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Genetic Engineering Strategies for Abiotic Stress Tolerance in Plants

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Plant Biology and Biotechnology

Abstract

Crop plants are affected by a variety of abiotic stresses such as salinity, drought, extreme temperatures, and oxidative stress and cause a significant yield loss (more than 50 %). In the near future, these abiotic stresses might increase because of global climate change. Abiotic stresses lead to dehydration or osmotic stress through reduced availability of water for vital cellular functions and maintenance of turgor pressure and also result in high production of reactive oxygen species (ROS). Plants are evolved with various mechanisms such as changes in cellular and metabolic processes to cope with the stress condition. Recent developments in molecular genetics have contributed greatly to our understanding of the biochemical and genetic basis of abiotic stress tolerance. This has led to the development of abiotic stress-tolerant plants with yield advantage by modulation of the expression of the genes that encode for enzymes involved in the biosynthesis of osmoprotectants (e.g., proline, sugars, sugar alcohol, glycine betaine, and polyamines), antioxidant enzymes, protective proteins (e.g., LEAs and HSPs), transporters, regulatory proteins, kinases, and transcription factors. More recently, posttranscriptional and posttranslational regulation mechanisms of the abiotic stress response, like microRNAs and ubiquitination, appear as promising new modulation targets to develop abiotic stress-tolerant plants and contribute to the development of more productive crops to feed the growing mass.

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References

  • Abbasi F, Onodera H, Toki S, Tanaka H, Komatsu S (2004) OsCDPK13, a calcium-dependent protein kinase gene from rice, is induced by cold and gibberellin in rice leaf sheath. Plant Mol Biol 55:541–552

    CAS  PubMed  Google Scholar 

  • Abe H, Yamaguchi-Shinozaki K, Urao T, Iwasaki T, Hosokawa D, Shinozaki K (1997) Role of arabidopsis MYC and MYB homologs in drought- and abscisic acid-regulated gene expression. Plant Cell 9:1859–1868

    CAS  PubMed Central  PubMed  Google Scholar 

  • Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell 15:63–78

    CAS  PubMed Central  PubMed  Google Scholar 

  • Abebe T, Guenzi AC, Martin B, Cushman JC (2003) Tolerance of mannitol-accumulating transgenic wheat to water stress and salinity. Plant Physiol 131:1748–1755

    CAS  PubMed Central  PubMed  Google Scholar 

  • Agarwal P, Agarwal P, Reddy MK, Sopory S (2006) Role of DREB transcription factors in abiotic and biotic stress tolerance in plants. Plant Cell Rep 25:1263–1274

    CAS  PubMed  Google Scholar 

  • Agarwal P, Shukla P, Gupta K, Jha B (2013) Bioengineering for salinity tolerance in plants: state of the art. Mol Biotechnol 54:102–123

    CAS  PubMed  Google Scholar 

  • Aharon R, Shahak Y, Wininger S, Bendov R, Kapulnik Y, Galili G (2003) Overexpression of a plasma membrane aquaporin in transgenic tobacco improves plant vigor under favorable growth conditions but not under drought or salt stress. Plant Cell 15:439–447

    CAS  PubMed Central  PubMed  Google Scholar 

  • Albrecht V, Weinl S, Blazevic D, D’Angelo C, Batistic O, Kolukisaoglu Ü, Bock R, Schulz B, Harter K, Kudla J (2003) The calcium sensor CBL1 integrates plant responses to abiotic stresses. Plant J 36:457–470

    CAS  PubMed  Google Scholar 

  • Alcazar R, Marco F, Cuevas JC, Patron M, Ferrando A, Carrasco P, Tiburcio AF, Altabella T (2006) Involvement of polyamines in plant response to abiotic stress. Biotechnol Lett 28:1867–1876

    CAS  PubMed  Google Scholar 

  • Alcázar R, Altabella T, Marco F, Bortolotti C, Reymond M, Koncz C, Carrasco P, Tiburcio A (2010) Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. Planta 231:1237–1249

    PubMed  Google Scholar 

  • Almeida AM, Villalobos E, Araujo SS, Leyman B et al (2005) Transformation of tobacco with an Arabidopsis thaliana gene involved in trehalose biosynthesis increases tolerance to several abiotic stresses. Euphytica 146:165–176

    CAS  Google Scholar 

  • Al-Taweel K, Iwaki T, Yabuta Y, Shigeoka S, Murata N, Wadano A (2007) A bacterial transgene for catalase protects translation of D1 protein during exposure of salt-stressed tobacco leaves to strong light. Plant Physiol 145:258–265

    CAS  PubMed Central  PubMed  Google Scholar 

  • An Z, Jing W, Liu Y, Zhang W (2008) Hydrogen peroxide generated by copper amine oxidase is involved in abscisic acid-induced stomatal closure in Vicia faba. J Exp Bot 59:815–825

    CAS  PubMed  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    CAS  PubMed  Google Scholar 

  • Apse MP, Aharon GS, Snedden WA, Blumwald E (1999) Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science 285:1256–1258

    CAS  PubMed  Google Scholar 

  • Ariizumi T, Kishitani S, Inatsugi R, Nishida I, Murata N, Toriyama K (2002) An increase in unsaturation of fatty acids in phosphatidylglycerol from leaves improves the rates of photosynthesis and growth at low temperatures in transgenic rice seedlings. Plant Cell Physiol 43:751–758

    CAS  PubMed  Google Scholar 

  • Asano T, Hakata M, Nakamura H, Aoki N, Komatsu S, Ichikawa H, Hirochika H, Ohsugi R (2011) Functional characterisation of OsCPK21, a calcium-dependent protein kinase that confers salt tolerance in rice. Plant Mol Biol 75:179–191

    CAS  PubMed  Google Scholar 

  • Asano T, Hayashi N, Kobayashi M, Aoki N, Miyao A, Mitsuhara I, Ichikawa H, Komatsu S, Hirochika H, Kikuchi S, Ohsugi R (2012) A rice calcium-dependent protein kinase OsCPK12 oppositely modulates salt-stress tolerance and blast disease resistance. Plant J 69:26–36

    CAS  PubMed  Google Scholar 

  • Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216

    CAS  Google Scholar 

  • Badawi GH, Kawano N, Yamauchi Y, Shimada E, Sasaki R, Kubo A, Tanaka K (2004) Over-expression of ascorbate peroxidase in tobacco chloroplasts enhances the tolerance to salt stress and water deficit. Physiol Plant 121:231–238

    CAS  PubMed  Google Scholar 

  • Bahieldin A, Mahfouz HT, Eissa HF, Saleh OM, Ramadan AM, Ahmed IA, Dyer WE, El-Itriby HA, Madkour MA (2005) Field evaluation of transgenic wheat plants stably expressing the HVA1 gene for drought tolerance. Physiol Plant 123:421–427

    CAS  Google Scholar 

  • Bartels D (2005) Desiccation tolerance studied in the resurrection plant Craterostigma plantagineum. Integr Comp Biol 45:696–701

    CAS  PubMed  Google Scholar 

  • Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. Crit Rev Plant Sci 24:23–58

    CAS  Google Scholar 

  • Battaglia M, Olvera-Carrillo Y, Garciarrubio A, Campos F, Covarrubias AA (2008) The enigmatic LEA proteins and other hydrophilins. Plant Physiol 148:6–24

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bhatnagar-Mathur P, Devi MJ, Reddy DS, Lavanya M, Vadez V, Serraj R, Yamaguchi-Shinozaki K, Sharma K (2007) Stress-inducible expression of At DREB1A in transgenic peanut (Arachis hypogaea L.) increases transpiration efficiency under water-limiting conditions. Plant Cell Rep 26:2071–2082

    CAS  PubMed  Google Scholar 

  • Bhatnagar-Mathur P, Vadez V, Sharma KK (2008) Transgenic approaches for abiotic stress tolerance in plants: retrospect and prospects. Plant Cell Rep 27:411–424

    CAS  PubMed  Google Scholar 

  • Bhattacharya E, Rajam MV (2006) Polyamine biosynthesis as a novel target for engineering crop plants for abiotic stress tolerance. J Plant Biol 33:99–105

    CAS  Google Scholar 

  • Bitrián M, Zarza X, Altabella T, Tiburcio AF, Alcázar R (2012) Polyamines under abiotic stress: metabolic crossroads and hormonal crosstalks in plants. Metabolites 2:516–528

    PubMed Central  PubMed  Google Scholar 

  • Bohnert HJ, Jensen RG (1996) Strategies for engineering water-stress tolerance in plants. Trends Biotechnol 14:89–97

    CAS  Google Scholar 

  • Bohnert HJ, Ayoubi P, Borchert C, Bressan RA et al (2001) A genomics approach towards salt stress tolerance. Plant Physiol Biochem 39:295–311

    CAS  Google Scholar 

  • Bors W, Langebartels C, Michel C, Sandermann H Jr (1989) Polyamines as radical scavengers and protectants against ozone damage. Phytochemistry 28:1589–1595

    CAS  Google Scholar 

  • Bouchereau A, Aziz A, Larher F, Martin-Tanguy J (1999) Polyamines and environmental challenges: recent development. Plant Sci 140:103–125

    CAS  Google Scholar 

  • Boudsocq M, Laurière C (2005) Osmotic signaling in plants – Multiple pathways mediated by emerging kinase families. Plant Physiol 138:1185–1194

