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Physiological, Metabolic, and Molecular Responses of Plants to Abiotic Stress

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Stress Signaling in Plants: Genomics and Proteomics Perspective, Volume 2

Abstract

Plants respond to environmental challenges inducing several physiological, metabolic, and molecular responses. These responses are oriented to avoid or endure the adverse environmental condition in non-adapted plant genotypes. Under abiotic stress conditions, plants trigger mechanisms to minimize water loss through stomata; this affects photosynthetic ability of plants by reducing CO2 intake and fixation, therefore favoring the production of ROS and the incidence of oxidative damage. Therefore, the main metabolic responses of plants to abiotic stress will be oriented to cope with water loss (inducing compatible osmolyte biosynthesis) and oxidative stress (inducing biosynthesis of antioxidant compounds). Integration of environmental stimuli and adequate modulation of the physiological response is achieved by synthesizing plant hormones (ABA, JA, SA, ET, PAs, CKs, or GAs), metabolites that act as endogenous regulators of different plant processes. Plant hormones usually act in cross talk so that different signaling pathways contribute to fine-tune specific stress and developmental responses. At the molecular level, this cross talk implies interaction with different transcription factors that bind to common and specific cis-acting elements in promoter regions of stress and hormone-inducible genes. Fundamental physiological and molecular information is essential to build up models and design strategies to improve or confer abiotic stress tolerance to elite crops. Based on this knowledge, different strategies are used to introgress these tolerance traits into cultivated species: marker-assisted selection of genotypes (QTLs, MABC, MARS, or GWAS), induction of polyploidy and mutagenesis followed by variant selection, and, finally, plant genetic transformation. Strategies used for crop improvement are discussed in detail, the physiological and molecular basis explained, and the potential advantages and drawbacks highlighted.

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Abbreviations

3-PGA:

3-Phosphoglycerate

ABA:

Abscisic acid

AB-QTL:

Advanced backcross QTL

ABRE:

ABA-responsive element

ADC:

Arginine decarboxylase

APX:

Ascorbate peroxidase

BABA:

β-amino butyric acid

CAT:

Catalase

CE:

Coupling element

CK:

Cytokinin

DHAR:

Dehydroascorbate reductase

DRE:

Dehydration-responsive element

EMS:

Ethylmethanesulfate

ET:

Ethylene

GA:

Gibberellin

GR:

Glutathione reductase

GWAS:

Genome-wide association studies

JA:

Jasmonic acid

MABC:

Marker-assisted backcrossing

MARS:

Marker-assisted recurrent selection

MDHAR:

Monodehydroascorbate reductase

MeJA:

Methyl jasmonate

NO:

Nitric oxide

Pro:

Proline

PSII:

Photosystem II

ROS:

Reactive oxygen species

SA:

Salicylic acid

SAMDC:

S-adenosyl methionine decarboxylase

SOD:

Superoxide dismutase

SPDS:

Spermidine decarboxylase synthase

SPMS:

Spermine synthase

References

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

    Article  CAS  PubMed  Google Scholar 

  • Agati G, Biricolti S, Guidi L, Ferrini F, Fini A, Tattini M (2011) The biosynthesis of flavonoids is enhanced similarly by UV radiation and root zone salinity in L. vulgare leaves. J Plant Physiol 168:204–212

    Article  CAS  PubMed  Google Scholar 

  • Alcázar R, Cuevas JC, Patron M, Altabella T, Tiburcio AF (2006) Abscisic acid modulates polyamine metabolism under water stress in Arabidopsis thaliana. Physiol Plant 128:448–455

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Alemán F, Nieves-Cordones M, Martínez V, Rubio F (2009) Differential regulation of the HAK5 genes encoding the high-affinity K+ transporters of Thellungiella halophila and Arabidopsis thaliana. Environ Exp Bot 65:263–269

    Article  CAS  Google Scholar 

  • Alet AI, Sánchez DH, Cuevas JC, Marina M, Carrasco P, Altabella T, Tiburcio AF, Ruiz OA (2012) New insights into the role of spermine in Arabidopsis thaliana under long-term salt stress. Plant Sci 182:94–100

    Article  CAS  PubMed  Google Scholar 

  • Allakhverdiev SI, Kreslavski VD, Klimov VV, Los D, Carpentier R, Mohanty P (2008) Heat stress: an overview of molecular responses in photosynthesis. Photosynth Res 98:541–550

    Article  CAS  PubMed  Google Scholar 

  • Allario T, Brumos J, Colmenero-Flores J, Tadeo F, Froelicher Y, Talon M, Navarro L, Ollitrault P, Morillon R (2011) Large changes in anatomy and physiology between diploid Rangpur lime (Citrus limonia) and its autotetraploid are not associated with large changes in leaf gene expression. J Exp Bot 62:2507–2519

    Article  CAS  PubMed  Google Scholar 

  • Allario T, Brumos J, Colmenero-Flores JM, Iglesias DJ, Pina JA, Navarro L, Talon M, Ollitrault P, Morillon R (2012) Tetraploid Rangpur lime rootstock increases drought tolerance via enhanced constitutive root abscisic acid production. Plant Cell Environ 36:856–868

    Article  PubMed  CAS  Google Scholar 

  • Alonso-Ramírez A, Rodríguez D, Reyes D, Jiménez JA, Nicolás G, López-Climent M, Gómez-Cadenas A, Nicolás C (2009) Cross-talk between gibberellins and salicylic acid in early stress responses in Arabidopsis thaliana seeds. Plant Signal Behav 4:750–751

    Article  PubMed  PubMed Central  Google Scholar 

  • Amtmann A (2009) Learning from evolution: Thellungiella generates new knowledge on essential and critical components of abiotic stress tolerance in plants. Mol Plant 2:3–12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arbona V, Gómez-Cadenas A (2015) Metabolomics of disease resistance in crops. Curr Issues Mol Biol 19:13–29

    PubMed  Google Scholar 

  • Arbona V, López-Climent MF, Pérez-Clemente RM, Gómez-Cadenas A (2009) Maintenance of a high photosynthetic performance is linked to flooding tolerance in citrus. Environ Exp Bot 66:135–142

    Article  CAS  Google Scholar 

  • Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639

    Article  CAS  PubMed  Google Scholar 

  • Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141:391–396

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Asensi-Fabado MA, Oliván A, Munné-Bosch S (2012) A comparative study of the hormonal response to high temperatures and stress reiteration in three Labiatae species. Environ Exp Bot 94:57–65

    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

    Article  CAS  Google Scholar 

  • Atwell BJ, Wang H, Scafaro AP (2014) Could abiotic stress tolerance in wild relatives of rice be used to improve Oryza sativa? Plant Sci 215–216:48–58

    Article  PubMed  CAS  Google Scholar 

  • Bailey-Serres J, Fukao T, Ronald P, Ismail A, Heuer S, Mackill D (2010) Submergence tolerant rice: SUB1’s journey from landrace to modern cultivar. Rice 3:138–147

    Article  Google Scholar 

  • Balestrazzi A, Botti S, Zelasco S, Biondi S, Franchin C, Calligari P, Racchi M, Turchi A, Lingua G, Berta G, Carbonera D (2009) Expression of the PsMTA1 gene in white poplar engineered with the MAT system is associated with heavy metal tolerance and protection against 8-hydroxy-2′-deoxyguanosine mediated-DNA damage. Plant Cell Rep 28:1179–1192

