Critical multifunctional role of the betaine aldehyde dehydrogenase gene in plants

References

• Matin R, Ebrahimi MA, Niazi A. Quantitative expression analysis of P5CS and BADH genes in cultivated Wheat Plants under Salt and ABA treatments. Iranian J Genet Plant Breed. 2014;3:43–48.
   Google Scholar
• Pan SM, Moreau RA, Yu C, et al. Betaine accumulation and betaine-aldehyde dehydrogenase in spinach leaves. Plant Physiol. 1981;67:1105–1108.
   PubMed Web of Science ®Google Scholar
• Weretilnyk EA, Hanson AD. Molecular cloning of a plant betaine-aldehyde dehydrogenase, an enzyme implicated in adaptation to salinity and drought. Proc Natl Acad Sci U S A. 1990;87:2745–2749.
   PubMed Web of Science ®Google Scholar
• Fitzgerald TL, Waters DL, Henry RJ. Betaine aldehyde dehydrogenase in plants. Plant Biol. 2008;11:119–130.
   Web of Science ®Google Scholar
• Bradbury LM, Fitzgerald TL, Henry RJ, et al. The gene for fragrance in rice. Plant Biotechnol J. 2005;3:363–370.
   PubMed Web of Science ®Google Scholar
• Weigel P, Weretilnyk EA, Hanson AD. Betaine aldehyde oxidation by spinach chloroplasts. Plant Physiol. 1986;82:753–759.
   PubMed Web of Science ®Google Scholar
• Arikit S, Yoshihashi T, Wanchana S, et al. Deficiency in the amino aldehyde dehydrogenase encoded by GmAMADH2, the homologue of rice Os2AP, enhances 2-acetyl-1-pyrroline biosynthesis in soybeans (Glycine max L.). Plant Biotechnol J. 2011;9:75–87.
   PubMed Web of Science ®Google Scholar
• Fujiwara T, Hori K, Ozaki K, et al. Enzymatic characterization of peroxisomal and cytosolic betaine aldehyde dehydrogenases in barley. Physiol Plant. 2008;134:22–30.
   PubMed Web of Science ®Google Scholar
• Shrestha K. Analysis of betaine aldehyde dehydrogenase encoding genes in wheat [MSc thesis]. Lismore (NSW): Southern Cross University; 2011.
   Google Scholar
• Wang YB, Guan LL, Xu YW, et al. Cloning and sequence analysis of the safflower betaine aldehyde dehydrogenase gene. Genet Mol Res. 2014;13:344–353.
   PubMed Web of Science ®Google Scholar
• Bradbury LM, Gillies SA, Brushett DJ, et al. Inactivation of an aminoaldehyde dehydrogenase is responsible for fragrance in rice. Plant Mol Biol. 2008;68:439–449.
   PubMed Web of Science ®Google Scholar
• Arakawa K, Katayama M, Takabe T. Levels of betaine and betaine aldehyde dehydrogenase activity in the green leaves, and etiolated leaves and roots of barley. Plant Cell Physiol. 1990;31:797–803.
   Web of Science ®Google Scholar
• Trossat C, Rathinasabapathi B, Hanson AD. Transgenically expressed betaine aldehyde dehydrogenase efficiently catalyzes oxidation of dimethylsulfoniopropionaldehyde and [omega]-aminoaldehydes. Plant Physiol. 1997;113:1457–1461.
   PubMed Web of Science ®Google Scholar
• Brauner F, Šebela M, Snégaroff J, et al. Pea seedling aminoaldehyde dehydrogenase: primary structure and active site residues. Plant Physiol Bioch. 2003;41:1–10.
   Web of Science ®Google Scholar
• Missihoun TD, Schmitz J, Klug R. Betaine aldehyde dehydrogenase genes from Arabidopsis with different sub-cellular localization affect stress responses. Planta. 2011;233:369–382.
   PubMed Web of Science ®Google Scholar
• Niu X, Zhang W, Lu BR, et al. An unusual posttranscriptional processing in two betaine aldehyde dehydrogenase loci of cereal crops directed by short, direct repeats in response to stress conditions. Plant Physiol. 2007;143:1929–1942.
