Overexpression of chloroplastic Zea mays NADP-malic enzyme (ZmNADP-ME) confers tolerance to salt stress in Arabidopsis thaliana.
Abiotic stress
C3 photosynthesis
C4 photosnthesis
Malic enzyme
Oxidative stress
Salt stress
Journal
Photosynthesis research
ISSN: 1573-5079
Titre abrégé: Photosynth Res
Pays: Netherlands
ID NLM: 100954728
Informations de publication
Date de publication:
Oct 2023
Oct 2023
Historique:
received:
07
10
2022
accepted:
29
07
2023
medline:
6
10
2023
pubmed:
10
8
2023
entrez:
10
8
2023
Statut:
ppublish
Résumé
The C4 plants photosynthesize better than C3 plants especially in arid environment. As an attempt to genetically convert C3 plant to C4, the cDNA of decarboxylating C4 type NADP-malic enzyme from Zea mays (ZmNADP-ME) that has lower Km for malate and NADP than its C3 isoforms, was overexpressed in Arabidopsis thaliana under the control of 35S promoter. Due to increased activity of NADP-ME in the transgenics the malate decarboxylation increased that resulted in loss of carbon skeletons needed for amino acid and protein synthesis. Consequently, amino acid and protein content of the transgenics declined. Therefore, the Chl content, photosynthetic efficiency (Fv/Fm), electron transport rate (ETR), the quantum yield of photosynthetic CO
Identifiants
pubmed: 37561272
doi: 10.1007/s11120-023-01041-x
pii: 10.1007/s11120-023-01041-x
doi:
Substances chimiques
malate dehydrogenase (oxaloacetate-decarboxylating) (NADP+)
EC 1.1.1.40
malic acid
817L1N4CKP
Malates
0
Hydrogen Peroxide
BBX060AN9V
NADP
53-59-8
Malate Dehydrogenase
EC 1.1.1.37
Amino Acids
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
57-76Subventions
Organisme : D. S. Kothari Post-Doctoral Fellowship
ID : BL/19-20/0157
Organisme : Science & Engineering Research Board, India
ID : EMR/2016/004976
Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer Nature B.V.
Références
Akram NA, Ashraf M (2011) Improvement in growth, chlorophyll pigments and photosynthetic performance in salt-stressed plants of sunflower (Helianthus animus L.) by foliar application of 5-aminolevulinic acid. Agrochimica 55:94–104
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
doi: 10.1007/s11120-013-9839-9
pubmed: 23649167
Aragao MEFD, Jolivet Y, Lima MGS, Dizengremel DFDM (1997) NaCl-induced changes of NAD(P) malic enzyme activities in Eucalyptus citriodora leaves. Trees Struct Funct 12:66–72. https://doi.org/10.1007/s004680050123
doi: 10.1007/s004680050123
Asada K (1999) The water–water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639. https://doi.org/10.1146/annurev.arplant.50.1.601
doi: 10.1146/annurev.arplant.50.1.601
pubmed: 15012221
Asai N, Nakajima N, Tamaoki M et al (2000) Role of malate synthesis mediated by phosphoenolpyruvate carboxylase in guard cells in the regulation of stomatal movement. Plant Cell Physiol 41:10–15
pubmed: 10750703
doi: 10.1093/pcp/41.1.10
Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113. https://doi.org/10.1146/annurev.arplant.59.032607.092759
doi: 10.1146/annurev.arplant.59.032607.092759
pubmed: 18444897
Badia MB, Mans R, Lis AV, Tronconi MA, Arias CL, Maurino VG, Andreo CS, Drincovich MF, van Maris AJ, Gerrard Wheeler MC (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
doi: 10.1111/febs.14013
pubmed: 28075062
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39(1):205–207
doi: 10.1007/BF00018060
Björkman O, Demmig B (1987) Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins. Planta 170:489–504. https://doi.org/10.1007/BF00402983
doi: 10.1007/BF00402983
pubmed: 24233012
