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Cytosolic GAPDH: a key mediator in redox signal transduction in plants

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  • Published:
Biologia Plantarum

Abstract

Glyceraldehyde-3-phosphate dehydrogenase (GAPDH) serves not only as a key enzyme in glycolysis, but also as a multifunctional protein in other biological processes, especially in response to abiotic stresses in plants. Cytosolic GAPDH (GAPC) is a typical redox protein with selected catalytic cysteine, which undergoes reversible redox post-translational modifications (RPTMs) on its thiol group by reacting with hydrogen peroxide and nitric oxide related species. Moreover, the modified GAPC may interact with certain signal transmitters such as phosphatidic acid, phospholipase D, and osmotic stress-activated protein kinase. All these observations suggest that GAPC serve as a key mediator in redox signal transduction in plants. In this review, we provide an up-to-date insight into molecular mechanisms after H2O2- and NO-dependent oxidation of GAPC. We also discuss GAPC catalytic functions and potential functions as a modified protein by RPTMs.

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Abbreviations

ABA:

abscisic acid

ATG3:

autophagy-related protein

BaMV:

bamboo mosaic virus

BPGA:

1,3-bisphosphoglyceric acid

DEA-NO:

diethylamine NONOate

DTT:

dithiothreitol

FER:

FERONIA

GAPC:

cytosolic GAPDH

GAPDH:

glyceraldehyde-3-phosphate dehydrogenase

G3P:

glyceraldehyde-3-phosphate

Grx:

glutaredoxins

GSNO:

nitrosoglutathione

MAP:

mitogen-activated protein

NtOSAK:

Nicotiana tabacum osmotic stress-activated protein kinase

OPP:

oxidative pentose phosphate

OXI1:

oxidative signal-inducible1

PA:

phosphatidic acid

PCD:

programmed cell death

PLD:

phospholipase D

QM:

quantum mechanics

RNS:

reactive nitrogen species

RPTM:

redox post-translational modification

ROS:

reactive oxygen species

SINAL7:

SEVEN IN ABSENTIA like7

SnRK2:

SNF1 (sucrose non-fermenting 1)-related protein kinase 2

SOH:

sulphenylation

SSG:

glutathionylation

Trx:

thioredoxins

References

  • Akter, S., Huang, J., Waszczak, C., Jacques, S., Gevaert, K., Van Breusegem, F., Messens, J.: Cysteines under ROS attack in plants: a proteomics view. — J. exp. Bot. 66: 2935–2944, 2015.

    Article  CAS  PubMed  Google Scholar 

  • Astier, J., Rasul, S., Koen, E., Manzoor, H., Besson-Bard, A., Lamotte, O., Jeandroz, S., Durner, J., Lindermayr, C., Wendehenne, D.: S-nitrosylation: an emerging posttranslational protein modification in plants. — Plant Sci. 181: 527–533, 2011.

    Article  CAS  PubMed  Google Scholar 

  • Bae, M.S., Cho, E.J., Choi, E.Y., Park, O.K.: Analysis of the Arabidopsis nuclear proteome and its response to cold stress. — Plant J. 36: 652–663, 2003.

    Article  CAS  PubMed  Google Scholar 

  • Baek, D., Jin, Y., Jeong, J.C., Lee, H.J., Moon, H., Lee, J., Shin, D., Kang, C.H., Kim, D.H., Nam, J., Lee, S.Y., Yun, D.J.: Suppression of reactive oxygen species by glyceraldehyde-3-phosphate dehydrogenase. — Phytochemistry 69: 333–338, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Bedhomme, M., Adamo, M., Marchand, C.H., Couturier, J., Rouhier, N., Lemaire, S.D., Zaffagnini, M., Trost, P.: Glutathionylation of cytosolic glyceraldehyde-3-phosphate dehydrogenase from the model plant Arabidopsis thaliana is reversed by both glutaredoxins and thioredoxins in vitro. — Biochem. J. 445: 337–347, 2012.

    Article  CAS  PubMed  Google Scholar 

  • Benhar, M., Forrester, M.T., Stamler, J.S.: Protein denitrosylation: enzymatic mechanisms and cellular functions. — Nat. Rev. mol. cell. Biol. 10: 721–732, 2009.

