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Signal transduction and biotechnology in response to environmental stresses

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  • Published:
Biologia Plantarum

Abstract

Providing sufficient food to burgeoning population from the steadily shrinking arable land seems to be very difficult in near future and is one of the foremost challenges for plant scientists. In addition, there are several biotic and abiotic stresses which frequently encounter crop plants during various stages of life cycle, resulting in considerable yield losses. Environmental stresses, including drought, flooding, salinity, temperature (both low and high), high radiation, and xenobiotics induce toxicity, membrane damage, excessive reactive oxygen species (ROS) production, reduced photosynthesis, and altered nutrient acquisition. Several indigenous defence mechanisms (physiological and molecular) are triggered in plants on exposure to environmental cues. Enhancement of resistance of crop plants to environmental stresses has been the topic of prime interest for agriculturalists and plant scientists since long. Development of water and salinity stress-tolerant crops through genetic engineering provides an avenue towards the reclamation of farmlands that have been lost due to salinity and lack of irrigation water/rainfall. Understanding the complexity of stress tolerance mechanisms in orthodox or model plants at the genetic and molecular levels improves feasibility of enhancing tolerance of sensitive crop plants.

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Abbreviations

ABA:

abscisic acid

AOX:

alternative oxidase

CDK:

cyclin dependent kinase

CDPK:

calcium-dependent protein kinase

DRE/CRT:

dehydration-responsive element/C-repeat

DREB:

DRE binding

EST:

expressed sequence tags

GM:

genetically modified

LEA:

late embryogenesis abundant

MAPK:

mitogen activated protein kinase

MYB:

myeloblastosis

NAC:

NAM-ATAF1, 2-CUC2 family

ROS:

reactive oxygen species

SOS:

salt overly sensitive

References

  • Agarwal, M., Hao, Y., Kapoor, A., Dong, C.H., Fujii, H., Zheng, X., Zhu, J.K.: A R2R3 type of MYB transcription factor is involved in the cold regulation of cbf genes and in acquired freezing tolerance. — J. biol. Chem. 281: 37636–37676, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Agarwal, P.K., Jha, B.: Transcription factors in plants and ABA dependent and independent abiotic stress signaling. — Biol. Plant. 54: 201–212, 2010.

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Ahmad, P., Ashraf, M., Younis, M., Hu, X., Kumar, A., Akram, N.A., Al-Qurainy, F.: Role of transgenic plants in agriculture and biopharming. — Biotechnol. Adv. 30: 524–540, 2012a.

    Article  CAS  PubMed  Google Scholar 

  • Ahmad, P., Bhardwaj, R., Tuteja, T.: Plant signaling under abiotic stress environment. - In: Ahmad, P., Prasad, M.N.V. (ed.): Environmental adaptations and Stress Tolerance of Plants in the Era of Climate Change. Pp. 297–323. Springer Science + Business Media, New York 2012b.

    Chapter  Google Scholar 

  • Ahmad, P., Jaleel, C.A., Sharma, S.: Antioxidant defense system, lipid peroxidation, proline metabolizing enzymes, and biochemical activities in two Morus alba genotypes subjected to NaCl stress. — Russian J. Plant Physiol. 57: 509–517, 2010.

    Article  CAS  Google Scholar 

  • Al-Doss, A.A., Smith, S.E.: Registration of AZ-97MEC and AZ-97MEC-ST very non-dormant alfalfa germplasm pools with increased shoot weight and differential response to saline irrigation. — Crop Sci. 38: 568–568, 1998.

    Article  Google Scholar 

  • Alzwiy, I.A., Morris, P.C.: A mutation in the Arabidopsis MAP kinase kinase 9 gene results in enhanced seedling stress tolerance. — Plant Sci. 173: 302–308, 2007.

    Article  CAS  Google Scholar 

  • Andeani, J.K., Mohsenzadeh, S., Mohabatkar, H.: Isolation and characterization of partial DREB gene from four Iranian Triticum aestivum cultivars. — World J. agr. Sci. 5: 561–566, 2009.

    CAS  Google Scholar 

  • Antonsson, B., Kassel, D.B., Di Paolo, G., Lutjens, R., Riederer, B.M., Grenningloh, G.: Signaling through MAP kinase networks in plants. — Arch. Biochem. Biophys. 452: 55–68, 2006.

    Article  CAS  Google Scholar 

  • Apse, M.P., Blumwald, E.: Engineering salt tolerance in plants. — Curr. Opin. Biotechnol. 13: 146–150, 2002.

    Article  CAS  PubMed  Google Scholar 

  • Ashraf, M., Akram, N.A.: Improving salinity tolerance of plants through conventional breeding and genetic engineering: an analytical comparison. — Biotechnol. Adv. 27: 744–752, 2009.

    Article  CAS  PubMed  Google Scholar 

  • Ashraf, M., O'Leary, O.J.: Effect of drought stress on growth, water relations and gas exchange of two lines of sunflower differing in degree of salt tolerance. — Int. J. Plant Sci. 157: 729–732, 1996.

    Article  Google Scholar 

  • Atkinson, N.J, Urwin, P.E.: The interaction of plant biotic and abiotic stresses; from gene to the field. — J. exp. Bot. 63: 695–709, 2012.

    Article  CAS  Google Scholar 

  • Batley, J., Edwards, D.: Genome sequence data: management, storage, and visualization. — Biotechniques 46: 333–336, 2009.

    Article  CAS  PubMed  Google Scholar 

  • Baxter, A., Mittler, R., Suzuki, N.: ROS as key players in plant stress signalling. — J. exp. Bot. 65: 1229–1240, 2014.

    Article  CAS  PubMed  Google Scholar 

  • Belhaj, K., Chaparro-Garcia, A., Kamoun, S., Patron, N.J., Nekrasov, V.: Editing plant genomes with CRISPR/Cas9. — Curr. Opin. Biotechnol. 32: 76–84, 2015.

    Article  CAS  PubMed  Google Scholar 

  • Beligni, M.V., Fath, A., Bethke, P.C., Lamattina, L., Jones, R.L.: Nitric oxide acts as an antioxidant and delays programmed cell death in barley aleurone layers. — Plant Physiol. 129: 1642–1645, 2002.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beligni, M.V., Lamattina, L.: Is nitric oxide toxic or protective? — Trends Plant Sci. 4: 299–300, 1999.

    Article  CAS  PubMed  Google Scholar 

  • Beligni, M.V., Lamattina, L.: Nitric oxide stimulates seed germination and de-etiolation and inhibits hypocotyl elongation, three light-inducible responses in plants. — Planta 210: 215–221, 2000.

    Article  CAS  PubMed  Google Scholar 

  • Bhat, S.R., Srinivasan, S.: Molecular and genetic analyses of transgenic plants: considerations and approaches. — Plant Sci. 163: 573–581, 2002.

    Article  Google Scholar 

  • Breusegem, F.V., Vranova, E., Dat, J.F, Inze, D.: The role of active oxygen species in plant signal transduction. — Plant Sci. 161: 405–414, 2001.

    Article  Google Scholar 

  • Bogdan, C.: Nitric oxide and the regulation of gene expression. — Trends cell. Biol. 11: 66–75, 2001.

    Article  CAS  PubMed  Google Scholar 

  • Buchanan, C.D., Lim, S., Salzman, R.A., Kagiampakis, I., Morishiqe, D.T., Weers, B.D., Klein, R.R., Pratt, L.H., Cordonnier-Pratt, M.M., Klein, P.E., Mullet, J.E.: Sorghum bicolor's transcriptome response to dehydration, high salinity and ABA. — Plant mol. Biol. 58: 699–720, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Burssens, S., Himanen, K., Van de Cotte, B., Beeckman, T., Van, M.M., Inze, D., Verbruggen, N.: Expression of cell cycle regulatory genes and morphological alterations in response to salt stress in Arabidopsis thaliana. — Planta 211: 632–640, 2000.