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
pubmed: 942051
doi: 10.1016/0003-2697(76)90527-3
Bräutigam A, Schliesky S, Külahoglu C et al (2014) Towards an integrative model of C4 photosynthetic subtypes: insights from comparative transcriptome analysis of NAD-ME, NADP-ME, and PEP-CK C4 species. J Exp Bot 65:3579. https://doi.org/10.1093/JXB/ERU100
doi: 10.1093/JXB/ERU100
pubmed: 24642845
pmcid: 4085959
Brown NJ, Palmer BG, Stanley S, Hajaji H, Janacek SH, Astley HM, Parsley K, Kajala K, Quick WP, Trenkamp S, Fernie AR (2010) 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(1):122–133
pubmed: 19807880
doi: 10.1111/j.1365-313X.2009.04040.x
Cao J, Govindjee (1990) Chlorophyll a fluorescence transient as an indicator of active and inactive photosystem II in thylakoid membranes. Biochim Biophys Acta 1015:180–188
pubmed: 2404518
doi: 10.1016/0005-2728(90)90018-Y
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
doi: 10.1093/Oxfordjournals.pcp.A029253
Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103:551–560
pubmed: 18662937
doi: 10.1093/aob/mcn125
Chen FF, Chien CY, Cho CC et al (2019a) C-terminal redox domain of Arabidopsis APR1 is a non-canonical thioredoxin domain with glutaredoxin function. Antioxidants. https://doi.org/10.3390/ANTIOX8100461
doi: 10.3390/ANTIOX8100461
pubmed: 31906147
pmcid: 7022523
Chen FF, Chien CY, Cho CC, Chang YY, Hsu CH (2019b) C-terminal redox domain of Arabidopsis APR1 is a non-canonical thioredoxin domain with glutaredoxin function. Antioxidants (basel) 8(10):461
pubmed: 31597378
pmcid: 6827007
doi: 10.3390/antiox8100461
Chen Q, Wang B, Ding H et al (2019c) Review: The role of NADP-malic enzyme in plants under stress. Plant Sci 281:206–212
pubmed: 30824053
doi: 10.1016/j.plantsci.2019.01.010
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
doi: 10.1007/s10529-007-9347-0
pubmed: 17516134
Chi W, Zhou JS, Zhang F, Wu NH (2004) Photosynthetic features of transgenic rice expressing sorghum C-4 type NADP-ME. Acta Bot Sin 46(7):873–882
Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16(6):735–743
pubmed: 10069079
doi: 10.1046/j.1365-313x.1998.00343.x
Daloso DM, Medeiros DB, Dos Anjos L, Yoshida T, Araújo WL, Fernie AR (2017) Metabolism within the specialized guard cells of plants. New Phytol 216(4):1018–1033
pubmed: 28984366
doi: 10.1111/nph.14823
Das K, Roychoudhury A (2014) Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Front Environ Sci 2:1–13. https://doi.org/10.3389/fenvs.2014.00053
doi: 10.3389/fenvs.2014.00053
Delauney AJ, Verma DPS (1993) Proline biosynthesis and osmoregulation in plants. Plant J 4:215–223. https://doi.org/10.1046/j.1365-313X.1993.04020215.x
doi: 10.1046/j.1365-313X.1993.04020215.x
Demmig B, Garab G, Adams W III, Govindjee (eds) (2014) Non photochemical quenching and energy dissipation in plants, algae and cyanobacteria. Advances in photosynthesis and respiration, vol 40. Springer, Dordrecht
Demmig B, Winter K, Kruger A, Czygan FC (1987) Photoinhibition and zeaxanthin formation in intact leaves : a possible role of the xanthophyll cycle in the dissipation of excess light energy. Plant Physiol 84:218–224
pubmed: 16665420
pmcid: 1056560
doi: 10.1104/pp.84.2.218
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
doi: 10.1007/s11103-008-9375-8
pubmed: 18622731
Drincovich MF, Casati P, Andreo CS (2001) NADP-malic enzyme from plants: a ubiquitous enzyme involved in different metabolic pathways. FEBS Lett 490:1–6
pubmed: 11172800
doi: 10.1016/S0014-5793(00)02331-0