    CAS  PubMed Central  PubMed  Google Scholar 

  • Boudsocq M, Sheen J (2013) CDPKs in immune and stress signaling. Trends Plant Sci 18:30–40

    CAS  PubMed Central  PubMed  Google Scholar 

  • Boyko A, Kovalchuk I (2008) Epigenetic control of plant stress response. Environ Mol Mutagen 49:61–72

    CAS  PubMed  Google Scholar 

  • Cabello JV, Lodeyro AF, Zurbriggen MD (2014) Novel perspectives for the engineering of abiotic stress tolerance in plants. Curr Opin Biotechnol 26:62–70

    CAS  PubMed  Google Scholar 

  • Cai G, Wang G, Wang L, Pan J, Liu Y, Li D (2014) ZmMKK1, a novel group A mitogen-activated protein kinase kinase gene in maize, conferred chilling stress tolerance and was involved in pathogen defense in transgenic tobacco. Plant Sci 214:57–73

    CAS  PubMed  Google Scholar 

  • Castiglioni P, Warner D, Bensen RJ, Anstrom DC et al (2008) Bacterial RNA chaperones confer abiotic stress tolerance in plants and improved grain yield in maize under water-limited conditions. Plant Physiol 147:446–455

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chae HB, Moon JC, Shin MR, Chi YH, Jung YJ, Lee SY, Nawkar GM, Jung HS, Hyun JK, Kim WY, Kang CH, Yun DJ, Lee KO (2013) Thioredoxin reductase type C (NTRC) orchestrates enhanced thermotolerance to Arabidopsis by its redox-dependent holdase chaperone function. Mol Plant 6:323–336

    CAS  PubMed  Google Scholar 

  • Chan Z, Grumet R, Loescher W (2011) Global gene expression analysis of transgenic, mannitol-producing, and salt-tolerant Arabidopsis thaliana indicates widespread changes in abiotic and biotic stress-related genes. J Exp Bot 62:4787–4803

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chatzidimitriadou K, Nianiou-Obeidat I, Madesis P, Perl-Treves R, Tsaftaris A (2009) Expression of SOD transgene in pepper confer stress tolerance and improve shoot regeneration. Electron J Biotechnol 12:7–8

    Google Scholar 

  • Checker V, Chhibbar A, Khurana P (2012) Stress-inducible expression of barley Hva1 gene in transgenic mulberry displays enhanced tolerance against drought, salinity and cold stress. Transgenic Res 21:939–957

    CAS  PubMed  Google Scholar 

  • Chen THH, Murata N (2002) Enhancement of tolerance of abiotic stress by metabolic engineering of betaines and other compatible solutes. Curr. Opin. Plant Biol. 5:250–257

    Google Scholar 

  • Chen THH, Murata N (2008) Glycinebetaine: an effective protectant against abiotic stress in plants. Trends Plant Sci 13:499–505

    CAS  PubMed  Google Scholar 

  • Chen THH, Murata N (2011) Glycinebetaine protects plants against abiotic stress: mechanisms and biotechnological applications. Plant Cell Environ 34:1–20

    PubMed  Google Scholar 

  • Chen M, Chen QJ, Niu XG, Zhang R, Lin HQ, Xu CY, Wang XC, Wang GY, Chen J (2007) Expression of OsNHX1 gene in maize confers salt tolerance and promotes plant growth in the field. Plant Soil Environ 11:490–498

    Google Scholar 

  • Cheong YH, Kim K-N, Pandey GK, Gupta R, Grant JJ, Luan S (2003) CBL1, a calcium sensor that differentially regulates salt, drought, and cold responses in Arabidopsis. Plant Cell 15:1833–1845

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cheong Y, Sung S, Kim B-G, Pandey G, Cho JS, Kim KN, Luan S (2010) Constitutive overexpression of the calcium sensor CBL5 confers osmotic or drought stress tolerance in Arabidopsis. Mol Cells 29:159–165

    CAS  PubMed  Google Scholar 

  • Chinnusamy V, Zhu J, Zhu JK (2007) Cold stress regulation of gene expression in plants. Trends Plant Sci 12:444–451

    CAS  PubMed  Google Scholar 

  • Cramer G, Urano K, Delrot S, Pezzotti M, Shinozaki K (2011) Effects of abiotic stress on plants: a systems biology perspective. BMC Plant Biol 11:163

    PubMed Central  PubMed  Google Scholar 

  • de Lima JC, Loss-Morais G, Margis R (2012) MicroRNAs play critical roles during plant development and in response to abiotic stresses. Genet Mol Biol 35:1069–1077

    PubMed Central  PubMed  Google Scholar 

  • Delauney AJ, Verma DPS (1993) Proline biosynthesis and osmoregulation in plants. Plant J 4:215–223

    CAS  Google Scholar 

  • Deng X, Hu W, Wei S, Zhou S, Zhang F, Han J, Chen L, Li Y, Feng J, Fang B, Luo Q, Li S, Liu Y, Yang G, He G (2013) TaCIPK29, a CBL-interacting protein kinase gene from wheat, confers salt stress tolerance in transgenic tobacco. PLoS One 8:e69881

    CAS  PubMed Central  PubMed  Google Scholar 

  • Diedhiou C, Popova O, Dietz KJ, Golldack D (2008) The SNF1-type serine-threonine protein kinase SAPK4 regulates stress-responsive gene expression in rice. BMC Plant Biol 8:49

    PubMed Central  PubMed  Google Scholar 

  • Dietz-Pfeilstetter A (2010) Stability of transgene expression as a challenge for genetic engineering. Plant Sci 179:164–167

    CAS  Google Scholar 

  • Drennan PM, Smith MT, Goldsworthy D, van Staden J (1993) The occurrence of trehalose in the leaves of the desiccation-tolerant angiosperm Myrothamnus flabellifolius Welw. J Plant Physiol 142:493–496

    CAS  Google Scholar 

  • Elbein AD, Pan YT, Pastuszak I, Carroll D (2003) New insights on trehalose: a multifunctional molecule. Glycobiology 13:17R–27R

    CAS  PubMed  Google Scholar 

  • Everard JD, Gucci R, Kann SC, Flore JA, Loescher WH (1994) Gas exchange and carbon partitioning in the leaves of celery (Apium graveolens L.) at various levels of root zone salinity. Plant Physiol 106:281–292

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fernandez O, Béthencourt L, Quero A, Sangwan RS, Clément C (2010) Trehalose and plant stress responses: friend or foe? Trends Plant Sci 15:409–417

    CAS  PubMed  Google Scholar 

  • Feuerstein BG, Marton LJ (1989) Specificity and binding in polyamine/nucleic acid interactions. In: Bachrach U, Heimer YM (eds) The physiology of polyamines, vol I. CRC Press, Boca Raton, pp 109–124

    Google Scholar 

  • Fowler S, Thomashow MF (2002) Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. Plant Cell 14:1675–1690

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fujita M, Fujita Y, Maruyama K, Seki M, Hiratsu K, Ohme-Takagi M, Tran LS, Yamaguchi-Shinozaki K, Shinozaki K (2004) A dehydration-induced NAC protein, RD26, is involved in a novel ABA-dependent stress-signaling pathway. Plant J 39:863–876

    CAS  PubMed  Google Scholar 

  • Fujita Y, Fujita M, Satoh R, Maruyama K, Parvez MM, Seki M, Hiratsu K, Ohme-Takagi M, Shinozaki K, Yamaguchi-Shinozaki K (2005) AREB1 is a transcription activator of novel ABRE-dependent ABA signaling that enhances drought stress tolerance in Arabidopsis. Plant Cell 17:3470–3488

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fukuda A, Nakamura A, Tagiri A, Tanaka H, Miyao A, Hirochika H, Tanaka Y (2004) Function, intracellular localization and the importance in salt tolerance of a vacuolar Na(+)/H(+) antiporter from rice. Plant Cell Physiol 45:146–159

    CAS  PubMed  Google Scholar 

  • Galau G, Hughes DW, Dure L III (1986) Abscisic acid induction of cloned cotton late embryogenesis-abundant (Lea) mRNAs. Plant Mol Biol 7:155–170

    CAS  PubMed  Google Scholar 

  • Gao F, Gao Q, Duan X, Yue G, Yang A, Zhang J (2006) Cloning of an H+-PPase gene from Thellungiella halophila and its heterologous expression to improve tobacco salt tolerance. J Exp Bot 57:3259–3270

    CAS  PubMed  Google Scholar 

  • Gao Z, He X, Zhao B, Zhou C, Liang Y, Ge R, Shen Y, Huang Z (2010) Overexpressing a putative aquaporin gene from wheat, TaNIP, enhances salt tolerance in transgenic Arabidopsis. Plant Cell Physiol 51:767–775

    CAS  PubMed  Google Scholar 

  • Gaxiola RA, Li J, Undurraga S, Dang LM, Allen GJ, Alper SL, Fink GR (2001) Drought and salt-tolerant plants result from overexpression of the AVP1 H+-pump. Proc Natl Acad Sci U S A 98:11444–11449

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930

    CAS  PubMed  Google Scholar 

  • Glenn EP, Brown JJ, Blumwald E (1999) Salt tolerance and crop potential of halophytes. Crit Rev Plant Sci 18:227–255