    CAS  PubMed  Google Scholar 

  • Brinkmann, H., Cerff, R., Salomon, M., Soll, J.: Cloning and sequence analysis of cDNAs encoding the cytosolic precursors of subunits GapA and GapB of chloroplast glyceraldehyde-3-phosphate dehydrogenase from pea and spinach. — Plant mol. Biol. 13: 81–94, 1989.

    Article  CAS  PubMed  Google Scholar 

  • Burza, A.M., Pekala, I., Sikora, J., Siedlecki, P., Małagocki, P., Bucholc, M., Koper, L., Zielenkiewicz, P., Dadlez, M., Dobrowolska, G.: Nicotiana tabacum osmotic stressactivated kinase is regulated by phosphorylation on Ser-154 and Ser-158 in the kinase activation loop. — J. biol. Chem. 281: 34299–34311, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Demidchik, V.: Mechanisms of oxidative stress in plants: from classical chemistry to cell biology. — Environ. exp. Bot. 109: 212–228, 2015.

    Article  CAS  Google Scholar 

  • Ferrer-Sueta, G., Manta, B., Botti, H., Radi, R., Trujillo, M., Denicola, A.: Factors affecting protein thiol reactivity and specificity in peroxide reduction. — Chem. Res. Toxicol. 24: 434–450, 2011.

    Article  CAS  PubMed  Google Scholar 

  • Fujii, H., Zhu, J.K.: Arabidopsis mutant deficient in 3 abscisic acid-activated protein kinases reveals critical roles in growth, reproduction, and stress. — Proc. nat. Acad. Sci. USA 106: 8380–8385, 2009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fujita, Y., Nakashima, K., Yoshida, T., Katagiri, T., Kidokoro, S., Kanamori, N., Umezawa, T., Fujita, M., Maruyama, K., Ishiyama, K., Kobayashi, M., Nakasone, S., Yamada, K., Ito, T., Shinozaki, K., Yamaguchi-Shinozaki, K.: Three SnRK2 protein kinases are the main positive regulators of abscisic acid signaling in response to water stress in Arabidopsis. — Plant Cell Physiol. 50: 2123–2132, 2009.

    Article  CAS  PubMed  Google Scholar 

  • Go, Y.M., Chandler, J.D., Jones, D.P.: The cysteine proteome. — Free Radicals Biol. Med. 84: 227–245, 2015.

    Article  CAS  Google Scholar 

  • Guo, L., Devaiah, S.P., Narasimhan, R., Pan, X.Q., Zhang, Y.Y., Zhang, W.H., Wang, X.M.: Cytosolic glyceraldehyde-3-phosphate dehydrogenases interact with phospholipase Dδ to transduce hydrogen peroxide signals in the Arabidopsis response to stress. — Plant Cell 24: 2200–2212, 2012.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo, L., Ma, F., Wei, F., Fanella, B., Allen, D.K., Wang, X.M.: Cytosolic phosphorylating glyceraldehyde-3-phosphate dehydrogenases affect Arabidopsis cellular metabolism and promote seed oil accumulation. — Plant Cell 26: 3023–3035, 2014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Han, S.J., Wang, Y., Zheng, X.Y., Jia, Q., Zhao, J.P., Bai, F., Hong, Y.G., Liu, Y.L.: Cytoplastic glyceraldehyde-3-phosphate dehydrogenases interact with ATG3 to negatively regulate autophagy and immunity in Nicotiana benthamiana. — Plant Cell 27: 1316–1331, 2015.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hancock, J.T., Henson, D., Nyirenda, M., Desikan, R., Harrison, J., Lewis, M., Hughes, J., Neill, S.J.: Proteomic identification of glyceraldehyde 3-phosphate dehydrogenase as an inhibitory target of hydrogen peroxide in Arabidopsis. — Plant Physiol. Biochem. 43: 828–835, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Henry, E., Fung, N., Liu, J., Drakakaki, G., Coaker, G.: Beyond glycolysis: GAPDHs are multi-functional enzymes involved in regulation of ROS, autophagy, and plant immune responses. — PLoS Genet. 11: e1005199, 2015.

    Article  Google Scholar 

  • Hess, D.T., Matsumoto, A., Kim, S.O., Marshall, H.E., Stamler, J.S.: Protein S-nitrosylation: purview and parameters. — Nat. Rev. mol. cell. Biol. 6: 150–166, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Hildebrandt, T., Knuesting, J., Berndt, C., Morgan, B., Scheibe, R.: Cytosolic thiol switches regulating basic cellular functions: GAPDH as an information hub? — Biol. Chem. 396: 523–537, 2015.