    Article  CAS  PubMed  Google Scholar 

  • Capiati, D.A., Pais, S.M., Tellez-Inon, M.T.: Wounding increases salt tolerance in tomato plants: Evidence on the participation of calmodulin-like activities in cross tolerance signalling. — J. exp. Bot. 57: 2391–2400, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Cardi, T.: Cisgenesis and genome editing: combining concepts and efforts for a smarter use of genetic resources in crop breeding. — Plant Breed. 135: 139–147, 2016.

    Article  CAS  Google Scholar 

  • Chen, N., Yang, Q., Pan, L., Chi, X., Chen, M., Hu, D., Yang, Z., Wang, T., Wang, M., Yu, S.: Identification of 30 MYB transcription factor genes and analysis of their expression during abiotic stress in peanut (Arachis hypogaea L.). — Gene 533: 332–345, 2014.

    Article  CAS  PubMed  Google Scholar 

  • Chen, W., Provart, N.J., Glazebrook, J., Katagiri, F., Chang, H.S., Eulgem, T., Mauch, F., Laun, S., Zou, G., Whitham, S.A., Budworth, P.R., Tao, Y., Xie, Z., Chen, X., Lam, S., Kreps, J.A., Harper, J.F., Si-Ammour, A., Mauch-Mani, B., Heinlein, M., Kobayashi, K., Hohn, T., Dangl, J.L., Wang, X., Zhu, T.: Expression profile matrix of Arabidopsis transcription factor genes suggests their putative functions in response to environmental stresses. — Plant Cell 14: 559–574, 2002.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheong, Y.H., Sung, S.J., Kim, B.G., Pandey, G.K., Cho, J.S., Kim, K.N., Luan, S.: Constitutive overexpression of the calcium sensor CBL5 confers osmotic or drought stress tolerance in Arabidopsis. — Mol. Cells 29: 159–165, 2010.

    Article  CAS  PubMed  Google Scholar 

  • Chinnusamy, V., Ohta, M., Kanrar, S., Lee, B., Hong, X., Agarwal, M., Zhu, J.K.: ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. — Genes Dev. 17: 1043–1054, 2003.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Choudhary, S.P., Yu, J.Q., Yamaguchi-Shinozaki, K., Shinozaki, K., Tran, L.S.: Benefits of brassinosteroid crosstalk. — Trends Plant Sci. 17: 594–605, 2012.

    Article  CAS  PubMed  Google Scholar 

  • Colcombet, J., Hirt, H.: Arabidopsis MAPKs: a complex signalling network involved in multiple biological processes. — Biochem. J. 413: 217–226, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Corpas, F., Hayashi, M., Mano, S., Nishimura, M., Barroso, J.B.: Peroxisomes are required for in vivo nitric oxide accumulation in the cytosol following salinity stress of Arabidopsis plants. — Plant Physiol. 151: 2083–2094, 2009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Corpas, F.J., Barroso, J.B.: Nitro-oxidative stress vs oxidative or nitrosative stress in higher plants. — New Phytol. 199: 633–635, 2013.

    Article  CAS  PubMed  Google Scholar 

  • Corpas, F.J., Barroso, J.B., Carreras, A., Valderrama, R., Palma, J.M., Leon, A.M., Sandalio, L.M., Del Rio, L.A.: Constitutive arginine dependent nitric oxide synthase activity in different organs of pea seedlings during plant development. — Planta 224: 246–254, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Cui, K., Xing, G., Liu, X., Xing, G., Wang, Y.: Effect of hydrogen peroxide on somatic embryogenesis of Lycium barbarum L. — Plant Sci. 146: 9–16, 1999.

    Article  CAS  Google Scholar 

  • Cui, M.H., Yoo, K.S., Hyoung, S., Nguyen, H.T.K., Kim, Y.Y., Kim, H.J., Ok, S.H., Yoo, S.D., Shin, J.S.: An Arabidopsis R2R3-MYB transcription factor, AtMYB20, negatively regulates type 2C serine/threonine protein phosphatases to enhance salt tolerance. — FEBS Lett. 587: 1773–1778, 2013.

    Article  CAS  PubMed  Google Scholar 

  • Cushman, J.C., Bohnert, H.J.: Genomic approaches to plant stress tolerance. — Curr. Opin. Plant Biol. 3: 117–122, 2000.

    Article  CAS  PubMed  Google Scholar 

  • Danquah, A., De Zelicourt, A., Colcombet, J., Hirt, H.: The role of ABA and MAPK signaling pathways in plant abiotic stress responses. — Biotechnol. Adv. 32: 40–52, 2014.

    Article  CAS  PubMed  Google Scholar 

  • Das, R., Pandey, G.K.: Expressional analysis and role of calcium regulated kinases in abiotic stress signaling. — Curr. Genom. 11: 2–13, 2010.

    Article  CAS  Google Scholar 

  • Delledonne, M., Xia, Y., Dixon, R.A., Lamb, C.: Nitric oxide functions as a signal in plant disease resistance. — Nature 394: 585–588 1998.

    Article  CAS  PubMed  Google Scholar 

  • Ding, Z., Li, S., An, X., Liu, X., Qin, H., Wang, D.: Transgenic expression of MYB15 confers enhanced sensitivity to abscisic acid and improved drought tolerance in Arabidopsis thaliana. — J. Genet. Genomics 36: 17–29, 2009.

    Article  CAS  PubMed  Google Scholar 

  • Du, H., Yang, S.S., Liang, Z., Feng, B.R., Liu, L., Huang, Y.B., Tang, Y.X.: Genome-wide analysis of the MYB transcription factor superfamily in soybean. — BMC Plant Biol. 12: 106, 2012.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dubos, C., Stracke, R., Grotewol, E., Weisshaar, B., Martin, C., Lepiniec, L.: MYB transcription factors in Arabidopsis. — Trends Plant Sci. 15: 573–581, 2010.

    Article  CAS  PubMed  Google Scholar 

  • Durner, J., Wendehenne, D., Klessig, D.F.: Defense gene induction in tobacco by nitric oxide, cyclic GMP and cyclic ADP-ribose. — Proc. nat. Acad. Sci. USA 95: 10328–10333, 1998.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Edel, K.H., Kudla, J. Increasing complexity and versatility: How the calcium signaling toolkit was shaped during plant land colonization. - Cell Calcium 57: 231–246, 2014.

    Article  PubMed  CAS  Google Scholar 

  • Edwards, D., Batley, J., Snowdon, R.J.: Accessing complex crop genomes with next-generation sequencing. — Theor. appl. Genet. 126: 1–11, 2013.

    Article  CAS  PubMed  Google Scholar 

  • Fan, W., Zhang, M., Zhang, H., Zhang, P.: Improved tolerance to various abiotic stresses in transgenic sweet potato (Ipomoea batatas) expressing spinach betaine aldehyde dehydrogenase. — Plos ONE 7: e37344, 2012.

    Article  CAS  Google Scholar 

  • Feller, A., Machemer, K., Braun, E.L, Grotewold, E.: Evolutionary and comparative analysis of MYB and bHLH plant transcription factors. — Plant J. 66: 94–116, 2011.