Doubnerová HV, Miedzińska L, Dobrá J, Vankova R, Ryšlavá H (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
doi: 10.1016/j.jplph.2013.10.017
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
doi: 10.1016/j.plantsci.2010.12.005
pubmed: 21421406
Dutta S, Mohanty S, Tripathy BC (2009) Role of temperature stress on chloroplast biogenesis and protein import in pea. Plant Physiol 150:1050–1061
pubmed: 19403728
pmcid: 2689951
doi: 10.1104/pp.109.137265
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
doi: 10.1104/pp.114.3.851
pubmed: 12223747
pmcid: 158371
Emami P, Razi H, Dastfal M (2016) Effect of salt stress on NADP-malic enzyme activity, proline and ionic contents of durum wheat genotypes. Biol Forum Int J 8(2):112–119
Ermakova M, Arrivault S, Giuliani R, Danila F, Alonso-Cantabrana H, Vlad D, Ishihara H, Feil R, Guenther M, Borghi GL, Covshoff S (2021) Installation of C4 photosynthetic pathway enzymes in rice using a single construct. Plant Biotechnol J 19(3):575–588
pubmed: 33016576
doi: 10.1111/pbi.13487
Fahnenstich H, Saigo M, Niessen M et al (2007) Alteration of organic acid metabolism in Arabidopsis overexpressing the maize C4 NADP-malic enzyme causes accelerated senescence during extended darkness. Plant Physiol 145:640–652. https://doi.org/10.1104/pp.107.104455
doi: 10.1104/pp.107.104455
pubmed: 17885087
pmcid: 2048770
Fu ZY, Bin ZZ, Hu XJ et al (2009) Cloning, identification, expression analysis and phylogenetic relevance of two NADP-dependent malic enzyme genes from hexaploid wheat. C R Biol 332(7):591–602. https://doi.org/10.1016/j.crvi.2009.03.002
doi: 10.1016/j.crvi.2009.03.002
pubmed: 19523599
Fu ZY, Zhang ZB, Liu ZH et al (2011) The effects of abiotic stresses on the NADP-dependent malic enzyme in the leaves of the hexaploid wheat. Biol Plant 55:196–200. https://doi.org/10.1007/s10535-011-0030-x
doi: 10.1007/s10535-011-0030-x
Furbank RT, Hatch MD (1987) Mechanism of C
pubmed: 16665838
pmcid: 1054376
doi: 10.1104/pp.85.4.958
Fushimi T, Umeda M, Shimazaki T et al (1994) Nucleotide sequence of a rice cDNA similar to a maize NADP-dependent malic enzyme. Plant Mol Biol 24:965–967. https://doi.org/10.1007/BF00014450
doi: 10.1007/BF00014450
pubmed: 8204833
Gegenheimer P (1990) Preparation of extracts from plants. Methods Enzymol 182:174–193
pubmed: 2314235
doi: 10.1016/0076-6879(90)82016-U
Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta Gen Subj 990:87–92
doi: 10.1016/S0304-4165(89)80016-9
Gerald EE, Carlos SA (1992) NADP-malic enzyme from plants. Phytochemistry 31:1845–1857. https://doi.org/10.1016/0031-9422(92)80322-6
doi: 10.1016/0031-9422(92)80322-6
Gharsallah C, Fakhfakh H, Grubb D, Gorsane F (2016) Effect of salt stress on ion concentration, proline content, antioxidant enzyme activities and gene expression in tomato cultivars. AoB Plants. https://doi.org/10.1093/aobpla/plw055
doi: 10.1093/aobpla/plw055
pubmed: 27543452
pmcid: 5091694
Goss T, Hanke G (2014) The end of the line: can ferredoxin and ferredoxin NADP(H) oxidoreductase determine the fate of photosynthetic electrons? Curr Protein Pept Sci 15:385–393. https://doi.org/10.2174/1389203715666140327113733
doi: 10.2174/1389203715666140327113733
pubmed: 24678667
pmcid: 4030315
Govindjee, Amesz J, Fork DC (eds) (1986) Light emission by plants and bacteria. Academic Press Inc., Orlando
Govindjee (1995) Sixty-three years since Kautsky: chlorophyll a fluorescence. Aust J Plant Physiol 22:131–160. https://doi.org/10.1071/PP9950131
doi: 10.1071/PP9950131
Gu JF, Qiu M, Yang JC (2013) Enhanced tolerance to drought in transgenic rice plants overexpressing C4 photosynthesis enzymes. Crop J 1(2):105–114