    Google Scholar 

  • Goddijn OJM, van Dun K (1999) Trehalose metabolism in plants. Trends Plant Sci 4:315–319

    PubMed  Google Scholar 

  • Goyal K, Walton LJ, Tunnacliffe A (2005) LEA proteins prevent protein aggregation due to water stress. Biochem J 388:151–157

    CAS  PubMed Central  PubMed  Google Scholar 

  • Groppa MD, Benavides MP (2008) Polyamines and abiotic stress: recent advances. Amino Acids 34:35–45

    CAS  PubMed  Google Scholar 

  • Gu L, Liu Y, Zong X, Liu L, Li DP, Li DQ (2010) Overexpression of maize mitogen-activated protein kinase gene, ZmSIMK1 in Arabidopsis increases tolerance to salt stress. Mol Biol Rep 37:4067–4073

    CAS  PubMed  Google Scholar 

  • Guo L, Wang ZY, Lin H, Cui WE, Chen J, Liu M, Chen ZL, Qu LJ, Gu H (2006) Expression and functional analysis of the rice plasma-membrane intrinsic protein gene family. Cell Res 16:277–286

    CAS  PubMed  Google Scholar 

  • Guo Q, Zhang J, Gao Q, Xing S, Li F, Wang W (2008) Drought tolerance through overexpression of monoubiquitin in transgenic tobacco. J Plant Physiol 165:1745–1755

    CAS  PubMed  Google Scholar 

  • Gupta B, Rajam MV (2013) Marker-free transgenic tomato with engineered mannitol accumulation confers tolerance to multiple abiotic stresses. Cell Dev Biol 2:113. doi:10.4172/2168-9296.1000113

    Google Scholar 

  • Gupta AS, Heinen JL, Holaday AS, Burke JJ, Allen RD (1993) Increased resistance to oxidative stress in transgenic plants that overexpress chloroplastic Cu/Zn superoxide dismutase. Proc Natl Acad Sci U S A 90:1629–1633

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gusta L, Benning N, Wu G, Luo X, Liu X, Gusta M, McHughen A (2009) Superoxide dismutase: an all-purpose gene for agri-biotechnology. Mol Breed 24:103–115

    CAS  Google Scholar 

  • Halliwell B (2006) Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiol 141:312–322

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hara M, Terashima S, Fukaya T, Kuboi T (2003) Enhancement of cold tolerance and inhibition of lipid peroxidation by citrus dehydrin in transgenic tobacco. Planta 217:290–298

    CAS  PubMed  Google Scholar 

  • Hasanuzzaman M, Nahar K, Alam MM, Roychowdhury R, Fujita M (2013) Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. Int J Mol Sci 14:9643–9684

    PubMed Central  PubMed  Google Scholar 

  • Hazarika P, Rajam MV (2011) Biotic and abiotic stress tolerance in transgenic tomatoes by constitutive expression of S-adenosylmethionine decarboxylase gene. Physiol Mol Biol Plants 17:115–128

    CAS  PubMed Central  PubMed  Google Scholar 

  • He C, Yan J, Shen G, Fu L, Holaday AS, Auld D, Blumwald E, Zhang H (2005) Expression of an Arabidopsis vacuolar sodium/proton antiporter gene in cotton improves photosynthetic performance under salt conditions and increases fiber yield in the field. Plant Cell Physiol 46:1848–1854

    CAS  PubMed  Google Scholar 

  • He C, Yang A, Zhang W, Gao Q, Zhang J (2010) Improved salt tolerance of transgenic wheat by introducing betA gene for glycine betaine synthesis. Plant Cell Tissue Organ Cult 101:65–78

    CAS  Google Scholar 

  • Hobo T, Kowyama Y, Hattori T (1999) A bZIP factor, TRAB1, interacts with VP1 and mediates abscisic acid-induced transcription. Proc Natl Acad Sci U S A 96:15348–15353

    CAS  PubMed Central  PubMed  Google Scholar 

  • Holtorf S, Apel K, Bohlmann H (1995) Comparison of different constitutive and inducible promoters for the overexpression of transgenes in Arabidopsis thaliana. Plant Mol Biol 29:637–646

    CAS  PubMed  Google Scholar 

  • Houde M, Dallaire S, N’Dong D, Sarhan F (2004) Overexpression of the acidic dehydrin WCOR410 improves freezing tolerance in transgenic strawberry leaves. Plant Biotechnol J 2:381–387

    CAS  PubMed  Google Scholar 

  • Hu L, Lu H, Liu Q, Chen X, Jiang X (2005) Overexpression of mtlD gene in transgenic Populus tomentosa improves salt tolerance through accumulation of mannitol. Tree Physiol 25:1273–1281

    CAS  PubMed  Google Scholar 

  • Hu H, Dai M, Yao J, Xiao B, Li X, Zhang Q, Xiong L (2006) Overexpressing a NAM, ATAF, and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice. Proc Natl Acad Sci U S A 103:12987–12992

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hu H, You J, Fang Y, Zhu X, Qi Z, Xiong L (2008) Characterization of transcription factor gene SNAC2 conferring cold and salt tolerance in rice. Plant Mol Biol 67:169–181

    CAS  PubMed  Google Scholar 

  • Hu W, Yuan Q, Wang Y, Cai R, Deng X, Wang J, Zhou S, Chen M, Chen L, Huang C, Ma Z, Yang G, He G (2012) Overexpression of a wheat aquaporin gene, TaAQP8, enhances salt stress tolerance in transgenic tobacco. Plant Cell Physiol 53:2127–2141

    CAS  PubMed  Google Scholar 

  • Hussain SS, Kayani MA, Amjad M (2011) Transcription factors as tools to engineer enhanced drought stress tolerance in plants. Biotechnol Prog 27:297–306

    CAS  PubMed  Google Scholar 

  • Hwa CM, Yang XC (2008) The AtMKK3 pathway mediates ABA and salt signaling in Arabidopsis. Acta Physiol Plant 30:277–286

    CAS  Google Scholar 

  • Iordachescu M, Imai R (2008) Trehalose biosynthesis in response to abiotic stresses. J Integr Plant Biol 50:1223–1229

    CAS  PubMed  Google Scholar 

  • Janska A, Marsik P, Zelenkova S, Ovesna J (2009) Cold stress and acclimation – what is important for metabolic adjustment? Plant Biol 12:395–405

    Google Scholar 

  • John R, Pandey R, Sopory SK, Rajam MV (2010) Engineering antioxidant enzymes for abiotic stress tolerance in plants. J Plant Biol 37:1–18

    Google Scholar 

  • Jy K, Hi C, MY I, Kim SY (2002) Arabidopsis basic leucine zipper proteins that mediate stress-responsive abscisic acid signaling. Plant Cell 14:343–357

    Google Scholar 

  • Karakas B, OziasAkins P, Stushnoff C, Suefferheld M, Rieger M (1997) Salinity and drought tolerance of mannitol-accumulating transgenic tobacco. Plant Cell Environ 20:609–616

    Google Scholar 

  • Kasuga M, Liu Q, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1999) Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat Biotechnol 17:287–291

    CAS  PubMed  Google Scholar 

  • Kasuga M, Miura S, Shinozaki K, Yamaguchi-Shinozaki K (2004) A combination of the Arabidopsis DREB1A gene and stress-inducible rd29A promoter improved drought- and low-temperature stress tolerance in tobacco by gene transfer. Plant Cell Physiol 45:346–350

    CAS  PubMed  Google Scholar 

  • Katiyar-Agarwal S, Agarwal M, Grover A (2003) Heat-tolerant basmati rice engineered by over-expression of hsp101. Plant Mol Biol 51:677–686

    CAS  PubMed  Google Scholar 

  • Katsuhara M, Koshio K, Shibasaka M, Hayashi Y, Hayakawa T, Kasamo K (2003) Over-expression of a barley aquaporin increased the shoot/root ratio and raised salt sensitivity in transgenic rice plants. Plant Cell Physiol 44:1378–1383

    CAS  PubMed  Google Scholar 

  • Kavi Kishor PB, Sreenivasulu N (2014) Is proline accumulation per se correlated with stress tolerance or is proline homeostasis a more critical issue? Plant Cell Environ 37:300–311

    CAS  PubMed  Google Scholar 

  • Kavitha K, Venkataraman G, Parida A (2008) An oxidative and salinity stress induced peroxisomal ascorbate peroxidase from Avicennia marina: molecular and functional characterization. Plant Physiol Biochem 46:794–804

    CAS  PubMed  Google Scholar 

  • Khraiwesh B, Zhu JK, Zhu J (2012) Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants – gene regulatory mechanisms. Biochim Biophys Acta 1819:137–148

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kim KN, Cheong YH, Gupta R, Luan S (2000) Interaction specificity of Arabidopsis calcineurin B-like calcium sensors and their target kinases. Plant Physiol 124:1844–1853

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kim S, Kang J, Cho DI, Park JH, Kim SY (2004) ABF2, an ABRE-binding bZIP factor, is an essential component of glucose signaling and its overexpression affects multiple stress tolerance. Plant J 40:75–87

    CAS  PubMed  Google Scholar 

  • Kim JM, To TK, Nishioka T, Seki M (2010) Chromatin regulation functions in plant abiotic stress responses. Plant Cell Environ 33:604–611

