Abstract
As compared to C3, C4 plants have higher photosynthetic rates and better tolerance to high temperature and drought. These traits are highly beneficial in the current scenario of global warming. Interestingly, all the genes of the C4 photosynthetic pathway are present in C3 plants, although they are involved in diverse non-photosynthetic functions. Non-photosynthetic isoforms of carbonic anhydrase (CA), phosphoenolpyruvate carboxylase (PEPC), malate dehydrogenase (MDH), the decarboxylating enzymes NAD/NADP-malic enzyme (NAD/NADP-ME), and phosphoenolpyruvate carboxykinase (PEPCK), and finally pyruvate orthophosphate dikinase (PPDK) catalyze reactions that are essential for major plant metabolism pathways, such as the tricarboxylic acid (TCA) cycle, maintenance of cellular pH, uptake of nutrients and their assimilation. Consistent with this view differential expression pattern of these non-photosynthetic C3 isoforms has been observed in different tissues across the plant developmental stages, such as germination, grain filling, and leaf senescence. Also abundance of these C3 isoforms is increased considerably in response to environmental fluctuations particularly during abiotic stress. Here we review the vital roles played by C3 isoforms of C4 enzymes and the probable mechanisms by which they help plants in acclimation to adverse growth conditions. Further, their potential applications to increase the agronomic trait value of C3 crops is discussed.
Similar content being viewed by others
References
Aivalakis G, Dimou M, Flemetakis E et al (2004) Immunolocalization of carbonic anhydrase and phosphoenolpyruvate carboxylase in developing seeds of Medicago sativa. Plant Physiol Biochem 42:181–186. https://doi.org/10.1016/j.plaphy.2004.01.006
Akhani H, Barroca J, Koteeva N et al (2005) Bienertia sinuspersici (Chenopodiaceae): a new species from southwest asia and discovery of a third terrestrial C4 plant without Kranz anatomy. Syst Bot 30:290–301. https://doi.org/10.1600/0363644054223684
Akhani H, Chatrenoor T, Dehghani M et al (2012) A new species of Bienertia (Chenopodiaceae) from Iranian salt deserts: a third species of the genus and discovery of a fourth terrestrial C 4 plant without Kranz anatomy. Plant Biosyst 146:550–559. https://doi.org/10.1080/11263504.2012.662921
Alessio GA, Pietrini F, Brilli F, Loreto F (2005) Characteristics of CO2 exchange between peach stems and the atmosphere. Funct Plant Biol 32:787–795. https://doi.org/10.1071/fp05070
Allakhverdiev SI (2020) Optimising photosynthesis for environmental fitness. Funct Plant Biol. https://doi.org/10.1071/FPv47n11_FO
Alvarez CE, Saigo M, Margarit E et al (2013) Kinetics and functional diversity among the five members of the NADP-malic enzyme family from Zea mays, a C4 species. Photosynth Res 115:65–80. https://doi.org/10.1007/s11120-013-9839-9
Alvarez CE, Bovdilova A, Höppner A et al (2019) Molecular adaptations of NADP-malic enzyme for its function in C4 photosynthesis in grasses. Nat Plants 5:755–765. https://doi.org/10.1038/s41477-019-0451-7
Aoyagi K, Bassham JA (1984) Pyruvate orthophosphate dikinase of C 3 seeds and leaves as compared to the enzyme from maize. Plant Physiol 75:387–392. https://doi.org/10.1104/pp.75.2.387
Aoyagi K, Chua N-H (1988) Cell-specific expression of pyruvate, Pi dikinase. Plant Physiol 86:364–368. https://doi.org/10.1104/pp.86.2.364
Araújo WL, Martins AO, Fernie AR, Tohge T (2014) 2-oxoglutarate: linking TCA cycle function with amino acid, glucosinolate, flavonoid, alkaloid, and gibberellin biosynthesis. Front Plant Sci. https://doi.org/10.3389/fpls.2014.00552
Araus JL, Sanchez-Bragado R, Vicente R (2021) Improving crop yield and resilience through optimization of photosynthesis: panacea or pipe dream? J Exp Bot 72:3936–3955. https://doi.org/10.1093/jxb/erab097
Arias CL, Pavlovic T, Torcolese G et al (2018) NADP-dependent malic enzyme 1 participates in the abscisic acid response in Arabidopsis thaliana. Front Plant Sci. https://doi.org/10.3389/fpls.2018.01637
Atkinson RRL, Mockford EJ, Bennett C et al (2016) C4 photosynthesis boosts growth by altering physiology, allocation and size. Nat Plants 2:16038. https://doi.org/10.1038/NPLANTS.2016.38
Aubry S, Brown NJ, Hibberd JM (2011) The role of proteins in C3 plants prior to their recruitment into the C4 pathway. J Exp Bot 62:3049–3059. https://doi.org/10.1093/jxb/err012
Aubry S, Kelly S, Kümpers BMC et al (2014) Deep evolutionary comparison of gene expression identifies parallel recruitment of trans-factors in two independent origins of c4 photosynthesis. PLoS Genet 10(6):e1004365. https://doi.org/10.1371/journal.pgen.1004365
Babayev H, Mehvaliyeva U, Aliyeva M et al (2014) The study of NAD-malic enzyme in Amaranthus cruentus L. under drought. Plant Physiol Biochem 81:84–89. https://doi.org/10.1016/j.plaphy.2013.12.022
Badia MB, Arias CL, Tronconi MA et al (2015) Enhanced cytosolic NADP-ME2 activity in A. thaliana affects plant development, stress tolerance and specific diurnal and nocturnal cellular processes. Plant Sci 240:193–203. https://doi.org/10.1016/j.plantsci.2015.09.015
Badia Mariana B, Mans R, Lis Alicia V et al (2017) Specific Arabidopsis thaliana malic enzyme isoforms can provide anaplerotic pyruvate carboxylation function in Saccharomyces cerevisiae. FEBS J 284:654–665. https://doi.org/10.1111/febs.14013
Badia MB, Maurino VG, Pavlovic T et al (2020) Loss of function of Arabidopsis NADP-malic enzyme 1 results in enhanced tolerance to aluminum stress. Plant J 101:653–665. https://doi.org/10.1111/tpj.14571
Bailey KJ, Gray JE, Walker RP, Leegood RC (2007) Coordinate regulation of phosphoenolpyruvate carboxylase and phosphoenolpyruvate carboxykinase by light and CO2 during C 4 photosynthesis. Plant Physiol 144:479–486. https://doi.org/10.1104/pp.106.093013
Bailey KJ, Leegood RC (2016) Nitrogen recycling from the xylem in rice leaves: dependence upon metabolism and associated changes in xylem hydraulics. J Exp Bot 67:2901–2911. https://doi.org/10.1093/jxb/erw132
Baldicchi A, Farinelli D, Micheli M et al (2015) Analysis of seed growth, fruit growth and composition and phospoenolpyruvate carboxykinase (PEPCK) occurrence in apricot (Prunus armeniaca L.). Sci Hortic (Amsterdam) 186:38–46. https://doi.org/10.1016/j.scienta.2015.01.025
Bandyopadhyay A, Datta K, Zhang J et al (2007) Enhanced photosynthesis rate in genetically engineered indica rice expressing pepc gene cloned from maize. Plant Sci 172:1204–1209. https://doi.org/10.1016/j.plantsci.2007.02.016
Batista-Silva W, da Fonseca-Pereira P, Martins AO et al (2020) Engineering improved photosynthesis in the era of synthetic biology. Plant Commun 1:100032. https://doi.org/10.1016/j.xplc.2020.100032
Beeler S, Liu H-C, Stadler M et al (2014) Plastidial NAD-dependent malate dehydrogenase is critical for embryo development and heterotrophic metabolism in Arabidopsis. Plant Physiol 164:1175–1190. https://doi.org/10.1104/pp.113.233866
Benedict CR, Beevers H (1961) Formation of sucrose from malate in germinating castor beans. I. Conversion of malate to phosphoenol-pyruvate. Plant Physiol 36:540–544. https://doi.org/10.1104/pp.36.5.540
Berkemeyer M, Scheibe R, Ocheretina O (1998) A novel, non-redox-regulated NAD-dependent malate dehydrogenase from chloroplasts of Arabidopsis thaliana L. J Biol Chem 273:27927–27933. https://doi.org/10.1074/jbc.273.43.27927
Berveiller D, Damesin C (2008) Carbon assimilation by tree stems: potential involvement of phosphoenolpyruvate carboxylase. Trees Struct Funct 22:149–157. https://doi.org/10.1007/s00468-007-0193-4
Berveiller D, Vidal J, Degrouard J et al (2007) Tree stem phosphoenolpyruvate carboxylase (PEPC): lack of biochemical and localization evidence for a C4-like photosynthesis system. New Phytol 176:775–781. https://doi.org/10.1111/j.1469-8137.2007.02283.x
Bläsing OE, Westhoff P, Svensson P (2000) Evolution of C4 phosphoenolpyruvate carboxylase inflaveria, a conserved serine residue in the carboxyl-terminal part of the enzyme is a major determinant for C4-specific characteristics. J Biol Chem 275:27917–27923. https://doi.org/10.1074/jbc.M909832199
Bloemen J, Mcguire MA, Aubrey DP et al (2013) Transport of root-respired CO2 via the transpiration stream affects aboveground carbon assimilation and CO2 efflux in trees. New Phytol 197:555–565. https://doi.org/10.1111/j.1469-8137.2012.04366.x
Bouargalne Y, Ben MR, El Omari R, Nhiri M (2018) Phosphoenolpyruvate carboxylase during maturation and germination sorghum seeds: enzyme activity and regulation. Russ J Plant Physiol 65:824–832. https://doi.org/10.1134/S1021443718060031
Braun HP, Zabaleta E (2007) Carbonic anhydrase subunits of the mitochondrial NADH dehydrogenase complex (complex I) in plants. Physiol Plant 57:289–296. https://doi.org/10.1111/ppl.12424
Bräutigam A, Gowik U (2016) Photorespiration connects C3 and C4 photosynthesis. J Exp Bot 67:2953–2962. https://doi.org/10.1093/jxb/erw056
Bräutigam A, Kajala K, Wullenweber J et al (2011) An mRNA blueprint for C4 photosynthesis derived from comparative transcriptomics of closely related C3 and C4 species. Plant Physiol 155:142–156. https://doi.org/10.1104/pp.110.159442