doi: 10.1016/j.cj.2013.10.002
Guidi L, Lo Piccolo E, Landi M (2019) Chlorophyll fluorescence, photoinhibition and abiotic stress: does it make any difference the fact to be a C3 or C4 species? Front in Plant Sci 14(10):174
doi: 10.3389/fpls.2019.00174
Guo P, Baum M, Grando S et al (2009) Differentially expressed genes between drought-tolerant and drought-sensitive barley genotypes in response to drought stress during the reproductive stage. J Exp Bot 60:3531–3544. https://doi.org/10.1093/jxb/erp194
doi: 10.1093/jxb/erp194
pubmed: 19561048
pmcid: 2724701
Hare PD, Cress WA, Van Staden J (1999) Proline synthesis and degradation: a model system for elucidating stress-related signal transduction. J Exp Bot 50:413–434
Hatch M (1987) C4 Photosynthesis: a unique blend of modified biochemistry, anatomy abd ultrastructure. Biochim Biophys Acta 895:81–106. https://doi.org/10.1016/0003-9861(88)90351-7
doi: 10.1016/0003-9861(88)90351-7
Hayat S, Hayat Q, Alyemeni MN et al (2012) Role of proline under changing environments: a review. Plant Signal Behav 7:1456–1466. https://doi.org/10.4161/psb.21949
doi: 10.4161/psb.21949
pubmed: 22951402
pmcid: 3548871
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
doi: 10.1016/J.PBI.2007.11.002
pubmed: 18203653
Hodges DM, DeLong JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207(4):604–611
doi: 10.1007/s004250050524
Huang H, Ullah F, Zhou DX et al (2019) Mechanisms of ROS regulation of plant development and stress responses. Front Plant Sci 10:1–10. https://doi.org/10.3389/fpls.2019.00800
doi: 10.3389/fpls.2019.00800
Jiang CD, Wang X, Gao HY, Lei S, Chow WS (2011) Systemic regulation of leaf anatomical structure, photosynthetic performance, and highlight tolerance in sorghum. Plant Physiol 155:1416–1424
pubmed: 21245193
pmcid: 3046595
doi: 10.1104/pp.111.172213
Jiang B, Ouyang N, Sun X, Tan Y, Sun Z, Yu D, Xin S, Duan M, Yuan D (2018) Under drought stress, the protective capability of photosynthetic apparatus of transgenic PEPC+PPDK rice was enhanced. MPB 16:798–806
Jilani A, Kar S, Bose S, Tripathy BC (1996) Regulation of the carotenoid content and chloroplast development by levulinic acid. Physiol Plant 96:139–145. https://doi.org/10.1111/j.1399-3054.1996.tb00194.x
doi: 10.1111/j.1399-3054.1996.tb00194.x
Kalemba EM, Alipour S, Wojciechowska N, Omaye S (2021) NAD(P)H drives the ascorbate-glutathione cycle and abundance of catalase in developing beech seeds differently in embryonic axes and cotyledons. Antioxidants. https://doi.org/10.3390/antiox10122021
doi: 10.3390/antiox10122021
pubmed: 34943124
pmcid: 8698623
Kanai R, Edwards G (1999) The biochemistry of C4 photosynthesis. In: Sage RF, Monson RK (eds) C4 plant biology. Physiological ecology series. Academic Press, San Diego, pp 49–87
Kandoi D, Mohanty S, Govindjee, Tripathy BC (2016) Towards efficient photosynthesis: overexpression of Zea mays phosphenolpyruvate carboxylase in Arabidopsis thaliana. Photosynth Res 130(1–3):47–72. https://doi.org/10.1007/s11120-016-0224-3
doi: 10.1007/s11120-016-0224-3
pubmed: 26897549
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
doi: 10.1007/S00709-017-1168-Y
pubmed: 28942523
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(8):1518–1527. https://doi.org/10.1111/pbi.13830
doi: 10.1111/pbi.13830
pubmed: 35467074
pmcid: 9342616
Karnovsky MJ (1965) A formaldehyde-glutaraldehyde fixative of high osmolality for use in electron microscopy. J Cell Biol 27:137–138