    Article  CAS  PubMed  Google Scholar 

  • Bandurska H, Cieślak M (2013) The interactive effect of water deficit and UV-B radiation on salicylic acid accumulation in barley roots and leaves. Environ Exp Bot 94:9–18

    Article  CAS  Google Scholar 

  • Barabasz A, Wilkowska A, Tracz K, Ruszczyńska A, Bulska E, Mills RF, Williams LE, Antosiewicz DM (2013) Expression of HvHMA2 in tobacco modifies Zn-Fe-Cd homeostasis. J Plant Physiol 170:1176–1186

    Article  CAS  PubMed  Google Scholar 

  • Barcia R, Pena LB, Zawoznik MS, Benavides MP, Gallego SM (2014) Osmotic adjustment and maintenance of the redox balance in root tissue may be key points to overcome a mild water deficit during the early growth of wheat. Plant Growth Regul 74:107–117

    Article  CAS  Google Scholar 

  • Bartoli CG, Casalongué CA, Simontacchi M, Marquez-Garcia B, Foyer CH (2013) Interactions between hormone and redox signalling pathways in the control of growth and cross tolerance to stress. Environ Exp Bot 94:73–88

    Google Scholar 

  • Bashir H, Ahmad J, Bagheri R, Nauman M, Qureshi MI (2013) Limited sulfur resource forces Arabidopsis thaliana to shift towards non-sulfur tolerance under cadmium stress. Environ Exp Bot 94:19–32

    Article  CAS  Google Scholar 

  • Bassal M, El-Hamahmy M (2011) Hot water dip and preconditioning treatments to reduce chilling injury and maintain postharvest quality of Navel and Valencia oranges during cold quarantine. Postharvest Biol Technol 60:186–191

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beck JJ, Smith L, Baig N (2014) An overview of plant volatile metabolomics, sample treatment and reporting considerations with emphasis on mechanical damage and biological control of weeds. Phytochem Anal 25:331–341

    Article  CAS  PubMed  Google Scholar 

  • Ben-Hayyim G, Moore GA (2007) Recent advances in breeding citrus for drought and saline stress tolerance. In: Jenks MA, Hasegawa PM, Jain SM (eds) Advances in molecular breeding toward drought and salt tolerant crops. Springer, Dordrecht, pp 627–642

    Chapter  Google Scholar 

  • Bettaieb I, Hamrouni-Sellami I, Bourgou S, Limam F, Marzouk B (2011) Drought effects on polyphenol composition and antioxidant activities in aerial parts of Salvia officinalis L. Acta Physiol Plant 33:1103–1111

    Article  CAS  Google Scholar 

  • Binder BYK, Peebles CAM, Shanks JV, San K-Y (2009) The effects of UV-B stress on the production of terpenoid indole alkaloids in Catharanthus roseus hairy roots. Biotechnol Prog 25:861–865

    Article  CAS  PubMed  Google Scholar 

  • Bortesi L, Fischer R (2014) The CRISPR/Cas9 system for plant genome editing and beyond. Biotechnol Adv 33:41–52

    Article  PubMed  CAS  Google Scholar 

  • Boyer J (1982) Plant productivity and environment. Science 218:443–448

    Article  CAS  PubMed  Google Scholar 

  • Bruce TJ, Matthes MC, Napier J, Pickett J (2007) Stressful “memories” of plants: evidence and possible mechanisms. Plant Sci 173:603–608

    Article  CAS  Google Scholar 

  • Brumós J, Colmenero-Flores JM, Conesa A, Izquierdo P, Sánchez G, Iglesias DJ, López-Climent MF, Gómez-Cadenas A, Talón M (2009) Membrane transporters and carbon metabolism implicated in chloride homeostasis differentiate salt stress responses in tolerant and sensitive Citrus rootstocks. Funct Integr Genomics 9:293–309

    Article  PubMed  CAS  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

    Article  CAS  PubMed  Google Scholar 

  • Cenci A, Guignon V, Roux N, Rouard M (2014) Genomic analysis of NAC transcription factors in banana (Musa acuminata) and definition of NAC orthologous groups for monocots and dicots. Plant Mol Biol 85:63–80

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Chen L, Song Y, Li S, Zhang L, Zou C, Yu D (2012) The role of WRKY transcription factors in plant abiotic stresses. Biochim Biophys Acta 1819:120–128

    Article  CAS  PubMed  Google Scholar 

  • Chen X, Wang Y, Lv B, Li J, Luo L, Lu S, Zhang X, Ma H, Ming F (2014) The NAC family transcription factor OsNAP confers abiotic stress response through the ABA pathway. Plant Cell Physiol 55:604–619

    Article  CAS  PubMed  Google Scholar 

  • Cheynier V, Comte G, Davies KM, Lattanzio V, Martens S (2013) Plant phenolics: recent advances on their biosynthesis, genetics, and ecophysiology. Plant Physiol Biochem 72:1–20

    Article  CAS  PubMed  Google Scholar 

  • Chiang YJ, Stushnof C, McSay AE, Jones ML, Bohnert HJ (2005) Overexpression of mannitol-1-phosphate dehydrogenase increases mannitol accumulation and adds protection against chilling injury in petunia. J Am Soc Hortic Sci 130:605–610

    CAS  Google Scholar 

  • Claeys H, Van Landeghem S, Dubois M, Maleux K, Inzé D (2014a) What is stress? Dose-response effects in commonly used in vitro stress assays. Plant Physiol 165:519–527

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Claeys H, De Bodt S, Inzé D (2014b) Gibberellins and DELLAs: central nodes in growth regulatory networks. Trends Plant Sci 19:231–239

    Article  CAS  PubMed  Google Scholar 

  • Clarke SM, Mur LAJ, Wood JE, Scott IM (2004) Salicylic acid dependent signaling promotes basal thermotolerance but is not essential for acquired thermotolerance in Arabidopsis thaliana. Plant J 38:432–447

    Article  CAS  PubMed  Google Scholar 

  • Clemens S (2006) Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88:1707–1719

    Article  CAS  PubMed  Google Scholar 

  • Colmenero-Flores JM, Rosales MA (2014) Interaction between salt and heat stress: when two wrongs make a right. Plant Cell Environ 37:1042–1045

    Article  CAS  PubMed  Google Scholar 

  • Cominelli E, Sala T, Calvi D, Gusmaroli G, Tonelli C (2008) Over-expression of the Arabidopsis AtMYB41 gene alters cell expansion and leaf surface permeability. Plant J 53:53–64

    Article  CAS  PubMed  Google Scholar 

  • Cortina C, Culiáñez-Macià FA (2005) Tomato abiotic stress enhanced tolerance by trehalose biosynthesis. Plant Sci 169:75–82

    Article  CAS  Google Scholar 

  • Cuevas JC, López-Cobollo R, Alcázar R, Zarza X, Koncz C, Altabella T, Salinas J, Tiburcio AF, Ferrando A (2008) Putrescine is involved in Arabidopsis freezing tolerance and cold acclimation by regulating abscisic acid levels in response to low temperature. Plant Physiol 148:1094–1105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cui J-X, Zhou Y-H, Ding J-G, Xia X-J, Shi K, Chen S-C, Asami T, Chen Z, Yu J-Q (2011) Role of nitric oxide in hydrogen peroxide-dependent induction of abiotic stress tolerance by brassinosteroids in cucumber. Plant Cell Environ 34:347–358