    Article  CAS  PubMed  Google Scholar 

  • Feng, J., Wang, C., Chen, Q., Chen, H., Ren, B., Li, X., Zuo, J.: S-nitrosylation of phosphotransfer proteins represses cytokinin signaling. — Nat. Commun. 4: 1529, 2013.

    Article  PubMed  CAS  Google Scholar 

  • Fichtner, F., Urrea Castellanos, R., Ulker, B.: Precision genetic modifications: a new era in molecular biology and crop improvement. — Planta 239: 921–939, 2014.

    Article  CAS  PubMed  Google Scholar 

  • Floris, M., Hany, M., Elodie, L., Christophe, R., Benoit, M.: Post-transcriptional regulation of gene expression in plants during abiotic stress. — Int. J. mol. Sci. 10: 3168–3185, 2009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fowler, S., Thomashow, M.F.: 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, 2002.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Foyer, C.H, Noctor, G.: Redox signaling in plants. — Antioxidants Redox Signal 18: 2087–2090, 2013.

    Article  CAS  Google Scholar 

  • Franz, S., Ehlert, B., Liese, A., Kurth, J., Cazalé, A., Romeis, T.: Calcium-dependent protein kinase CPK21 functions in abiotic stress response in Arabidopsis thaliana. — Mol. Plant 4: 83–96, 2011.

    Article  CAS  PubMed  Google Scholar 

  • Fu, Z.Q, Dong, X.: Systemic acquired resistance: turning local infection into global defense. — Annu. Rev. Plant Biol. 64: 839–863, 2013.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Gadjev, I., Vanderauwera, S., Gechev, T.S., Laloi, C., Minkov, I.N., Shulaev, V., Apel, K., Inze, D., Mittler, R., Van, B.F.: Transcriptomic footprints disclose specificity of reactive oxygen species signaling in Arabidopsis. — Plant Physiol. 141: 436–445, 2006.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao, Q., Ren, Q., Liou, L.C., Bao, X., Zhang, Z.: Mitochondrial DNA protects against salt stress-induced cytochrome cmediated apoptosis in yeast. — FEBS Lett. 585: 2507–2512, 2011.

    Article  CAS  PubMed  Google Scholar 

  • Gas, E., Flores-Perez, U., Sauret-Gueto, S., Rodriguez-Concepcion, M.: Hunting for plant nitric oxide synthase provides new evidence of a central role for plastids in nitric oxide metabolism. — Plant Cell 21: 18–23, 2009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Giri, J.: Glycine betaine and abiotic stress tolerance in plants. — Plant Signal Behav. 4: 1746–1751, 2011.

    Article  CAS  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Granier, C., Inze, D., Tardieu, F.: Spatial distribution of cell division rate can be deduced from that of p34cdc2 kinase activity in maize leaves grown at contrasting temperatures and soil water conditions. — Plant Physiol. 124: 1393–1402, 2000.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grover, A., Sahi, C., Sanan, N., Grover, A.: Taming abiotic stresses in plants through genetic engineering: current strategies and perspective. — Plant Sci. 143: 101–111, 1999.

    Article  CAS  Google Scholar 

  • Grun, S., Lindermayr, C., Sell, S., Durner, J.: Nitric oxide and gene regulation in plants. — J. exp. Bot. 57: 507–516, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Gupta, K.J., Igamberdiev, A.U.: The anoxic plant mitochondrion as a nitrite: NO reductase. — Mitochondrion 11: 537–543. 2011.

    Article  CAS  PubMed  Google Scholar 

  • Gupta, K.J., Shah, J.K., Brotman, Y., Jahnke, Y., Willmitzer, L., Kaiser, W.M., Bauwe, H., Igamberdiev, A.U.: Inhibition of aconitase by nitric oxide leads to induction of the alternative oxidase and to a shift of metabolism towards biosynthesis of amino acids. — J. exp. Bot. 63: 1773–1784, 2012.

    Article  CAS  PubMed  Google Scholar 

  • Ha, S., Vankova, R., Yamaguchi-Shinozaki, K., Shinozaki, K., Tran, L.S.: Cytokinins: metabolism and function in plant adaptation to environmental stresses. — Trends Plant Sci. 17: 172–179, 2012.

    Article  CAS  PubMed  Google Scholar 

  • Habib, N., Ashraf, M.: Effect of exogenously applied nitric oxide on water relations and ionic composition of rice (Oryza sativa L.) plants under salt stress. — Pak. J. Bot. 46: 111–116, 2014.

    Google Scholar 

  • Hamilton, J.P., Buell, C.R.: Advances in plant genome sequencing. — Plant J. 70: 177–190, 2012.

    Article  CAS  PubMed  Google Scholar 

  • Hancock, J.T., Neill, S.J., Wilson, I.D.: Nitric oxide and ABA in the control of plant function. — Plant Sci. 181: 555–559, 2012.

    Article  CAS  Google Scholar 

  • Hasanuzzaman, M., Nahar, K., Alam, M.M., Roychowdhury, F., Fujita, M.: Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. — Int. J. mol. Sci. 14: 9643–9684, 2013.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hasegawa, P.M., Bressan, R.A., Zhu, J.K., Bohnert, H.J.: Plant cellular and molecular responses to high salinity. — Ann. Rev. Plant Physiol. Plant mol. Biol. 51: 463–499, 2000.

    Article  CAS  Google Scholar 

  • He, Y., Tang, R.H., Hao, Y., Stevens, R.D., Cook, C.W., Ahn, S.M., Jing, L., Yang, Z., Chen, L., Guo, F., Fiorani, F., Jackson, R.B., Crawford, N.M., Pei, Z.M.: Nitric oxide represses the Arabidopsis floral transition. — Science 305: 1968–1971, 2004.

    Article  CAS  PubMed  Google Scholar 

  • Hollington, P.A.: Technological breakthroughs in screening/breeding wheat varieties for salt tolerance. - In: Gupta, S.K., Sharma, S.K., Tyagi, N.K. (Ed.): Proceedings of the National Conference “Salinity Management in Agriculture”. Pp. 273–289, Central Soil Salinity Research Institute, Karnal 2000.

    Google Scholar 

  • Hong, Y., Zhang, H., Huang, L., Li, D., Song, F.: Overexpression of a stress-responsive NAC transcription factor gene ONAC022 improves drought and salt tolerance in rice. - Front. Plant Sci. in press, 2016.

    Google Scholar 

  • Hsieh, T.H., Lee, J.T., Yang, P.T., Chiu, L.H., Charng, Y., Wang, Y.C., Chan, M.T.: Heterology expression of the Arabidopsis C repeat/dehydration response element binding factor 1 gene confers elevated tolerance to chilling and oxidative stresses in transgenic tomato. — Plant Physiol. 129: 1086–1094, 2002.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Huang, W., Miao, M., Kud, J., Niu, X., Ouyang, B., Zhang, J., Ye, Z., Kuhl, J.C., Liu, Y., Xiao, F.: SlNAC1, a stressrelated transcription factor, is fine-tuned on both the transcriptional and the post-translational level. — New Phytol. 197: 1214–1224, 2013.

    Article  CAS  PubMed  Google Scholar 

  • Huda, K.M.K., Banu, M.S.A., Tuteja, R., Tuteja, N.: Global calcium transducer P-type Ca2+-ATPases open new avenues for agriculture by regulating stress signalling. — J. exp. Bot. 64: 3099–3109, 2013.

    Article  CAS  PubMed  Google Scholar 

  • Ichimura, K., Mizoguchi, T., Yoshida, R., Yuasa, T., Shinozaki, K.: Various abiotic stresses rapidly activate Arabidopsis MAP kinases ATMPK4 and ATMPK6. — Plant J. 24: 655–665, 2000.