Krause GH, Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basics. Annu Rev Plant Physiol Plant Mol Biol 42:313–349
doi: 10.1146/annurev.pp.42.060191.001525
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
doi: 10.1104/pp.010449
pubmed: 11788759
pmcid: 148956
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
doi: 10.1104/pp.010448
pubmed: 11788758
pmcid: 148954
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(369):699–705. https://doi.org/10.1093/jexbot/53.369.699
doi: 10.1093/jexbot/53.369.699
pubmed: 11886890
Li X, Zhang C, Dai C, Zhou J, Ren C, Zhang J (2017) Phosphoenolpyruvate carboxylase regulation in C4-PEPC-expressing transgenic rice during early responses to drought stress. Physiol Plant 159(2):178–200
pubmed: 27592839
doi: 10.1111/ppl.12506
Lee M, Choi Y, Burla B, Kim Y-Y, Jeon B, Maeshima M, Yoo J-Y, Martinoia E, Lee Y (2008) The ABC transporter AtABCB14 is a malate importer and modulates stomatal response to CO
pubmed: 18776898
doi: 10.1038/ncb1782
Lin H, Arrivault S, Coe RA, Karki S, Covshoff S, Bagunu E, Lunn JE, Stitt M, Furbank RT, Hibberd JM, Quick WP (2020) A partial C4 photosynthetic biochemical pathway in rice. Front Plant Sci 11:564463
pubmed: 33178234
pmcid: 7593541
doi: 10.3389/fpls.2020.564463
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. https://doi.org/10.1007/s11103-007-9133-3
doi: 10.1007/s11103-007-9133-3
pubmed: 17245561
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2
pubmed: 11846609
doi: 10.1006/meth.2001.1262
Madan S, Nainawatee HS, Jain RK, Chowdhury JB (1995) Proline and proline metabolising enzymes in in-vitro selected NaCl-tolerant Brassica juncea L. under salt stress. Ann Bot 76:51–57. https://doi.org/10.1006/anbo.1995.1077
doi: 10.1006/anbo.1995.1077
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
doi: 10.1093/jxb/err024
pubmed: 21459769
Medeiros DB, Martins SC, Cavalcanti JHF, Daloso D, Martinoia E, Nunes-Nesi A, DaMatta F, Fernie AR, Araujo W (2016) Enhanced photosynthesis and growth in atquac1 knockout mutants are due to altered organic acid accumulation and an increase in both stomatal and mesophyll conductance. Plant Physiol 170:86–101
pubmed: 26542441
doi: 10.1104/pp.15.01053
Mittova V, Theodoulou FL, Kiddle G, Gómez L, Volokita M, Tal M, Foyer CH, Guy M (2003) Coordinate induction of glutathione biosynthesis and glutathione-metabolizing enzymes is correlated with salt tolerance in tomato. FEBS Lett 554(3):417–421. https://doi.org/10.1016/S0014-5793(03)01214-6
doi: 10.1016/S0014-5793(03)01214-6
pubmed: 14623104
Müller P, Li XP, Niyogi KK (2001) Non-photochemical quenching: a response to excess light energy. Plant Physiol 125:1558–1566
pubmed: 11299337
pmcid: 1539381
doi: 10.1104/pp.125.4.1558
Müller GL, Lara MV, Oitaven P et al (2018) Improved water use efficiency and shorter life cycle of Nicotiana tabacum due to modification of guard and vascular companion cells. Sci Rep 8:4380. https://doi.org/10.1038/s41598-018-22431-5
doi: 10.1038/s41598-018-22431-5
pubmed: 29531244
pmcid: 5847574
Nascimento E, Silva D, Ribeiro RV et al (2011) Salt stress induced damages on the photosynthesis of physic nut young plants. Sci Agric 68:62–68. https://doi.org/10.1590/S0103-90162011000100010
doi: 10.1590/S0103-90162011000100010
Netondo GW, Onyango JC, Beck E (2004) Sorghum and salinity. Crop Sci 44:806–811. https://doi.org/10.2135/CROPSCI2004.8060
doi: 10.2135/CROPSCI2004.8060
Nellaepalli S, Kodru S, Tirupathi M, Subramanyam R (2012) Anaerobiosis induced state transition: a non photochemical reduction of PQ pool mediated by NDH in Arabidopsis thaliana. PLoS ONE 11:e49839