    Article  CAS  PubMed  Google Scholar 

  • Dave R, Singh PK, Tripathi P, Shri M, Dixit G, Dwivedi S, Chakrabarty D, Trivedi PK, Sharma YK, Dhankher OP, Corpas FJ, Barroso JB, Tripathi RD (2013) Arsenite tolerance is related to proportional thiolic metabolite synthesis in rice (Oryza sativa L.). Arch Environ Contam Toxicol 64:235–242

    Article  CAS  PubMed  Google Scholar 

  • De Ollas C, Hernando B, Arbona V, Gómez-Cadenas A (2013) Jasmonic acid transient accumulation is needed for abscisic acid increase in citrus roots under drought stress conditions. Physiol Plant 147:296–306

    Article  PubMed  CAS  Google Scholar 

  • Deluc LG, Grimplet J, Wheatley MD, Tillett RL, Quilici DR, Osborne C, Schooley DA, Schlauch KA, Cushman JC, Cramer GR (2007) Transcriptomic and metabolite analyses of Cabernet Sauvignon grape berry development. BMC Genomics 8:429

    Article  PubMed  PubMed Central  Google Scholar 

  • Denekamp M, Smeekens SC (2003) Integration of wounding and osmotic stress signals determines the expression of the AtMYB102 transcription factor gene 1. Plant Physiol 132:1415–1423

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Des Marais DL, Juenger TE (2010) Pleiotropy, plasticity, and the evolution of plant abiotic stress tolerance. Ann N Y Acad Sci 1206:56–79

    Article  CAS  PubMed  Google Scholar 

  • Diévart A, Clark SE (2004) LRR-containing receptors regulating plant development and defense. Development 131:251–261

    Article  PubMed  CAS  Google Scholar 

  • Ding Y, Fromm M, Avramova Z (2012) Multiple exposures to drought “train” transcriptional responses in Arabidopsis. Nat Commun 3:740

    Article  PubMed  CAS  Google Scholar 

  • Djoukeng JD, Arbona V, Argamasilla R, Gomez-Cadenas A (2008) Flavonoid profiling in leaves of citrus genotypes under different environmental situations. J Agric Food Chem 56:11087–11097

    Article  CAS  PubMed  Google Scholar 

  • Dolferus R (2014) To grow or not to grow: a stressful decision for plants. Plant Sci 229:247–261

    Article  CAS  PubMed  Google Scholar 

  • Dombrecht B, Xue GP, Sprague SJ, Kirkegaard JA, Ross JJ, Reid JB, Fitt GP, Sewelam N, Schenk PM, Manners JM, Kazan K (2007) MYC2 differentially modulates diverse jasmonate-dependent functions in Arabidopsis. Plant Cell 19:2225–2245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dumas M-E (2012) Metabolome 2.0: quantitative genetics and network biology of metabolic phenotypes. Mol Biosyst 8:2494–2502

    Article  CAS  PubMed  Google Scholar 

  • Elobeid M, Göbel C, Feussner I, Polle A (2012) Cadmium interferes with auxin physiology and lignification in poplar. J Exp Bot 63:1413–1421

    Article  CAS  PubMed  Google Scholar 

  • Espinoza A, San Martín A, López-Climent M, Ruiz-Lara S, Gómez-Cadenas A, Casaretto JA (2013) Engineered drought-induced biosynthesis of α-tocopherol alleviates stress-induced leaf damage in tobacco. J Plant Physiol 170:1285–1294

    Article  CAS  PubMed  Google Scholar 

  • Fowler SG, Cook D, Thomashow MF (2005) Low temperature induction of Arabidopsis CBF1, 2, and 3 is gated by the circadian clock. Plant Physiol 137:961–968

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fujita M, Fujita Y, Maruyama K, Seki M, Hiratsu K, Ohme-Takagi M, Tran L-SP, 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

    Article  CAS  PubMed  Google Scholar 

  • Fujita Y, Fujita M, Shinozaki K, Yamaguchi-Shinozaki K (2011) ABA-mediated transcriptional regulation in response to osmotic stress in plants. J Plant Res 124:509–525

    Article  CAS  PubMed  Google Scholar 

  • Fujita Y, Yoshida T, Yamaguchi-Shinozaki K (2013) Pivotal role of the AREB/ABF-SnRK2 pathway in ABRE-mediated transcription in response to osmotic stress in plants. Physiol Plant 147:15–27

    Article  CAS  PubMed  Google Scholar 

  • Furihata T, Maruyama K, Fujita Y, Umezawa T, Yoshida R, Shinozaki K, Yamaguchi-Shinozaki K (2006) Abscisic acid-dependent multisite phosphorylation regulates the activity of a transcription activator AREB1. Proc Natl Acad Sci U S A 103:1988–1993

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Geiger D, Maierhofer T, Al-Rasheid KAS, Scherzer S, Mumm P, Liese A, Ache P, Wellmann C, Marten I, Grill E et al (2011) Stomatal closure by fast abscisic acid signaling is mediated by the guard cell anion channel SLAH3 and the receptor RCAR1. Sci Signal 4:ra32

    Google Scholar 

  • Gepstein S, Glick BR (2013) Strategies to ameliorate abiotic stress-induced plant senescence. Plant Mol Biol 82(6):623–633

    Google Scholar 

  • Ghars MA, Parre E, Debez A, Bordenave M, Richard L, Leport L, Bouchereau A, Savouré A, Abdelly C (2008) Comparative salt tolerance analysis between Arabidopsis thaliana and Thellungiella halophila, with special emphasis on K+/Na+ selectivity and proline accumulation. J Plant Physiol 165:588–599

    Article  CAS  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

    Article  CAS  PubMed  Google Scholar 

  • Golldack D, Li C, Mohan H, Probst N (2014) Tolerance to drought and salt stress in plants: unraveling the signaling networks. Front Plant Sci 5:151

    Article  PubMed  PubMed Central  Google Scholar 

  • Granier C, Aguirrezabal L, Chenu K, Cookson SJ, Dauzat M, Hamard P, Thioux J-J, Rolland G, Bouchier-Combaud S, Lebaudy A, Muller B, Simonneau T, Tardieu F (2006) PHENOPSIS, an automated platform for reproducible phenotyping of plant responses to soil water deficit in Arabidopsis thaliana permitted the identification of an accession with low sensitivity to soil water deficit. New Phytol 169:623–635

    Article  PubMed  Google Scholar 

  • Hamel L-P, Nicole M-C, Duplessis S, Ellis BE (2012) Mitogen-activated protein kinase signaling in plant-interacting fungi: distinct messages from conserved messengers. Plant Cell 24:1327–1351

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hauser F, Waadt R, Schroeder JI (2011) Evolution of abscisic acid synthesis and signaling mechanisms. Curr Biol 21:346–355

    Article  CAS  Google Scholar 

  • Hauvermale AL, Ariizumi T, Steber CM (2012) Gibberellin signaling: a theme and variations on DELLA repression. Plant Physiol 160:83–92

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hess N, Klode M, Anders M, Sauter M (2011) The hypoxia responsive transcription factor genes ERF71/HRE2 and ERF73/HRE1 of Arabidopsis are differentially regulated by ethylene. Physiol Plant 143:41–49