    Article  CAS  PubMed  Google Scholar 

  • Holtgrefe, S., Gohlke, J., Starmann, J., Druce, S., Klocke, S., Altmann, B., Wojtera, J., Lindermayr, C., Scheibe, R.: Regulation of plant cytosolic glyceraldehyde 3-phosphate dehydrogenase isoforms by thiol modifications. — Physiol. Plant. 133: 211–228, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Huang, G.T., Ma, S.L., Bai, L.P., Zhang, L., Ma, H., Jia, P., Liu, J., Zhong, M., Guo, Z.F.: Signal transduction during cold, salt, and drought stresses in plants. — Mol. Biol. Rep. 39: 969–987, 2012.

    Article  PubMed  Google Scholar 

  • Jeong, M.J., Park, S.C., Kwon, H.B., Byun, M.O.: Isolation and characterization of the gene encoding glyceraldehyde-3-phosphate dehydrogenase. — Biochem. biophys. Res. Commun. 278: 192–196, 2000.

    Article  CAS  PubMed  Google Scholar 

  • Jiang, Y., Yang, B., Harris, N.S., Deyholos, M.K.: Comparative proteomic analysis of NaCl stress-responsive proteins in Arabidopsis roots. — J. exp. Bot. 58: 3591–3607, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Krasensky, J., Jonak, C.: Drought, salt, and temperature stressinduced metabolic rearrangements and regulatory networks. — J. exp. Bot. 63: 1593–1608, 2012.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumaraswamy, G.K., Guerra, T., Qian, X., Zhang, S., Bryant, D.A., Dismukes, G.C.: Reprogramming the glycolytic pathway for increased hydrogen production in cyanobacteria: metabolic engineering of NAD+-dependent GAPDH. — Energy Environ. Sci. 6: 3722–3731, 2013.

    Article  CAS  Google Scholar 

  • Lin, A., Wang, Y., Tang, J., Xue, P., Li, C., Liu, L., Hu, B., Yang, F., Loake, G.J., Chu, C.: Nitric oxide and protein Snitrosylation are integral to hydrogen peroxide-induced leaf cell death in rice. — Plant Physiol. 158: 451–464, 2012.

    Article  CAS  PubMed  Google Scholar 

  • Lindermayr, C., Saalbach, G., Durner, J.: Proteomic identification of S-nitrosylated proteins in Arabidopsis. — Plant Physiol. 137: 921–930, 2005.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu, Y., Schiff, M., Czymmek, K., Tallóczy, Z., Levine, B., Dinesh-Kumar, S.P.: Autophagy regulates programmed cell death during the plant innate immune response. — Cell 121: 567–577, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Morigasaki, S., Shimada, K., Ikner, A., Yanagida, M., Shiozaki, K.: Glycolytic enzyme GAPDH promotes peroxide stress signaling through multistep phosphorelay to a MAPK cascade. — Mol. Cell 30: 108–113, 2008.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Munoz-Bertomeu, J., Cascales-Minana, B., Irles-Segura, A., Mateu, I., Nunes-Nesi, A., Fernie, A.R., Segura, J., Ros, R.: The plastidial glyceraldehyde-3-phosphate dehydrogenase is critical for viable pollen development in Arabidopsis. — Plant Physiol. 152:1830–1841, 2010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Munoz-Bertomeu, J., Cascales-Minana, B., Mulet, J.M., Baroja-Fernandez, E., Pozueta-Romero, J., Kuhn, J.M., Segura, J., Ros, R.: Plastidial glyceraldehyde-3-phosphate dehydrogenase deficiency leads to altered root development and affects the sugar and amino acid balance in Arabidopsis. — Plant Physiol. 151: 541–558, 2009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nicholls, C., Li, H., Liu, J.P.: GAPDH: a common enzyme with uncommon functions. — Clin. exp. Pharmacol. Physiol. 39: 674–679, 2012.

    Article  CAS  PubMed  Google Scholar 

  • Niu, L., Liao, W.: Hydrogen peroxide signaling in plant development and abiotic responses: crosstalk with nitric oxide and calcium. — Front. Plant Sci. 7: 230, 2016.