   PubMed Web of Science ®Google Scholar
• Fitzgerald TL, Waters DLE, Henry RJ. The effect of salt on betaine aldehyde dehydrogenase transcript levels and 2-acetyl-1-pyrroline concentration in fragrant and non-fragrant rice (Oryza sativa). Plant Sci. 2008;175:539–546.
   Web of Science ®Google Scholar
• Fitzgerald MA, McCouch SR, Hall RD. Not just a grain of rice: the quest for quality. Trends Plant Sci. 2009;14:133–139.
   PubMed Web of Science ®Google Scholar
• Yang C, Zhou Y, Fan J, et al. SpBADH of the halophyte Sesuvium portulacastrum strongly confers drought tolerance through ROS scavenging in transgenic Arabidopsis. Plant Physiol Bioch. 2015;96:377–387.
   PubMed Web of Science ®Google Scholar
• Vinocur B, Altman A. Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Curr Opin Biotech. 2006;16:123–132.
   Web of Science ®Google Scholar
• Zingaretti S, Demore P, Morceli T, et al. Glycine betaine biosynthesis genes differentially expressed in sugarcane under water stress. BMC Proceedings. [cited 2017 Oct 29] 2014;8:P123. [2 p.] DOI:10.1186/1753-6561-8-S4-P123
   Google Scholar
• Liu H, Yu C, Li H, et al. Overexpression of ShDHN, a dehydrin gene from Solanum habrochaites enhances tolerance to multiple abiotic stresses in tomato. Plant Sci. 2015;231:198–211.
   PubMed Web of Science ®Google Scholar
• Sinha AK, Jaggi M, Raghuram B, et al. Mitogen-activated protein kinase signaling in plants under abiotic stress. Plant Signaling Behave. 2011;6:196–203.
   PubMedGoogle Scholar
• Bartels D, Sunkar R. Drought and salt tolerance in plants. Crit Rev Plant Sci. 2005;24:23–58.
   Web of Science ®Google Scholar
• Ashraf M, Foolad M. Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot. 2007;59:206–216.
   Web of Science ®Google Scholar
• Yu HQ, Wang YG, Yong TM, et al. Heterologous expression of betaine aldehyde dehydrogenase gene from Ammopiptanthus nanus confers high salt and heat tolerance to Escherichia coli. Gene. 2014;549:77–84.
   PubMed Web of Science ®Google Scholar
• Legaria J, Rajsbaum R, Munoz-Clares R, et al. Molecular characterization of two genes encoding betaine aldehyde dehydrogenase from amaranth. Expression in leaves under short-term exposure to osmotic stress or abscisic acid. Gene. 1998;218:69–76.
   PubMed Web of Science ®Google Scholar
• Jia GX, Zhu ZQ, Chang FQ, et al. Transformation of tomato with the BADH gene from Atriplex improves salt tolerance. Plant Cell Rep. 2002;21:141–146.
   Web of Science ®Google Scholar
• Li QL, Gao XR, Yu XH, et al. Molecular cloning and characterization of betaine aldehyde dehydrogenase gene from Suaeda liaotungensis and its use in improved tolerance to salinity in transgenic tobacco. Biotechnol Lett. 2003;25:1431–1436.
   PubMed Web of Science ®Google Scholar
• Zhang N, Si HJ, Wen G, et al. Enhanced drought and salinity tolerance in transgenic potato plants with a BADH gene from spinach. Plant Biotechnol Rep. 2011;5:71–77.
   Web of Science ®Google Scholar
• Yan LP, Liu CL, Liang HM, et al. Physiological responses to salt stress of T2 alfalfa progenies carrying a transgene for betaine aldehyde dehydrogenase. Plant Cell Tissue Org Cult (PCTOC). 2012;108:191–199.
   Web of Science ®Google Scholar
• Amarawathi Y, Singh R, Singh AK, et al. Mapping of quantitative trait loci for basmati quality traits in rice (Oryza sativa L.). Mol Breed. 2008;21:49–65.
   Web of Science ®Google Scholar
• Golestan Hashemi FS, Rafii M, Ismail MR, et al. Opportunities of marker-assisted selection for rice fragrance through marker–trait association analysis of microsatellites and gene-based markers. Plant Biol. 2015;17:953–961.