    Article  CAS  PubMed  Google Scholar 

  • Hobo T, Asada M, Kowyama Y, Hattori T (1999) ACGT-containing abscisic acid response element (ABRE) and coupling element 3 (CE3) are functionally equivalent. Plant J 19:679–689

    Article  CAS  PubMed  Google Scholar 

  • Hong S-W, Vierling E (2000) Mutants of Arabidopsis thaliana defective in the acquisition of tolerance to high temperature stress. Proc Natl Acad Sci U S A 97:4392–4397

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoque MA, Okuma E, Banu MNA, Nakamura Y, Shimoishi Y, Murata Y (2007) Exogenous proline mitigates the detrimental effects of salt stress more than exogenous betaine by increasing antioxidant enzyme activities. J Plant Physiol 164:553–561

    Article  CAS  PubMed  Google Scholar 

  • Horváth E, Szalai G, Janda T (2007) Induction of abiotic stress tolerance by salicylic acid signaling. J Plant Growth Regul 26:290–300

    Article  CAS  Google Scholar 

  • Hossain Z, Mandal AKA, Datta SK, Biswas AK (2006) Isolation of a NaCl-tolerant mutant of Chrysanthemum morifolium by gamma radiation: in vitro mutagenesis and selection by salt stress. Funct Plant Biol 33:91

    Article  CAS  Google Scholar 

  • Hsieh T-H, Li C-W, Su R-C, Cheng C-P, Sanjaya, Tsai Y-C, Chan M-T (2010) A tomato bZIP transcription factor, SlAREB, is involved in water deficit and salt stress response. Planta 231:1459–1473

    Article  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

    Article  CAS  PubMed  Google Scholar 

  • Hua D, Wang C, He J, Liao H, Duan Y, Zhu Z, Guo Y, Chen Z, Gong Z (2012) A plasma membrane receptor kinase, GHR1, mediates abscisic acid- and hydrogen peroxide-regulated stomatal movement in Arabidopsis. Plant Cell 24:2546–2561

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang J, Zhang Y, Peng J-S, Zhong C, Yi H-Y, Ow DW, Gong J-M (2012) Fission yeast HMT1 lowers seed cadmium through phytochelatin-dependent vacuolar sequestration in Arabidopsis. Plant Physiol 158:1779–1788

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang G-Q, Li W, Zhou W, Zhang J-M, Li D-D, Gong S-Y, Li X-B (2013) Seven cotton genes encoding putative NAC domain proteins are preferentially expressed in roots and in responses to abiotic stress during root development. Plant Growth Regul 71:101–112

    Article  CAS  Google Scholar 

  • Hubbard KE, Nishimura N, Hitomi K, Getzoff ED, Schroeder JI (2010) Early abscisic acid signal transduction mechanisms : newly discovered components and newly emerging questions. Genes Dev 24:1695–1708

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iriti M, Faoro F (2009) Chemical diversity and defence metabolism: how plants cope with pathogens and ozone pollution. Int J Mol Sci 10:3371–3399

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ithal N, Reddy AR (2004) Rice flavonoid pathway genes, OsDfr and OsAns, are induced by dehydration, high salt and ABA, and contain stress responsive promoter elements that interact with the transcription activator, OsC1-MYB. Plant Sci 166:1505–1513

    Article  CAS  Google Scholar 

  • Janská A, Marsík P, Zelenková S, Ovesná J (2010) Cold stress and acclimation—what is important for metabolic adjustment? Plant Biol 12:395–405

    Article  PubMed  CAS  Google Scholar 

  • Jensen MK, Lindemose S, de Masi F, Reimer JJ, Nielsen M, Perera V, Workman CT, Turck F, Grant MR, Mundy J, Petersen M, Skriver K (2013) ATAF1 transcription factor directly regulates abscisic acid biosynthetic gene NCED3 in Arabidopsis thaliana. FEBS Open Bio 3:321–327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jeon J, Kim NY, Kim S, Kang NY, Novák O, Ku S-J, Cho C, Lee DJ, Lee E-J, Strnad M, Kim J (2010) A subset of cytokinin two-component signaling system plays a role in cold temperature stress response in Arabidopsis. J Biol Chem 285:23371–23386

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jha UC, Chaturvedi SK, Bohra A, Basu PS, Khan MS, Barh D (2014) Abiotic stresses, constraints and improvement strategies in chickpea. Plant Breed 133:163–178

    Article  Google Scholar 

  • Jia H, Wang N (2014) Targeted genome editing of sweet orange using Cas9/sgRNA. PLoS One 9:e93806

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jin S, Daniell H (2014) Expression of γ-tocopherol methyltransferase in chloroplasts results in massive proliferation of the inner envelope membrane and decreases susceptibility to salt and metal-induced oxidative stresses by reducing reactive oxygen species. Plant Biotechnol J 12(9):1274–1285

    Google Scholar 

  • Jung C, Seo JS, Han SW, Koo YJ, Kim CH, Song SI, Nahm BH, Choi YD, Cheong J-J (2008) Overexpression of AtMYB44 enhances stomatal closure to confer abiotic stress tolerance in transgenic Arabidopsis. Plant Physiol 146:623–635

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kang G, Li G, Guo T (2014) Molecular mechanism of salicylic acid-induced abiotic stress tolerance in higher plants. Acta Physiol Plant 36:2287–2297

    Article  CAS  Google Scholar 

  • Kaplan F, Guy CL (2004) β-amylase induction and the protective role of maltose during temperature shock. Plant Physiol 135:1674–1684

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karowe DN, Grubb C (2011) Elevated CO2 increases constitutive phenolics and trichomes, but decreases inducibility of phenolics in Brassica rapa (Brassicaceae). J Chem Ecol 37:1332–1340

    Article  CAS  PubMed  Google Scholar 

  • Kawakami A, Sato Y, Yoshida M (2008) Genetic engineering of rice capable of synthesizing fructans and enhancing chilling tolerance. J Exp Bot 59:793–802

    Article  CAS  PubMed  Google Scholar 

  • Kazan K, Manners JM (2013) MYC2: the master in action. Mol Plant 6:686–703

    Article  CAS  PubMed  Google Scholar 

  • Keunen E, Peshev D, Vangronsveld J, Van den Ende W, Cuypers A (2013) Plant sugars are crucial players in the oxidative challenge during abiotic stress: extending the traditional concept. Plant Cell Environ 36:1242–1255

    Article  CAS  PubMed  Google Scholar 

  • Kim SY (2006) The role of ABF family bZIP class transcription factors in stress response. Physiol Plant 126:519–527

    CAS  Google Scholar 

  • Kim SH, Ahn YO, Ahn M-J, Lee H-S, Kwak S-S (2012) Down-regulation of β-carotene hydroxylase increases β-carotene and total carotenoids enhancing salt stress tolerance in transgenic cultured cells of sweetpotato. Phytochemistry 74:69–78

    Article  CAS  PubMed  Google Scholar 

  • Kinoshita T, Seki M (2014) Epigenetic memory for stress response and adaptation in plants. Plant Cell Physiol 55:1859–1863

    Article  CAS  PubMed  Google Scholar 

  • Kleinow T, Himbert S, Krenz B, Jeske H, Koncz C (2009) NAC domain transcription factor ATAF1 interacts with SNF1-related kinases and silencing of its subfamily causes severe developmental defects in Arabidopsis. Plant Sci 177:360–370