    PubMed  PubMed Central  Google Scholar 

  • Noctor, G., Lelarge-Trouverie, C., Mhamdi, A.: The metabolomics of oxidative stress. — Phytochemistry 112: 33–53, 2015.

    Article  CAS  PubMed  Google Scholar 

  • Peralta, D.A., Araya, A., Busi, M.V., Gomez-Casati, D.F.: The E3 ubiquitin-ligase SEVEN IN ABSENTIA like 7 monoubiquitinates glyceraldehyde-3-phosphate dehydrogenase 1 isoform in vitro and is required for its nuclear localization in Arabidopsis thaliana. — Int. J. Biochem. cell. Biol. 70: 48–56, 2016.

    Article  CAS  PubMed  Google Scholar 

  • Peralta, D., Bronowska, A.K., Morgan, B., Dóka, É., Van, L.K., Nagy, P., Gräter, F., Dick, T.P.: A proton relay enhances H2O2 sensitivity of GAPDH to facilitate metabolic adaptation. — Nat. chem. Biol. 11:156-163, 2015.

  • Petersen, J., Brinkmann, H., Cerff, R.: Origin, evolution, and metabolic role of a novel glycolytic GAPDH enzyme recruited by land plant plastids. — J. mol. Evol. 57: 16–26, 2003.

    Article  CAS  PubMed  Google Scholar 

  • Piattoni, C.V., Guerrero, S.A., Iglesias, A.A..: A differential redox regulation of the pathways metabolizing glyceraldehyde-3-phosphate tunes the production of reducing power in the cytosol of plant cells. — Int. J. mol. Sci. 14: 8073–8092, 2013.

    Article  PubMed  PubMed Central  Google Scholar 

  • Piszczatowski, R.T., Rafferty, B.J., Rozado, A., Tobak, S., Lents, N.H.: The glyceraldehyde 3-phosphate dehydrogenase gene (GAPDH) is regulated by myeloid zinc finger 1 (MZF-1) and is induced by calcitriol. - Biochem. biophys. Res. Commun. 451: 137–141, 2014.

    Article  CAS  PubMed  Google Scholar 

  • Plaxton, W.C.: The organization and regulation of plant glycolysis. — Annu. Rev. Plant Biol. 47: 185–214, 1996.

    Article  CAS  Google Scholar 

  • Prasanth, K.R., Huang, Y.W., Liou, M.R., Wang, R.Y., Hu, C.C., Tsai, C.H., Meng, M., Lin, N.S., Hsu, Y.H.: Glyceraldehyde 3-phosphate dehydrogenase negatively regulates the replication of Bamboo mosaic virus and its associated satellite RNA. — J. Virol. 85: 8829–8840, 2011.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rahantaniaina, M.S., Tuzet, A., Mhamdi, A., Noctor, G.: Missing links in understanding redox signaling via thiol/disulfide modulation: how is glutathione oxidized in plants? - Front. Plant Sci. 4: 477, 2013.

    Article  PubMed  PubMed Central  Google Scholar 

  • Reczek, C.R., Chandel, N.S.: ROS-dependent signal transduction. — Curr. Opin. Cell Biol. 33: 8–13, 2015.

    Article  CAS  PubMed  Google Scholar 

  • Rius, S.P., Casati, P., Iglesias, A.A., Gomez-Casati, D.F.: Characterization of an Arabidopsis thaliana mutant lacking a cytosolic non-phosphorylating glyceraldehyde-3-phosphate dehydrogenase. — Plant mol. Biol. 61: 945–957, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Rius, S.P., Casati, P., Iglesias, A.A., Gomez-Casati, D.F.: Characterization of Arabidopsis lines deficient in GAPC-1, a cytosolic NAD-dependent glyceraldehyde-3-phosphate dehydrogenase. - Plant Physiol. 148: 1655–1667, 2008.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roos, G., Foloppe, N., Messens, J.: Understanding the pK(a) of redox cysteines: the key role of hydrogen bonding. - Antioxid. Redox Signal. 18: 94–127, 2013.

    Article  CAS  PubMed  Google Scholar 

  • Schieber, M., Chandel, N.S.: ROS function in redox signaling and oxidative stress. — Curr. Biol. 24: R453–R462, 2014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmidt, R., Schippers, J.H.: ROS-mediated redox signaling during cell differentiation in plants. — Biochim. biophys Acta 1850: 1497–1508, 2015.