   PubMed Web of Science ®Google Scholar
• Shi W, Yang Y, Chen S, et al. Discovery of a new fragrance allele and the development of functional markers for the breeding of fragrant rice varieties. Mol Breed. 2008;22:185–192.
   Web of Science ®Google Scholar
• Wakte KV, Kad TD, Zanan RL, et al. Mechanism of 2-acetyl-1-pyrroline biosynthesis in Bassia latifolia Roxb. flowers. Physiol Mol Biol Plants. 2011;17:231–237.
   PubMedGoogle Scholar
• Gaur A, Wani S, Pandita D, et al. Understanding the fragrance in rice. J Rice Res. [cited 2017 Oct 29] 2016;4:1000e125. [4 p.] DOI:10.4172/2375-4338.1000e125
   Google Scholar
• Lorieux M, Petrov M, Huang N, et al. Aroma in rice: genetic analysis of a quantitative trait. Theor Appl Genet. 1996;93:1145–1151.
   PubMed Web of Science ®Google Scholar
• Jin Q, Waters D, Cordeiro GM, et al. A single nucleotide polymorphism (SNP) marker linked to the fragrance gene in rice (Oryza sativa L.). Plant Sci. 2003;165:359–364.
   Web of Science ®Google Scholar
• Golestan Hashemi FS, Rafii M, Ismail MR, et al. The genetic and molecular origin of natural variation for the fragrance trait in an elite Malaysian aromatic rice through quantitative trait loci mapping using SSR and gene-based markers. Gene. 2015;555:101–107.
   PubMed Web of Science ®Google Scholar
• Vemireddy R, Noor S, Satyavathi V, et al. Discovery and mapping of genomic regions governing economically important traits of Basmati rice. BMC Plant Biol. [cited 2017 Oct 29] 2015;15:207. [19 p.] DOI:10.1186/s12870-015-0575-5
   PubMed Web of Science ®Google Scholar
• Golestan Hashemi FS, Rafii M, Ismail MR, et al. Biochemical, genetic and molecular advances of fragrance characteristics in rice. Crit Rev Plant Sci. 2013;32:445–457.
   Web of Science ®Google Scholar
• Manimaran P, Ramkumar G, Sakthivel K, et al. Suitability of non-lethal marker and marker-free systems for development of transgenic crop plants: present status and future prospects. Biotechnol Adv. 2011;29:703–714.
   PubMed Web of Science ®Google Scholar
• Daniell H, Muthukumar B, Lee S. Marker free transgenic plants: engineering the chloroplast genome without the use of antibiotic selection. Curr Genet. 2001;39:109–116.
   PubMed Web of Science ®Google Scholar
• Daniell H, Ruiz ON, Dhingra A. Chloroplast genetic engineering to improve agronomic traits. In: Pena L, editor. Transgenic plants: methods and protocols. Totowa (NJ): Humana Press; 2004. p. 111–137. (Methods in Molecular Biology, vol. 286).
   Google Scholar
• Bock R. Plastid biotechnology: prospects for herbicide and insect resistance, metabolic engineering and molecular farming. Curr Opin Biotech. 2007;18:100–106.
   PubMed Web of Science ®Google Scholar
• Daniell H. Production of biopharmaceuticals and vaccines in plants via the chloroplast genome. Biotechnol J. 2006;1:1071–1079.
   PubMedGoogle Scholar
• Yu HQ, Zhou XY, Wang YG, et al. A betaine aldehyde dehydrogenase gene from Ammopiptanthus nanus enhances tolerance of Arabidopsis to high salt and drought stresses. Plant Growth Regul. 2017;83:265–276.
   Web of Science ®Google Scholar
• Bao Y, Zhao R, Li F, et al. Simultaneous expression of Spinacia oleracea chloroplast choline monooxygenase (CMO) and betaine aldehyde dehydrogenase (BADH) genes contribute to dwarfism in transgenic Lolium perenne. Plant Mol Biol Rep. 2011;29:379–388.
   Web of Science ®Google Scholar
• Takabe T, Rai V, Hibino T, Metabolic engineering of glycinebetaine. In: Rai AK, Takabe T, editors. Abiotic stress tolerance in plants. Dordrecht (Netherland): Springer; 2006. p. 137–151.