    Article  CAS  PubMed  Google Scholar 

  • Ichimura, K.: Mitogen-activated protein k inase cascades in plants, a new nomenclature. — Trends Plant Sci. 7: 301–308, 2002.

    Article  CAS  Google Scholar 

  • Igamberdiev, A.U., Hill, R.D.: Nitrate, NO and haemoglobin in plant adaptation to hypoxia: an alternative to classic fermentation pathways. — J. exp. Bot. 55: 2473–2482, 2004.

    Article  CAS  PubMed  Google Scholar 

  • Ito, Y., Katsura, K., Maruyama, K., Taji, T., Kobayashi, M., Seki, M., Shinozaki, K., Yamaguchi-Shinozaki, K.: Functional analysis of rice REB1/CBF-type transcription factors involved in cold-responsive gene expression in transgenic rice. — Plant Cell Physiol. 47: 141–153, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Jasid, S., Simontacchi, M., Bartoli, C.G., Puntarulo, S.: Chloroplasts as a nitric oxide cellular source. Effect of reactive nitrogen species on chloroplastic lipids and proteins. — Plant Physiol. 142: 1246–1255, 2006.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jeong, M.J., Lee, S.K., Kim, B.G., Kwon, T.R., Cho, W.S., Park, Y.T., Lee, J.O., Kwon, H.B., Byun, M.O., Park, S.C.: A rice (Oryza sativa L.) MAP kinase gene, OsMAPK44, is involved in response to abiotic stresses. — Plant Cell Tissue Organ Cult. 85: 151–160, 2006.

    Article  CAS  Google Scholar 

  • Jewell, M.C., Campbell, B.C., Godwin, I.D.: Transgenic plants for abiotic stress resistance. - In: Kole, C., Michler, C.H., Abbott, A.G., Hall, T.C. (ed.): Transgenic Crop Plants. Pp. 67–132. Springer, Heidelberg 2010.

    Chapter  Google Scholar 

  • Jiang, S., Zhang, D., Wang, L., Pan, J., Liu, Y., Kong, X., Zhou, Y., Li, D.: A maize calcium-dependent protein kinase gene, ZmCPK4, positively regulated abscisic acid signaling and enhanced drought stress tolerance in transgenic Arabidopsis. — Plant Physiol. Biochem. 71: 112–120, 2013.

    Article  CAS  PubMed  Google Scholar 

  • Jiang, X., Zhang, C., Lu, P., Jiang, G., Liu, X., Dai, F., Gao, J.: RhNAC3, a stress-associated NAC transcription factor, has a role in dehydration tolerance through regulating osmotic stress-related genes in rose petals. — Plant Biotechnol. J. 12: 38–48, 2014.

    Article  CAS  PubMed  Google Scholar 

  • Jin, H., Martin, C.: Multifunctionality and diversity within the plant MYB-gene family. — Plant mol. Biol. 41: 577–585, 1999.

    Article  CAS  PubMed  Google Scholar 

  • Jogaiah, S., Govind, S.R., Tran, L.S.: Systems biology-based approaches toward understanding drought tolerance in food crops. — Crit. Rev. Biotechnol. 33: 23–39, 2013.

    Article  PubMed  Google Scholar 

  • John, R., Anjum, N.A., Sopory, S.K., Akram, N.A., Ashraf, M.: Some key physiological and molecular processes for cold acclimation: an overview. — Biol. Plant. 60: 603–618, 2016.

    Article  CAS  Google Scholar 

  • Johnson, J.W., Box, J.E., Manandhar, J.B., Ramseur, E.L., Cunfer, B.M.: Breeding for Rooting Potential under Stress Conditions. - Colloques de l'INRA, France 1991.

    Google Scholar 

  • Johnson, N.: Genetic engineering vs. Natural breeding: What’s the difference? http://grist.org/food/genetic-engineering-vsnatural-breeding-whats-the-difference/, 2013.

    Google Scholar 

  • Jung, C., Seo, J.S., Han, S.W., Koo, Y.J., Kim, C.H., Song, S.I.K., Nahm, B.H., Do Choi, Y., Cheong, J.J.: Overexpression of AtMYB44 enhances stomatal closure to confer abiotic stress tolerance in transgenic Arabidopsis. — Plant Physiol. 146: 623–635, 2008.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Katiyar, A., Smita, S., Lenka, S.K., Rajwanshi, R., Chinnusamy, V., Bansal, K.C.: Genome-wide classification and expression analysis of MYB transcription factor families in rice and Arabidopsis. — BMC Genomics 13: 544, 2012.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaur, N., Gupta, A.K.: Signal transduction pathways under abiotic stresses in plants. — Curr. Sci. 88: 1771–1780, 2005.

    CAS  Google Scholar 

  • Keita, K., Takeru, O., Yuichi, U.: Functional characterization and expression profiling of a DREB2-type gene from lettuce (Lactuca sativa L.). — Plant Cell Tissue Organ Cult. 116: 97–109, 2014.

    Article  CAS  Google Scholar 

  • Kim, J.H., Nguyen, N.H., Jeong, C.Y., Nguyen, N.T., Hong, S.W., Lee, H.: Loss of the R2R3 MYB, AtMyb73, causes hyper-induction of the SOS1 and SOS3 genes in response to high salinity in Arabidopsis. — J. Plant Physiol. 170: 1461–1465, 2013.

    Article  CAS  PubMed  Google Scholar 

  • Kline, K.G., Sussman, M.R, Jones, A.M.: Abscisic acid receptors. — Plant Physiol. 154: 479–482 2010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Knight, H., Brandt, S., Knight M.R.: A history of stress alters drought calcium signalling pathways in Arabidopsis. — Plant J. 16: 681–687, 1998.

    Article  CAS  PubMed  Google Scholar 

  • Knight, H., Veale, E.L., Warren, G.J., Knight, M.R.: The sfr6 mutation in Arabidopsis suppresses low temperature induction of genes dependent on the CRT/DRE sequence motif. — Plant Cell 11: 875–1886, 1999.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Knight, M.R., Campbell, A.K., Smith, S.M., Trewavas, A.J.: Transgenic aequorin reports the effects of touch and cold shock and elicitors on cytosolic calcium. — Nature 352: 524–526, 1991.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Kosova, K., Vitamvas, P., Prasil, I.T., Renaut, J.: Plant proteome changes under abiotic stress-contribution of proteomics studies to understanding plant stress response. — J. Proteomics 7: 1301–1322, 2011.

    Article  CAS  Google Scholar 

  • Kovtun, Y., Chiu, W.L, Tena, G., Sheen, J.: Functional analysis of oxidative stress activated mitogen-activated protein kinase cascade in plants. — Proc. nat. Acad. Sci. USA 97: 2940–2945, 2000.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ku, H.M., Vision, T., Liu, J., Tanksley, S.D.: Comparing sequenced segments of the tomato and Arabidopsis genomes: large-scale duplication followed by selective gene loss creates a network of synteny. — Proc. nat. Acad. Sci. USA 97: 9121–9126, 2000.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kyriakis, J.M., Avruch, J.: Sounding the alarm: protein kinase cascades activated by stress and inflammation. — J. biol. Chem. 271: 24313–24316, 1996.

    Article  CAS  PubMed  Google Scholar 

  • Latini, A., Rasi, C., Sperandei, M., Cantale, C., Iannetta, M., Dettori, M., Amar, K., Galeffi, P.: Identification of a DREB-related gene in Triticum durum and its expression under water stress conditions. — Ann. appl. Biol. 150: 187–195, 2007.

