005) Sorghum bicolor’s transcriptome response to dehydration, high salinity and ABA. Plant Mol Biol 58:699-720.
Cold	Zea mays	Decrease activity	Selinioti et al., 1985Selinioti E, Karabourniotis G, Manetas Y and Gavalas NA (1985) Modulation of phosphoenolpyruvate carboxylase by 3-phosphoglycerate: Probable physiological significance for C4-photosynthesis. J Plant Physiol 121:353-360.; Angelopoulos and Gavalas, 1988Angelopoulos K and Gavalas NA (1988) Reversible cold inactivation of C4-phosphoenolpyruvate carboxylase: Factors affecting reactivation and stability. J Plant Physiol 132:714-719.; Chinthapalli et al., 2003Chinthapalli B, Murmu J and Raghavendra AS (2003) Dramatic difference in the responses of phosphoenolpyruvate carboxylase to temperature in leaves of C3 and C4 plants. J Exp Bot 54:707-714.
Heat	Zea mays	Increase activity	Crafts-Brandner and Salvucci, 2002Crafts-Brandner SJ and Salvucci ME (2002) Sensitivity of photosynthesis in a C4 plant, maize, to heat stress. Plant Physiol 129:1773-1780.; Chinthapalli et al., 2003Chinthapalli B, Murmu J and Raghavendra AS (2003) Dramatic difference in the responses of phosphoenolpyruvate carboxylase to temperature in leaves of C3 and C4 plants. J Exp Bot 54:707-714.
Nitrogen deficiency	Zea mays	Decrease transcript/protein	Sugiharto and Sugiyama, 1992Sugiharto B, Suzuki I, Burnell JN and Sugiyama T (1992) Glutamine induces the N-dependent accumulation of mRNAs encoding phosphoenolpyruvate carboxylase and carbonic anhydrase in detached maize leaf tissue. Plant Physiol 100:2066-2070.; Sugiharto et al., 1992Sugiharto B, Suzuki I, Burnell JN and Sugiyama T (1992) Glutamine induces the N-dependent accumulation of mRNAs encoding phosphoenolpyruvate carboxylase and carbonic anhydrase in detached maize leaf tissue. Plant Physiol 100:2066-2070.; *Sugiharto et al., 1990*Sugiharto B, Miyata K, Nakamoto H, Sasakawa H and Sugiyama T (1990) Regulation of expression of carbon-assimilating enzymes by nitrogen in maize leaf. Plant Physiol 92:963-969.
Cadmium excess	Zea mays	Decrease activity	Wang et al., 2009Wang H, Zhao SC, Liu RL, Zhou W and Jin JY (2009) Changes of photosynthetic activities of maize (Zea mays L.) seedlings in response to cadmium stress. Photosynthetica 47:277-283.
Ozone excess	Zea mays	Decrease transcript/protein	Leitao et al., 2007b Leitao L, Maoret JJ and Biolley JP (2007b) Changes in PEP carboxylase, Rubisco and Rubisco activase mRNA levels from maize (Zea mays) exposed to a chronic ozone stress. Biol Res 40:137-153.; *Leitao et al., 2007a*Leitao L, Bethenod O and Biolley JP (2007a) The impact of ozone on juvenile maize (Zea mays L.) plant photosynthesis: Effects on vegetative biomass, pigmentation, and carboxylases (PEPc and Rubisco). Plant Biol (Stuttg) 9:478-488.

[1] Send correspondence to
Nelson J.M. Saibo. Universidade NOVA de Lisboa, Instituto de Tecnologia Química e Biológica António Xavier, Avenida da República, 2780-157 Oeiras, Portugal. E-mail: saibo@itqb.unl.pt

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C₄ Phosphoenolpyruvate Carboxylase: Evolution and transcriptional regulation