   Google Scholar
• Burnet M, Lafontaine PJ, Hanson AD. Assay, purification, and partial characterization of choline monooxygenase from spinach. Plant Physiol. 1995;108:581–588.
   PubMed Web of Science ®Google Scholar
• Rathinasabapathi B, Burnet M, Russell BL, et al. Choline monooxygenase, an unusual iron-sulfur enzyme catalyzing the first step of glycine betaine synthesis in plants: prosthetic group characterization and cDNA cloning. Proc Natl Acad Sci U S A. 1997;94:3454–3458.
   PubMed Web of Science ®Google Scholar
• Pál M, Szalai G, Janda T. Speculation: polyamines are important in abiotic stress signaling. Plant Sci. 2015;237:16–23.
   PubMed Web of Science ®Google Scholar
• Sánchez-Rodríguez E, Romero L, Ruiz J. Accumulation on free polyamines enhanced antioxidant response in fruit of grafting tomato plants under water stress. J Plant Physiol. 2016;190:72–78.
   PubMed Web of Science ®Google Scholar
• Rhee H, Kim EJ, Lee J. Physiological polyamines: simple primordial stress molecules. J Cell Mol Med. 2007;11:685–703.
   PubMed Web of Science ®Google Scholar
• Ashraf M, Akram NA, Al-Qurainy F, et al. Drought tolerance: roles of organic osmolytes, growth regulators and mineral nutrients. Adv Agron. 2011;111:249–296.
   Web of Science ®Google Scholar
• Alcázar R, Altabella T, Marco F, et al. Polyamine: molecules with regulatory functions in plant abiotic stress tolerance. Planta. 2010;23:1237–1249.
   Google Scholar
• Šebela M, Brauner F, Radová A, et al. Characterisation of a homogeneous plant aminoaldehyde dehydrogenase. Biochim Biophys Acta (BBA)-Protein Struct Mol Enzymol. 2000;1480:329–341.
   PubMedGoogle Scholar
• Mo Z, Huang J, Xiao D, et al. Supplementation of 2-Ap, Zn and La improves 2-acetyl-1-pyrroline concentrations in detached aromatic rice panicles in vitro. PloS One. [cited 2017 Oct 29] 2016;11:e0149523. [15 p.] DOI:10.1371/journal.pone.0149523
   PubMed Web of Science ®Google Scholar
• Smékalová V, Doskočilová A, Komis G, et al. Crosstalk between secondary messengers, hormones and MAPK modules during abiotic stress signalling in plants. Biotechnol Adv. 2014;32:2–11.
   PubMed Web of Science ®Google Scholar
• Uga Y, Yamamoto E, Kanno N, et al. A major QTL controlling deep rooting on rice chromosome 4. Sci Rep. 2013;3:3040.
   PubMed Web of Science ®Google Scholar
• Shamsudin NAA, Swamy BM, Ratnam W, et al. Marker assisted pyramiding of drought yield QTLs into a popular Malaysian rice cultivar, MR219. BMC Genet. [cited 2017 Oct 29] 2016;17:1. [14 p.] DOI:10.1186/s12863-016-0334-0
   PubMed Web of Science ®Google Scholar
• Ashraf M. Inducing drought tolerance in plants: recent advances. Biotechnol Adv. 2010;28:169–183.
   PubMed Web of Science ®Google Scholar
• Jena K, Mackill D. Molecular markers and their use in marker-assisted selection in rice. Crop Sci. 2008;48:1266–1276.
   Web of Science ®Google Scholar
• Nayyar H, Satwinder K, Kumar S, et al. Involvement of polyamines in the contrasting sensitivity of chickpea (Cicer arietinum L.) and soybean (Glycine max (L.) Merrill.) to water deficit stress. Bot Bull Acad Sinica. 2005;46:333–338.
   Google Scholar
• Groppa M, Benavides M. Polyamines and abiotic stress: recent advances. Amino Acids. 2008;34:35–45.
   PubMed Web of Science ®Google Scholar
• Hong Y, Zhang W, Wang X. Phospholipase D and phosphatidic acid signalling in plant response to drought and salinity. Plant Cell Environ. 2010;33:627–635.