Brown Naomi J, Palmer Ben G, Stanley S et al (2009) C4 acid decarboxylases required for C4 photosynthesis are active in the mid-vein of the C3 species Arabidopsis thaliana, and are important in sugar and amino acid metabolism. Plant J 61:122–133. https://doi.org/10.1111/j.1365-313X.2009.04040.x
Burgess AJ, Retkute R, Herman T, Murchie EH (2017) Exploring relationships between canopy architecture, light distribution, and photosynthesis in contrasting rice genotypes using 3D canopy reconstruction. Front Plant Sci. https://doi.org/10.3389/fpls.2017.00734
Busch FA, Sage TL, Cousins AB, Sage RF (2013) C3 plants enhance rates of photosynthesis by reassimilating photorespired and respired CO2. Plant Cell Environ 36:200–212. https://doi.org/10.1111/j.1365-3040.2012.02567.x
Cao J, Cheng G, Wang L et al (2021) Genome-wide identification and analysis of the phosphoenolpyruvate carboxylase gene family in Suaeda aralocaspica, an annual halophyte with single-cellular C4 anatomy. Front Plant Sci. https://doi.org/10.3389/fpls.2021.665279
Carmo-Silva AE, Bernardes Da Silva A, Keys AJ et al (2008) The activities of PEP carboxylase and the C4 acid decarboxylases are little changed by drought stress in three C4 grasses of different subtypes. Photosynth Res 97:223–233. https://doi.org/10.1007/s11120-008-9329-7
Carmo-Silva E, Andralojc PJ, Scales JC et al (2017) Phenotyping of field-grown wheat in the UK highlights contribution of light response of photosynthesis and flag leaf longevity to grain yield. J Exp Bot 68:3473–3486. https://doi.org/10.1093/jxb/erx169
Casati P, Spampinato CP, Andreo CS (1997) Characteristics and physiological function of NADP-malic enzyme from wheat. Plant Cell Physiol 38:928–934. https://doi.org/10.1093/oxfordjournals.pcp.a029253
Chastain CJ, Heck JW, Colquhoun TA et al (2006) Posttranslational regulation of pyruvate, orthophosphate dikinase in developing rice (Oryza sativa) seeds. Planta 224:924–934. https://doi.org/10.1007/s00425-006-0259-3
Chastain CJ, Failing CJ, Manandhar L et al (2011) Functional evolution of C4 pyruvate, orthophosphate dikinase. J Exp Bot 62:3083–3091. https://doi.org/10.1093/jxb/err058
Chatterjee J, Coe RA, Acebron K et al (2021) A low CO2-responsive mutant of Setaria viridis reveals that reduced carbonic anhydrase limits C4photosynthesis. J Exp Bot 72:3122–3136. https://doi.org/10.1093/jxb/erab039
Chen Z-H, Walker RP, Acheson RM et al (2000) Are isocitrate lyase and phosphoenolpyruvate carboxykinase involved in gluconeogenesis during senescence of barley leaves and cucumber cotyledons? Plant Cell Physiol 41:960–967. https://doi.org/10.1093/pcp/pcd021
Chen Z-H, Walker RP, Técsi LI et al (2004) Phosphoenolpyruvate carboxykinase in cucumber plants is increased both by ammonium and by acidification, and is present in the phloem. Planta 219:48–58. https://doi.org/10.1007/s00425-004-1220-y
Chen Z, Sun L, Liu P et al (2015) Malate synthesis and secretion mediated by a manganese-enhanced malate dehydrogenase confers superior manganese tolerance in Stylosanthes guianensis. Plant Physiol 167:176–188. https://doi.org/10.1104/pp.114.251017
Chen T, Wu H, Wu J et al (2017) Absence of OsβCA1 causes a CO2 deficit and affects leaf photosynthesis and the stomatal response to CO2 in rice. Plant J 90:344–357. https://doi.org/10.1111/tpj.13497
Chen Q, Wang B, Ding H et al (2019) Review: the role of NADP-malic enzyme in plants under stress. Plant Sci 281:206–212. https://doi.org/10.1016/j.plantsci.2019.01.010
Chen Y, Fu Z, Zhang H et al (2020) Cytosolic malate dehydrogenase 4 modulates cellular energetics and storage reserve accumulation in maize endosperm. Plant Biotechnol J 18:2420–2435. https://doi.org/10.1111/pbi.13416
Chen L, Ganguly DR, Shafik SH et al (2022) Elucidating the role of SWEET13 in phloem loading of the C4 grass Setaria viridis. Plant J 109:615–632. https://doi.org/10.1111/tpj.15581
Cheng Y, Long M (2007) A cytosolic NADP-malic enzyme gene from rice (Oryza sativa L.) confers salt tolerance in transgenic Arabidopsis. Biotechnol Lett 29:1129–1134. https://doi.org/10.1007/s10529-007-9347-0
Chi W, Yang J, Wu N, Zhang F (2004) Four rice genes encoding NADP malic enzyme exhibit distinct expression profiles. Biosci Biotechnol Biochem 68:1865–1874. https://doi.org/10.1271/bbb.68.1865
Christin PA, Petitpierre B, Salamin N et al (2009) Evolution of C4 phosphoenolpyruvate carboxykinase in grasses, from genotype to phenotype. Mol Biol Evol 26:357–365. https://doi.org/10.1093/molbev/msn255
Clayton H, Saladié M, Rolland V et al (2017) Loss of the chloroplast transit peptide from an ancestral C3 carbonic anhydrase is associated with C4 evolution in the grass genus Neurachne. Plant Physiol 173:1648–1658. https://doi.org/10.1104/pp.16.01893
Córdoba JP, Marchetti F, Soto D et al (2016) The CA domain of the respiratory complex i is required for normal embryogenesis in Arabidopsis thaliana. J Exp Bot 67:1589–1603. https://doi.org/10.1093/jxb/erv556
Córdoba JP, Fassolari M, Marchetti F et al (2019) Different types domains are present in complex I from immature seeds and of CA adult plants in Arabidopsis thaliana. Plant Cell Physiol 60:986–998. https://doi.org/10.1093/pcp/pcz011
Correia PMP, da Silva AB, Vaz M et al (2021) Efficient regulation of CO2 assimilation enables greater resilience to high temperature and drought in maize. Front Plant Sci. https://doi.org/10.3389/fpls.2021.675546
Cousins AB, Pracharoenwattana I, Zhou W et al (2008) Peroxisomal malate dehydrogenase is not essential for photorespiration in Arabidopsis but its absence causes an increase in the stoichiometry of photorespiratory CO2 release. Plant Physiol 148:786–795. https://doi.org/10.1104/pp.108.122622
Cui H (2021) Challenges and approaches to crop improvement through C3-to-C4 engineering. Front Plant Sci 12:715391. https://doi.org/10.3389/fpls.2021.715391
Dąbrowska-Bronk J, Komar DN, Rusaczonek A et al (2016) β-carbonic anhydrases and carbonic ions uptake positively influence Arabidopsis photosynthesis, oxidative stress tolerance and growth in light dependent manner. J Plant Physiol 203:44–54. https://doi.org/10.1016/j.jplph.2016.05.013
Danila FR, Thakur V, Chatterjee J et al (2021) Bundle sheath suberisation is required for C4 photosynthesis in a Setaria viridis mutant. Commun Biol 4:254. https://doi.org/10.1038/s42003-021-01772-4
Delgado-Alvarado A, Walker Robert P, Leegood Richard C (2007) Phosphoenolpyruvate carboxykinase in developing pea seeds is associated with tissues involved in solute transport and is nitrogen-responsive. Plant Cell Environ 30:225–235. https://doi.org/10.1111/j.1365-3040.2006.01622.x
Detarsio E, Maurino VG, Alvarez CE et al (2008) Maize cytosolic NADP-malic enzyme (ZmCytNADP-ME): a phylogenetically distant isoform specifically expressed in embryo and emerging roots. Plant Mol Biol 68:355. https://doi.org/10.1007/s11103-008-9375-8
Dimario RJ, Cousins AB (2019) A single serine to alanine substitution decreases bicarbonate affinity of phospho enol pyruvate carboxylase in C4 Flaveria trinervia. J Exp Bot 70:995–1004. https://doi.org/10.1093/jxb/ery403
DiMario RJ, Quebedeaux JC, Longstreth D et al (2016) The cytoplasmic carbonic anhydrases βCA2 and βCA4 are required for optimal plant growth at low CO2. Plant Physiol 171:280–293. https://doi.org/10.1104/pp.15.01990
DiMario RJ, Clayton H, Mukherjee A et al (2017) Plant carbonic anhydrases: structures, locations, evolution, and physiological roles. Mol Plant 10:30–46. https://doi.org/10.1016/j.molp.2016.09.001
DiMario RJ, Kophs AN, Pathare VS et al (2020) Kinetic variation in grass phospho enol pyruvate carboxylases provides opportunity to enhance C4 photosynthetic efficiency. Plant J 105:1677–1688. https://doi.org/10.1111/tpj.15141
DiMario RJ, Giuliani R, Ubierna N et al (2022) Lack of leaf carbonic anhydrase activity eliminates the C4 carbon-concentrating mechanism requiring direct diffusion of CO2 into bundle sheath cells. Plant Cell Environ 45:1382–1397. https://doi.org/10.1111/pce.14291
Dimou M, Paunescu A, Aivalakis G et al (2009) Co-localization of carbonic anhydrase and phosphoenolpyruvate carboxylase and localization of pyruvate kinase in roots and hypocotyls of etiolated Glycine max seedlings. Int J Mol Sci 10:2896–2910. https://doi.org/10.3390/ijms10072896
Ding ZS, Sun XF, Huang SH et al (2015) Response of photosynthesis to short-term drought stress in rice seedlings overexpressing C4 phosphoenolpyruvate carboxylase from maize and millet. Photosynthetica 53:481–488. https://doi.org/10.1007/s11099-015-0126-1
Dong OX, Ronald PC (2021) Targeted DNA insertion in plants. Proc Natl Acad Sci 118(22):e2004834117. https://doi.org/10.1073/pnas.2004834117
Doubnerová V, Ryšlavá H (2011) What can enzymes of C4 photosynthesis do for C3 plants under stress? Plant Sci 180:575–583. https://doi.org/10.1016/j.plantsci.2010.12.005