    Article  CAS  Google Scholar 

  • Ko J-H, 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

    Article  CAS  PubMed  Google Scholar 

  • Krasensky J, Jonak C (2012) Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. J Exp Bot 63:1593–1608

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lata C, Prasad M (2011) Role of DREBs in regulation of abiotic stress responses in plants. J Exp Bot 62:4731–4748

    Article  CAS  PubMed  Google Scholar 

  • Lee S-J, Kang J-Y, Park H-J, Kim MD, Bae MS, Choi H-I, Kim SY (2010) DREB2C interacts with ABF2, a bZIP protein regulating abscisic acid-responsive gene expression, and its overexpression affects abscisic acid sensitivity. Plant Physiol 153:716–727

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li H-J, Yang A-F, Zhang X-C, Gao F, Zhang J-R (2007) Improving freezing tolerance of transgenic tobacco expressing sucrose: sucrose 1-fructosyltransferase gene from Lactuca sativa. Plant Cell Tissue Organ Cult 89:37–48

    Article  CAS  Google Scholar 

  • Liu G-Y, Zhang Y-X, Chai T-Y (2011) Phytochelatin synthase of Thlaspi caerulescens enhanced tolerance and accumulation of heavy metals when expressed in yeast and tobacco. Plant Cell Rep 30:1067–1076

    Article  CAS  PubMed  Google Scholar 

  • Liu G-T, Wang J-F, Cramer G, Dai Z-W, Duan W, Xu H-G, Wu B-H, Fan P-G, Wang L-J, Li S-H (2012) Transcriptomic analysis of grape (Vitis vinifera L.) leaves during and after recovery from heat stress. BMC Plant Biol 12:174

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lobell DB, Gourdji SM (2012) The influence of climate change on global crop productivity. Plant Physiol 160:1686–1697

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • López-Climent MF, Arbona V, Pérez-Clemente RM, Gómez-Cadenas A (2008) Relationship between salt tolerance and photosynthetic machinery performance in citrus. Environ Exp Bot 62:176–184

    Article  CAS  Google Scholar 

  • Lu J, Charles MT, Vigneault C, Goyette B, Raghavan GSV (2010) Effect of heat treatment uniformity on tomato ripening and chilling injury. Postharvest Biol Technol 56:155–162

    Article  CAS  Google Scholar 

  • Lynch T, Erickson BJ, Finkelstein RR (2012) Direct interactions of ABA-insensitive(ABI)-clade protein phosphatase(PP)2Cs with calcium-dependent protein kinases and ABA response element-binding bZIPs may contribute to turning off ABA response. Plant Mol Biol 80:647–658

    Article  CAS  PubMed  Google Scholar 

  • Madlung A (2013) Polyploidy and its effect on evolutionary success: old questions revisited with new tools. Heredity 110:99–104

    Article  CAS  PubMed  Google Scholar 

  • Manzaneda AJ, Rey PJ, Bastida JM, Weiss-Lehman C, Raskin E, Mitchell-Olds T (2012) Environmental aridity is associated with cytotype segregation and polyploidy occurrence in Brachypodium distachyon (Poaceae). New Phytol 193:797–805

    Article  PubMed  Google Scholar 

  • Mao X, Zhang H, Qian X, Li A, Zhao G, Jing R (2012) TaNAC2, a NAC-type wheat transcription factor conferring enhanced multiple abiotic stress tolerances in Arabidopsis. J Exp Bot 63:2933–2946

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marshall A, Aalen RB, Audenaert D, Beeckman T, Broadley MR, Butenko MA, Caño-Delgado AI, de Vries S, Dresselhaus T, Felix G, Graham NS, Foulkes J, Granier C, Greb T, Grossniklaus U, Hammond JP, Heidstra R, Hodgman C, Hothorn M, Inzé D, Ostergaard L, Russinova E, Simon R, Skirycz A, Stahl Y, Zipfel C, De Smet I (2012) Tackling drought stress: receptor-like kinases present new approaches. Plant Cell 24:2262–2278

    Google Scholar 

  • Mba C, Afza R, Jain SM, Gregorio GB, Zapata-Arias FJ (2007) Induced mutations for enhancing salinity tolerance in rice. In: Jenks MA, Hasegawa PM, Jain SM (eds) Advances in molecular breeding toward drought and salt tolerant crops. Springer, Dordrecht, pp 413–454

    Chapter  Google Scholar 

  • McClinchey SL, Kott LS (2007) Production of mutants with high cold tolerance in spring canola (Brassica napus). Euphytica 162:51–67

    Article  CAS  Google Scholar 

  • Mengiste T, Chen X, Salmeron J, Dietrich R (2003) The BOTRYTIS SUSCEPTIBLE1 gene encodes an R2R3MYB transcription factor protein that is required for biotic and abiotic stress responses in Arabidopsis. Plant Cell 15:2551–2565

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Minocha R, Majumdar R, Minocha SC (2014) Polyamines and abiotic stress in plants: a complex relationship. Front Plant Sci 5:175

    Article  PubMed  PubMed Central  Google Scholar 

  • Miranda JA, Avonce N, Suárez R, Thevelein JM, Van Dijck P, Iturriaga G (2007) A bifunctional TPS-TPP enzyme from yeast confers tolerance to multiple and extreme abiotic-stress conditions in transgenic Arabidopsis. Planta 226:1411–1421

    Article  CAS  PubMed  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  CAS  PubMed  Google Scholar 

  • Mittler R, Blumwald E (2015) The roles of ROS and ABA in systemic acquired acclimation. Plant Cell 27:64–70

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miura K, Tada Y (2014) Regulation of water, salinity, and cold stress responses by salicylic acid. Front Plant Sci 5:4

    Article  PubMed  PubMed Central  Google Scholar 

  • Moghe GD, Shiu S-H (2014) The causes and molecular consequences of polyploidy in flowering plants. Ann N Y Acad Sci 1320:16–34

    Article  CAS  PubMed  Google Scholar 

  • Molinari HBC, Marur CJ, Filho JCB, Kobayashi AK, Pileggi M, Júnior RPL, Pereira LFP, Vieira LGE (2004) Osmotic adjustment in transgenic citrus rootstock Carrizo citrange (Citrus sinensis Osb. x Poncirus trifoliata L. Raf.) overproducing proline. Plant Sci 167:1375–1381

    Article  CAS  Google Scholar 

  • Moura JCMS, Bonine CAV, de Oliveira Fernandes Viana J, Dornelas MC, Mazzafera P (2010) Abiotic and biotic stresses and changes in the lignin content and composition in plants. J Integr Plant Biol 52:360–376

    Article  CAS  PubMed  Google Scholar 

  • Munné-Bosch S, Alegre L (2013) Cross-stress tolerance and stress “memory” in plants: an integrated view. Environ Exp Bot 94:1–2

    Article  Google Scholar 

  • Muñoz-Amatriaín M, Cuesta-Marcos A, Endelman JB, Comadran J, Bonman JM, Bockelman HE, Chao S, Russell J, Waugh R, Hayes PM, Muehlbauer GJ (2014) The USDA barley core collection: genetic diversity, population structure, and potential for genome-wide association studies. PLoS One 9:e94688

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nakashima K, Yamaguchi-Shinozaki K (2013) ABA signaling in stress-response and seed development. Plant Cell Rep 32:959–970