    Article  CAS  Google Scholar 

  • Leshem, Y.Y., Haramaty, E.: The characterization and contrasting effects of the nitric oxide free radical in vegetative stress and senescence of Pisum sativum Linn. foliage. — J. Plant Physiol. 148: 258–263, 1996.

    Article  CAS  Google Scholar 

  • Li, X., Zhang, D., Li, H., Wang, Y., Zhang, Y., Wood, A.J.: EsDREB2B, a novel truncated DREB2-type transcription factor in the desert legume Eremosparton songoricum, enhances tolerance to multiple abiotic stresses in yeast and transgenic tobacco. — BMC Plant Biol. 14: 44, 2014.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lindermayr, C., Sell, S., Muller, B., Leister, D., Durner, J.: Redox regulation of the NPR1-TGA1 system of Arabidopsis thaliana by nitric oxide. — Plant Cell 22: 2894–2907, 2010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lippold, F., Sanchez, D.H., Musialak, M., Schlereth, A., Scheible, W.R., Hincha, D.K., Udvardi, M.K.: AtMyb41 regulates transcriptional and metabolic responses to osmotic stress in Arabidopsis. — Plant Physiol. 149: 1761–1772, 2009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu, J., Zhu, K.: A calcium sensor homolog required for plant salt tolerance. — Science 280: 1943–1945, 1998.

    Article  CAS  PubMed  Google Scholar 

  • Liu, Q., Kasuga, M., Sakuma, Y., Abe, H., Miura, S., Yamaguchi-Shinozaki, K., Shinozaki, K.: 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, 1998.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu, W.Z., Kong, D.D., Gu, X.X., Gao, H.B., Wang, J.Z., Xia, M., Gao, Q., Tian, L.L., Xu, Z.H., Bao, F., Hu, Y., Ye, N.S., Pei, Z.M., He, Y.K.: Cytokinins can act as suppressors of nitric oxide in Arabidopsis. — Proc. nat. Acad. Sci. USA. 110: 1548–1553, 2013.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lucca, P., Hurrell, R., Potrykus, I.: Genetic engineering approaches to improve the bioavailability and the level of iron in rice grains. — Theor. appl. Genet. 102: 392–397, 2001.

    Article  CAS  Google Scholar 

  • Ma, N.N., Zuo, Y.Q., Liang, X.Q., Yin, B., Wang, G.D., Meng, Q.W.: The multiple stress-responsive transcription factor SlNAC1 improves the chilling tolerance of tomato. — Physiol. Plant. 149: 474–486, 2013.

    Article  CAS  PubMed  Google Scholar 

  • Ma, Q., Dai, X., Xu, Y., Guo, J., Liu, Y., Chen, N. et al.: Enhanced tolerance to chilling stress in OsMYB3R-2 transgenic rice is mediated by alteration in cell cycle and ectopic expression of stress genes. — Plant Physiol. 150: 244–256, 2009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma, N., Feng, H., Meng, X., Li, D., Yang, D., Wu, C., Meng, Q.: Overexpression of tomato SlNAC1 transcription factor alters fruit pigmentation and softening. — BMC Plant Biol. 14: 351, 2014.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mandal, M.K., Chandra-Shekara, A.C., Jeong, R.D., Yu, K., Zhu, S., Chanda, B., Navarre, D., Kachroo, A., Kachroo, P.: Oleic acid-dependent modulation of nitric oxide associated protein levels regulates nitric oxide-mediated defense signaling in Arabidopsis. — Plant Cell 24: 1654–1674, 2012.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Manzoor, H., Chiltz, A., Madani, S., Vatsa, P., Schoefs, B., Pugin, A., Garcia-Brugger, A.: Calcium signatures and signaling in cytosol and organelles of tobacco cells induced by plant defense elicitors. — Cell Calcium 51: 434–444, 2012.

    Article  CAS  PubMed  Google Scholar 

  • Martinez-Ballesta, M.C., Carvajal, M.: New challenges in plant aquaporin biotechnology. — Plant Sci. 217: 71–77, 2014.

    Article  CAS  Google Scholar 

  • May, M.J, Vernoux, T., Leaver, C., Van Montagu, M., Inze, D.: Glutathione homeostasis in plants: implications for environmental sensing and plant development. — J. exp. Bot. 49: 649–667, 1998.

    CAS  Google Scholar 

  • Michael, T.P., Jackson, S.: The first 50 plant genomes. — Plant Genome 6: 10.3835, 2013.

  • Mikolajczyk, M., Awotunde, O.S., Muszynska, G., Klessig, D.F., Dobrowolska, G.: Osmotic stress induces rapid activation of a salicylic acid induced protein kinase and homolog of protein kinase ASK1 in tobacco cells. — Plant Cell 12: 165–178, 2000.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mittler, R., Vanderauwera, S., Gollery, G, Breusegem, F.V.: Reactive oxygen gene network of plants. — Trends Plant Sci. 9: 490–498. 2004.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Mizoi, J., Shinozaki, K., Yamaguchi-Shinozaki, K.: AP2/ERF family transcription factors in plant abiotic stress responses. — Biochim. biophys. Acta. 1819: 86–96, 2012.

    Article  CAS  PubMed  Google Scholar 

  • Mochida, K., Shinozaki, K.: Advances in omics and bioinformatics tools for systems analyses of plant functions. — Plant Cell Physiol. 52: 2017–2038, 2011.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moller, I.M., Sweetlove, L.J.: ROS signalling - specificity is required. — Trends Plant Sci. 15: 370–374, 2010.

    Article  CAS  PubMed  Google Scholar 

  • Mukhtar, M.S., Nishimura, M.T., Dangl, J.: NPR1 in plant defense: it’s not over’ til it’s turned over. — Cell 137: 804–806, 2009.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Nakashima, K., Tran, L.S.P., Nguyen, D.V., Fujita, M., Maruyama, K., Todaka, D., Todaka, D., Ito, Y., Hayashi, N., Shinozaki, K., Yamaguchi-Shinozaki, K.: 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, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Nasreen, S.J., Amudha, J., Pandey, S.S.: Isolation and characterization of soybean DREB 3 transcriptional activator. — J. appl. Biol. Biotechnol. 1: 9–12, 2013.

    Google Scholar 

  • Nayak, S.N., Balaji, J., Upadhyaya, H.D., Hash, C.T., Kishor, P.B.K., Chattopadhyay, D., Rodriquez, L.M., Matthew W. Blair, M.W., Baum, M., McNally, K., This, D., Hoisington, D.A., Varshney, R.K.: Isolation and sequence analysis of DREB2A homologues in three cereal and two legume species. — Plant Sci. 177: 460–467, 2009.

    Article  CAS  Google Scholar 

  • Neill, S., Barros, R., Bright, J., Desikan, R., Hancock, J., Harrison, J., Morris, P., Ribeiro, P., Wilson, I.: Nitric oxide, stomatal closure, and abiotic stress. — J. exp. Bot. 59: 165–176, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Nomura, H., Shiina, T.: Calcium signaling in plant endosymbiotic organelles: mechanism and role in physiology. — Mol. Plant 7: 1094–1104, 2014.

    Article  CAS  PubMed  Google Scholar 

  • Nuruzzaman, M., Sharoni, A.M., Kikuchi, S.: Roles of NAC transcription factors in the regulation of biotic and abiotic stress responses in plants. — Front. Microbiol. 4: 1–16, 2013.