Doubnerová V, Miedzińska L, Dobrá J et al (2014) Phosphoenolpyruvate carboxylase, NADP-malic enzyme, and pyruvate, phosphate dikinase are involved in the acclimation of Nicotiana tabacum L. to drought stress. J Plant Physiol 171:19–25. https://doi.org/10.1016/j.jplph.2013.10.017
Driever SM, Kromdijk J (2013) Will C3 crops enhanced with the C4 CO2-concentrating mechanism live up to their full potential (yield)? J Exp Bot 64:3925–3935. https://doi.org/10.1093/jxb/ert103
Eastmond PJ, Dennis DT, Rawsthorne S (1997) Evidence that a malate/inorganic phosphate exchange translocator imports carbon across the leucoplast envelope for fatty acid synthesis in developing castor seed endosperm. Plant Physiol 114:851–856. https://doi.org/10.1104/pp.114.3.851
Eastmond PJ, Germain V, Lange PR et al (2000) Postgerminative growth and lipid catabolism in oilseeds lacking the glyoxylate cycle. Proc Natl Acad Sci 97:5669–5674. https://doi.org/10.1073/pnas.97.10.5669
Eastmond PJ, Astley HM, Parsley K et al (2015) Arabidopsis uses two gluconeogenic gateways for organic acids to fuel seedling establishment. Nat Commun 6:6659
Edwards GE, Kanai R, Black CC (1971) Phosphoenolpyruvate carboxykinase in leaves of certain plants which fix CO2 by the C4-dicarboxylic acid cycle of photosynthesis. Biochem Biophys Res Commun 45:278–285. https://doi.org/10.1016/0006-291X(71)90814-X
Emms DM, Covshoff S, Hibberd JM, Kelly S (2016) Independent and parallel evolution of new genes by gene duplication in two origins of C4 photosynthesis provides new insight into the mechanism of phloem loading in C4 species. Mol Biol Evol 33:1796–1806. https://doi.org/10.1093/molbev/msw057
Engelmann S, Bläsing OE, Westhoff P (2002) Serine 774 and amino acids 296 to 437 comprise the major C4 determinants of the C4 phosphoenolpyruvate carboxylase of Flaveria trinervia. FEBS Lett 524:11–14. https://doi.org/10.1016/S0014-5793(02)02975-7
Engineer CB, Ghassemian M, Anderson JC et al (2014) Carbonic anhydrases, EPF2 and a novel protease mediate CO2 control of stomatal development. Nature 513:246. https://doi.org/10.1038/nature13452
Ermakova M, Arrivault S, Giuliani R et al (2020a) Installation of C4 photosynthetic pathway enzymes in rice using a single construct. Plant Biotechnol J 19:575–588. https://doi.org/10.1111/pbi.13487
Ermakova M, Danila FR, Furbank RT, von Caemmerer S (2020b) On the road to C4 rice: advances and perspectives. Plant J 101:940–950. https://doi.org/10.1111/tpj.14562
Espie GS, Colman B (1986) Inorganic carbon uptake during photosynthesis : I. A theoretical analysis using the isotopic disequilibrium technique. Plant Physiol 80:863–869. https://doi.org/10.1104/pp.80.4.863
Éva C, Oszvald M, Tamás L (2019) Current and possible approaches for improving photosynthetic efficiency. Plant Sci 280:433–440. https://doi.org/10.1016/j.plantsci.2018.11.010
Famiani F, Cultrera NGM, Battistelli A et al (2005) Phosphoenolpyruvate carboxykinase and its potential role in the catabolism of organic acids in the flesh of soft fruit during ripening. J Exp Bot 56:2959–2969. https://doi.org/10.1093/jxb/eri293
Fan Z, Li J, Lu M et al (2013) Overexpression of phosphoenolpyruvate carboxylase from Jatropha curcas increases fatty acid accumulation in Nicotiana tabacum. Acta Physiol Plant 35:2269–2279. https://doi.org/10.1007/s11738-013-1264-3
Faske M, Backhausen JE, Sendker M et al (1997) Transgenic tobacco plants expressing pea chloroplast Nmdh cDNA in sense and antisense orientation: effects on NADP-malate dehydrogenase level, stability of transformants, and plant growth. Plant Physiol 115:705–715. https://doi.org/10.1104/pp.115.2.705
Feldman AB, Leung H, Baraoidan M et al (2017) Increasing leaf vein density via mutagenesis in rice results in an enhanced rate of photosynthesis, smaller cell sizes and can reduce interveinal mesophyll cell number. Front Plant Sci. https://doi.org/10.3389/fpls.2017.01883
Feria AB, Bosch N, Sánchez A et al (2016) Phosphoenolpyruvate carboxylase (PEPC) and PEPC-kinase (PEPC-k) isoenzymes in Arabidopsis thaliana: role in control and abiotic stress conditions. Planta 244:901–913. https://doi.org/10.1007/s00425-016-2556-9
Ferreira FJ, Guo C, Coleman JR (2008) Reduction of plastid-localized carbonic anhydrase activity results in reduced Arabidopsis seedling survivorship. Plant Physiol 147:585–594. https://doi.org/10.1104/pp.108.118661
Finnegan PM, Suzuki S, Ludwig M, Burnell JN (1999) Phosphoenolpyruvate carboxykinase in the C4 monocot Urochloa panicoides is encoded four differentially expressed genes. Plant Physiol 120:1033–1041. https://doi.org/10.1104/pp.120.4.1033
Fromm S, Braun HP, Peterhansel C (2016a) Mitochondrial gamma carbonic anhydrases are required for complex I assembly and plant reproductive development. New Phytol 211:194–207. https://doi.org/10.1111/nph.13886
Fromm S, Göing J, Lorenz C et al (2016b) Depletion of the “gamma-type carbonic anhydrase-like” subunits of complex I affects central mitochondrial metabolism in Arabidopsis thaliana. Biochim Biophys Acta Bioenerg 1857:60–71. https://doi.org/10.1016/j.bbabio.2015.10.006
Fromm S, Senkler J, Zabaleta E et al (2016c) The carbonic anhydrase domain of plant mitochondrial complex I. Physiol Plant 157:289–296. https://doi.org/10.1111/ppl.12424
Furbank RT (2011) Evolution of the C4 photosynthetic mechanism: are there really three C 4 acid decarboxylation types? J Exp Bot 62:3103–3108. https://doi.org/10.1093/jxb/err080
Gerrard Wheeler MC, Tronconi MA, Drincovich MF et al (2005) A comprehensive analysis of the NADP-Malic enzyme gene family of Arabidopsis. Plant Physiol 139:39–51. https://doi.org/10.1104/pp.105.065953
Gerrard Wheeler MC, Arias CL, Tronconi MA et al (2008) Arabidopsis thaliana NADP-malic enzyme isoforms: high degree of identity but clearly distinct properties. Plant Mol Biol 67:231–242. https://doi.org/10.1007/s11103-008-9313-9
Gietl C (1990) Glyoxysomal malate dehydrogenase from watermelon is synthesized with an amino-terminal transit peptide. Proc Natl Acad Sci 87:5773–5777. https://doi.org/10.1073/pnas.87.15.5773
Gietl C (1992a) Malate dehydrogenase isoenzymes: cellular locations and role in the flow of metabolites between the cytoplasm and cell organelles. Biochim Biophys Acta Bioenerg 1100:217–234. https://doi.org/10.1016/0167-4838(92)90476-T
Gietl C (1992b) Partitioning of malate dehydrogenase isoenzymes into glyoxysomes, mitochondria, and chloroplasts. Plant Physiol 100:557–559. https://doi.org/10.1104/pp.100.2.557
Gietl C, Lehnerer M, Olsen O (1990) Mitochondrial malate dehydrogenase from watermelon: sequence of cDNA clones and primary structure of the higher-plant precursor protein. Plant Mol Biol 14:1019–1030. https://doi.org/10.1007/BF00019398
Giuliani R, Karki S, Covshoff S et al (2019) Knockdown of glycine decarboxylase complex alters photorespiratory carbon isotope fractionation in Oryza sativa leaves. J Exp Bot 70:2773–2786. https://doi.org/10.1093/jxb/erz083
Górska AM, Gouveia P, Borba AR et al (2021) ZmOrphan94 transcription factor downregulates ZmPEPC1 gene expression in maize bundle sheath cells. Front Plant Sci. https://doi.org/10.3389/fpls.2021.559967
Gowik U, Westhoff P (2011) The path from C3 to C4 photosynthesis. Plant Physiol 155:56–63. https://doi.org/10.1104/pp.110.165308
Gowik U, Burscheidt J, Akyildiz M et al (2004) cis-Regulatory elements for mesophyll-specific gene expression in the C4 plant Flaveria trinervia, the promoter of the C4 phosphoenolpyruvate carboxylase gene. Plant Cell 16:1077–1090. https://doi.org/10.1105/tpc.019729
Gu J-F, Qiu M, Yang J-C (2013) Enhanced tolerance to drought in transgenic rice plants overexpressing C4 photosynthesis enzymes. Crop J 1:105–114. https://doi.org/10.1016/j.cj.2013.10.002
Guillet C, Just D, Bénard N et al (2002) A fruit-specific phosphoenolpyruvate carboxylase is related to rapid growth of tomato fruit. Planta 214:717–726. https://doi.org/10.1007/s00425-001-0687-z
Hatch MD (1987) C4 photosynthesis: a unique elend of modified biochemistry, anatomy and ultrastructure. BBA Rev Bioenerg 895:81–106. https://doi.org/10.1016/S0304-4173(87)80009-5
Hatch MD, Slack CR (1966) Photosynthesis by sugar-cane leaves. A new carboxylation reaction and the pathway of sugar formation. Biochem J 101:103–111. https://doi.org/10.1042/bj1010103
Hatch MD, Kagawa T, Craig S (1975) Subdivision of C4-pathway species based on differing C4 acid decarboxylating systems and ultrastructural features. Funct Plant Biol 2:111–128. https://doi.org/10.1071/PP9750111
Hebbelmann I, Selinski J, Wehmeyer C et al (2012) Multiple strategies to prevent oxidative stress in Arabidopsis plants lacking the malate valve enzyme NADP-malate dehydrogenase. J Exp Bot 63:1445–1459. https://doi.org/10.1093/jxb/err386
Henry RJ, Furtado A, Rangan P (2020) Pathways of photosynthesis in non-leaf tissues. Biology (Basel) 9:1–13. https://doi.org/10.3390/biology9120438
Heyno E, Innocenti G, Lemaire SD et al (2014) Putative role of the malate valve enzyme NADP–malate dehydrogenase in H2O2 signalling in Arabidopsis. Philos Trans R Soc B Biol Sci 369:20130228. https://doi.org/10.1098/rstb.2013.0228