    Article  CAS  PubMed  Google Scholar 

  • Nakashima K, Takasaki H, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2012) NAC transcription factors in plant abiotic stress responses. Biochim Biophys Acta 1819:97–103

    Article  CAS  PubMed  Google Scholar 

  • Narusaka Y, Nakashima K, Shinwari ZK, Sakuma Y, Furihata T, Abe H, Narusaka M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Interaction between two cis-acting elements, ABRE and DRE, in ABA-dependent expression of Arabidopsis rd29A gene in response to dehydration and high-salinity stresses. Plant J 34:137–148

    Article  CAS  PubMed  Google Scholar 

  • Neeraja CN, Maghirang-Rodriguez R, Pamplona A, Heuer S, Collard BCY, Septiningsih EM, Vergara G, Sanchez D, Xu K, Ismail AM, Mackill DJ (2007) A marker-assisted backcross approach for developing submergence-tolerant rice cultivars. Theor Appl Genet 115:767–776

    Article  CAS  PubMed  Google Scholar 

  • Nekrasov V, Staskawicz B, Weigel D, Jones JDG, Kamoun S (2013) Targeted mutagenesis in the model plant Nicotiana benthamiana using Cas9 RNA-guided endonuclease. Nat Biotechnol 31:691–693

    Article  CAS  PubMed  Google Scholar 

  • Nishiyama Y, Allakhverdiev SI, Yamamoto H, Hayashi H (2004) Singlet oxygen inhibits the repair of photosystem ii by suppressing the translation elongation of the D1 protein in Synechocystis sp. PCC 6803. Biochemistry 43:11321–11330

    Article  CAS  PubMed  Google Scholar 

  • Nishizawa A, Yabuta Y, Shigeoka S (2008) Galactinol and raffinose constitute a novel function to protect plants from oxidative damage. Plant Physiol 147:1251–1263

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Noctor G, Queval G, Mhamdi A, Chaouch S, Foyer CH (2011) Glutathione. Arabidopsis Book 9:1–32

    Article  Google Scholar 

  • Noctor G, Mhamdi A, Foyer CH (2014) The roles of reactive oxygen metabolism in drought: not so cut and dried. Plant Physiol 164:1636–1648

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oa RW, Kim EH, Kim YS, Park S, Koo YJ, Choi YD, Chung Y, Lee I, Kim J (2009) Methyl jasmonate reduces grain yield by mediating stress signals to alter spikelet development. Plant Physiol 149:1751–1760

    Article  Google Scholar 

  • Orabi SA, Mekki BB, Sharara FA (2013) Alleviation of adverse effects of salt stress on Faba bean (Vicia faba L.) plants by exogenous application of salicylic acid. World Appl Sci J 27:418–427

    Google Scholar 

  • Osakabe Y, Mizuno S, Tanaka H, Maruyama K, Osakabe K, Todaka D, Fujita Y, Kobayashi M, Shinozaki K, Yamaguchi-Shinozaki K (2010) Overproduction of the membrane-bound receptor-like protein kinase 1, RPK1, enhances abiotic stress tolerance in Arabidopsis. J Biol Chem 285:9190–9201

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Osakabe Y, Yamaguchi-Shinozaki K, Shinozaki K, Tran L-SP (2013) Sensing the environment: key roles of membrane-localized kinases in plant perception and response to abiotic stress. J Exp Bot 64:445–458

    Article  CAS  PubMed  Google Scholar 

  • Pateraki I, Kanellis AK (2010) Stress and developmental responses of terpenoid biosynthetic genes in Cistus creticus subsp. creticus. Plant Cell Rep 29:629–641

    Article  CAS  PubMed  Google Scholar 

  • Peleg Z, Blumwald E (2011) Hormone balance and abiotic stress tolerance in crop plants. Curr Opin Plant Biol 14:290–295

    Article  CAS  PubMed  Google Scholar 

  • Pennycooke JC, Jones ML, Stushnoff C (2003) Down-regulating alpha-galactosidase enhances freezing tolerance in transgenic petunia. Plant Physiol 133:901–909

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Persak H, Pitzschke A (2014) Dominant repression by Arabidopsis transcription factor MYB44 causes oxidative damage and hypersensitivity to abiotic stress. Int J Mol Sci 15:2517–2537

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Petrusa LM, Winicov I (1997) Proline status in salt-tolerant and salt-sensitive alfalfa cell lines and plants in response to NaCl. Plant Physiol Biochem 35:303–310

    CAS  Google Scholar 

  • Pham J, Liu J, Bennett MH, Mansfield JW, Desikan R (2012) Arabidopsis histidine kinase 5 regulates salt sensitivity and resistance against bacterial and fungal infection. New Phytol 194:168–180

    Article  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

    Article  CAS  Google Scholar 

  • Puranik S, Sahu PP, Srivastava PS, Prasad M (2012) NAC proteins: regulation and role in stress tolerance. Trends Plant Sci 17:369–381

    Article  CAS  PubMed  Google Scholar 

  • Rai MK, Kalia RK, Singh R, Gangola MP, Dhawan AK (2011) Developing stress tolerant plants through in vitro selection—an overview of the recent progress. Environ Exp Bot 71:89–98

    Article  Google Scholar 

  • Rajjou L, Maya B, Romain H, Caroline R, Adrien M, Claudette J, Job D (2006) Proteomic investigation of the effect of salicylic acid on Arabidopsis seed germination and establishment of early defense mechanisms. Plant Physiol 141:910–923

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Redillas MCFR, Jeong JS, Kim YS, Jung H, Bang SW, Choi YD, Ha S-H, Reuzeau C, Kim J-K (2012) The overexpression of OsNAC9 alters the root architecture of rice plants enhancing drought resistance and grain yield under field conditions. Plant Biotechnol J 10:792–805

    Article  CAS  PubMed  Google Scholar 

  • Reginato M, Abdala G, Miersch O, Ruiz O, Moschetti E, Luna V (2012) Changes in the levels of jasmonates and free polyamines induced by Na2SO4 and NaCl in roots and leaves of the halophyte Prosopis strombulifera. Biologia 67:689–697

    Article  CAS  Google Scholar 

  • Ren X-L, Qi G-N, Feng H-Q, Zhao S, Zhao S-S, Wang Y, Wu W-H (2013) Calcineurin B-like protein CBL10 directly interacts with AKT1 and modulates K+ homeostasis in Arabidopsis. Plant J 74:258–266

    Article  CAS  PubMed  Google Scholar 

  • Reynolds M, Pask A, Mullan D (eds) (2012) Physiological breeding I: interdisciplinary approaches to improve crop adaptation. International Maize and Wheat Improvement Center, Mexico, p 188

    Google Scholar 

  • Rivero RM, Mestre TC, Mittler R, Rubio F, Garcia-Sanchez F, Martinez V (2014) The combined effect of salinity and heat reveals a specific physiological, biochemical and molecular response in tomato plants. Plant Cell Environ 37:1059–1073

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez MC, Petersen M, Mundy J (2010) Mitogen-activated protein kinase signaling in plants. Annu Rev Plant Biol 61:621–649

    Article  CAS  PubMed  Google Scholar 

  • Roy SJ, Negrão S, Tester M (2014) Salt resistant crop plants. Curr Opin Biotechnol 26:115–124