doi: 10.1371/journal.pone.0049839
Neubauer C, Schreiber U (1987) The polyphasic rise of chlorophyll fluorescence upon onset of strong continuous illumination: I. Saturation characteristics and partial control by the photosystem II acceptor side. Zeitschrift Für Naturforschung C 42:1246–1254
doi: 10.1515/znc-1987-11-1217
Nguyen HT, Leipner J, Stamp P, Guerra-Peraza O (2009) Low temperature stress in maize (Zea mays L.) induces genes involved in photosynthesis and signal transduction as studied by suppression subtractive hybridization. Plant Physiol Biochem 47:116–122. https://doi.org/10.1016/j.plaphy.2008.10.010
doi: 10.1016/j.plaphy.2008.10.010
pubmed: 19042136
Nickrent DL (1994) From field to film: rapid sequencing methods for field-collected plant species. Biotechniques 16(3):470–475
pubmed: 8185922
Niyogi KK (1999) Photoprotection revisited: genetic and molecular approaches. Annu Rev Plant Physiol Plant Mol Biol 50:333–359
pubmed: 15012213
doi: 10.1146/annurev.arplant.50.1.333
Padhi B, Chauhan G, Kandoi D, Stirbet A, Tripathy BC, Govindjee G (2021) A comparison of chlorophyll fluorescence transient measurements, using Handy PEA and FluorPen fluorometers. Photosynthetica 59:399–408. https://doi.org/10.32615/ps.2021.026
doi: 10.32615/ps.2021.026
Papageorgiou GC, Govindjee (eds) (2004) Chlorophyll A fluorescence: a signature of photosynthesis. Advances in photosynthesis and respiration, vol 19. Springer, Dordrecht
Pattanayak GK, Tripathy BC (2002) Catalytic function of a novel protein protochlorophyllide oxidoreductase C of Arabidopsis thaliana. Biochem Biophys Res Commun 291(4):921–924
pubmed: 11866453
doi: 10.1006/bbrc.2002.6543
Pattanayak GK, Biswal AK, Reddy VS, Tripathy BC (2005) Light dependent regulation of chlorophyll b biosynthesis in chlorophyllide a oxygenase overexpressing tobacco plants. Biochem Biophys Res Commun 326(2):466–471
pubmed: 15582600
doi: 10.1016/j.bbrc.2004.11.049
Pérez-Arellano I, Carmona-Alvarez F, Martínez AI, Rodríguez-Díaz J, Cervera J (2010) Pyrroline-5-carboxylate synthase and proline biosynthesis: from osmotolerance to rare metabolic disease. Protein Sci 19(3):372–382
pubmed: 20091669
pmcid: 2866264
doi: 10.1002/pro.340
Pinto ME, Casati P, Hsu T-P et al (1999) Effects of UV-B radiation on growth, photosynthesis, UV-B-absorbing compounds and NADP-malic enzyme in bean (Phaseolus vulgaris L.) grown under different nitrogen conditions. J Photochem Photobiol B Biol 48:200–209. https://doi.org/10.1016/S1011-1344(99)00031-7
doi: 10.1016/S1011-1344(99)00031-7
Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous-equations for assaying chlorophyll-a and chlorophyll-B extracted with 4 different solvents—verification of the concentration of chlorophyll standards by atomic-absorption spectroscopy. Biochim Biophys Acta 975:384–394. https://doi.org/10.1016/S0005-2728(89)80347-0
doi: 10.1016/S0005-2728(89)80347-0
Putter J (1974) Peroxidase. In: Bergmeyer HU (ed) Methods of enzymatic analysis. Verlag Chemie, Weinhan, pp 685–690
doi: 10.1016/B978-0-12-091302-2.50033-5
Qi X, Xu W, Zhang J, Guo R, Zhao M, Hu L, Li Y (2017) Physiological characteristics and metabolomics of transgenic wheat containing the maize C4 phosphoenolpyruvate carboxylase (PEPC) gene under high temperature stress. Protoplasma 254(2):1017–1030
pubmed: 27491550
doi: 10.1007/s00709-016-1010-y
Qureshi MI, Abdin MZ, Ahmad J, Iqbal M (2013) Effect of long-term salinity on cellular antioxidants, compatible solute and fatty acid profile of Sweet Annie (Artemisia annua L.). Phytochemistry 95:215–223