    Article  CAS  PubMed  Google Scholar 

  • Seidler N.W.: GAPDH: Biological Properties and Diversity. - Springer, Dordrecht 2012.

    Google Scholar 

  • Sengupta, R., Holmgren, A.: Thioredoxin and thioredoxin reductase in relation to reversible S-nitrosylation. — Antioxid. Redox Signal. 18: 259–269, 2013.

    Article  CAS  PubMed  Google Scholar 

  • Sevilla, F., Camejo, D., Ortiz-Espin, A., Calderon, A., Lazaro, J.J., Jimenez, A.: The thioredoxin/peroxiredoxin/sulfiredoxin system: current overview on its redox function in plants and regulation by reactive oxygen and nitrogen species. — J. exp. Bot. 66: 2945–2955, 2015.

    Article  CAS  PubMed  Google Scholar 

  • Shao, H.B., Chu, L.Y., Shao, M.A., Jaleel, C.A., Mi, H.M.: Higher plant antioxidants and redox signaling under environmental stresses. — Compt. rend. Biol. 331: 433–441, 2008.

    Article  CAS  Google Scholar 

  • Spadaro, D., Yun, B.W., Spoel, S.H., Chu, C., Wang, Y.Q., Loake, G.J.: The redox switch: dynamic regulation of protein function by cysteine modifications. — Physiol. Plant. 138: 360–371, 2010.

    Article  CAS  PubMed  Google Scholar 

  • Suzuki, N., Koussevitzky, S., Mittler, R., Miller, G..: ROS and redox signalling in the response of plants to abiotic stress. — Plant Cell Environ. 35: 259–270, 2012.

    Article  CAS  PubMed  Google Scholar 

  • Tien, Y.C., Chuankhayan, P., Huang, Y.C., Chen, C.D., Alikhajeh, J., Chang, S.L., Chen, C.J..: Crystal structures of rice (Oryza sativa) glyceraldehyde-3-phosphate dehydrogenase complexes with NAD and sulfate suggest involvement of Phe37 in NAD binding for catalysis. — Plant mol. Biol. 80: 389–403, 2012.

    Article  CAS  PubMed  Google Scholar 

  • Trapet, P., Kulik, A., Lamotte, O., Jeandroz, S., Bourque, S., Nicolas-Frances, V., Rosnoblet, C., Besson-Bard, A., Wendehenne, D.: NO signaling in plant immunity: a tale of messengers. — Phytochemistry 112: 72–79, 2015.

    Article  CAS  PubMed  Google Scholar 

  • Tristan, C., Shahani, N., Sedlak, T.W., Sawa, A.: The diverse functions of GAPDH: views from different subcellular compartments. — Cell. Signal. 23: 317–323, 2011.

    Article  CAS  PubMed  Google Scholar 

  • Vescovi, M., Zaffagnini, M., Festa, M., Trost, P., Lo Schiavo, F., Costa, A.: Nuclear accumulation of cytosolic glyceraldehyde-3-phosphate dehydrogenase in cadmiumstressed Arabidopsis roots. — Plant Physiol. 162: 333–346, 2013.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, P., Du, Y., Hou, Y.J., Zhao, Y., Hsu, C.C., Yuan, F., Zhu, X., Tao, W.A., Song, C.P., Zhu, J.K.: Nitric oxide negatively regulates abscisic acid signaling in guard cells by S-nitrosylation of OST1. — Proc. nat. Acad. Sci. USA 112: 613–618, 2015.

    Article  CAS  PubMed  Google Scholar 

  • Wang, X.Y., Chen, Y.F., Zou, J.J., Wu, W.H.: Involvement of a cytoplasmic glyceraldehyde-3-phosphate dehydrogenase GapC-2 in low-phosphate-induced anthocyanin accumulation in Arabidopsis. — Chin. Sci. Bull. 52: 1764–1770, 2007.

    Article  CAS  Google Scholar 

  • Wang, X., Devaiah, S.P., Zhang, W., Welti, R.: Signaling functions of phosphatidic acid. — Progr. Lipid Res. 45: 250–278, 2006.