Hibberd JM, Covshoff S (2010) The regulation of gene expression required for C4 photosynthesis. Annu Rev Plant Biol 61:181–207. https://doi.org/10.1146/annurev-arplant-042809-112238
Hibberd JM, Quick WP (2002) Characteristics of C4 photosynthesis in stems and petioles of C3 flowering plants. Nature 415:451. https://doi.org/10.1038/415451a
Hibberd JM, Sheehy JE, Langdale JA (2008) Using C4 photosynthesis to increase the yield of rice-rationale and feasibility. Curr Opin Plant Biol 11:228–231. https://doi.org/10.1016/j.pbi.2007.11.002
Hines KM, Chaudhari V, Edgeworth KN et al (2021) Absence of carbonic anhydrase in chloroplasts affects C3 plant development but not photosynthesis. Proc Natl Acad Sci 118(33):e2107425118. https://doi.org/10.1073/pnas.2107425118
Hu H, Boisson-Dernier A, Israelsson-Nordström M et al (2010) Carbonic anhydrases are upstream regulators of CO2-controlled stomatal movements in guard cells. Nat Cell Biol 12:87–93. https://doi.org/10.1038/ncb2009
Hu L, Li Y, Xu W et al (2012) Improvement of the photosynthetic characteristics of transgenic wheat plants by transformation with the maize C 4 phosphoenolpyruvate carboxylase gene. Plant Breed 131:385–391. https://doi.org/10.1111/j.1439-0523.2012.01960.x
Hu H, Rappel W-J, Occhipinti R et al (2015) Distinct cellular locations of carbonic anhydrases mediate carbon dioxide control of stomatal movements. Plant Physiol 169:1168–1178. https://doi.org/10.1104/pp.15.00646
Huang YX, Goto Y, Nonaka S et al (2015a) Overexpression of the phosphoenolpyruvate carboxykinase gene (SlPEPCK) promotes soluble sugar accumulation in fruit and post-germination growth of tomato (Solanum lycopersicum L.). Plant Biotechnol 32:281–289. https://doi.org/10.5511/plantbiotechnology.15.1019a
Huang YX, Yin YG, Sanuki A et al (2015b) Phosphoenolpyruvate carboxykinase (PEPCK) deficiency affects the germination, growth and fruit sugar content in tomato (Solanum lycopersicum L.). Plant Physiol Biochem 96:417–425. https://doi.org/10.1016/j.plaphy.2015.08.021
Huang J, Li Z, Biener G et al (2017) Carbonic anhydrases function in anther cell differentiation downstream of the receptor-like kinase EMS1. Plant Cell 29:1335–1356. https://doi.org/10.1105/tpc.16.00484
Huang J, Niazi AK, Young D et al (2018) Self-protection of cytosolic malate dehydrogenase against oxidative stress in Arabidopsis. J Exp Bot 69:3491–3505. https://doi.org/10.1093/jxb/erx396
Hyskova V, Ryslava H (2016) Unusual properties and functions of plant pyruvate orthophospate dikinase. Biochem Anal Biochem 5:e161. https://doi.org/10.4172/2161-1009.1000e161
Ignatova L, Rudenko N, Zhurikova E et al (2019) Carbonic anhydrases in photosynthesizing cells of C3 higher plants. Metabolites 9:73. https://doi.org/10.3390/metabo9040073
Imaizumi N, Ku MSB, Ishihara K et al (1997) Characterization of the gene for pyruvate, orthophosphate dikinase from rice, a C3 plant, and a comparison of structure and expression between C3 and C4 genes for this protein. Plant Mol Biol 34:701–716. https://doi.org/10.1023/A:1005884515840
Jansson C, Vogel J, Hazen S et al (2018) Climate-smart crops with enhanced photosynthesis. J Exp Bot 69:3801–3809. https://doi.org/10.1093/jxb/ery213
Jenner HL, Winning BM, Millar AH et al (2001) NAD malic enzyme and the control of carbohydrate metabolism in potato tubers. Plant Physiol 126:1139–1149. https://doi.org/10.1104/pp.126.3.1139
Jiang C, Tholen D, Xu JM et al (2014) Increased expression of mitochondria-localized carbonic anhydrase activity resulted in an increased biomass accumulation in Arabidopsis thaliana. J Plant Biol 57:366–374. https://doi.org/10.1007/s12374-014-0330-8
Jiang Q, Li X, Niu F et al (2017) iTRAQ-based quantitative proteomic analysis of wheat roots in response to salt stress. Proteomics. https://doi.org/10.1002/pmic.201600265
Jiao D, Huang X, Li X et al (2002) Photosynthetic characteristics and tolerance to photo-oxidation of transgenic rice expressing C4 photosynthesis enzymes. Photosynth Res 72:85–93. https://doi.org/10.1023/A:1016062117373
Jurić I, Hibberd JM, Blatt M, Burroughs NJ (2019) Computational modelling predicts substantial carbon assimilation gains for C3 plants with a single-celled C4 biochemical pump. PLoS Comput Biol 15(9):e1007373. https://doi.org/10.1371/journal.pcbi.1007373
Kaachra A, Vats SK, Kumar S (2018) Heterologous expression of key C and N metabolic enzymesimproves Re-assimilation of photorespired CO2 and NH3, and growth. Plant Physiol 177:1396–1409. https://doi.org/10.1104/pp.18.00379
Kajala K, Brown NJ, Williams BP et al (2012) Multiple Arabidopsis genes primed for recruitment into C4 photosynthesis. Plant J 69:47–56. https://doi.org/10.1111/j.1365-313X.2011.04769.x
Kandoi D, Mohanty S, Govindjee TBC (2016) Towards efficient photosynthesis: overexpression of Zea mays phosphoenolpyruvate carboxylase in Arabidopsis thaliana. Photosynth Res 130:47–72. https://doi.org/10.1007/s11120-016-0224-3
Kandoi D, Mohanty S, Tripathy BC (2018) Overexpression of plastidic maize NADP-malate dehydrogenase (ZmNADP-MDH) in Arabidopsis thaliana confers tolerance to salt stress. Protoplasma 255:547–563. https://doi.org/10.1007/s00709-017-1168-y
Kandoi D, Ruhil K, Govindjee G, Tripathy BC (2022) Overexpression of cytoplasmic C4 Flaveria bidentis carbonic anhydrase in C3 Arabidopsis thaliana increases amino acids, photosynthetic potential, and biomass. Plant Biotechnol J 20:1518–1532. https://doi.org/10.1111/pbi.13830
Kang H-G, Park S, Matsuoka M, An G (2005) White-core endosperm floury endosperm-4 in rice is generated by knockout mutations in the C4-type pyruvate orthophosphate dikinase gene (OsPPDKB). Plant J 42:901–911. https://doi.org/10.1111/j.1365-313X.2005.02423.x
Karki S, Rizal G, Quick WP (2013) Improvement of photosynthesis in rice (Oryza sativa L.) by inserting the C4 pathway. Rice 6:1–8. https://doi.org/10.1186/1939-8433-6-28
Kim P, Xue CY, Song HD et al (2020) Tissue-specific activation of DOF11 promotes rice resistance to sheath blight disease and increases grain weight via activation of SWEET14. Plant Biotechnol J 19:409–411. https://doi.org/10.1111/pbi.13489
Kromdijk J, Ubierna N, Cousins AB, Griffiths H (2014) Bundle-sheath leakiness in C4 photosynthesis: a careful balancing act between CO2 concentration and assimilation. J Exp Bot 65:3443–3457. https://doi.org/10.1093/jxb/eru157
Kubis A, Bar-Even A (2019) Synthetic biology approaches for improving photosynthesis. J Exp Bot 70:1425–1433. https://doi.org/10.1093/jxb/erz029
Lai LB, Tausta SL, Nelson TM (2002a) Differential regulation of transcripts encoding cytosolic nadp-malic enzyme in C3 and C4 Flaveria species. Plant Physiol 128:140–149. https://doi.org/10.1104/pp.010449
Lai LB, Wang L, Nelson TM (2002b) Distinct but conserved functions for two chloroplastic nadp-malic enzyme isoforms in C3 and C4 Flaveria species. Plant Physiol 128:125–139. https://doi.org/10.1104/pp.010448
Laporte MM, Shen B, Tarczynski MC (2002) Engineering for drought avoidance: expression of maize NADP‐malic enzyme in tobacco results in altered stomatal function. J Exp Bot 53:699–705. https://doi.org/10.1093/jexbot/53.369.699
Lappe RR, Baier JW, Boehlein SK et al (2018) Functions of maize genes encoding pyruvate phosphate dikinase in developing endosperm. Proc Natl Acad Sci 115:E24–E33. https://doi.org/10.1073/pnas.1715668115
Lazova GN, Kicheva MI, Popova LP (2000) The effect of abscisic acid and methyl jasmonate on carbonic anhydrase activity in pea. Photosynthetica 36:631–634. https://doi.org/10.1023/A:1007016810034
Leakey ADB, Ferguson JN, Pignon CP et al (2019) Water use efficiency as a constraint and target for improving the resilience and productivity of C 3 and C 4 crops. Annu Rev Plant Biol 70:781–808. https://doi.org/10.1146/annurevarplant-042817-040305
Leegood RC, ap Rees T (1978) Dark fixation of CO2 during gluconeogenesis by the cotyledons of Cucurbita pepo L. Planta 140:275–282. https://doi.org/10.1007/bf00390260
Leeson GW (2018) The growth, ageing and urbanisation of our world. J Popul Ageing 11:107–115. https://doi.org/10.1007/s12062-018-9225-7
Li XR, Wang L, Ruan YL (2010) Developmental and molecular physiological evidence for the role of phosphoenolpyruvate carboxylase in rapid cotton fibre elongation. J Exp Bot 61:287–295. https://doi.org/10.1093/jxb/erp299
Li Q, Zhao J, Zhang J et al (2016) Ectopic expression of the chinese cabbage malate dehydrogenase gene promotes growth and aluminum resistance in Arabidopsis. Front Plant Sci 7:1–11. https://doi.org/10.3389/fpls.2016.01180
Lian L, Wang X, Zhu Y et al (2014) Physiological and photosynthetic characteristics of indica Hang2 expressing the sugarcane PEPC gene. Mol Biol Rep 41:2189–2197. https://doi.org/10.1007/s11033-014-3070-4
Lin H, Karki S, Coe RA et al (2016) Targeted knockdown of GDCH in rice leads to a photorespiratory-deficient phenotype useful as a building block for C4 rice. Plant Cell Physiol 57:919–932. https://doi.org/10.1093/pcp/pcw033
Lin HC, Arrivault S, Coe RA et al (2020) A partial C4 photosynthetic biochemical pathway in rice. Front Plant Sci. https://doi.org/10.3389/fpls.2020.564463