    Article  Google Scholar 

  • Olsen, A.N., Ernst, H.A., Leggio, L.L., Skriver, K.: NAC transcription factors, structurally distinct, functionally diverse. — Trends Plant Sci. 10: 79–87, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Osakabe, Y., Osakabe, K., Shinozaki, K., Tran, L.S.: Response of plants to water stress. — Front. Plant Sci. 5: 86, 2014a.

    Article  PubMed  PubMed Central  Google Scholar 

  • Osakabe, Y., Yamaguchi-Shinozaki, K., Shinozaki, K., Tran, L.S.: Sensing the environment: key roles of membranelocalized kinases in plant perception and response to abiotic stress. — J. exp. Bot. 64: 445–458, 2013.

    Article  CAS  PubMed  Google Scholar 

  • Osakabe, Y., Yamaguchi-Shinozaki, K., Shinozaki, K., Tran, L.S.: ABA control of plant macroelement membrane transport systems in response to water deficit and high salinity. — New Phytol. 202: 35–49, 2014b.

    Article  PubMed  Google Scholar 

  • Palmieri, M.C., Sell, S., Huang, X., Scherf, M., Werner, T., Durner, J., Lindermayr, C.: Nitric oxide-responsive genes and promoters in Arabidopsis thaliana: a bioinformatics approach. — J. exp. Bot. 59: 177–186, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Pandey, R., Muller, A., Napoli, C.A., Selinger, D.A., Pikaard, C.S., Richards, E.J., Bender, J., Mount, D.W., Jorgensen, R.A.: Analysis of histone acetyltransferase and histone deacetylase families of Arabidopsis thaliana suggests functional diversification of chromatin modification among multicellular eukaryotes. — Nucl. Acids Res. 30: 5036–5055, 2002.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pasquali, G., Biricolti, S., Locatelli, F., Baldoni, E., Mattana, M.: Osmyb4 expression improves adaptive responses to drought and cold stress in transgenic apples. — Plant Cell Rep. 27: 1677–1686, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Paulovich, A.G., Toczyski, D.P., Hartwell, L.H.: When checkpoints fail. — Cell 88: 315–321, 1997.

    Article  CAS  PubMed  Google Scholar 

  • Paz-Ares, J., Ghosal, D., Wienand, U., Peterson, P.A., Saedler, H.: The regulatory c1 locus of Zea mays encodes a protein with homology to myb proto-oncogene products and with structural similarities to transcriptional activators. — EMBO J. 6: 3553–3558, 1987.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Perez-Clemente, R.M., Vives, V., Zandalinas, S.I., Lopez-Climent, M.F., Munoz, V., Gomez-Cadenas, A.: Biotechnological approaches to study plant responses to stress. — Biomed. Res. Int. 10: 1155, 2013.

    Google Scholar 

  • Perez-Massot, E., Banakar, R., Gomez-Galera, S., Zorrilla-Lopez, U., Sanahuja, G., Arjo, G., Miralpeix, B., Vamvaka, E., Farre, G., Rivera, S.M., Dashevskaya, S., Berman, J., Sabalza, M., Yuan, D., Bai, C., Bassie, L., Twyman, R.M., Capell, T., Christou, P., Zhu, C.: The contribution of transgenic plants to better health through improved nutrition: opportunities and constraints. — Genes Nutr. 8: 29–34, 2013.

    Article  PubMed  Google Scholar 

  • Piterkova, J., Luhova, L., Hofman, J., Tureckova, V., Novak, O., Petrivalsky, M., Fellner, M.: Nitric oxide is involved in light-specific responses of tomato during germination under normal and osmotic stress conditions. — Ann. Bot. 110: 767–776, 2012.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Planchet, E., Gupta, K.J., Sonoda, M., Kaiser, W.M.: Nitric oxide emission from tobacco leaves and cell suspensions: rate limiting factors and evidence for the involvement of mitochondrial electron transport. — Plant J. 41: 732–743, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Popova, Y., Thayumanavan, P., Lonati, E., Agrochao, M., Thevelein, J.M.: Transport and signaling through the phosphate-binding site of the yeast Pho84 phosphate transceptor. — Proc. natl Acad. Sci. USA 107: 2890–2895, 2010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qiao, L.X., Ding, X., Wang, H.C., Sui, J.M., Wang, J.S.: Characterization of the β-1,3-glucanase gene in peanut (Arachis hypogaea L.) by cloning and genetic transformation. — Genet. mol. Res. 13: 1893–1904, 2014.

    Article  CAS  PubMed  Google Scholar 

  • Qin, F., Sakuma, Y., Li, J., Liu, Q., Li, Y.Q., Shinozaki, K., Yamagucgi-Shinozaki, K.: Cloning and functional analysis of a novel DREB1/CBF transcription factor involved in cold-responsive gene expression in Zea mays L. — Plant Cell Physiol. 45: 1042–1052, 2004.

    Article  CAS  PubMed  Google Scholar 

  • Qin, Y., Zhao, L., Skaggs, M.I., Andreuzza, S., Tsukamoto, T., Panoli, A., Wallace, K.N., Smith, S., Siddiqi, I., Yang, Z., Yadegari, R.: Actin-related protein 6 regulates female meiosis by modulating meiotic gene expression in Arabidopsis. — Plant Cell 26: 1612–1628, 2014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rahal, A., Kumar, A., Singh, V., Yadav, B., Tiwari, R., Chakraborty, S., Dhama, K.: Oxidative stress, prooxidants, and antioxidants: the interplay. — Biomed. Res. Int. 76: 19, 2014.

    Google Scholar 

  • Ramel, F., Birtic, S., Ginies, C., Soubigou-Taconnat, L., Triantaphylides, C., Havaux, M.: Carotenoid oxidation products are stress signals that mediate gene responses to singlet oxygen in plants. — Proc. nat. Acad. Sci. USA 109: 5535–5540, 2012.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ravikumar, G., Manimaran, P., Voleti, S.R., Subrahmanyam, D., Sundaram, R.M., Bansal, K.C., Viraktamath, B.C., Balachandran, S.M.: Stress-inducible expression of AtDREB1A transcription factor greatly improves drought stress tolerance in transgenic indica rice. - Transgenic Res. 23: 421–439, 2014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reddy, V.S., Reddy, A.S.: Proteomics of calcium signaling components in plants. — Phytochemistry 65: 1745–1776, 2004.

    Article  CAS  PubMed  Google Scholar 

  • Reichheld, J.P., Vernoux, T., Lardon, F., Van Montagu, M., Inze, D.: Specific checkpoints regulate plant cell cycle progression in response to oxidative stress. — Plant J. 17: 647–656, 1999.

    Article  CAS  Google Scholar 

  • Reichmann, J.L., Heard, J., Martin, G., Reuber, L., Jiang, C.Z., Keddie, J., Adam, L., Pineda, O., Ratcliffe, O.J., Samaha, R.R., Creelman, R., Pilgrim, M., Broun, P., Zhang, J.Z., Ghandehari, D., Sherman, B.K., Yu, J.L.: Arabidopsis transcription factors, genome-wide comparative analysis among eukaryotes. — Science 290: 2105–2110, 2000.

    Article  Google Scholar 

  • Rosinski, J.A., Atchley, W.R.: Molecular evolution of the Myb family of transcription factors: evidence for polyphyletic origin. — J. Mol. Evol. 46: 74–83, 1998.

    Article  CAS  PubMed  Google Scholar 

  • Rumer, S., Gupta, K.J., Kaiser, W.M.: Oxidation of hydroxylamines to NO by plant cells. — Plant Signal Behav. 4: 853–855, 2009.