    Article  CAS  PubMed  Google Scholar 

  • Sainz M, Díaz P, Monza J, Borsani O (2010) Heat stress results in loss of chloroplast Cu/Zn superoxide dismutase and increased damage to Photosystem II in combined drought-heat stressed Lotus japonicus. Physiol Plant 140:46–56

    Article  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

    Article  CAS  PubMed  PubMed Central  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Santiago J, Dupeux F, Betz K, Antoni R, Gonzalez-Guzman M, Rodriguez L, Márquez JA, Rodriguez PL (2012) Structural insights into PYR/PYL/RCAR ABA receptors and PP2Cs. Plant Sci 182:3–11

    Article  CAS  PubMed  Google Scholar 

  • Schaller GE, Kieber JJ, Shiu S-H (2008) Two-component signaling elements and histidyl-aspartyl phosphorelays. Arabidopsis Book 6:e0112

    Article  PubMed  PubMed Central  Google Scholar 

  • Schenke D, Böttcher C, Scheel D (2011) Crosstalk between abiotic ultraviolet-B stress and biotic (flg22) stress signalling in Arabidopsis prevents flavonol accumulation in favor of pathogen defence compound production. Plant Cell Environ 34:1849–1864

    Article  CAS  PubMed  Google Scholar 

  • Schiml S, Fauser F, Puchta H (2014) The CRISPR/Cas system can be used as nuclease for in planta gene targeting and as paired nickases for directed mutagenesis in Arabidopsis resulting in heritable progeny. Plant J 80(6):1139–1150

    Google Scholar 

  • Schwechheimer C, Willige BC (2009) Shedding light on gibberellic acid signalling. Curr Opin Plant Biol 12:57–62

    Article  CAS  PubMed  Google Scholar 

  • Sen A, Alikamanoglu S (2014) Characterization of drought-tolerant sugar beet mutants induced with gamma radiation using biochemical analysis and isozyme variations. J Sci Food Agric 94:367–372

    Article  CAS  PubMed  Google Scholar 

  • Setter TL (2012) Analysis of constituents for phenotyping drought tolerance in crop improvement. Front Physiol 3:180

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shan Q, Wang Y, Li J, Gao C (2014) Genome editing in rice and wheat using the CRISPR/Cas system. Nat Protoc 9:2395–2410

    Article  CAS  PubMed  Google Scholar 

  • Shi H, Chen L, Ye T, Liu X, Ding K, Chan Z (2014) Modulation of auxin content in Arabidopsis confers improved drought stress resistance. Plant Physiol Biochem 82:209–217

    Article  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

    Article  CAS  PubMed  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K, Seki M (2003) Regulatory network of gene expression in the drought and cold stress responses. Curr Opin Plant Biol 6:410–417

    Article  CAS  PubMed  Google Scholar 

  • Shiu S-H, Bleecker AB (2001) Plant receptor-like kinase gene family: diversity, function, and signaling. Sci Signal 2001:re22

    Google Scholar 

  • Showalter AM, Keppler B, Lichtenberg J, Gu D, Welch LR (2010) A bioinformatics approach to the identification, classification, and analysis of hydroxyproline-rich glycoproteins. Plant Physiol 153:485–513

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sicher RC, Timlin D, Bailey B (2012) Responses of growth and primary metabolism of water-stressed barley roots to rehydration. J Plant Physiol 169:686–695

    Article  CAS  PubMed  Google Scholar 

  • Simpson SD, Nakashima K, Narusaka Y, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Two different novel cis -acting elements of erd1, a clpA homologous Arabidopsis gene function in induction by dehydration stress and dark-induced senescence. Plant J 33:259–270

    Article  CAS  PubMed  Google Scholar 

  • Sinha AK, Jaggi M, Raghuram B, Tuteja N (2011) Mitogen-activated protein kinase signaling in plants under abiotic stress. Plant Signal Behav 6:196–203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stracke R, Werber M, Weisshaar B (2001) The R2R3-MYB gene family in Arabidopsis thaliana. Curr Opin Plant Biol 4:447–456

    Article  CAS  PubMed  Google Scholar 

  • Su L-T, Li J-W, Liu D-Q, Zhai Y, Zhang H-J, Li X-W, Zhang Q-L, Wang Y, Wang Q-Y (2014) A novel MYB transcription factor, GmMYBJ1, from soybean confers drought and cold tolerance in Arabidopsis thaliana. Gene 538:46–55

    Article  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

    Article  CAS  PubMed  Google Scholar 

  • Suzuki N, Rivero RM, Shulaev V, Blumwald E, Mittler R (2014) Abiotic and biotic stress combinations. New Phytol 203:32–43

    Article  PubMed  Google Scholar 

  • Syvertsen JP, Garcia-Sanchez F (2014) Multiple abiotic stresses occurring with salinity stress in citrus. Environ Exp Bot 103:128–137

    Article  CAS  Google Scholar 

  • Tanaka H, Osakabe Y, Katsura S, Mizuno S, Maruyama K, Kusakabe K, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2012) Abiotic stress-inducible receptor-like kinases negatively control ABA signaling in Arabidopsis. Plant J 70:599–613

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Teixeira EI, Fischer G, van Velthuizen H, Walter C, Ewert F (2013) Global hot-spots of heat stress on agricultural crops due to climate change. Agric For Meteorol 170:206–215

    Article  Google Scholar 

  • Tran L-SP, Urao T, Qin F, Maruyama K, Kakimoto T, Shinozaki K, Yamaguchi-Shinozaki K (2007) Functional analysis of AHK1/ATHK1 and cytokinin receptor histidine kinases in response to abscisic acid, drought, and salt stress in Arabidopsis. Proc Natl Acad Sci U S A 104:20623–20628

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tran LP, Shinozaki K, Yamaguchi-shinozaki K (2010) Role of cytokinin responsive two-component system in ABA and osmotic stress signalings. Plant Signal Behav 5:148–150

    Article  CAS  PubMed  PubMed Central  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Urano K, Yoshiba Y, Nanjo T, Igarashi Y, Seki M, Sekiguchi F, Yamaguchi-Shinozaki K, Shinozaki K (2003) Characterization of Arabidopsis genes involved in biosynthesis of polyamines in abiotic stress responses and developmental stages. Plant Cell Environ 26:1917–1926

    Article  CAS  Google Scholar 

  • Verslues PE, Agarwal M, Katiyar-Agarwal S, Zhu J, Zhu J-K (2006) Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status. Plant J 45:523–539

    Article  CAS  PubMed  Google Scholar 

  • Vincent D, Lapierre C, Pollet B, Cornic G, Negroni L, Zivy M (2005) Water deficits affect caffeate O-methyltransferase, lignification, and related enzymes in maize leaves. A proteomic investigation. Plant Physiol 137:949–960

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Volkova L, Tausz M, Bennett LT, Dreyer E (2009) Interactive effects of high irradiance and moderate heat on photosynthesis, pigments, and tocopherol in the tree-fern Dicksonia antarctica. Funct Plant Biol 36:1046

    Article  CAS  Google Scholar 

  • Wang Z, Dane F (2013) NAC (NAM/ATAF/CUC) transcription factors in different stresses and their signaling pathway. Acta Physiol Plant 35:1397–1408

    Article  CAS  Google Scholar 

  • Wang YH, Irving HR (2011) Developing a model of plant hormone interactions. Plant Signal Behav 6:494–500