   PubMed Web of Science ®Google Scholar
• Choudhury S, Panda P, Sahoo L, et al. Reactive oxygen species signaling in plants under abiotic stress. Plant Signaling Behav. [cited 2017 Oct 29] 2013;8:e23681. [7 p.] DOI:10.4161/psb.23681
   PubMed Web of Science ®Google Scholar
• Yao Y, Liu X, Li Z, et al. Drought-induced H2O2 accumulation in subsidiary cells is involved in regulatory signaling of stomatal closure in maize leaves. Planta. 2013;238:217–227.
   PubMed Web of Science ®Google Scholar
• Miura K, Okamoto H, Okuma E, et al. SIZ1 deficiency causes reduced stomatal aperture and enhanced drought tolerance via controlling salicylic acid-induced accumulation of reactive oxygen species in Arabidopsis. Plant J. 2013;73:91–104.
   PubMed Web of Science ®Google Scholar
• Zhou XF, Jin YH, Yoo CY, et al. CYCLIN H; 1 regulates drought stress responses and blue light-induced stomatal opening by inhibiting reactive oxygen species accumulation in Arabidopsis. Plant Physiol. 2013;162:1030–1041.
   PubMed Web of Science ®Google Scholar
• Shen H, Liu C, Zhang Y, et al. OsWRKY30 is activated by MAP kinases to confer drought tolerance in rice. Plant Mol Biol. 2010;80:241–253.
   Web of Science ®Google Scholar
• Tang N, Zhang H, Li X, et al. Constitutive activation of transcription factor OsbZIP46 improves drought tolerance in rice. Plant Physiol. 2012;158:1755–1768.
   PubMed Web of Science ®Google Scholar
• Jammes F, Yang X, Xiao S, et al. Two Arabidopsis guard cell-preferential MAPK genes, MPK9 and MPK12, function in biotic stress response. Plant Signaling Behav. 2011;6:1875–1877.
   PubMedGoogle Scholar
• Salam MA, Jammes F, Hossain MA, et al. MAP kinases, MPK9 and MPK12, regulate chitosan-induced stomatal closure. Biosci Biotech Bioch. 2012;76:1785–1787.
   PubMed Web of Science ®Google Scholar
• Salam MA, Jammes F, Hossain MA, et al. Two guard cell-preferential MAPKs, MPK9 and MPK12, regulate YEL signalling in Arabidopsis guard cells. Plant Biol. 2013;15:436–442.
   PubMed Web of Science ®Google Scholar
• Yu L, Nie J, Cao C, et al. Phosphatidic acid mediates salt stress response by regulation of MPK6 in Arabidopsis thaliana. New Phytol. 2010;188:762–773.
   PubMed Web of Science ®Google Scholar
• Tsugama D, Liu S, Takano T. Drought-induced activation and rehydration-induced inactivation of MPK6 in Arabidopsis. Biochem Biophys Res Commun. 2012;426:626–629.
   PubMed Web of Science ®Google Scholar
• Kim SH, Woo DH, Kim JM, et al. Arabidopsis MKK4 mediates osmotic-stress response via its regulation of MPK3 activity. Biochem Biophys Res Commun. 2011;412:150–154.
   PubMed Web of Science ®Google Scholar
• Shi J, Zhang L, An H, et al. GhMPK16, a novel stress-responsive group D MAPK gene from cotton, is involved in disease resistance and drought sensitivity. BMC Mol Biol. [cited 2017 Oct 29] 2011;12:1. [15 p.] DOI:10.1186/1471-2199-12-22
   PubMed Web of Science ®Google Scholar
• Wang J, Ding H, Zhang A, et al. A novel mitogen-activated protein kinase gene in maize (Zea mays), ZmMPK3, is involved in response to diverse environmental cues. J Integr Plant Biol. 2010;52:442–452.
   PubMed Web of Science ®Google Scholar
• Ahmad R, Hussain J, Jamil M, et al. Glycinebetaine synthesizing transgenic potato plants exhibit enhanced tolerance to salt and cold stresses. Pak J Bot. 2014;46:1987–1993.
   Web of Science ®Google Scholar
• Zhang L, Gao M, Hu J, et al. Modulation role of abscisic acid (ABA) on growth, water relations and glycinebetaine metabolism in two maize (Zea mays L.) cultivars under drought stress. Int J Mol Sci. 2012;13:3189–3202.