pubmed: 23871298
doi: 10.1016/j.phytochem.2013.06.026
Ruban AV, Murchie EH (2012) Assessing the photoprotective effectiveness of non-photochemical chlorophyll fluorescence quenching: a new approach. Biochim Biophys Acta 1817:977–982
pubmed: 22503831
doi: 10.1016/j.bbabio.2012.03.026
Sage RF (2004) The evolution of C4 photosynthesis. New Phytol 161:341–370
pubmed: 33873498
doi: 10.1111/j.1469-8137.2004.00974.x
Sage RF, Sage TL, Kocacinar F (2012) Photorespiration and the evolution of C4 photosynthesis. Annu Rev Plant Biol 63:19–47
pubmed: 22404472
doi: 10.1146/annurev-arplant-042811-105511
Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, New York
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
doi: 10.1104/pp.108.3.949
pubmed: 12228518
pmcid: 157444
Schansker G, Strasser RJ (2005) Quantification of non-QB-reducing centers in leaves using a far-red pre-illumination. Photosynth Res 84:145–151. https://doi.org/10.1007/s11120-004-7156-z
doi: 10.1007/s11120-004-7156-z
pubmed: 16049767
Schreiber U (2004) Pulse-amplitude-modulation (PAM) fluorometry and saturation pulse method: an overview. In: Papageorgiou GC, Govindjee (eds) Chlorophyll a fluorescence: a signature of photosynthesis. Advances in photosynthesis and respiration, vol 19. Springer, Dordrecht, pp 279–319
doi: 10.1007/978-1-4020-3218-9_11
Schreiber U, Armond P (1978) Heat-induced changes of chlorophyll fluorescence in isolated chloroplasts and related heat-damage at the pigment level. Biochim Biophys Acta 502:138–151
pubmed: 638138
doi: 10.1016/0005-2728(78)90138-X
Schreiber U, Bilger W, Neubauer C (1995) Chlorophyll fluorescence as a nonintrusive indicator for rapid assessment of in vivo photosynthesis. In: Schulze E-D, Caldwell M (eds) Ecophysiology of photosynthesis, Springer Study edn, vol 100. Springer, Berlin, pp 49–70
doi: 10.1007/978-3-642-79354-7_3
Shao H, Liu Z, Zhang Z, Chen Q, Chu L, Brestic M (2011) Biological roles of crop NADP-malic enzymes and molecular mechanisms involved in abiotic stress. Afr J Biotech 25:4947–4953
Shi Q, Sun H, Timm S, Zhang S, Huang W (2022) Photorespiration alleviates photoinhibition of photosystem I under fluctuating light in tomato. Plants (basel) 11(2):195. https://doi.org/10.3390/plants11020195
doi: 10.3390/plants11020195
pubmed: 35050082
Sicher R, Bunce J, Barnaby J, Bailey B (2015) Water-deficiency effects on single leaf gas exchange and on C4 pathway enzymes of maize genotypes with differing abiotic stress tolerance. Photosynthetica 53:3–10. https://doi.org/10.1007/s11099-015-0074-9
doi: 10.1007/s11099-015-0074-9
Singh J, Garai S, Das S, Thakur JK, Tripathy BC (2022) Role of C4 photosynthetic enzyme isoforms in C3 plants and their potential applications in improving agronomic traits in crops. Photosynth Res 154(3):233–258
pubmed: 36309625
doi: 10.1007/s11120-022-00978-9
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
doi: 10.1104/pp.98.4.1233
pubmed: 16668781
pmcid: 1080338
Speer M, Kaiser WM (1991) Ion Relations of symplastic and apoplastic space in leaves from Spinacia oleracea L. and Pisum sativum L. under salinity. Plant Physiol 97:990–997. https://doi.org/10.1104/PP.97.3.990
doi: 10.1104/PP.97.3.990
pubmed: 16668541
pmcid: 1081114
Sun X, Han G, Meng Z et al (2019) Roles of malic enzymes in plant development and stress responses. Plant Signal Behav 14:10. https://doi.org/10.1080/15592324.2019.1644596
doi: 10.1080/15592324.2019.1644596
Swain A, Behera D, Karmakar S et al (2021) Morphophysiological alterations in transgenic rice lines expressing PPDK and ME genes from the C4 model Setaria italica. J Plant Physiol. https://doi.org/10.1016/j.jplph.2021.153482