    PubMed  Google Scholar 

  • Kirch HH, Bartels D, Wei Y, Schnable PS, Wood AJ (2004) The ALDH gene superfamily of Arabidopsis. Trends Plant Sci 9:371–377

    CAS  PubMed  Google Scholar 

  • Ko JH, Yang SH, Han K-H (2006) Upregulation of an Arabidopsis RING-H2 gene, XERICO, confers drought tolerance through increased abscisic acid biosynthesis. Plant J 47:343–355

    CAS  PubMed  Google Scholar 

  • Kong X, Pan J, Zhang M, Xing XIN, Zhou YAN, Liu Y, Li D, Li D (2011) ZmMKK4, a novel group C mitogen-activated protein kinase kinase in maize (Zea mays), confers salt and cold tolerance in transgenic Arabidopsis. Plant Cell Environ 34:1291–1303

    CAS  PubMed  Google Scholar 

  • Kotak S, Larkindale J, Lee U, von Koskull-Doring P, Vierling E, Scharf KD (2007) Complexity of the heat stress response in plants. Curr Opin Plant Biol 10:310–316

    CAS  PubMed  Google Scholar 

  • Kovtun Y, Chiu WL, Tena G, Sheen J (2000) Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proc Natl Acad Sci U S A 97:2940–2945

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kumar K, Sinha AK (2013) Overexpression of constitutively active mitogen activated protein kinase kinase 6 enhances tolerance to salt stress in rice. Rice (NY) 6:25

    Google Scholar 

  • Kumar SV, Sharma ML, Rajam MV (2006) Polyamine biosynthetic pathway as a novel target for potential applications in agriculture and biotechnology. Physiol Mol Biol Plants 12:13–28

    CAS  Google Scholar 

  • Kumria R, Rajam MV (2002) Ornithine decarboxylase transgene in tobacco affects polyamines, in vitro morphogenesis and response to salt stress. J Plant Physiol 159:983–990

    CAS  Google Scholar 

  • Kusano T, Berberich T, Tateda C, Takahashi Y (2008) Polyamines: essential factors for growth and survival. Planta 228:367–381

    CAS  PubMed  Google Scholar 

  • Laloi C, Apel K, Danon A (2004) Reactive oxygen signalling: the latest news. Curr Opin Plant Biol 7:323–328

    CAS  PubMed  Google Scholar 

  • Lechner E, Leonhardt N, Eisler H, Parmentier Y, Alioua M, Jacquet H, Leung J, Genschik P (2011) MATH/BTB CRL3 receptors target the homeodomain-leucine zipper ATHB6 to modulate abscisic acid signaling. Dev Cell 21:1116–1128

    CAS  PubMed  Google Scholar 

  • Lee JH, Kim W (2011) Regulation of abiotic stress signal transduction by E3 ubiquitin ligases in Arabidopsis. Mol Cells 31:201–208

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lee YP, Kim SH, Bang JW, Lee HS, Kwak SS, Kwon SY (2007) Enhanced tolerance to oxidative stress in transgenic tobacco plants expressing three antioxidant enzymes in chloroplasts. Plant Cell Rep 26:591–598

    CAS  PubMed  Google Scholar 

  • Lee HK, Cho SK, Son O, Xu Z, Hwang I, Kim WT (2009) Drought stress-induced Rma1H1, a RING membrane-anchor E3 ubiquitin ligase homolog, regulates aquaporin levels via ubiquitination in transgenic Arabidopsis plants. Plant Cell Online 21:622–641

    CAS  Google Scholar 

  • Li B, Wei A, Song C, Li N, Zhang J (2008) Heterologous expression of the TsVP gene improves the drought resistance of maize. Plant Biotechnol J 6:146–159

    CAS  PubMed  Google Scholar 

  • Li H, Jiang H, Bu Q, Zhao Q, Sun J, Xie Q, Li C (2011a) The Arabidopsis RING finger E3 ligase RHA2b acts additively with RHA2a in regulating abscisic acid signaling and drought response. Plant Physiol 156:550–563

    CAS  PubMed Central  PubMed  Google Scholar 

  • Li M, Li Y, Li H, Wu G (2011b) Overexpression of AtNHX5 improves tolerance to both salt and drought stress in Broussonetia papyrifera (L.) Vent. Tree Physiol 31:349–357

    CAS  PubMed  Google Scholar 

  • Li M, Lin X, Li H, Pan X, Wu G (2011c) Overexpression of AtNHX5 improves tolerance to both salt and water stress in rice (Oryza sativa L.). Plant Cell Tissue Organ Cult 107:283–293

    CAS  Google Scholar 

  • Li DD, Xia XL, Yin WL, Zhang HC (2013) Two poplar calcineurin B-like proteins confer enhanced tolerance to abiotic stresses in transgenic Arabidopsis thaliana. Biol Plant 57:70–78

    CAS  Google Scholar 

  • Li G, Santoni V, Maurel C (2014) Plant aquaporins: roles in plant physiology. Biochim Biophys Acta 1840:1574–1582

    CAS  PubMed  Google Scholar 

  • Lian HL, Yu X, Ye Q, Ding XS, Kitagawa Y, Kwak SS, Su WA, Tang ZC (2004) The role of aquaporin RWC3 in drought avoidance in rice. Plant Cell Physiol 45:481–489

    CAS  PubMed  Google Scholar 

  • Liang J, Zhou M, Zhou X, Jin Y, Xu M, Lin J (2013) JcLEA, a novel LEA-like protein from Jatropha curcas, confers a high level of tolerance to dehydration and salinity in Arabidopsis thaliana. PLoS One 8:e83056

    PubMed Central  PubMed  Google Scholar 

  • Lindemose S, Shea C, Jensen M, Skriver K (2013) Structure, function and networks of transcription factors involved in abiotic stress responses. Int J Mol Sci 14:5842–5878

    CAS  PubMed Central  PubMed  Google Scholar 

  • Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10:1391–1406

    CAS  PubMed Central  PubMed  Google Scholar 

  • Liu H, Wang Q, Yu M, Zhang Y, Wu Y, Zhang H (2008) Transgenic salt-tolerant sugar beet (Beta vulgaris L.) constitutively expressing an Arabidopsis thaliana vacuolar Na/H antiporter gene, AtNHX3, accumulates more soluble sugar but less salt in storage roots. Plant Cell Environ 31:1325–1334

    CAS  PubMed  Google Scholar 

  • Lu Z, Liu D, Liu S (2007) Two rice cytosolic ascorbate peroxidases differentially improve salt tolerance in transgenic Arabidopsis. Plant Cell Rep 26:1909–1917

    CAS  PubMed  Google Scholar 

  • Lu W, Chu X, Li Y, Wang C, Guo X (2013) Cotton GhMKK1 induces the tolerance of salt and drought stress, and mediates defence responses to pathogen infection in transgenic Nicotiana benthamiana. PLoS One 8:e68503

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lv S, Zhang K, Gao Q, Lian L, Song Y, Zhang J (2008) Overexpression of an H+-PPase Gene from Thellungiella halophila in cotton enhances salt tolerance and improves growth and photosynthetic performance. Plant Cell Physiol 49:1150–1164

    CAS  PubMed  Google Scholar 

  • Lv SL, Lian LJ, Tao PL, Li ZX, Zhang KW, Zhang JR (2009) Overexpression of Thellungiella halophila H+-PPase (TsVP) in cotton enhances drought stress resistance of plants. Planta 229:899–910

    CAS  PubMed  Google Scholar 

  • Lyzenga WJ, Stone SL (2012) Abiotic stress tolerance mediated by protein ubiquitination. J Exp Bot 63:599–616

    CAS  PubMed  Google Scholar 

  • Ma SY, Wu WH (2007) AtCPK23 functions in Arabidopsis responses to drought and salt stresses. Plant Mol Biol 65:511–518

    CAS  PubMed  Google Scholar 

  • Maeda T, Wurgler-Murphy SM, Saito H (1994) A two-component system that regulates an osmosensing MAP kinase cascade in yeast. Nature 369:242–245

    CAS  PubMed  Google Scholar 

  • Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444:139–158

    CAS  PubMed  Google Scholar 

  • Malik MK, Slovin JP, Hwang CH, Zimmerman JL (1999) Modified expression of a carrot small heat shock protein gene, Hsp17.7, results in increased or decreased thermotolerance. Plant J 20:89–99

    CAS  PubMed  Google Scholar 

  • Maqbool A, Abbas W, Rao AQ, Irfan M, Zahur M, Bakhsh A, Riazuddin S, Husnain T (2010) Gossypium arboreum GHSP26 enhances drought tolerance in Gossypium hirsutum. Biotechnol Prog 26:21–25

    CAS  PubMed  Google Scholar 

  • Marco F, Alcázar R, Altabella T, Carrasco P, Gill SS, Tuteja N, Tiburcio AF (2012) Polyamines in developing stress-resistant crops. In: Tuteja N, Gill SS, Tiburcio AF, tuteja R (eds) Improving crop resistance to abiotic stress. Wiley-VCH Verlag GmbH & Co., KGaA, Weinheim, pp 623–635

    Google Scholar 

  • Mastrangelo AM, Marone D, Laidò G, De Leonardis AM, De Vita P (2012) Alternative splicing: enhancing ability to cope with stress via transcriptome plasticity. Plant Sci 185–186:40–49

    PubMed  Google Scholar 

  • Matsuda O, Iba K (2005) Trienoic fatty acids and stress responses in higher plants. Plant Biotechnol 22:423–430