   PubMed Web of Science ®Google Scholar
• Wang ML, Guo C, Wang N, et al. Cloning and characterization of a novel betaine aldehyde dehydrogenase gene from Suaeda corniculata. Genet Mol Res. [cited 2017 Oct 29] 2016;15:15027848. [14 p.] DOI:https://doi.org/10.4238/gmr.15027848
   Web of Science ®Google Scholar
• Jamil A, Riaz S, Ashraf M, et al. Gene expression profiling of plants under salt stress. Crit Rev Plant Sci. 2011;30:435–458.
   Web of Science ®Google Scholar
• Munns R, Tester M. Mechanisms of salinity tolerance. Annu Rev Plant Biol. 2008;59:651–681.
   PubMed Web of Science ®Google Scholar
• Ward JM, Hirschi KD, Sze H. Plants pass the salt. Trends Plant Sci. 2003;8:200–201.
   PubMed Web of Science ®Google Scholar
• Lv DW, Zhu GR, Zhu D, et al. Proteomic and phosphoproteomic analysis reveals the response and defense mechanism in leaves of diploid wheat T. monococcum under salt stress and recovery. J Proteomics. 2016;143:93–105.
   PubMed Web of Science ®Google Scholar
• Wu H, Liu X, You L, et al. Effects of salinity on metabolic profiles, gene expressions, and antioxidant enzymes in halophyte Suaeda salsa. J Plant Growth Regul. 2012;31:332–341.
   Web of Science ®Google Scholar
• Di H, Tian Y, Zu H, et al. Enhanced salinity tolerance in transgenic maize plants expressing a BADH gene from Atriplex micrantha. Euphytica. 2015;206:775–783.
   Web of Science ®Google Scholar
• Tang W, Sun J, Liu J, et al. RNAi-directed downregulation of betaine aldehyde dehydrogenase 1 (OsBADH1) results in decreased stress tolerance and increased oxidative markers without affecting glycine betaine biosynthesis in rice (Oryza sativa). Plant Mol Biol. 2014;86:443–454.
   PubMed Web of Science ®Google Scholar
• He Q, Yu J, Kim TS, et al. Resequencing reveals different domestication rate for BADH1 and BADH2 in rice (Oryza sativa). PloS One. [cited 2017 Oct 29] 2015;10:e0134801. [12 p.] DOI:10.1371/journal.pone.0134801
   PubMed Web of Science ®Google Scholar
• Ning J, Li X, Hicks LM, et al. A Raf-like MAPKKK gene DSM1 mediates drought resistance through reactive oxygen species scavenging in rice. Plant Physiol. 2010;152:876–890.
   PubMed Web of Science ®Google Scholar
• Kim JM, Woo DH, Kim SH, et al. Arabidopsis MKKK20 is involved in osmotic stress response via regulation of MPK6 activity. Plant Cell Rep. 2012;31:217–224.
   PubMed Web of Science ®Google Scholar
• Su SH, Suarez-Rodriguez MC, Krysan P. Genetic interaction and phenotypic analysis of the Arabidopsis MAP kinase pathway mutations mekk1 and mpk4 suggests signaling pathway complexity. FEBS Lett. 2007;581:3171–3177.
   PubMed Web of Science ®Google Scholar
• Kumar K, Rao KP, Sharma P, et al. Differential regulation of rice mitogen activated protein kinase kinase (MKK) by abiotic stress. Plant Physiol Bioch. 2008;46:891–897.
   PubMed Web of Science ®Google Scholar
• Zhao Q, Guo HW. Paradigms and paradox in the ethylene signaling pathway and interaction network. Mol Plant. 2011;4:626–634.
   PubMed Web of Science ®Google Scholar
• Xu J, Li Y, Wang Y, et al. Activation of MAPK kinase 9 induces ethylene and camalexin biosynthesis and enhances sensitivity to salt stress in Arabidopsis. J Biol Chem. 2008;283:26996–27006.