Linden P, Keech O, Stenlund H et al (2016) Reduced mitochondrial malate dehydrogenase activity has a strong effect on photorespiratory metabolism as revealed by 13C labelling. J Exp Bot 67:3123–3135. https://doi.org/10.1093/jxb/erw030
Liu S, Cheng Y, Zhang X et al (2007) Expression of an NADP-malic enzyme gene in rice (Oryza sativa L.) is induced by environmental stresses; over-expression of the gene in Arabidopsis confers salt and osmotic stress tolerance. Plant Mol Biol 64:49–58. https://doi.org/10.1007/s11103-007-9133-3
Liu X, Li X, Zhang C et al (2016) Phosphoenolpyruvate carboxylase regulation in C4-PEPC-expressing transgenic rice during early responses to drought stress. Physiol Plant 159:178–200. https://doi.org/10.1111/ppl.12506
Liu X, Li X, Dai C et al (2017) Improved short-term drought response of transgenic rice over-expressing maize C4 phosphoenolpyruvate carboxylase via calcium signal cascade. J Plant Physiol 218:206–221. https://doi.org/10.1016/j.jplph.2017.08.005
Lo SF, Chatterjee J, Biswal AK et al (2022) Closer vein spacing by ectopic expression of nucleotide-binding and leucine-rich repeat proteins in rice leaves. Plant Cell Rep 41:319–335. https://doi.org/10.1007/s00299-021-02810-5
Lu Y, Tian Y, Shen R et al (2020) Targeted, efficient sequence insertion and replacement in rice. Nat Biotechnol 38:1402–1407. https://doi.org/10.1038/s41587-020-0581-5
Ludwig M (2011) The molecular evolution of β-carbonic anhydrase in Flaveria. J Exp Bot. https://doi.org/10.1093/jxb/err071
Ludwig M (2016) Evolution of carbonic anhydrase in C4 plants. Curr Opin Plant Biol 31:16–22. https://doi.org/10.1016/j.pbi.2016.03.003
Ludwig M, Busch FA, Khoshravesh R, Covshoff S (2021) Editorial: understanding C4 evolution and function. Front Plant Sci. https://doi.org/10.3389/fpls.2021.774818
Lundgren MR, Dunning LT, Olofsson JK et al (2019) C4 anatomy can evolve via a single developmental change. Ecol Lett 22:302–312. https://doi.org/10.1111/ele.13191
Maheshwari C, Coe RA, Karki S et al (2021) Targeted knockdown of ribulose-1, 5-bisphosphate carboxylase-oxygenase in rice mesophyll cells. J Plant Physiol 260:153395. https://doi.org/10.1016/j.jplph.2021.153395
Maier A, Zell MB, Maurino VG (2011) Malate decarboxylases: evolution and roles of NAD(P)-ME isoforms in species performing C4 and C3 photosynthesis. J Exp Bot 62:3061–3069. https://doi.org/10.1093/jxb/err024
Majeau N, Arnoldo MA, Coleman JR (1994) Modification of carbonic anhydrase activity by antisense and over-expression constructs in transgenic tobacco. Plant Mol Biol 25:377–385. https://doi.org/10.1007/BF00043867
Malone S, Chen ZH, Bahrami AR et al (2007) Phosphoenolpyruvate carboxykinase in Arabidopsis: changes in gene expression, protein and activity during vegetative and reproductive development. Plant Cell Physiol 48:441–450. https://doi.org/10.1093/pcp/pcm014
Marshall JS, Stubbs JD, Taylor WC (1996) Two genes encode highly similar chloroplastic NADP-malic enzymes in Flaveria: implications for the evolution of C4 photosynthesis. Plant Physiol 111:1251–1261. https://doi.org/10.1104/pp.111.4.1251
Marshall JS, Stubbs JD, Chitty JA et al (1997) Expression of the C4 Me1 gene from Flaveria bidentis requires an interaction between 5[prime] and 3[prime] sequences. Plant Cell 9:1515–1525. https://doi.org/10.1105/tpc.9.9.1515
Martinoia E, Rentsch D (1994) Malate compartmentation-responses to a complex metabolism. Annu Rev Plant Physiol Plant Mol Biol 45:447–467. https://doi.org/10.1146/annurev.pp.45.060194.002311
Masumoto C, Miyazawa SI, Ohkawa H et al (2010) Phosphoenolpyruvate carboxylase intrinsically located in the chloroplast of rice plays a crucial role in ammonium assimilation. Proc Natl Acad Sci 107:5226–5231. https://doi.org/10.1073/pnas.0913127107
Maurino VG, Gerrard Wheeler MC, Andreo CS, Drincovich MF (2009) Redundancy is sometimes seen only by the uncritical: does Arabidopsis need six malic enzyme isoforms? Plant Sci 176:715–721. https://doi.org/10.1016/j.plantsci.2009.02.012
McGonigle B, Nelson T (1995) C4 isoform of NADP-malate dehydrogenase (cDNA Cloning and expression in leaves of C4, C3, and C3–C4 intermediate species of Flaveria). Plant Physiol 108:1119–1126. https://doi.org/10.1104/pp.108.3.1119
Méchin V, Thévenot C, Le Guilloux M et al (2007) Developmental analysis of maize endosperm proteome suggests a pivotal role for pyruvate orthophosphate dikinase. Plant Physiol 143:1203–1219. https://doi.org/10.1104/pp.106.092148
Menezes-Blackburn D, Bol R, Klumpp E et al (2021) Citric acid effect on the abundance, size and composition of water-dispersible soil colloids and its relationship to soil phosphorus desorption: a case study. J Soil Sci Plant Nutr 21:2436–2446. https://doi.org/10.1007/s42729-021-00534-9
Miyao M, Masumoto C, Miyazawa SI, Fukayama H (2011) Lessons from engineering a single-cell C 4 photosynthetic pathway into rice. J Exp Bot 62:3021–3029. https://doi.org/10.1093/jxb/err023
Momayyezi M, McKown AD, Bell SCS, Guy RD (2020) Emerging roles for carbonic anhydrase in mesophyll conductance and photosynthesis. Plant J 101:831–844. https://doi.org/10.1111/tpj.14638
Moody NR, Christin PA, Reid JD (2020) Kinetic modifications of C4 PEPC are qualitatively convergent, but larger in Panicum Than in Flaveria. Front Plant Sci. https://doi.org/10.3389/fpls.2020.01014
Moons A, Valcke R, Van Montagu M (1998) Low-oxygen stress and water deficit induce cytosolic pyruvate orthophosphate dikinase (PPDK) expression in roots of rice, a C3 plant. Plant J 15:89–98. https://doi.org/10.1046/j.1365-313x.1998.00185.x
Moroney JV, Bartlett SG, Samuelsson G (2004) Carbonic anhydrases in plants and algae. Plant Cell Environ 24:141–153. https://doi.org/10.1111/j.1365-3040.2001.00669.x
Muñoz-Vargas MA, González-Gordo S, Palma JM, Corpas FJ (2020) Inhibition of NADP-malic enzyme activity by H2S and NO in sweet pepper (Capsicum annuum L.) fruits. Physiol Plant 168:278–288. https://doi.org/10.1111/ppl.13000
Musrati RA, Kollarova M, Mernik N, Mikulasova D (1998) Malate dehydrogenase: distribution, function and properties. Gen Physiol Biophys 17:193–210
Nan N, Wang J, Shi Y et al (2020) Rice plastidial NAD-dependent malate dehydrogenase 1 negatively regulates salt stress response by reducing the vitamin B6 content. Plant Biotechnol J 18:172–184. https://doi.org/10.1111/pbi.13184
Niklaus M, Kelly S (2019) The molecular evolution of C 4 photosynthesis: opportunities for understanding and improving the world’s most productive plants. J Exp Bot 70:859–869. https://doi.org/10.1093/jxb/ery416
Nomura M, Mai HT, Fujii M et al (2006) Phosphoenolpyruvate carboxylase plays a crucial role in limiting nitrogen fixation in Lotus japonicus nodules. Plant Cell Physiol 47:613–621. https://doi.org/10.1093/pcp/pcj028
Nowicka B, Ciura J, Szymańska R, Kruk J (2018) Improving photosynthesis, plant productivity and abiotic stress tolerance—current trends and future perspectives. J Plant Physiol 231:415–433. https://doi.org/10.1016/j.jplph.2018.10.022
Nunes-Nesi A, Carrari F, Lytovchenko A et al (2005) Enhanced photosynthetic performance and growth as a consequence of decreasing mitochondrial malate dehydrogenase activity in transgenic tomato plants. Plant Physiol 137:611–622. https://doi.org/10.1104/pp.104.055566
Nunes-Nesi A, Sulpice R, Gibon Y, Fernie AR (2008) The enigmatic contribution of mitochondrial function in photosynthesis. J Exp Bot 59:1675–1684. https://doi.org/10.1093/jxb/ern002
O’Leary B, Park J, Plaxton WC (2011) The remarkable diversity of plant PEPC (phosphoenolpyruvate carboxylase): recent insights into the physiological functions and post-translational controls of non-photosynthetic PEPCs. Biochem J 436:15. https://doi.org/10.1042/BJ20110078
Ort DR, Merchant SS, Alric J et al (2015) Redesigning photosynthesis to sustainably meet global food and bioenergy demand. Proc Natl Acad Sci USA 112:8529–8536. https://doi.org/10.1073/pnas.1424031112
Osborn HL, Alonso-Cantabrana H, Sharwood RE et al (2017) Effects of reduced carbonic anhydrase activity on CO2 assimilation rates in Setaria viridis: a transgenic analysis. J Exp Bot 68:299–310. https://doi.org/10.1093/jxb/erw357
Osuna L, Pierre JN, González MC et al (1999) Evidence for a slow-turnover form of the Ca2+-independent phosphoenolpyruvate carboxylase kinase in the aleurone-endosperm tissue of germinating barley seeds. Plant Physiol 119:511–520. https://doi.org/10.1104/pp.119.2.511
Parsley K, Hibberd JM (2006) The Arabidopsis PPDK gene is transcribed from two promoters to produce differentially expressed transcripts responsible for cytosolic and plastidic proteins. Plant Mol Biol 62:339–349. https://doi.org/10.1007/s11103-006-9023-0
Paulus JK, Schlieper D, Groth G (2013) Greater efficiency of photosynthetic carbon fixation due to single amino-acid substitution. Nat Commun. https://doi.org/10.1038/ncomms2504
Penfield S, Rylott EL, Gilday AD et al (2004) Reserve mobilization in the Arabidopsis endosperm fuels hypocotyl elongation in the dark, is independent of abscisic acid, and requires Phosphoenolpyruvate Carboxykinase1. Plant Cell 16:2705–2718. https://doi.org/10.1105/tpc.104.024711