    CAS  Google Scholar 

  • Matsukura S, Mizoi J, Yoshida T, Todaka D, Ito Y, Maruyama K, Shinozaki K, Yamaguchi-Shinozaki K (2010) Comprehensive analysis of rice DREB2-type genes that encode transcription factors involved in the expression of abiotic stress-responsive genes. Mol Gen Genomics 283:185–196

    CAS  Google Scholar 

  • Matsumura T, Tabayashi N, Kamagata Y, Souma C, Saruyama H (2002) Wheat catalase expressed in transgenic rice can improve tolerance against low temperature stress. Physiol Plant 116:317–327

    CAS  Google Scholar 

  • Mazzucotelli E, Mastrangelo AM, Crosatti C, Guerra D, Stanca AM, Cattivelli L (2008) Abiotic stress response in plants: when post-transcriptional and post-translational regulations control transcription. Plant Sci 174:420–431

    CAS  Google Scholar 

  • McElroy D, Rothenberg M, Wu R (1990) Structural characterization of a rice actin gene. Plant Mol Biol 14:163–171

    CAS  PubMed  Google Scholar 

  • McKersie BD, Bowley SR, Harjanto E, Leprince O (1996) Water-deficit tolerance and field performance of transgenic alfalfa overexpressing superoxide dismutase. Plant Physiol 111:1177–1181

    CAS  PubMed Central  PubMed  Google Scholar 

  • Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33:453–467

    CAS  PubMed  Google Scholar 

  • Mittler R (2006) Abiotic stress, the field environment and stress combination. Trends Plant Sci 11:15–19

    CAS  PubMed  Google Scholar 

  • Mittler R, Blumwald E (2010) Genetic engineering for modern agriculture: challenges and perspectives. Annu Rev Plant Biol 61:443–462

    CAS  PubMed  Google Scholar 

  • Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K, Gollery M, Shulaev V, Van Breusegem F (2011) ROS signaling: the new wave? Trends Plant Sci 16:300–309

    CAS  PubMed  Google Scholar 

  • Miura K, Jin JB, Hasegawa PM (2007) Sumoylation, a post-translational regulatory process in plants. Curr Opin Plant Biol 10:495–502

    CAS  PubMed  Google Scholar 

  • Miura K, Ohta M, Nakazawa M, Ono M, Hasegawa PM (2011) ICE1 Ser403 is necessary for protein stabilization and regulation of cold signaling and tolerance. Plant J 67:269–279

    CAS  PubMed  Google Scholar 

  • Mizoi J, Yamaguchi-Shinozaki K (2012) Molecular approaches to improve rice abiotic stress tolerance. In: Yang Y (ed) Rice protocols, vol 956, Methods in molecular biology. Springer Science + Business Media LLC, New York, pp 269–283

    Google Scholar 

  • MONSANTO: petition for the determination of non-regulated status for MON 87460. http://www.aphis.usda.gov/brs/aphisdocs/09_05501p.pdf. Assessed 29 Jul 2012

  • Moriwaki T, Yamamoto Y, Aida T, Funahashi T, Shishido T, Asada M, Prodhan S, Komamine A, Motohashi T (2008) Overexpression of the Escherichia coli catalase gene, katE, enhances tolerance to salinity stress in the transgenic indica rice cultivar, BR5. Plant Biotechnol Rep 2:41–46

    Google Scholar 

  • Moschou PN, Wu J, Cona A, Tavladoraki P, Angelini R, Roubelakis-Angelakis KA (2012) The polyamines and their catabolic products are significant players in the turnover of nitrogenous molecules in plants. J Exp Bot 63:5003–5015

    CAS  PubMed  Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681

    CAS  PubMed  Google Scholar 

  • Murata N, Ishizaki-Nishizawa O, Higashi S, Hayashi H, Tasaka Y, Nishida I (1992) Genetically engineered alteration in the chilling sensitivity of plants. Nature 356:710–713

    CAS  Google Scholar 

  • Nakashima K, Yamaguchi-Shinozaki K (2005) Molecular studies on stress-responsive gene expression in Arabidopsis and improvement of stress tolerance in crop plants by regulon biotechnology. JARQ Jpn Agric Res Q 39:221–229

    CAS  Google Scholar 

  • Nakashima K, Yamaguchi-Shinozaki K (2006) Regulons involved in osmotic stress-responsive and cold stress-responsive gene expression in plants. Physiol Plant 126:62–71

    CAS  Google Scholar 

  • Nakashima K, Shinwari Z, Sakuma Y, Seki M, Miura S, Shinozaki K, Yamaguchi-Shinozaki K (2000) Organization and expression of two Arabidopsis DREB2 genes encoding DRE-binding proteins involved in dehydration- and high-salinity-responsive gene expression. Plant Mol Biol 42:657–665

    CAS  PubMed  Google Scholar 

  • Nakashima K, Tran LS, Van Nguyen D, Fujita M, Maruyama K, Todaka D, Ito Y, Hayashi N, Shinozaki K, Yamaguchi-Shinozaki K (2007) Functional analysis of a NAC-type transcription factor OsNAC6 involved in abiotic and biotic stress-responsive gene expression in rice. Plant J 51:617–630

    CAS  PubMed  Google Scholar 

  • Ning J, Li X, Hicks LM, Xiong L (2010) A Raf-Like MAPKKK gene DSM1 mediates drought resistance through reactive oxygen species scavenging in rice. Plant Physiol 152:876–890

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nishida I, Murata N (1996) Chilling sensitivity in plants and cyanobacteria: the crucial contribution of membrane lipids. Annu Rev Plant Physiol Plant Mol Biol 47:541–568

    CAS  PubMed  Google Scholar 

  • Odell JT, Nagy F, Chua NH (1985) Identification of DNA sequences required for activity of the cauliflower mosaic virus 35S promoter. Nature 313:810–812

    CAS  PubMed  Google Scholar 

  • Ohta M, Hayashi Y, Nakashima A, Hamada A, Tanaka A, Nakamura T, Hayakawa T (2002) Introduction of a Na+/H+ antiporter gene from Atriplex gmelini confers salt tolerance to rice. FEBS Lett 532:279–282

    CAS  PubMed  Google Scholar 

  • Park BJ, Liu Z, Kanno A, Kameya T (2005) Genetic improvement of Chinese cabbage for salt and drought tolerance by constitutive expression of a B. napus LEA gene. Plant Sci 169:553–558

    CAS  Google Scholar 

  • Park E-J, Jeknic Z, Pino M-T, Murata N, Chen Tony H-H (2007) Glycinebetaine accumulation is more effective in chloroplasts than in the cytosol for protecting transgenic tomato plants against abiotic stress. Plant Cell Environ 30:994–1005

    CAS  PubMed  Google Scholar 

  • Pasapula V, Shen G, Kuppu S, Paez-Valencia J, Mendoza M, Hou P, Chen J, Qiu X, Zhu L, Zhang X, Auld D, Blumwald E, Zhang H, Gaxiola R, Payton P (2011) Expression of an Arabidopsis vacuolar H+-pyrophosphatase gene (AVP1) in cotton improves drought- and salt tolerance and increases fibre yield in the field conditions. Plant Biotechnol J 9:88–99

    CAS  PubMed  Google Scholar 

  • Pellegrineschi A, Reynolds M, Pacheco M, Brito RM, Almeraya R, Yamaguchi-Shinozaki K, Hoisington D (2004) Stress-induced expression in wheat of the Arabidopsis thaliana DREB1A gene delays water stress symptoms under greenhouse conditions. Genome 47:493–500

    CAS  PubMed  Google Scholar 

  • Peng Y, Lin W, Cai W, Arora R (2007) Overexpression of a Panax ginseng tonoplast aquaporin alters salt tolerance, drought tolerance and cold acclimation ability in transgenic Arabidopsis plants. Planta 226:729–740

    CAS  PubMed  Google Scholar 

  • Prabhavathi V, Rajam MV (2007) Polyamine accumulation in transgenic eggplant enhances tolerance to multiple abiotic stresses and fungal resistance. Plant Biotechnol 24:273–282

    CAS  Google Scholar 

  • Prabhavathi V, Yadav JS, Kumar PA, Rajam MV (2002) Abiotic stress tolerance in transgenic eggplant (Solanum melongena L.) by introduction of bacterial mannitol phosphodehydrogenase gene. Mol Breed 9:137–147

    CAS  Google Scholar 

  • Prashanth SR, Sadhasivam V, Parida A (2008) Over expression of cytosolic copper/zinc superoxide dismutase from a mangrove plant Avicennia marina in indica Rice var Pusa Basmati-1 confers abiotic stress tolerance. Transgenic Res 17:281–291

    CAS  PubMed  Google Scholar 

  • Puhakainen T, Hess MW, Makela P, Svensson J, Heino P, Palva ET (2004) Overexpression of multiple dehydrin genes enhances tolerance to freezing stress in Arabidopsis. Plant Mol Biol 54:743–753

    CAS  PubMed  Google Scholar 

  • Pujni D, Chaudhary A, Rajam MV (2007) Increased tolerance to salinity and drought in transgenic indica rice by mannitol accumulation. J Plant Biochem Biotechnol 16:1–7