doi: 10.1016/j.jplph.2021.153482
pubmed: 34330009
Szabados L, Savouré A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15:89–97. https://doi.org/10.1016/J.TPLANTS.2009.11.009
doi: 10.1016/J.TPLANTS.2009.11.009
pubmed: 20036181
Takeuchi Y, Akagi H, Kamasawa N et al (2000) Aberrant chloroplasts in transgenic rice plants expressing a high level of maize NADP-dependent malic enzyme. Planta 211:265–274
pubmed: 10945221
doi: 10.1007/s004250000282
Tsuchida H, Tamai T, Fukayama H et al (2001) High level expression of C4-specific NADP-malic enzyme in leaves and impairment of photoautotrophic growth in a C3 plant, rice. Plant Cell Physiol 42:138–145. https://doi.org/10.1093/pcp/pce013
doi: 10.1093/pcp/pce013
pubmed: 11230567
Turan S, Tripathy BC (2015) Salt-stress induced modulation of chlorophyll biosynthesis during de-etiolation of rice seedlings. Physiol Plant 153:477–491. https://doi.org/10.1111/ppl.12250
doi: 10.1111/ppl.12250
pubmed: 25132047
Verslues PE, Sharma S (2010) Proline metabolism and its implications for plant-environment interaction. Arabidopsis 8:e0140. https://doi.org/10.1199/tab.0140
doi: 10.1199/tab.0140
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
doi: 10.1126/SCIENCE.1220177
Walter Michael H, Grima-Pettenati J, Feuillet C (1994) Characterization of a bean (Phaseolus vulgaris L.) malic-enzyme gene. Eur J Biochem 224:999–1009. https://doi.org/10.1111/j.1432-1033.1994.t01-1-00999.x
doi: 10.1111/j.1432-1033.1994.t01-1-00999.x
Wang Y, Long SP, Zhu XG (2014) Elements required for an efficient NADP-malic enzyme type C4 photosynthesis. Plant Physiol 164:2231–2246. https://doi.org/10.1104/pp.113.230284
doi: 10.1104/pp.113.230284
pubmed: 24521879
pmcid: 3982775
Wheeler MCG, 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
doi: 10.1104/pp.105.065953
pubmed: 16113210
Wheeler MC, Arias CL, Tronconi MA, Maurino VG, Andreo CS, Drincovitch MF (2008) Arabidopsis thaliana NADP-malic enzyme isoforms: high degree of identity but clearly distinct properties. Plant Mol Biol 67(3):231–242. https://doi.org/10.1007/s11103-008-9313-9
doi: 10.1007/s11103-008-9313-9
pubmed: 18288573
Wingler A, Walker RP, Chen Z, Leegood RC (1999) Phosphoenolpyruvate carboxykinase is involved in the decarboxylation of aspartate in the bundle sheath of maize. Plant Physiol 120:539–546
pubmed: 10364405
pmcid: 59292
doi: 10.1104/pp.120.2.539
Zell MB, Fahnenstich H, Maier A et al (2010) Analysis of Arabidopsis with highly reduced levels of malate and fumarate sheds light on the role of these organic acids as storage carbon molecules. Plant Physiol 152:1251–1262. https://doi.org/10.1104/pp.109.151795
doi: 10.1104/pp.109.151795
pubmed: 20107023
pmcid: 2832245
Zhu X-G, Long SP, Ort DR (2008) What is the maximum efficiency with which photosynthesis can convert solar energy into biomass? Curr Opin Biotechnol 19:153–159. https://doi.org/10.1016/j.copbio.2008.02.004
doi: 10.1016/j.copbio.2008.02.004
pubmed: 18374559
Zlatev ZS, Yordanov IT (2004) Effects of soil drought on photosynthesis and chlorophyll fluorescence in bean plants. J Plant Physiol 30:3–18
Zhang Q, Li Y, Xu W, Zhang Y, Qi X, Fang Y, Peng C (2021) 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
pubmed: 33257233
doi: 10.1016/j.plaphy.2020.11.030
Zhao H, Wang Y, Lyu MA, Zhu XG (2022) Two major metabolic factors for an efficient NADP-malic enzyme type C4 photosynthesis. Plant Physiol 189(1):84–98
pubmed: 35166833
pmcid: 9070817
doi: 10.1093/plphys/kiac051