Penfield S, Clements S, Bailey Karen J et al (2011) Expression and manipulation of Phosphoenolpyruvate Carboxykinase 1 identifies a role for malate metabolism in stomatal closure. Plant J 69:679–688. https://doi.org/10.1111/j.1365-313X.2011.04822.x
Peng C, Xu W, Hu L et al (2018) Effects of the maize C4 phosphoenolpyruvate carboxylase (ZmPEPC) gene on nitrogen assimilation in transgenic wheat. Plant Growth Regul 84:191–205. https://doi.org/10.1007/s10725-017-0332-x
Perales M, Eubel H, Heinemeyer J et al (2005) Disruption of a nuclear gene encoding a mitochondrial gamma carbonic anhydrase reduces complex I and supercomplex I+III2 levels and alters mitochondrial physiology in Arabidopsis. J Mol Biol 350:263–277. https://doi.org/10.1016/j.jmb.2005.04.062
Peterhansel C, Horst I, Niessen M et al (2010) Photorespiration. Arab B 8:e0130. https://doi.org/10.1199/tab.0130
Pracharoenwattana I, Cornah JE, Smith SM (2007) Arabidopsis peroxisomal malate dehydrogenase functions in β-oxidation but not in the glyoxylate cycle. Plant J 50:381–390. https://doi.org/10.1111/j.1365-313X.2007.03055.x
Price GD, von Caemmerer S, Evans JR et al (1994) Specific reduction of chloroplast carbonic anhydrase activity by antisense RNA in transgenic tobacco plants has a minor effect on photosynthetic CO2 assimilation. Planta 193:331–340. https://doi.org/10.1007/BF00201810
Qi X, Xu W, Zhang J et al (2017) Physiological characteristics and metabolomics of transgenic wheat containing the maize C4 phosphoenolpyruvate carboxylase (PEPC) gene under high temperature stress. Protoplasma 254:1017–1030. https://doi.org/10.1007/s00709-016-1010-y
Qian B, Li X, Liu X et al (2015) Enhanced drought tolerance in transgenic rice over-expressing of maize C4 phosphoenolpyruvate carboxylase gene via NO and Ca2+. J Plant Physiol 175:9–20. https://doi.org/10.1016/j.jplph.2014.09.019
Qin N, Xu W, Hu L et al (2016) Drought tolerance and proteomics studies of transgenic wheat containing the maize C4 phosphoenolpyruvate carboxylase (PEPC) gene. Protoplasma 253:1503–1512. https://doi.org/10.1007/s00709-015-0906-2
Rangan P, Furtado A, Henry RJ (2016) New evidence for grain specific C4 photosynthesis in wheat. Sci Rep 6:31721. https://doi.org/10.1038/srep31721
Rao X, Lu N, Li G et al (2016) Comparative cell-specific transcriptomics reveals differentiation of C4 photosynthesis pathways in switchgrass and other C4 lineages. J Exp Bot 67:1649–1662. https://doi.org/10.1093/jxb/erv553
Raven JA (2001) A role for mitochondrial carbonic anhydrase in limiting CO2 leakage from low CO2-grown cells of Chlamydomonas reinhardtii. Plant Cell Environ 24:261–265. https://doi.org/10.1046/j.1365-3040.2001.00662.x
Ren CG, Li X, Liu XL et al (2014) Hydrogen peroxide regulated photosynthesis in C4-pepc transgenic rice. Plant Physiol Biochem 74:218–229. https://doi.org/10.1016/j.plaphy.2013.11.011
Reyna-Llorens I, Hibberd JM (2017) Recruitment of pre-existing networks during the evolution of C 4 photosynthesis. Philos Trans R Soc B Biol Sci. https://doi.org/10.1098/rstb.2016.0386
Reyna-Llorens I, Burgess SJ, Reeves G et al (2018) Ancient duons may underpin spatial patterning of gene expression in C4 leaves. Proc Natl Acad Sci 115:1931–1936. https://doi.org/10.1073/pnas.1720576115
Riazunnisa K, Padmavathi L, Bauwe H, Raghavendra AS (2006) Markedly low requirement of added CO2 for photosynthesis by mesophyll protoplasts of pea (Pisum sativum): possible roles of photorespiratory CO2 and carbonic anhydrase. Physiol Plant 128:763–772. https://doi.org/10.1111/j.1399-3054.2006.00803.x
Rolletschek H, Borisjuk L, Radchuk R et al (2004) Seed-specific expression of a bacterial phosphoenolpyruvate carboxylase in Vicia narbonensis increases protein content and improves carbon economy. Plant Biotechnol J 2:211–219. https://doi.org/10.1111/j.1467-7652.2004.00064.x
Rosche E, Westhoff P (1995) Genomic structure and expression of the pyruvate, orthophosphate dikinase gene of the dicotyledonous C4 plant Flaveria trinervia (Asteraceae). Plant Mol Biol 29:663–678. https://doi.org/10.1007/BF00041157
Rosnow JJ, Edwards GE, Roalson EH (2014) Positive selection of Kranz and non-Kranz C4 phosphoenolpyruvate carboxylase amino acids in Suaedoideae (Chenopodiaceae). J Exp Bot 65:3595–3607. https://doi.org/10.1093/jxb/eru053
Ruan CJ, Shao HB, Teixeira Da Silva JA (2012) A critical review on the improvement of photosynthetic carbon assimilation in C3 plants using genetic engineering. Crit Rev Biotechnol 32:1–21. https://doi.org/10.3109/07388551.2010.533119
Rudenko NN, Fedorchuk TP, Vetoshkina DV et al (2018) Influence of knockout of At4g20990 gene encoding α-CA4 on photosystem II light-harvesting antenna in plants grown under different light intensities and day lengths. Protoplasma 255:69–78. https://doi.org/10.1007/s00709-017-1133-9
Rudenko NN, Borisova-Mubarakshina MM, Ignatova LK et al (2020a) Role of plant carbonic anhydrases under stress conditions. In: Hossain A (ed) Plant stress physiology. IntechOpen, London. https://doi.org/10.5772/intechopen.91971
Rudenko NN, Fedorchuk TP, Terentyev VV et al (2020b) The role of carbonic anhydrase α-CA4 in the adaptive reactions of photosynthetic apparatus: the study with α-CA4 knockout plants. Protoplasma 257:489–499. https://doi.org/10.1007/s00709-019-01456-1
Rylott EL, Gilday AD, Graham IA (2003) The gluconeogenic enzyme phosphoenolpyruvate carboxykinase in Arabidopsis is essential for seedling establishment. Plant Physiol 131:1834–1842. https://doi.org/10.1104/pp.102.019174
Sadras V, Grassini P, Steduto P (2012) Status of Water Use Efficiency of Main Crops. State World’s L Water Resour Food Agric FAO Themat Rep No 7 pp 41. http://www.fao.org/fileadmin/templates/solaw/files/thematic_reports/TR_07_web.pdf. Accessed 1 Jan 2012
Sage RF, Zhu X-G (2011) Exploiting the engine of C4 photosynthesis. J Exp Bot 62:2989–3000. https://doi.org/10.1093/jxb/err179
Sales CRG, Wang Y, Evers JB, Kromdijk J (2021) Improving C4photosynthesis to increase productivity under optimal and suboptimal conditions. J Exp Bot 72:5942–5960. https://doi.org/10.1093/jxb/erab327
Sangwan RS, Singh N, Plaxton WC (1992) Phosphoenolpyruvate carboxylase activity and concentration in the endosperm of developing and germinating castor oil seeds. Plant Physiol 99:445–449. https://doi.org/10.1104/pp.99.2.445
Schaaf J, Walter MH, Hess D (1995) Primary metabolism in plant defense (regulation of a bean malic enzyme gene promoter in transgenic tobacco by developmental and environmental cues). Plant Physiol 108:949–960. https://doi.org/10.1104/pp.108.3.949
Schlüter U, Weber APM (2020) Regulation and evolution of C4 photosynthesis. Annu Rev Plant Biol 71:183–215. https://doi.org/10.1146/annurev-arplant-042916-040915
Schreier TB, Cléry A, Schläfli M et al (2018) Plastidial NAD-dependent malate dehydrogenase: a moonlighting protein involved in early chloroplast development through its interaction with an FtsH12-FtsHi protease complex. Plant Cell 30:1745–1769. https://doi.org/10.1105/tpc.18.00121
Schuler ML, Mantegazza O, Weber APM (2016) Engineering C4 photosynthesis into C3 chassis in the synthetic biology age. Plant J 87:51–65. https://doi.org/10.1111/tpj.13155
Schulze J, Shi L, Blumenthal J et al (1998) Inhibition of alfalfa root nodule phosphoenolpyruvate carboxylase through an antisense strategy impacts nitrogen fixation and plant growth. Phytochemistry 49:341–346. https://doi.org/10.1016/S0031-9422(98)00221-0
Sedelnikova OV, Hughes TE, Langdale JA (2018) Understanding the genetic basis of C4 Kranz anatomy with a view to engineering C3 crops. Annu Rev Genet 52:249–270. https://doi.org/10.1146/annurev-genet-120417-031217
Selinski J, Scheibe R (2019) Malate valves: old shuttles with new perspectives. Plant Biol 21:21–30. https://doi.org/10.1111/plb.12869
Selinski J, König N, Wellmeyer B et al (2014) The plastid-localized NAD-dependent malate dehydrogenase is crucial for energy homeostasis in developing Arabidopsis thaliana seeds. Mol Plant 7:170–186. https://doi.org/10.1093/mp/sst151
Sen P, Ghosh S, Sarkar SN et al (2017) Pyramiding of three C4 specific genes towards yield enhancement in rice. Plant Cell Tissue Organ Cult 128:145–160. https://doi.org/10.1007/s11240-016-1094-2
Sew YS, Ströher E, Fenske R, Millar AH (2016) Loss of mitochondrial malate dehydrogenase activity alters seed metabolism impairing seed maturation and post-germination growth in Arabidopsis. Plant Physiol 171:849–863. https://doi.org/10.1104/pp.16.01654
Shearer HL, Turpin DH, Dennis DT (2004) Characterization of NADP-dependent malic enzyme from developing castor oil seed endosperm. Arch Biochem Biophys 429:134–144. https://doi.org/10.1016/j.abb.2004.07.001
Sheehy JE, Mitchell PL, Hardy B (2008) Charting new pathways to C4 rice. IRRI Books, International Rice Research Institute (IRRI), Los Banos, p 281815. https://doi.org/10.22004/ag.econ.281815
Sheen J (1991) Molecular mechanisms underlying the differential expression of maize pyruvate, orthophosphate dikinase genes. Plant Cell 3:225–245. https://doi.org/10.1105/tpc.3.3.225