   PubMed Web of Science ®Google Scholar
• Persak H, Pitzschke A. Tight interconnection and multi-level control of Arabidopsis MYB44 in MAPK cascade signalling. PloS One. [cited 2017 Oct 29] 2013;8:e57547. [14 p.] DOI:10.1371/journal.pone.0057547
   PubMed Web of Science ®Google Scholar
• Liu XM, Nguyen XC, Kim KE, et al. Phosphorylation of the zinc finger transcriptional regulator ZAT6 by MPK6 regulates Arabidopsis seed germination under salt and osmotic stress. Biochem Biophys Res Commun. 2013;430:1054–1059.
   PubMed Web of Science ®Google Scholar
• Chattopadhayay MK, Tiwari BS, Chattopadhyay G, et al. Protective role of exogenous polyamines on salinity-stressed rice (Oryza sativa) plants. Physiol. Plantarum. 2002;116:192–199.
   PubMed Web of Science ®Google Scholar
• Basu R, Ghosh B. Polyamines in various rice (Oryza sativa) genotypes with respect to sodium chloride salinity. Physiol Plant. 1991;82:575–581.
   Web of Science ®Google Scholar
• El-Shintinawy F. Photosynthesis in two wheat cultivars differing in salt susceptibility. Photosynthetica. 2001;38:615–620.
   Web of Science ®Google Scholar
• Zapata PJ, Serrano M, Pretel MT, et al. Polyamines and ethylene changes during germination of different plant species under salinity. Plant Sci. 2004;167:781–788.
   Web of Science ®Google Scholar
• Mutlu F, Bozcuk S. Effects of salinity on the contents of polyamines and some other compounds in sunflower plants differing in salt tolerance. Russ J Plant Physiol. 2005;52:29–34.
   Web of Science ®Google Scholar
• Ahmed F, Rafii M, Ismail MR, et al. Waterlogging tolerance of crops: breeding, mechanism of tolerance, molecular approaches, and future prospects. BioMed Res Int. 2013;2013:1–10.
   Web of Science ®Google Scholar
• Mitsuya S, Yokota Y, Fujiwara T, et al. OsBADH1 is possibly involved in acetaldehyde oxidation in rice plant peroxisomes. FEBS Lett. 2009;583:3625–3629.
   PubMed Web of Science ®Google Scholar
• Theocharis A, Clément C, Barka EA. Physiological and molecular changes in plants grown at low temperatures. Planta. 2012;235:1091–1105.
   PubMed Web of Science ®Google Scholar
• Mittler R, Finka A, Goloubinoff P. How do plants feel the heat ? Trends Biochem Sci. 2012;37:118–125.
   PubMed Web of Science ®Google Scholar
• Sangwan V, Dhindsa RS. In vivo and in vitro activation of temperature-responsive plant map kinases. FEBS Lett. 2002;531:561–564.
   PubMed Web of Science ®Google Scholar
• Zhu X, Feng Y, Liang G, et al. Aequorin-based luminescence imaging reveals stimulus-and tissue-specific Ca 2+ dynamics in Arabidopsis plants. Mol Plant. 2013;6:444–455.
   PubMed Web of Science ®Google Scholar
• Nongpiur R, Soni P, Karan R, et al. Histidine kinases in plants: cross talk between hormone and stress responses. Plant Signaling Behav. 2012;7:1230–1237.
   PubMed Web of Science ®Google Scholar
• Arisz SA, Wijk R, Roels W, et al. Rapid phosphatidic acid accumulation in response to low temperature stress in Arabidopsis is generated through diacylglycerol kinase. Front Plant Sci. 2013;4:1–15.
   PubMed Web of Science ®Google Scholar
• Delage E, Ruelland E, Guillas I, et al. Arabidopsis type-III phosphatidylinositol 4-kinases beta1 and beta2 are upstream of the phospholipase C pathway triggered by cold exposure. Plant Cell Physiol. 2012;53:565–576.
   PubMed Web of Science ®Google Scholar
• Ludwig AA, Romeis T, Jones JD. CDPK-mediated signalling pathways: specificity and cross-talk. J Exp Bot. 2004;55:181–188.
   PubMed Web of Science ®Google Scholar
• Solanke AU, Sharma AK. Signal transduction during cold stress in plants. Physiol Mol Biol Plant. 2008;14:69–79.
   Google Scholar
• Sun Y, Fu L, Chen L, et al. Characterization of two winter wheat varieties' responses to freezing in a frigid region of the People's Republic of China. Can J Plant Sci. 2017;97:808–815.