    Article  CAS  Google Scholar 

  • Wawer, I., Bucholc, M., Astier, J., Anielska-Mazur, A., Dahan, J., Kulik, A., Wyslouch-Cieszynska, A., Zareba-Koziol, M., Krzywinska, E., Dadlez, M., Dobrowolska, G., Wendehenne, D.: Regulation of Nicotiana tabacum osmotic stress-activated protein kinase and its cellular partner GAPDH by nitric oxide in response to salinity. — Biochem. J. 429: 73–83, 2010.

    Article  CAS  PubMed  Google Scholar 

  • Winterbourn, C.C., Hampton, M.B.: Thiol chemistry and specificity in redox signaling. — Free Radicals Biol. Med. 45: 549–561, 2008.

    Article  CAS  Google Scholar 

  • Wojtera-Kwiczor, J., Gross, F., Leffers, H.M., Kang, M., Schneider, M., Scheibe, R.: Transfer of a redox-signal through the cytosol by redox-dependent microcompartmentation of glycolytic enzymes at mitochondria and actin cytoskeleton. — Front. Plant Sci. 3: 1–19, 2013.

    Article  Google Scholar 

  • Yang, T., Wang, L., Li, C., Liu, Y., Zhu, S., Qi, Y., Liu, X., Lin, Q., Luan, S., Yu, F.: Receptor protein kinase FERONIA controls leaf starch accumulation by interacting with glyceraldehyde-3-phosphate dehydrogenase. — Biochem. biophys. Res. Commun. 465: 77–82, 2015.

    Article  CAS  PubMed  Google Scholar 

  • Yu, M., Yun, B.W., Spoel, S.H., Loake, G.J.: A sleigh ride through the SNO: regulation of plant immune function by protein S-nitrosylation. — Curr. Opin. Plant Biol. 15: 424–430, 2012.

    Article  CAS  PubMed  Google Scholar 

  • Zachgo, S., Hanke, G.T., Scheibe, R.: Plant cell micro-compartments: a redox-signaling perspective. — Biol. Chem. 394: 203–216, 2013.

    Article  CAS  PubMed  Google Scholar 

  • Zaffagnini, M., Fermani, S., Calvaresi, M., Orru, R., Iommarini, L., Sparla, F., Falini, G., Bottoni, A., Trost, P.: Tuning cysteine reactivity and sulfenic acid stability by protein microenvironment in glyceraldehyde-3-phosphate dehydrogenases of Arabidopsis thaliana. — Antioxid. Redox Signal. 24: 502–517, 2016.

    Article  CAS  PubMed  Google Scholar 

  • Zaffagnini, M., Fermani, S., Costa, A., Lemaire, S.D., Trost, P.: Plant cytoplasmic GAPDH: redox post-translational modifications and moonlighting properties. — Front. Plant Sci. 4: 450, 2013a.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zaffagnini, M., Morisse, S., Bedhomme, M., Marchand, C.H., Festa, M., Rouhier, N., Lemaire, D., Trost, P.: Mechanisms of nitrosylation and denitrosylation of cytoplasmic glyceraldehyde-3-phosphate dehydrogenase from Arabidopsis thaliana. — J. biol. Chem. 288: 22777–22789, 2013b.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, X.H., Rao, X.L., Shi, H.T., Li, R.J., Lu, Y.T.: Overexpression of a cytosolic glyceraldehyde-3-phosphate dehydrogenase gene OsGAPC3 confers salt tolerance in rice. — Plant Cell Tissue Organ Cult. 107: 1–11, 2011.

    Article  CAS  Google Scholar 

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  1. College of Life Sciences, Northwest A&F University, 712100, Yangling, Shaanxi, P.R. China

    S. S. Yang & Q. H. Zhai

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  1. S. S. Yang
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Acknowledgments: We are greatly acknowledged to the National Natural Science Foundation of China (Nos. 31271625 and 31671609), the State Key Laboratory of Soil Erosion and Dryland Farming on Loess Plateau, Institute of Soil and Water Conservation, Chinese Academy of Sciences (No. 10502), the National Basic Research Program of China (2015CB150402), and the National Natural Science Foundation of China (No. 51479189).

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Yang, S.S., Zhai, Q.H. Cytosolic GAPDH: a key mediator in redox signal transduction in plants. Biol Plant 61, 417–426 (2017). https://doi.org/10.1007/s10535-017-0706-y

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