    CAS  Google Scholar 

  • Qi YC, Liu WQ, Qiu LY, Zhang SM, Ma L, Zhang H (2010) Overexpression of glutathione S-transferase gene increases salt tolerance of arabidopsis. Russ J Plant Physiol 57:233–240

    CAS  Google Scholar 

  • Qin F, Kakimoto M, Sakuma Y, Maruyama K, Osakabe Y, Tran LSP, Shinozaki K, Yamaguchi-Shinozaki K (2007) Regulation and functional analysis of ZmDREB2A in response to drought and heat stresses in Zea mays L. Plant J 50:54–69

    CAS  PubMed  Google Scholar 

  • Qiu QS, Guo Y, Dietrich MA, Schumaker KS, Zhu JK (2002) Regulation of SOS1, a plasma membrane Na+/H+ exchanger in Arabidopsis thaliana, by SOS2 and SOS3. Proc Natl Acad Sci U S A 99:8436–8441

    CAS  PubMed Central  PubMed  Google Scholar 

  • Queitsch C, Hong SW, Vierling E, Lindquist S (2000) Heat shock protein 101 plays a crucial role in thermotolerance in Arabidopsis. Plant Cell 12:479–492

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ratcliffe OJ, Riechmann JL (2002) Arabidopsis transcription factors and the regulation of flowering time: a genomic perspective. Curr Issues Mol Biol 4:77–91

    CAS  PubMed  Google Scholar 

  • Redillas Mark CFR, Park S-H, Lee JW, Kim YS, Jeong JS, Jung H, Bang SW, Hahn T-R, Kim J-K (2012) Accumulation of trehalose increases soluble sugar contents in rice plants conferring tolerance to drought and salt stress. Plant Biotechnol Rep 6:89–96

    Google Scholar 

  • Reiser V, Raitt DC, Saito H (2003) Yeast osmosensor Sln1 and plant cytokinin receptor Cre1 respond to changes in turgor pressure. J Cell Biol 161:1035–1040

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rhodes D, Hanson AD (1993) Quaternary ammonium and tertiary sulfonium compounds in higher plants. Annu Rev Plant Physiol Plant Mol Biol 44:357–384

    CAS  Google Scholar 

  • Rohila JS, Jain RK, Wu R (2002) Genetic improvement of basmati rice for salt and drought tolerance by regulated expression of a barley Hva1 cDNA. Plant Sci 163:525–532

    CAS  Google Scholar 

  • Roxas VP, Smith RK, Allen ER, Allen RD (1997) Overexpression of glutathione S-transferase/glutathione peroxidase enhances the growth of transgenic tobacco seedlings during stress. Nat Biotechnol 15:988–991

    CAS  PubMed  Google Scholar 

  • Rus AM, Estañ MT, Gisbert C, Garcia-Sogo B, Serrano R, Caro M, Moreno V, Bolarín MC (2001) Expressing the yeast HAL1 gene in tomato increases fruit yield and enhances K+/Na+ selectivity under salt stress. Plant Cell Environ 24:875–880

    CAS  Google Scholar 

  • Ryu MY, Cho SK, Kim WT (2010) The Arabidopsis C3H2C3-type RING E3 ubiquitin ligase AtAIRP1 is a positive regulator of an abscisic acid-dependent response to drought stress. Plant Physiol 154:1983–1997

    CAS  PubMed Central  PubMed  Google Scholar 

  • Saidi Y, Finka A, Goloubinoff P (2011) Heat perception and signalling in plants: a tortuous path to thermotolerance. New Phytol 190:556–565

    CAS  PubMed  Google Scholar 

  • Saijo Y, Hata S, Kyozuka J, Shimamoto K, Izui K (2000) Over-expression of a single Ca2+-dependent protein kinase confers both cold and salt/drought tolerance on rice plants. Plant J 23:319–327

    CAS  PubMed  Google Scholar 

  • Sakuma Y, Maruyama K, Osakabe Y, Qin F, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2006a) Functional analysis of an Arabidopsis transcription factor, DREB2A, involved in drought-responsive gene expression. Plant Cell 18:1292–1309

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sakuma Y, Maruyama K, Qin F, Osakabe Y, Shinozaki K, Yamaguchi-Shinozaki K (2006b) Dual function of an Arabidopsis transcription factor DREB2A in water-stress-responsive and heat-stress-responsive gene expression. Proc Natl Acad Sci U S A 103:18822–18827

    CAS  PubMed Central  PubMed  Google Scholar 

  • Šamajová O, Plíhal O, Al-Yousif M, Hirt H, Šamaj J (2013) Improvement of stress tolerance in plants by genetic manipulation of mitogen-activated protein kinases. Biotechnol Adv 31:118–128

    PubMed  Google Scholar 

  • Sarwat M, Naqvi AR (2013) Heterologous expression of rice calnexin (OsCNX) confers drought tolerance in Nicotiana tabacum. Mol Biol Rep 40:5451–5464

    CAS  PubMed  Google Scholar 

  • Sato Y, Yokoya S (2008) Enhanced tolerance to drought stress in transgenic rice plants overexpressing a small heat-shock protein, sHSP17.7. Plant Cell Rep 27:329–334

    CAS  PubMed  Google Scholar 

  • Schuber F (1989) Influence of polyamines on membrane functions. Biochem J 260:1–10

    CAS  PubMed Central  PubMed  Google Scholar 

  • Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y, Kamiya A, Nakajima M, Enju A, Sakurai T, Satou M, Akiyama K, Taji T, Yamaguchi-Shinozaki K, Carninci P, Kawai J, Hayashizaki Y, Shinozaki K (2002) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J 31:279–292

    CAS  PubMed  Google Scholar 

  • Seo P, Park MJ, Park CM (2013) Alternative splicing of transcription factors in plant responses to low temperature stress: mechanisms and functions. Planta 237:1415–1424

    CAS  PubMed Central  PubMed  Google Scholar 

  • Shen B, Jensen RG, Bohnert HJ (1997) Mannitol protects against oxidation by hydroxyl radicals. Plant Physiol 115:527–532

    CAS  PubMed Central  PubMed  Google Scholar 

  • Shi H, Quintero FJ, Pardo JM, Zhu JK (2002) The putative plasma membrane Na(+)/H(+) antiporter SOS1 controls long-distance Na(+) transport in plants. Plant Cell 14:465–477

    CAS  PubMed Central  PubMed  Google Scholar 

  • Shi H, Lee BH, Wu SJ, Zhu JK (2003) Overexpression of a plasma membrane Na+/H+ antiporter gene improves salt tolerance in Arabidopsis thaliana. Nat Biotechnol 21:81–85

    CAS  PubMed  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (2000) Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways. Curr Opin Plant Biol 3:217–223

    CAS  PubMed  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58:221–227

    CAS  PubMed  Google Scholar 

  • Shitamichi N, Matsuoka D, Sasayama D, Furuya T, Nanmori T (2013) Over-expression of MAP3Kδ4, an ABA-inducible Raf-like MAP3K that confers salt tolerance in Arabidopsis. Plant Biotechnol J 30:111–118

    CAS  Google Scholar 

  • Shiu SH, Shih MC, Li WH (2005) Transcription factor families have much higher expansion rates in plants than in animals. Plant Physiol 139:18–26

    CAS  PubMed Central  PubMed  Google Scholar 

  • Shou H, Bordallo P, Fan JB, Yeakley JM, Bibikova M, Sheen J, Wang K (2004a) Expression of an active tobacco mitogen-activated protein kinase kinase kinase enhances freezing tolerance in transgenic maize. Proc Natl Acad Sci U S A 101:3298–3303

    CAS  PubMed Central  PubMed  Google Scholar 

  • Shou H, Bordallo P, Wang K (2004b) Expression of the Nicotiana protein kinase (NPK1) enhanced drought tolerance in transgenic maize. J Exp Bot 55:1013–1019

    CAS  PubMed  Google Scholar 

  • Sivamani E, Bahieldin A, Wraith JM, Al Niemi T, Dyer WE, Ho TD, Qu R (2000) Improved biomass productivity and water use efficiency under water deficit conditions in transgenic wheat constitutively expressing the barley HVA1 gene. Plant Sci 155:1–9

    CAS  PubMed  Google Scholar 

  • Steponkus PL, Uemura M, Joseph RA, Gilmour SJ, Thomashow MF (1998) Mode of action of the COR15a gene on the freezing tolerance of Arabidopsis thaliana. Proc Natl Acad Sci U S A 95:14570–14575

    CAS  PubMed Central  PubMed  Google Scholar 

  • Stiller I, Dulai S, Kondrak M, Tarnai R, Szabo L, Toldi O, Banfalvi Z (2008) Effects of drought on water content and photosynthetic parameters in potato plants expressing the trehalose-6-phosphate synthase gene of Saccharomyces cerevisiae. Planta 227:299–308

    CAS  PubMed  Google Scholar 

  • Sui N, Li M, Zhao SJ, Li F, Liang H, Meng QW (2007) Overexpression of glycerol-3-phosphate acyltransferase gene improves chilling tolerance in tomato. Planta 226:1097–1108

    CAS  PubMed  Google Scholar 

  • Sun W, Bernard C, van de Cotte B, Van Montagu M, Verbruggen N (2001) At-HSP17.6A, encoding a small heat-shock protein in Arabidopsis, can enhance osmotolerance upon overexpression. Plant J 27:407–415