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang F, Cui X, Sun Y, Dong C-H (2013) Ethylene signaling and regulation in plant growth and stress responses. Plant Cell Rep 32(7):1099–1109

    Article  CAS  PubMed  Google Scholar 

  • Wilkinson S, Davies WJ (2010) Drought, ozone, ABA and ethylene: new insights from cell to plant to community. Plant Cell Environ 33:510–525

    Article  CAS  PubMed  Google Scholar 

  • Wohlbach DJ, Quirino BF, Sussman MR (2008) Analysis of the Arabidopsis histidine kinase ATHK1 reveals a connection between vegetative osmotic stress sensing and seed maturation. Plant Cell 20:1101–1117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wojas S, Hennig J, Plaza S, Geisler M, Siemianowski O, Skłodowska A, Ruszczyńska A, Bulska E, Antosiewicz DM (2009) Ectopic expression of Arabidopsis ABC transporter MRP7 modifies cadmium root-to-shoot transport and accumulation. Environ Pollut 157:2781–2789

    Article  CAS  PubMed  Google Scholar 

  • Wu Y, Deng Z, Lai J, Zhang Y, Yang C, Yin B, Zhao Q, Zhang L, Li Y, Yang C, Xie Q (2009) Dual function of Arabidopsis ATAF1 in abiotic and biotic stress responses. Cell Res 19:1279–1290

    Article  CAS  PubMed  Google Scholar 

  • Wu GA, Prochnik S, Jenkins J, Salse J, Hellsten U, Murat F, Perrier X, Ruiz M, Scalabrin S, Terol J, Takita MA, Labadie K, Poulain J, Couloux A, Jabbari K, Cattonaro F, Del Fabbro C, Pinosio S, Zuccolo A, Chapman J, Grimwood J, Tadeo FR, Estornell LH, Muñoz-Sanz JV, Ibanez V, Herrero-Ortega A, Aleza P, Pérez-Pérez J, Ramón D, Brunel D, Luro F, Chen C, Farmerie WG, Desany B, Kodira C, Mohiuddin M, Harkins T, Fredrikson K, Burns P, Lomsadze A, Borodovsky M, Reforgiato G, Freitas-Astúa J, Quetier F, Navarro L, Roose M, Wincker P, Schmutz J, Morgante M, Machado MA, Talon M, Jaillon O, Ollitrault P, Gmitter F, Rokhsar D (2014) Sequencing of diverse mandarin, pummelo and orange genomes reveals complex history of admixture during citrus domestication. Nat Biotechnol 32:656–662

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xia X-J, Zhou Y-H, Ding J, Shi K, Asami T, Chen Z, Yu J-Q (2011) Induction of systemic stress tolerance by brassinosteroid in Cucumis sativus. New Phytol 191:706–720

    Article  CAS  PubMed  Google Scholar 

  • Xing W, Rajashekar C (1999) Alleviation of water stress in beans by exogenous glycine betaine. Plant Sci 148:185–192

    Article  CAS  Google Scholar 

  • Xu Z-S, Xia L-Q, Chen M, Cheng X-G, Zhang R-Y, Li L-C, Zhao Y-X, Lu Y, Ni Z-Y, Liu L, Qiu Z-G, Ma Y-Z (2007) Isolation and molecular characterization of the Triticum aestivum L. ethylene-responsive factor 1 (TaERF1) that increases multiple stress tolerance. Plant Mol Biol 65:719–732

    Article  CAS  PubMed  Google Scholar 

  • Xu W, Jia L, Shi W, Liang J, Zhou F, Li Q, Zhang J (2013) Abscisic acid accumulation modulates auxin transport in the root tip to enhance proton secretion for maintaining root growth under moderate water stress. New Phytol 197:139–150

    Article  CAS  PubMed  Google Scholar 

  • Xue G-P, Way HM, Richardson T, Drenth J, Joyce PA, McIntyre CL (2011) Overexpression of TaNAC69 leads to enhanced transcript levels of stress up-regulated genes and dehydration tolerance in bread wheat. Mol Plant 4:697–712

    Article  CAS  PubMed  Google Scholar 

  • Yan F, Deng W, Wang X, Yang C, Li Z (2012) Maize (Zea mays L.) homologue of ABA-insensitive (ABI) 5 gene plays a negative regulatory role in abiotic stresses response. Plant Growth Regul 68:383–393

    Article  CAS  Google Scholar 

  • Yang C-Y, Hsu F-C, Li J-P, Wang N-N, Shih M-C (2011a) The AP2/ERF transcription factor AtERF73/HRE1 modulates ethylene responses during hypoxia in Arabidopsis. Plant Physiol 156:202–212

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang R, Deng C, Ouyang B, Ye Z (2011b) Molecular analysis of two salt-responsive NAC-family genes and their expression analysis in tomato. Mol Biol Rep 38:857–863

    Article  CAS  PubMed  Google Scholar 

  • Yang Z-B, Eticha D, Rotter B, Rao IM, Horst WJ (2011c) Physiological and molecular analysis of polyethylene glycol-induced reduction of aluminium accumulation in the root tips of common bean (Phaseolus vulgaris). New Phytol 192:99–113

    Article  CAS  PubMed  Google Scholar 

  • Yao Y, Xu G, Mou D, Wang J, Ma J (2012) Subcellular Mn compartation, anatomic and biochemical changes of two grape varieties in response to excess manganese. Chemosphere 89:150–157

    Article  CAS  PubMed  Google Scholar 

  • Yaycili O, Alİkamanoğlu S (2012) Induction of salt-tolerant potato (Solanum tuberosum L) mutants with gamma irradiation and characterization of genetic variations via RAPD-PCR analysis. Turk J Biol 36:405–412

    CAS  Google Scholar 

  • Yoshida T, Mogami J, Yamaguchi-Shinozaki K (2014) ABA-dependent and ABA-independent signaling in response to osmotic stress in plants. Curr Opin Plant Biol 21C:133–139

    Article  CAS  Google Scholar 

  • Yuan S, Lin HH (2008) Role of salicylic acid in plant abiotic stress. Z Naturforsch C 63:313–320

    CAS  PubMed  Google Scholar 

  • Zhang G, Chen M, Li L, Xu Z, Chen X, Guo J, Ma Y (2009) Overexpression of the soybean GmERF3 gene, an AP2/ERF type transcription factor for increased tolerances to salt, drought, and diseases in transgenic tobacco. J Exp Bot 60:3781–3796

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This publication is supported by Ministerio de Economía (Spain) and Universitat Jaume I through grants AGL2013-42038-R and P1 1B2013-23, respectively. V.V. and S.I.Z. were recipient of pre-doctoral fellowships from Universitat Jaume I. M.M. was recipient of Santiago Grisolia fellowship from Generalitat Valenciana (Spain).

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Correspondence to Vicent Arbona .

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Arbona, V., Manzi, M., Zandalinas, S.I., Vives-Peris, V., Pérez-Clemente, R.M., Gómez-Cadenas, A. (2017). Physiological, Metabolic, and Molecular Responses of Plants to Abiotic Stress. In: Sarwat, M., Ahmad, A., Abdin, M., Ibrahim, M. (eds) Stress Signaling in Plants: Genomics and Proteomics Perspective, Volume 2. Springer, Cham. https://doi.org/10.1007/978-3-319-42183-4_1

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