    Article  PubMed  PubMed Central  Google Scholar 

  • Saijo, Y., Hata, S., Kyozuka, J., Shimamoto, K., Izui, K.: Overexpression of single calcium dependent protein kinase confers both cold and salt/drought tolerance on rice plants. — Plant J. 28: 319–327, 2000.

    Article  Google Scholar 

  • Sakihama, Y., Nakamura, S., Yamazaki, H.: Nitric oxide production mediated by nitrate reductase in the green alga Chlamydomonas reinhardtii: an alternative NO production pathway in photosynthetic organisms. — Plant Cell Physiol. 43: 290–297, 2002.

    Article  CAS  PubMed  Google Scholar 

  • Sakuma, Y., Liu, Q., Dubouzet, J.G., Abe, H., Shinozaki, K., Yamaguchi-Shinozaki, K.: DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration and cold-inducible gene expression. — Biochem. biophys. Res. Commun. 290: 998–1009, 2002.

    Article  CAS  PubMed  Google Scholar 

  • Sanchez-Calvo, B., Barroso, J.B., Corpas, F.J.: Hypothesis, nitro-fatty acids play a role in plant metabolism. — Plant Sci. 199–200: 1–6, 2013.

    Article  PubMed  CAS  Google Scholar 

  • Sangam, S., Jayasree, D., Reddy, K.J., Chari, P.V.B., Sreenivasulu, N., Kavi Kishor, P.B.: Salt tolerance in plants-transgenic approaches. — J. Plant Biotechnol. 7: 1–15, 2005.

    Google Scholar 

  • Sarwat, M., Ahmad, P., Nabi, G., Hu, X.: Ca2+ signals: The versatile decoders of environmental cues. — Crit. Rev. Biotechnol. 33: 97–109, 2013.

    Article  CAS  PubMed  Google Scholar 

  • Sazegari, S., Niazi, A.: Isolation and molecular characterization of wheat (Triticum aestivum) dehydration responsive element binding factor (DREB) isoforms. — Aust. J. Crop Sci. 6: 1037–1044, 2012.

    CAS  Google Scholar 

  • Schweighofer, A., Hirt, H., Meskiene, I.: Plant PP2C phosphatases: emerging functions in stress signaling. — Trends Plant Sci. 9: 236–243, 2004.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Sreenivasulu, N., Sopory, S.K., Kavi Kishor, P.B.: Deciphering the regulatory mechanisms of abiotic stress tolerance in plants by genomic approaches. — Gene 388: 1–13, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Sreenivasulu, N., Varshney, R.K., Kavi Kishor, P.B., Weschke, W.: Tolerance to abiotic stress in cereals: a functional genomics approach. - In: Gupta, P.K., Varshney, R.K. (ed.): Cereal Genomics. Pp. 483–414. Kluwer Academic Publishers, Dordrecht 2004.

    Google Scholar 

  • Stohr, C., Strube, F., Marx, G., Ullrich, W.R., Rockel, P.: A plasma membrane-bound enzyme of tobacco roots catalyses the formation of nitric oxide from nitrite. — Planta 212: 835–841, 2001.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Sun, Y., Li, Y., Hu, X., Yang, Q., Kang, J., Zhang, T.: Molecular cloning and characterization of a novel gene encoding DREB protein from Buchloe dactyloides (Nutt.). — J. agr. Sci. 4: 12–22, 2012.

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Tada, Y., Spoel, S.H., Pajerowska-Mukhtar, K., Mou, Z., Song, J., Wang, C., Zuo, J., Dong, X.: Plant immunity requires conformational changes of NPR1 via S-nitrosylation and thioredoxins. — Science 321: 952–956, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Tamminen, I., Makela, P., Heino, P., Palva, E.T.: Ectopic expression of ABI3 gene enhances freezing tolerance in response to abscisic acid and low temperature in Arabidopsis thaliana. — Plant J. 25: 1–8, 2001.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Thao, N.P., Tran, L.S.: Potentials toward genetic engineering of drought-tolerant soybean. — Crit. Rev. Biotechnol. 32: 349–362, 2012.

    Article  PubMed  CAS  Google Scholar 

  • Thomashow, M.F.: Plant cold acclimation, freezing tolerance genes and regulatory mechanisms. — Annu. Rev. Plant Physiol. Plant mol. Biol. 50: 571–599, 1999.

    Article  CAS  PubMed  Google Scholar 

  • Tran, L.S., Mochida, K.: Functional genomics of soybean for improvement of productivity in adverse conditions. — Funct. Integr. Genomics 10: 447–462, 2010.

    Article  CAS  PubMed  Google Scholar 

  • Tran, L.S., Nakashima, K., Sakuma, Y., Osakabe, Y., Qin, F., Simpson, S.D., Maruyama, K., Fujita, Y., Shinozaki, K., Yamaguchi-Shinozaki, K.: Co-expression of the stress inducible zinc finger homeodomain ZFHD1 and NAC transcription factors enhances expression of the ERD1 gene in Arabidopsis. — Plant J. 49: 46–63, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Trewavas, A.J., Malho, R.J.: Signal perception and transduction: the origin of the phenotype. — Plant Cell 9: 1181–1195, 1997.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tun, N.N., Santa-Catarina, C., Begum, T., Silveira, V., Handro, W., Floh, E.I., Scherer, G.F.: Polyamines induce rapid biosynthesis of nitric oxide (NO) in Arabidopsis thaliana seedlings. — Plant Cell Physiol. 47: 346–354, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Tuteja, N., Ahmad, P., Panda, B.B., Tuteja, R.: Genotoxic stress in plants: shedding light on DNA damage, repair and DNA repair helicases. — Mutation Res. 681: 134–149, 2009.

    Article  CAS  PubMed  Google Scholar 

  • Tuteja, N., Mahajan, S.: Further characterization of calcineurin B-like protein and its interacting partner CBL-interacting protein kinase from Pisum sativum. — Plant Signal Behav. 2: 358–361, 2007.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ulm, R., Revenkova, E., Sansebastiano, G.P., Bechtold, N., Paszkowski, J.: Mitogen-activated protein kinase phosphatase is required for genotoxic stress relief in Arabidopsis. — Genes Dev. 15: 699–709, 2001.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Umezawa, T., Fujita, M., Fujita, Y., Yamaguchi-Shinozaki, K., Shinozaki, K.: Engineering drought tolerance in plants: discovering and tailoring genes to unlock the future. — Curr. Opin. Plant Biotechnol. 17: 113–122, 2006.

    Article  CAS  Google Scholar 

  • Urao, T., Katagiri, T., Mizoguchi, T., Yamaguchi-Shinozaki, K., Hayashida, N., Shinozaki, K.: Two genes that encode Ca2+ dependent protein kinases are induced by drought and high-salt stresses in Arabidopsis thaliana. — Mol. gen. Genet. 244: 331–340, 1994.

    Article  CAS  PubMed  Google Scholar 

  • Uzilday, B., Turkan, I., Ozgur, R., Sekmen, A.H.: Strategies of ROS regulation and antioxidant defense during transition from C3 to C4 photosynthesis in the genus Flaveria under PEG-induced osmotic stress. — J. Plant Physiol. 171: 65–75, 2014.

    Article  CAS  PubMed  Google Scholar 

  • Valliyodan, B., Nguyen, H.T.: Understanding regulatory networks and engineering for enhanced drought tolerance in plants. — Curr. Opin. Plant Biotechnol. 9: 189–195, 2006.