    CAS  PubMed  Google Scholar 

  • Sunkar R (2010) MicroRNAs with macro-effects on plant stress responses. Semin Cell Dev Biol 21:805–811

    CAS  PubMed  Google Scholar 

  • Sunkar R, Bartels D, Kirch HH (2003) Overexpression of a stress-inducible aldehyde dehydrogenase gene from Arabidopsis thaliana in transgenic plants improves stress tolerance. Plant J 35:452–464

    CAS  PubMed  Google Scholar 

  • Sunkar R, Li YF, Jagadeeswaran G (2012) Functions of microRNAs in plant stress responses. Trends Plant Sci 17:196–203

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Takahashi T, Kakehi JI (2010) Polyamines: ubiquitous polycations with unique roles in growth and stress responses. Ann Bot 105:1–6

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tang W, Peng X, Newton RJ (2005) Enhanced tolerance to salt stress in transgenic loblolly pine simultaneously expressing two genes encoding mannitol-1-phosphate dehydrogenase and glucitol-6-phosphate dehydrogenase. Plant Physiol Biochem 43:139–146

    CAS  PubMed  Google Scholar 

  • Tarczynski MC, Jensen RG, Bohnert HJ (1992) Expression of a bacterial mtlD gene in transgenic tobacco leads to production and accumulation of mannitol. Proc Natl Acad Sci U S A 89:2600–2604

    CAS  PubMed Central  PubMed  Google Scholar 

  • Teige M, Scheikl E, Eulgem T, Dóczi R, Ichimura K, Shinozaki K, Dangl JL, Hirt H (2004) The MKK2 pathway mediates cold and salt stress signaling in Arabidopsis. Mol Cell 15:141–152

    CAS  PubMed  Google Scholar 

  • Theocharis A, Clément C, Barka E (2012) Physiological and molecular changes in plants grown at low temperatures. Planta 235:1091–1105

    CAS  PubMed  Google Scholar 

  • Thomas JC, Sepahi M, Arendall B, Bohnert HJ (1995) Enhancement of seed germination in high salinity by engineering mannitol expression in Arabidopsis thaliana. Plant Cell Environ 18:801–806

    CAS  Google Scholar 

  • Tran LS, Nakashima K, Sakuma Y, Simpson SD, Fujita Y, Maruyama K, Fujita M, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2004) Isolation and functional analysis of Arabidopsis stress-inducible NAC transcription factors that bind to a drought-responsive cis-element in the early responsive to dehydration stress 1 promoter. Plant Cell 16:2481–2498

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tripathi V, Parasuraman B, Laxmi A, Chattopadhyay D (2009) CIPK6, a CBL-interacting protein kinase is required for development and salt tolerance in plants. Plant J 58:778–790

    CAS  PubMed  Google Scholar 

  • Tuteja N (2007) Mechanisms of high salinity tolerance in plants. Methods Enzymol 428:419–438

    CAS  PubMed  Google Scholar 

  • Tuteja N, Mahajan S (2007) Calcium signaling network in plants: an overview. Plant Signal Behav 2:79–85

    PubMed Central  PubMed  Google Scholar 

  • Tuteja N, Sopory SK (2008) Chemical signaling under abiotic stress environment in plants. Plant Signal Behav 3:525–536

    PubMed Central  PubMed  Google Scholar 

  • Umezawa T, Yoshida R, Maruyama K, Yamaguchi-Shinozaki K, Shinozaki K (2004) SRK2C, a SNF1-related protein kinase 2, improves drought tolerance by controlling stress-responsive gene expression in Arabidopsis thaliana. Proc Natl Acad Sci U S A 101:17306–17311

    CAS  PubMed Central  PubMed  Google Scholar 

  • Uno Y, Furihata T, Abe H, Yoshida R, Shinozaki K, Yamaguchi-Shinozaki K (2000) Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. Proc Natl Acad Sci U S A 97:11632–11637

    CAS  PubMed Central  PubMed  Google Scholar 

  • Upchurch R (2008) Fatty acid unsaturation, mobilization, and regulation in the response of plants to stress. Biotechnol Lett 30:967–977

    CAS  PubMed  Google Scholar 

  • Urao T, Yakubov B, Satoh R, Yamaguchi-Shinozaki K, Seki M, Hirayama T, Shinozaki K (1999) A transmembrane hybrid-type histidine kinase in Arabidopsis functions as an osmosensor. Plant Cell 11:1743–1754

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ushimaru T, Nakagawa T, Fujioka Y, Daicho K, Naito M, Yamauchi Y, Nonaka H, Amako K, Yamawaki K, Murata N (2006) Transgenic Arabidopsis plants expressing the rice dehydroascorbate reductase gene are resistant to salt stress. J Plant Physiol 163:1179–1184

    CAS  PubMed  Google Scholar 

  • Valmonte GR, Arthur K, Higgins CM, MacDiarmid RM (2014) Calcium-dependent protein kinases in plants: evolution, expression and function. Plant Cell Physiol 55:551–569

    CAS  PubMed  Google Scholar 

  • Verbruggen N, Hermans C (2008) Proline accumulation in plants: a review. Amino Acids 35:753–759

    CAS  PubMed  Google Scholar 

  • Vinocur B, Altman A (2005) Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Curr Opin Biotechnol 16:123–132

    CAS  PubMed  Google Scholar 

  • Waie B, Rajam MV (2003) Effect of increased polyamine biosynthesis on stress responses in transgenic tobacco by introduction of human S-adenosylmethionine gene. Plant Sci 164:727–734

    CAS  Google Scholar 

  • Wan X, Mo A, Liu S, Yang L, Li L (2011) Constitutive expression of a peanut ubiquitin-conjugating enzyme gene in Arabidopsis confers improved water-stress tolerance through regulation of stress-responsive gene expression. J Biosci Bioeng 111:478–484

    CAS  PubMed  Google Scholar 

  • Wang CT, Song W (2013) Calcium-dependent protein kinase gene ZmCPK12 from maize confers tolerance to drought and salt stresses in transgenic plants. Acta Physiol Plant 35:1659–1666

    CAS  Google Scholar 

  • Wang W, Vinocur B, Altman A (2003) Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218:1–14

    CAS  PubMed  Google Scholar 

  • Wang Y, Ying Y, Chen J, Wang X (2004) Transgenic Arabidopsis overexpressing Mn-SOD enhanced salt-tolerance. Plant Sci 167:671–677

    CAS  Google Scholar 

  • Wang FZ, Wang QB, Kwon SY, Kwak SS, Su WA (2005) Enhanced drought tolerance of transgenic rice plants expressing a pea manganese superoxide dismutase. J Plant Physiol 162:465–472

    CAS  PubMed  Google Scholar 

  • Wang M, Gu D, Liu T, Wang Z, Guo X, Hou W, Bai Y, Chen X, Wang G (2007) Overexpression of a putative maize calcineurin B-like protein in Arabidopsis confers salt tolerance. Plant Mol Biol 65:733–746

    CAS  PubMed  Google Scholar 

  • Wang X, Li Y, Ji W, Bai X, Cai H, Zhu D, Sun XL, Chen LJ, Zhu YM (2011) A novel Glycine soja tonoplast intrinsic protein gene responds to abiotic stress and depresses salt and dehydration tolerance in transgenic Arabidopsis thaliana. J Plant Physiol 168:1241–1248

    CAS  PubMed  Google Scholar 

  • Wang RK, Li LL, Cao ZH, Zhao Q, Li M, Zhang LY, Hao YJ (2012) Molecular cloning and functional characterization of a novel apple MdCIPK6L gene reveals its involvement in multiple abiotic stress tolerance in transgenic plants. Plant Mol Biol 79:123–135

    CAS  PubMed  Google Scholar 

  • Wani SH, Singh NB, Haribhushan A, Mir JI (2013) Compatible solute engineering in plants for abiotic stress tolerance – role of glycine betaine. Curr Genom 14:157–165

    CAS  Google Scholar 

  • Waterer D, Benning N, Wu G, Luo X, Liu X, Gusta M, McHughen A, Gusta L (2010) Evaluation of abiotic stress tolerance of genetically modified potatoes (Solanum tuberosum cv. Desiree). Mol Breed 25:527–540

    CAS  Google Scholar 

  • Wu CA, Yang GD, Meng QW, Zheng CC (2004) The cotton GhNHX1 gene encoding a novel putative tonoplast Na(+)/H(+) antiporter plays an important role in salt stress. Plant Cell Physiol 45:600–607

    CAS  PubMed  Google Scholar 

  • Xiang Y, Huang Y, Xiong L (2007) Characterization of stress-responsive CIPK genes in rice for stress tolerance improvement. Plant Physiol 144:1416–1428

    CAS  PubMed Central  PubMed  Google Scholar 

  • Xiang Y, Tang N, Du H, Ye H, Xiong L (2008) Characterization of OsbZIP23 as a key player of the basic leucine zipper transcription factor family for conferring abscisic acid sensitivity and salinity and drought tolerance in rice. Plant Physiol 148:1938–1952

    CAS  PubMed Central  PubMed  Google Scholar 

  • Xiao B, Huang Y, Tang N, Xiong L (2007) Over-expression of a LEA gene in rice improves drought resistance under the field conditions. Theor Appl Genet 115:35–46