Shen WJ, Chen GX, Xu JG et al (2015) Overexpression of maize phosphoenolpyruvate carboxylase improves drought tolerance in rice by stabilization the function and structure of thylakoid membrane. Photosynthetica 53:436–446. https://doi.org/10.1007/s11099-015-0111-8
Shevela D, Eaton-Rye JJ, Shen JR, Govindjee (2012) Photosystem II and the unique role of bicarbonate: a historical perspective. Biochim Biophys Acta Bioenergetics 1817:1134–1151. https://doi.org/10.1016/j.bbabio.2012.04.003
Shi J, Yi K, Liu Y et al (2015) Phosphoenolpyruvate carboxylase in Arabidopsis leaves plays a crucial role in carbon and nitrogen metabolism. Plant Physiol 167:671–681. https://doi.org/10.1104/pp.114.254474
Shi W, Yue L, Guo J et al (2020) Identification and evolution of C4 photosynthetic pathway genes in plants. BMC Plant Biol. https://doi.org/10.1186/s12870-020-02339-x
Singh J, Thakur JK (2018) Photosynthesis and abiotic stress in plants. In: Vats S (ed) Biotic and abiotic stress tolerance in plants. Springer, Singapore, pp 27–46. https://doi.org/10.1007/978-981-10-9029-5_2
Singh J, Reddy GM, Agarwal A et al (2012) Molecular and structural analysis of C4-specific PEPC isoform from Pennisetum glaucum plays a role in stress adaptation. Gene 500:224–231. https://doi.org/10.1016/j.gene.2012.03.018
Singh J, Pandey P, James D et al (2014) Enhancing C3 photosynthesis: an outlook on feasible interventions for crop improvement. Plant Biotechnol J 12:1217–1230. https://doi.org/10.1111/pbi.12246
Smith RG, Gauthier DA, Dennis DT, Turpin DH (1992) Malate- and pyruvate-dependent fatty acid synthesis in leucoplasts from developing castor endosperm. Plant Physiol 98:1233–1238. https://doi.org/10.1104/pp.98.4.1233
Song J, Zou X, Liu P et al (2022) Differential expressions and enzymatic properties of malate dehydrogenases in response to nutrient and metal stresses in Stylosanthes guianensis. Plant Physiol Biochem 170:325–337. https://doi.org/10.1016/j.plaphy.2021.12.012
Soto D, Cõrdoba JP, Villarreal F et al (2015) Functional characterization of mutants affected in the carbonic anhydrase domain of the respiratory complex I in Arabidopsis thaliana. Plant J 83:831–844. https://doi.org/10.1111/tpj.12930
Soufari H, Parrot C, Kuhn L et al (2020) Specific features and assembly of the plant mitochondrial complex I revealed by cryo-EM. Nat Commun. https://doi.org/10.1038/s41467-020-18814-w
Stemler AJ (1997) The case for chloroplast thylakoid carbonic anhydrase. Physiol Plant 99:348–353. https://doi.org/10.1034/j.1399-3054.1997.990220.x
Studer AJ, Gandin A, Kolbe AR et al (2014) A limited role for carbonic anhydrase in c4 photosynthesis as revealed by a ca1ca2 double mutant in maize. Plant Physiol 165:608–617. https://doi.org/10.1104/pp.114.237602
Stutz SS, Edwards GE, Cousins AB (2014) Single-cell C4 photosynthesis: efficiency and acclimation of Bienertia sinuspersici to growth under low light. New Phytol 202:220–232. https://doi.org/10.1111/nph.12648
Sui X, Shan N, Hu L et al (2017) The complex character of photosynthesis in cucumber fruit. J Exp Bot 68:1625–1637. https://doi.org/10.1093/jxb/erx034
Sun L, Liang C, Chen Z et al (2014) Superior aluminium (Al) tolerance of Stylosanthes is achieved mainly by malate synthesis through an Al-enhanced malic enzyme, SgME1. New Phytol 202:209–219. https://doi.org/10.1111/nph.12629
Sun X, Han G, Meng Z et al (2019) Roles of malic enzymes in plant development and stress responses. Plant Signal Behav 14(10):e1644596. https://doi.org/10.1080/15592324.2019.1644596
Sunderhaus S, Dudkina NV, Jänsch L et al (2006) Carbonic anhydrase subunits form a matrix-exposed domain attached to the membrane arm of mitochondrial complex I in plants. J Biol Chem 281:6482–6488. https://doi.org/10.1074/jbc.M511542200
Taniguchi Y, Ohkawa H, Masumoto C et al (2008) Overproduction of C4 photosynthetic enzymes in transgenic rice plants: an approach to introduce the C4-like photosynthetic pathway into rice. J Exp Bot 59:1799–1809. https://doi.org/10.1093/jxb/ern016
Tanz SK, Tetu SG, Vella NGF, Ludwig M (2009) Loss of the transit peptide and an increase in gene expression of an ancestral chloroplastic carbonic anhydrase were instrumental in the evolution of the cytosolic C4 carbonic anhydrase in Flaveria. Plant Physiol 150:1515–1529. https://doi.org/10.1104/pp.109.137513
Taylor L, Nunes-Nesi A, Parsley K et al (2010) Cytosolic pyruvate, orthophosphate dikinase functions in nitrogen remobilization during leaf senescence and limits individual seed growth and nitrogen content. Plant J 62:641–652. https://doi.org/10.1111/j.1365-313X.2010.04179.x
Tesfaye M, Temple SJ, Allan DL et al (2001) Overexpression of malate dehydrogenase in transgenic alfalfa enhances organic acid synthesis and confers tolerance to aluminum. Plant Physiol 127:1836–1844. https://doi.org/10.1104/pp.010376
Teng X, Zhong M, Zhu X et al (2019) FLOURY ENDOSPERM16 encoding a NAD-dependent cytosolic malate Odehydrogenase plays an important role in starch synthesis and seed development in rice. Plant Biotechnol J 17:1914–1927. https://doi.org/10.1111/pbi.13108
Tetu SG, Tanz SK, Vella N et al (2007) The Flaveria bidentis β-carbonic anhydrase gene family encodes cytosolic and chloroplastic isoforms demonstrating distinct organ-specific expression patterns. Plant Physiol 144:1316–1327. https://doi.org/10.1104/pp.107.098152
Tomaz T, Bagard M, Pracharoenwattana I et al (2010) Mitochondrial malate dehydrogenase lowers leaf respiration and alters photorespiration and plant growth in Arabidopsis. Plant Physiol 154:1143–1157. https://doi.org/10.1104/pp.110.161612
Trejo-Téllez LI, Stenzel R, Gómez-Merino FC, Schmitt JM (2010) Transgenic tobacco plants overexpressing pyruvate phosphate dikinase increase exudation of organic acids and decrease accumulation of aluminum in the roots. Plant Soil 326:187–198. https://doi.org/10.1007/s11104-009-9994-0
Tronconi MA, Fahnenstich H, Gerrard Weehler MC et al (2008) Arabidopsis NAD-malic enzyme functions as a homodimer and heterodimer and has a major impact on nocturnal metabolism. Plant Physiol 146:1540. https://doi.org/10.1104/pp.107.114975
Tronconi MA, Andreo CS, Drincovich MF (2018) Chimeric structure of plant malic enzyme family: different evolutionary scenarios for NAD- and NADP-dependent isoforms. Front Plant Sci 9:1–15. https://doi.org/10.3389/fpls.2018.00565
Tronconi MA, Hüdig M, Schranz ME, Maurino VG (2020) Independent recruitment of duplicated β-subunit-coding NAD-ME genes aided the evolution of C4 photosynthesis in Cleomaceae. Front Plant Sci. https://doi.org/10.3389/fpls.2020.572080
Truong SK, McCormick RF, Rooney WL, Mullet JE (2015) Harnessing genetic variation in leaf angle to increase productivity of sorghum bicolor. Genetics 201:1229–1238. https://doi.org/10.1534/genetics.115.178608
Van Der Merwe MJ, Osorio S, Moritz T et al (2009) Decreased mitochondrial activities of malate dehydrogenase and fumarase in tomato lead to altered root growth and architecture via diverse mechanisms. Plant Physiol 149:653–669. https://doi.org/10.1104/pp.108.130518
von Caemmerer S, Quinn V, Hancock NC et al (2004) Carbonic anhydrase and C4 photosynthesis: a transgenic analysis. Plant Cell Environ 27:697–703. https://doi.org/10.1111/j.1365-3040.2003.01157.x
von Caemmerer S, Quick WP, Furbank RT (2012) The development of C4 rice: current progress and future challenges. Science 336:1671–1672. https://doi.org/10.1126/science.1220177
von Caemmerer S, Edwards GE, Koteyeva N, Cousins AB (2014) Single cell C4 photosynthesis in aquatic and terrestrial plants: a gas exchange perspective. Aquat Bot 118:71–80. https://doi.org/10.1016/j.aquabot.2014.05.009
Voznesenskaya EV, Franceschi VR, Kiirats O et al (2001) Kranz anatomy is not essential for terrestrial C4 plant photosynthesis. Nature 414:543–546. https://doi.org/10.1038/35107073
Voznesenskaya EV, Franceschi VR, Kiirats O et al (2002) Proof of C4 photosynthesis without Kranz anatomy in Bienertia cycloptera (Chenopodiaceae). Plant J 31:649–662. https://doi.org/10.1046/j.1365-313X.2002.01385.x
Walker RP, Acheson RM, Técsi LI, Leegood RC (1997) Phosphoenolpyruvate carboxykinase in C4 plants: its role and regulation. Aust J Plant Physiol 24:459–468. https://doi.org/10.1071/PP97007
Walker RP, Chen Z-H, Técsi LI et al (1999) Phosphoenolpyruvate carboxykinase plays a role in interactions of carbon and nitrogen metabolism during grape seed development. Planta 210:9–18. https://doi.org/10.1007/s004250050648
Wang QF, Zhao Y, Yi Q et al (2010) Overexpression of malate dehydrogenase in transgenic tobacco leaves: enhanced malate synthesis and augmented Al-resistance. Acta Physiol Plant 32:1209–1220. https://doi.org/10.1007/s11738-010-0522-x
Wang Q, Fristedt R, Yu X et al (2012) The γ-carbonic anhydrase subcomplex of mitochondrial complex I is essential for development and important for photomorphogenesis of Arabidopsis. Plant Physiol 160:1373–1383. https://doi.org/10.1104/pp.112.204339
Wang Y, Bräutigam A, Weber APM, Zhu XG (2014) Three distinct biochemical subtypes of C4 photosynthesis? A modelling analysis. J Exp Bot 65:3567–3578. https://doi.org/10.1093/jxb/eru058