   Web of Science ®Google Scholar
• Ichimura K, Mizoguchi T, Yoshida R, et al. Various abiotic stresses rapidly activate Arabidopsis MAP kinases ATMPK4 and ATMPK6. Plant J. 2000;24:655–665.
   PubMed Web of Science ®Google Scholar
• Teige M, Scheikl E, Eulgem T, et al. The MKK2 pathway mediates cold and salt stress signaling in Arabidopsis. Mol Cell. 2004;15:141–152.
   PubMed Web of Science ®Google Scholar
• Ichimura K, Mizoguchi T, Irie K, et al. Isolation of ATMEKK1 (a MAP Kinase Kinase Kinase)-interacting proteins and analysis of a MAP kinase cascade in Arabidopsis. Biochem Biophys Res Commun. 1998;253:532–543.
   PubMed Web of Science ®Google Scholar
• Pitzschke A, Schikora A, Hirt H. MAPK cascade signalling networks in plant defence. Curr Opin Plant Biol. 2009;12:421–426.
   PubMed Web of Science ®Google Scholar
• Matsuoka D, Nanmori T, Sato KI, et al. Activation of AtMEK1, an Arabidopsis mitogen-activated protein kinase kinase, in vitro and in vivo: analysis of active mutants expressed in E. coli and generation of the active form in stress response in seedlings. Plant J. 2002;29:637–647.
   PubMed Web of Science ®Google Scholar
• Evrard A, Kumar M, Lecourieux D, et al. Regulation of the heat stress response in Arabidopsis by MPK6-targeted phosphorylation of the heat stress factor HsfA2. Peer J. [cited 2017 Oct 29] 2013;1:e59. [21 p.] DOI:10.7717/peerj.59
   PubMed Web of Science ®Google Scholar
• Singer SD, Zou J, Weselake RJ. Abiotic factors influence plant storage lipid accumulation and composition. Plant Sci. 2016;243:1–9.
   PubMed Web of Science ®Google Scholar
• Suzuki N, Rivero RM, Shulaev V, et al. Abiotic and biotic stress combinations. New Phytol. 2014;203:32–43.
   PubMed Web of Science ®Google Scholar
• Mittler R. Abiotic stress, the field environment and stress combination. Trends Plant Sci. 2006;11:15–19.
   PubMed Web of Science ®Google Scholar
• Knight H, Knight MR. Abiotic stress signalling pathways: specificity and cross-talk. Trends Plant Sci. 2001;6:262–267.
   PubMed Web of Science ®Google Scholar
• Wani SH, Kumar V, Shriram V, et al. Phytohormones and their metabolic engineering for abiotic stress tolerance in crop plants. Crop J. 2016;4:162–176.
   Google Scholar
• Wang Z, Huang B. Physiological recovery of Kentucky bluegrass from simultaneous drought and heat stress. Crop Sci. 2004;44:1729–1736.
   Web of Science ®Google Scholar
• Rizhsky L, Liang H, Mittler R. The combined effect of drought stress and heat shock on gene expression in tobacco. Plant Physiol. 2002;130:1143–1151.
   PubMed Web of Science ®Google Scholar
• Rizhsky L, Liang H, Shuman J, et al. When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiol. 2004;134:1683–1696.
   PubMed Web of Science ®Google Scholar
• Fan W, Zhang M, Zhang H, et al. Improved tolerance to various abiotic stresses in transgenic sweet potato (Ipomoea batatas) expressing spinach betaine aldehyde dehydrogenase. PLoS One. [cited 2017 Oct 29] 2012;7:e37344. [14 p.] DOI:10.1371/journal.pone.0037344
   PubMed Web of Science ®Google Scholar
• Gay F, Maraval I, Roques S, et al. Effect of salinity on yield and 2-acetyl-1-pyrroline content in the grains of three fragrant rice cultivars (Oryza sativa L.) in Camargue (France). Field Crops Res. 2010;117:154–160.
   Web of Science ®Google Scholar
• Cheng LR, Wang JM, Uzokwe V, et al. Genetic analysis of cold tolerance at seedling stage and heat tolerance at anthesis in rice (Oryza sativa L.). J Integr Agric. 2012;11:359–367.
   Web of Science ®Google Scholar