    CAS  PubMed  Google Scholar 

  • Xing Y, Jia W, Zhang J (2008) AtMKK1 mediates ABA-induced CAT1 expression and H2O2 production via AtMPK6-coupled signaling in Arabidopsis. Plant J 54:440–451

    CAS  PubMed  Google Scholar 

  • Xiong L, Yang Y (2003) Disease resistance and abiotic stress tolerance in rice are inversely modulated by an abscisic acid–inducible mitogen-activated protein kinase. Plant Cell 15:745–759

    CAS  PubMed Central  PubMed  Google Scholar 

  • Xu P, Yang C (2013) Emerging role of SUMOylation in plant development. Plant Signal Behav 8:e24727

    PubMed Central  PubMed  Google Scholar 

  • Xu D, Duan X, Wang B, Hong B, Ho T, Wu R (1996) Expression of a late embryogenesis abundant protein gene, HVA1, from barley confers tolerance to water deficit and salt stress in transgenic rice. Plant Physiol 110:249–257

    CAS  PubMed Central  PubMed  Google Scholar 

  • Xu J, Tian YS, Peng RH, Xiong AS, Zhu B, Jin XF, Gao F, Fu XY, Hou XL, Yao QH (2010) AtCPK6, a functionally redundant and positive regulator involved in salt/drought stress tolerance in Arabidopsis. Planta 231:1251–1260

    CAS  PubMed  Google Scholar 

  • Xue ZY, Zhi DY, Xue GP, Zhang H, Zhao YX, Xia GM (2004) Enhanced salt tolerance of transgenic wheat (Tritivum aestivum L.) expressing a vacuolar Na+/H+ antiporter gene with improved grain yields in saline soils in the field and a reduced level of leaf Na+. Plant Sci 167:849–859

    CAS  Google Scholar 

  • Xue T, Li X, Zhu W, Wu C, Yang G, Zheng C (2009) Cotton metallothionein GhMT3a, a reactive oxygen species scavenger, increased tolerance against abiotic stress in transgenic tobacco and yeast. J Exp Bot 60:339–349

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yang A, Duan X, Gu X, Gao F, Zhang J (2005) Efficient transformation of beet (Beta vulgaris) and production of plants with improved salt-tolerance. Plant Cell Tissue Organ Cult 83:259–270

    CAS  Google Scholar 

  • Yang Q, Chen ZZ, Zhou XF, Yin HB, Li X, Xin XF, Hong XH, Zhu JK, Gong Z (2009) Overexpression of SOS (Salt Overly Sensitive) genes increases salt tolerance in transgenic Arabidopsis. Mol Plant 2:22–31

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yang C, Li D, Mao D, Liu XUE, Ji C, Li X, Zhao X, Cheng Z, Chen C, Zhu L (2013) Overexpression of microRNA319 impacts leaf morphogenesis and leads to enhanced cold tolerance in rice (Oryza sativa L.). Plant Cell Environ 36:2207–2218

    CAS  PubMed  Google Scholar 

  • Yokoi S, Higashi SI, Kishitani S, Murata N, Toriyama K (1998) Introduction of the cDNA for shape Arabidopsis glycerol-3-phosphate acyltransferase (GPAT) confers unsaturation of fatty acids and chilling tolerance of photosynthesis on rice. Mol Breed 4:269–275

    CAS  Google Scholar 

  • Zhang HX, Blumwald E (2001) Transgenic salt-tolerant tomato plants accumulate salt in foliage but not in fruit. Nat Biotechnol 19:765–768

    CAS  PubMed  Google Scholar 

  • Zhang YY, Xie Q (2007) Ubiquitination in abscisic acid-related pathway. J Integr Plant Biol 49:87–93

    CAS  Google Scholar 

  • Zhang HX, Hodson JN, Williams JP, Blumwald E (2001) Engineering salt-tolerant Brassica plants: characterization of yield and seed oil quality in transgenic plants with increased vacuolar sodium accumulation. Proc Natl Acad Sci U S A 98:12832–12836

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang YY, Li Y, Gao T, Zhu H, Wang DJ, Zhang HW, Ning YS, Liu LJ, Wu YR, Chu CC, Guo HS, Xie Q (2008) Arabidopsis SDIR1 enhances drought tolerance in crop plants. Biosci Biotechnol Biochem 72:2251–2254

    CAS  PubMed  Google Scholar 

  • Zhang N, Wen G, Si H-J, Du H-H, Liu B-L, Wang D (2011a) Enhanced drought and salinity tolerance in transgenic potato plants with a BADH gene from spinach. Plant Biotechnol Rep 5:71–77

    Google Scholar 

  • Zhang X, Zou Z, Gong P, Zhang J, Ziaf K, Li H, Xiao F, Ye Z (2011b) Over-expression of microRNA169 confers enhanced drought tolerance to tomato. Biotechnol Lett 33:403–409

    CAS  PubMed  Google Scholar 

  • Zhang J, Li D, Zou D, Luo F, Wang X, Zheng Y, Li X (2013) A cotton gene encoding a plasma membrane aquaporin is involved in seedling development and in response to drought stress. Acta Biochim Biophys Sin 45:104–114

    CAS  PubMed  Google Scholar 

  • Zhao F, Zhang H (2006) Salt and paraquat stress tolerance results from co-expression of the Suaeda salsa glutathione S-transferase and catalase in transgenic rice. Plant Cell Tissue Organ Cult 86:349–358

    CAS  Google Scholar 

  • Zhao FY, Zhang XJ, Li PH, Zhao YX, Zhang H (2006a) Co-expression of the Suaeda salsa SsNHX1 and Arabidopsis AVP1 confer greater salt tolerance to transgenic rice than the single SsNHX1. Mol Breed 17:341–353

    Google Scholar 

  • Zhao F, Guo S, Zhang H, Zhao Y (2006b) Expression of yeast SOD2 in transgenic rice results in increased salt tolerance. Plant Sci 170:216–224

    CAS  Google Scholar 

  • Zhao J, Zhi D, Xue Z, Liu H, Xia G (2007) Enhanced salt tolerance of transgenic progeny of tall fescue (Festuca arundinacea) expressing a vacuolar Na+/H+ antiporter gene from Arabidopsis. J Plant Physiol 164:1377–1383

    CAS  PubMed  Google Scholar 

  • Zheng X, Chen B, Lu G, Han B (2009) Overexpression of a NAC transcription factor enhances rice drought and salt tolerance. Biochem Biophys Res Commun 379:985–989

    CAS  PubMed  Google Scholar 

  • Zhifang G, Loescher WH (2003) Expression of a celery mannose 6-phosphate reductase in Arabidopsis thaliana enhances salt tolerance and induces biosynthesis of both mannitol and a glucosyl-mannitol dimer. Plant Cell Environ 26:275–283

    CAS  Google Scholar 

  • Zhou S, Chen X, Zhang X, Li Y (2008) Improved salt tolerance in tobacco plants by co-transformation of a betaine synthesis gene BADH and a vacuolar Na+/H+ antiporter gene SeNHX1. Biochem Lett 30:369–376

    CAS  Google Scholar 

  • Zhou GA, Chang RZ, Qiu LJ (2010) Overexpression of soybean ubiquitin-conjugating enzyme gene GmUBC2 confers enhanced drought and salt tolerance through modulating abiotic stress-responsive gene expression in Arabidopsis. Plant Mol Biol 72:357–367

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhou M, Li D, Li Z, Hu Q, Yang C, Zhu L, Luo H (2013) Constitutive expression of a miR319 gene alters plant development and enhances salt and drought tolerance in transgenic creeping bentgrass. Plant Physiol 161:1375–1391

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhu J, Dong CH, Zhu JK (2007a) Interplay between cold-responsive gene regulation, metabolism and RNA processing during plant cold acclimation. Curr Opin Plant Biol 10:290–295

    CAS  PubMed  Google Scholar 

  • Zhu SY, Yu XC, Wang XJ, Zhao R, Li Y, Fan RC, Shang Y, Du SY, Wang XF, Wu FQ, Xu YH, Zhang XY, Zhang DP (2007b) Two calcium-dependent protein kinases, CPK4 and CPK11, regulate abscisic acid signal transduction in Arabidopsis. Plant Cell 19:3019–3036

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zong X, Li DP, Gu LK, Li DQ, Liu LX, Hu XL (2009) Abscisic acid and hydrogen peroxide induce a novel maize group C MAP kinase gene, ZmMPK7, which is responsible for the removal of reactive oxygen species. Planta 229:485–495

    CAS  PubMed  Google Scholar 

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Acknowledgments

R.A. acknowledges support from the Ramón y Cajal Program (RYC-2011-07847) of the Ministerio de Ciencia e Innovación (Spain) and the Marie Curie Career Integration Grant (DISEASENVIRON, PCIG10-GA-2011-303568) of the European Union. Research has been supported by the Spanish Ministerio de Ciencia e Innovación (BIO2011-29683 and CSD2007-00036) and the Generalitat de Catalunya (SGR2009-1060).

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Marco, F., Bitrián, M., Carrasco, P., Rajam, M.V., Alcázar, R., Tiburcio, A.F. (2015). Genetic Engineering Strategies for Abiotic Stress Tolerance in Plants. In: Bahadur, B., Venkat Rajam, M., Sahijram, L., Krishnamurthy, K. (eds) Plant Biology and Biotechnology. Springer, New Delhi. https://doi.org/10.1007/978-81-322-2283-5_29

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