Wang L, Lu Q, Wen X, Lu C (2015a) Enhanced sucrose loading improves rice yield by increasing grain size. Plant Physiol 169:2848–2862. https://doi.org/10.1104/pp.15.01170
Wang ZA, Li Q, Ge XY et al (2015b) The mitochondrial malate dehydrogenase 1 gene GhmMDH1 is involved in plant and root growth under phosphorus deficiency conditions in cotton. Sci Rep 5:10343. https://doi.org/10.1038/srep10343
Wang Z, Li H, Liu X et al (2015c) Reduction of pyruvate orthophosphate dikinase activity is associated with high temperature-induced chalkiness in rice grains. Plant Physiol Biochem 89:76–84. https://doi.org/10.1016/j.plaphy.2015.02.011
Wang QJ, Sun H, Dong QL et al (2016) The enhancement of tolerance to salt and cold stresses by modifying the redox state and salicylic acid content via the cytosolic malate dehydrogenase gene in transgenic apple plants. Plant Biotechnol J 14:1986–1997. https://doi.org/10.1111/pbi.12556
Wang H, Ham TH, Im DE et al (2020) A new SNP in rice gene encoding pyruvate phosphate dikinase (PPDK) associated with floury endosperm. Genes (Basel) 11:465. https://doi.org/10.3390/genes11040465
Watson-Lazowski A, Papanicolaou A, Sharwood R, Ghannoum O (2018) Investigating the NAD-ME biochemical pathway within C4 grasses using transcript and amino acid variation in C4 photosynthetic genes. Photosynth Res 138:233–248. https://doi.org/10.1007/s11120-018-0569-x
Weber APM, Bar-Even A (2019) Update: improving the efficiency of photosynthetic carbon reactions. Plant Physiol 179:803–812. https://doi.org/10.1104/pp.18.01521
Weichert H, Högy P, Mora-Ramirez I et al (2017) Grain yield and quality responses of wheat expressing a barley sucrose transporter to combined climate change factors. J Exp Bot 68:5511–5525. https://doi.org/10.1093/jxb/erx366
Wienkoop S, Zoeller D, Ebert B et al (2004) Cell-specific protein profiling in Arabidopsis thaliana trichomes: identification of trichome-located proteins involved in sulfur metabolism and detoxification. Phytochemistry 65:1641–1649. https://doi.org/10.1016/j.phytochem.2004.03.026
Williams TG, Flanagan LB, Coleman JR (1996) Photosynthetic gas exchange and discrimination against 13CO2 and C18O16O in tobacco plants modified by an antisense construct to have low chloroplastic carbonic anhydrase. Plant Physiol 112:319–326. https://doi.org/10.1104/pp.112.1.319
Williams BP, Burgess SJ, Reyna-Llorens I et al (2016) An Untranslated cis -element regulates the accumulation of multiple C 4 enzymes in Gynandropsis gynandra mesophyll cells. Plant Cell 28:454–465. https://doi.org/10.1105/tpc.15.00570
Yadav S, Mishra A, Jha B (2018) Elevated CO2 leads to carbon sequestration by modulating C4 photosynthesis pathway enzyme (PPDK) in Suaeda monoica and S. fruticosa. J Photochem Photobiol B Biol 178:310–315. https://doi.org/10.1016/j.jphotobiol.2017.11.022
Yadav S, Mishra A (2020) Ectopic expression of C4 photosynthetic pathway genes improves carbon assimilation and alleviate stress tolerance for future climate change. Physiol Mol Biol Plants 26:195–209. https://doi.org/10.1007/s12298-019-00751-8
Yadav S, Rathore MS, Mishra A (2020) The pyruvate-phosphate dikinase (C4-SmPPDK) gene from suaeda monoica enhances photosynthesis, carbon assimilation, and abiotic stress tolerance in a C3 plant under elevated CO2 conditions. Front Plant Sci. https://doi.org/10.3389/fpls.2020.00345
Yamamoto N, Kubota T, Masumura T et al (2014) Molecular cloning, gene expression and functional expression of a phosphoenolpyruvate carboxylase Osppc1 in developing rice seeds: implication of involvement in nitrogen accumulation. Seed Sci Res 24:23–36. https://doi.org/10.1017/S0960258513000354
Yamamoto N, Kinoshita Y, Sugimoto T, Masumura T (2017) Role of nitrogen-responsive plant-type phosphoenolpyruvate carboxylase in the accumulation of seed storage protein in ancient wheat (spelt and kamut). Soil Sci Plant Nutr 63:23–28. https://doi.org/10.1080/00380768.2016.1275039
Yamamoto N, Sugimoto T, Takano T et al (2020) The plant-type phosphoenolpyruvate carboxylase Gmppc2 is developmentally induced in immature soy seeds at the late maturation stage: a potential protein biomarker for seed chemical composition. Biosci Biotechnol Biochem 84:552–562. https://doi.org/10.1080/09168451.2019.1696179
Yao Y-X, Dong Q-L, Zhai H et al (2011) The functions of an apple cytosolic malate dehydrogenase gene in growth and tolerance to cold and salt stresses. Plant Physiol Biochem 49:257–264. https://doi.org/10.1016/j.plaphy.2010.12.009
Yazdanpanah F, Maurino VG, Mettler-Altmann T et al (2019) NADP-MALIC ENZYME 1 affects germination after seed storage in Arabidopsis thaliana. Plant Cell Physiol 60:318–328. https://doi.org/10.1093/pcp/pcy213
Yokochi Y, Yoshida K, Hahn F et al (2021) Redox regulation of NADP-malate dehydrogenase is vital for land plants under fluctuating light environment. Proc Natl Acad Sci USA 118(6):e2016903118. https://doi.org/10.1073/pnas.2016903118
You L, Zhang J, Li L et al (2020) Involvement of abscisic acid, ABI5, and PPC2 in plant acclimation to low CO2. J Exp Bot 71:4093–4108. https://doi.org/10.1093/jxb/eraa148
Yu S, Zhang X, Guan Q et al (2007) Expression of a carbonic anhydrase gene is induced by environmental stresses in Rice (Oryza sativa L.). Biotechnol Lett 29:89–94. https://doi.org/10.1007/s10529-006-9199-z
Zabaleta E, Martin MV, Braun H-P (2012) A basal carbon concentrating mechanism in plants? Plant Sci 187:97–104. https://doi.org/10.1016/j.plantsci.2012.02.001
Zamani-Nour S, Lin HC, Walker BJ et al (2021) Overexpression of the chloroplastic 2-oxoglutarate/malate transporter disturbs carbon and nitrogen homeostasis in rice. J Exp Bot 72:137–152. https://doi.org/10.1093/jxb/eraa343
Zhang HF, Xu WG, Wang HW et al (2014) Pyramiding expression of maize genes encoding phosphoenolpyruvate carboxylase (PEPC) and pyruvate orthophosphate dikinase (PPDK) synergistically improve the photosynthetic characteristics of transgenic wheat. Protoplasma 251:1163–1173. https://doi.org/10.1007/s00709-014-0624-1
Zhang Y, Giuliani R, Zhang Y et al (2018a) Characterization of maize leaf pyruvate orthophosphate dikinase using high throughput sequencing. J Integr Plant Biol 60:670–690. https://doi.org/10.1111/jipb.12656
Zhang YH, Wang EM, Zhao TF et al (2018b) Characteristics of chlorophyll fluorescence and antioxidant-oxidant balance in PEPC and PPDK transgenic rice under aluminum stress. Russ J Plant Physiol 65:49–56. https://doi.org/10.1134/S1021443718010211
Zhang X, Pu P, Tang Y et al (2019) C4 photosynthetic enzymes play a key role in wheat spike bracts primary carbon metabolism response under water deficit. Plant Physiol Biochem 142:163–172. https://doi.org/10.1016/j.plaphy.2019.06.013
Zhang Q, Li Y, Xu W et al (2021a) Joint expression of Zmpepc, Zmppdk, and Zmnadp-me is more efficient than expression of one or two of those genes in improving the photosynthesis of Arabidopsis. Plant Physiol Biochem 158:410–419. https://doi.org/10.1016/j.plaphy.2020.11.030
Zhang Q, Qi X, Xu W et al (2021b) Response of transgenic Arabidopsis expressing maize C4 photosynthetic enzyme genes to high light. Plant Signal Behav. https://doi.org/10.1080/15592324.2021.1885894
Zhou H, Liu SK, Yang CP (2011) Over-expression of a NAD-malic enzyme gene from rice in Arabidopsis thaliana confers tolerances to several abiotic stresses. Adv Mater Res 393:863–866. https://doi.org/10.4028/www.scientific.net/AMR.393-395.863
Zhou Y, Yang Z, Xu Y et al (2018) Soybean NADP-malic enzyme functions in malate and citrate metabolism and contributes to their efflux under Al stress. Front Plant Sci 8:2246. https://doi.org/10.3389/fpls.2017.02246
Zhu S, Chen Z, Xie B et al (2021) A phosphate starvation responsive malate dehydrogenase, GmMDH12 mediates malate synthesis and nodule size in soybean (Glycine max). Environ Exp Bot. https://doi.org/10.1016/j.envexpbot.2021.104560
Acknowledgements
This work was supported by research Grants No. DST-SERB-EMR/2016/004976 and BT/PR11896/BPA/118/3/2014 from the Govt. of India to BCT. Jitender Singh acknowledges the CSIR-SRA fellowship no. 13(9101-A)/2019-pool, from Government of India. The authors are also thankful to International Centre for Genetic Engineering and Biotechnology (ICGEB) and National Institute of Plant Genome Research (NIPGR), New Delhi for administrative support. The authors sincerely thank Prof. Govindjee, Department of Plant Biology, University of Illinois at Urbana-Champaign, USA for critical reading and technical editing of the manuscript.
Author information
Authors and Affiliations
Contributions
JS, JKT, and BCT: conceptualized the idea. JS, BCT, JKT, SG, and SD wrote the manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Singh, J., Garai, S., Das, S. et al. Role of C4 photosynthetic enzyme isoforms in C3 plants and their potential applications in improving agronomic traits in crops. Photosynth Res 154, 233–258 (2022). https://doi.org/10.1007/s11120-022-00978-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11120-022-00978-9