    Article  CAS  Google Scholar 

  • Vannini, C., Campa, M., Iriti, M., Genga, A., Faoro, F., Carravieri, S., Maruyama, K., Fujita, Y., Shinozaki, K., Yamaguchi-Shinozaki, K.: Evaluation of transgenic tomato plants ectopically expressing the rice Osmyb4 gene. — Plant Sci. 173: 231–239, 2007.

    Article  CAS  Google Scholar 

  • Varshney, R.K., Mohan, S.M., Gaur, P.M., Gangarao, N.V.P.R., Pandey, M.K., Bohra, A., Sawargaonkar, S.L., Chitikineni, A., Kimurto, P.K., Janila, P., Saxena, K.B., Fikre, A., Sharma, M., Rathore, A., Pratap, A., Tripathi, S., Datta, S., Chaturvedi, S.K., Mallikarjuna, N., Anuradha, G., Babbar, A., Choudhary, A.K., Mhase, M.B., Bharadwaj, C., Mannur, D.M., Harer, P.N., Guo, B., Liang, X., Nadarajan, N., Gowda, C.L.: Achievements and prospects of genomicsassisted breeding in three legume crops of the semi-arid tropics. — Biotechnol. Adv. 31: 1120–1134, 2013.

    Article  PubMed  Google Scholar 

  • Vernoux, T., Wilson, R.C., Seeley, K.A., Reichheld, J.P., Muroy, S., Brown, S., Maughand, S.C., Cobbettd, C.S., Montagua, M.V., Inzea, D., Maya, M.K., Sung, Z.R.: The root meristemless1/cadmium sensitive2 gene defines a glutathione-dependent pathway involved in initiation and maintenance of cell division during postembryonic root development. — Plant Cell 12: 97–110, 2000.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Villanueva, C., Giulivi, C.: Subcellular and cellular locations of nitric oxide synthase isoforms as determinants of health and disease. — Free Radicals Biol. Med. 49: 307–316, 2010.

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Viswanathan, C., Zhu, J.K.: Molecular perspectives on crosstalk and specificity in abiotic stress signaling in plants. — J. exp. Bot. 55: 225–236, 2004.

    Google Scholar 

  • Voytas, D.F., Gao, C.: Precision genome engineering and agriculture: opportunities and regulatory challenges. PLoS Biol. 12: e1001877, 2014.

    Article  Google Scholar 

  • Wang, J., Ding, B., Guo, Y., Li, M., Chen, S., Huang, G., Xie, X.: Overexpression of a wheat phospholipase D gene, TaPLDα, enhances tolerance to drought and osmotic stress in Arabidopsis thaliana. — Planta 240: 103–115, 2014.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Wang, Y.M., He, C.F.: Isolation and characterization of a coldinduced DREB gene from Aloe vera L. — Plant mol. Biol. Rep. 25: 121–132, 2007.

    Article  CAS  Google Scholar 

  • Wendel, J.F., Jackson S.A., Meyers, B.C., Wing, R.A.: Evolution of plant genome architecture. - Genome Biol. in press, 2016.

    Google Scholar 

  • Wimalasekera, R., Tebartz, F., Scherer, G.F.: Polyamines polyamine oxidases and nitric oxide in development, abiotic and biotic stresses. — Plant Sci. 181: 593–603, 2011.

    Article  CAS  PubMed  Google Scholar 

  • Wurzinger, B., Mair, A., Pfister, B., Teige, M.: Crosstalk of calcium dependent protein kinase and MAP kinase signaling. — Plant Signal Behav. 6: 8–12, 2011.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiong, L., Yang, Y.: Disease resistance and abiotic stress tolerance in rice are inversely modulated by an abscisic acid-inducible mitogen-activated protein kinase. — Plant Cell 5:745–59. 2003.

    Article  CAS  Google Scholar 

  • Xiong, Y.W., Fei, S.Z.: Functional and phylogenetic analysis of a DREB/CBF-like gene in perennial ryegrass (Lolium perenne L.). — Planta 224: 878–888, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Xu, D.B., Gao, S.Q., Ma, Y.Z., Xu, Z.S., Zhao, C.P., Tang, Y.M., Li, X.Y., Li, L.C., Chen, Y.F., Chen, M.: ABI-like transcription factor gene TaABL1 from wheat improves multiple abiotic stress tolerances in transgenic plants. Funct. Integr. Genomics 14: 717–30, 2014.

    Article  CAS  PubMed  Google Scholar 

  • Xu, J., Li, Y., Wang, Y., Liu, H., Lei, L., Yang, H., Liu, G., Ren, D.: Activation of MAPK kinase 9 induces ethylene and camalexin biosynthesis and enhances sensitivity to salt stress in Arabidopsis. — J. biol. Chem. 283: 26996–26106, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Xu, Y., Hu, W., Liu, J., Zhang, J., Jia, C., Miao, H., Xu, B., Jin, Z.: A banana aquaporin gene, MaPIP1, is involved in tolerance to drought and salt stresses. — BMC Plant Biol. 14: 59, 2014.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Xu, Y.Z., Arrieta-Montiel, M.P., Virdi, K.S., De Paula, W.B.M., Widhalm, J.R., Basset, G.J., Davila, J.I., Elthon, T.E., Elowsky, C.G., Sato, S.J., Clemente, T.E., Mackenzie, S.A.: MutS HOMOLOG1 is a nucleoid protein that alters mitochondrial and plastid properties and plant response to high light. — Plant Cell 23: 3428–3441, 2011.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamaguchi-Shinozaki, K., Shinozaki, K.: Organization of cisacting regulatory elements in osmotic-and cold-stressresponsive promoters. — Trends Plant Sci. 10: 88–94, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Yang, K.Y., Liu, Y., Zhang, S.: Activation of a mitogen activated protein kinase pathway is involved in disease resistance in tobacco. — Proc. nat. Acad. Sci. USA 98: 741–746, 2001.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang, Z., Nakabayashi, R., Okazaki, Y., Mori, T., Takamatsu, S., Kitanaka, S., Kikuchi, J., Saito, K.: Toward better annotation in plant metabolomics: isolation and structure elucidation of 36 specialized metabolites from Oryza sativa (rice) by using MS/MS and NMR analyses. — Metabolomics 10: 543–555, 2014.

    Article  CAS  PubMed  Google Scholar 

  • Yi, M., Weaver, D., Eisner, V., Várnai, P., Hunyady, L., Ma, J., Csordás, G., Hajnóczky, G.: Switch from ER-mitochondrial to SR-mitochondrial calcium coupling during muscle differentiation. — Cell Calcium 52: 355–365, 2012.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoo, J.H., Park, C.Y., Kim, J.C., Heo, W.D., Cheong, M.S., Park, H.C., Kim, M.C., Moon, B.C., Choi, M.S., Kang, Y.H., Lee, J.H.: Direct interaction of a divergent CaM isoform and the transcription factor, MYB2, enhances salt tolerance in Arabidopsis. — J. biol. Chem. 280: 3697–3706, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Yu, L., Nie, J., Cao, C., Jin, Y., Yan, M., Wang, F., Liu, J., Xiao, Y., Liang, Y., Zhang, W.: Phosphatidic acid mediates salt stress response by regulation of MPK6 in Arabidopsis thaliana. — New Phytol. 188: 762–773, 2010.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, L., Zhao, G., Xia, C., Jia, J., Liu, X., Kong, X.: A wheat R2R3-MYB gene, TaMYB30-B, improves drought stress tolerance in transgenic Arabidopsis. — J. exp. Bot. 63: 5873–5885, 2012.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, P., Yang, P., Zhang, Z., Han, B., Wang, W., Wang, Y., Cao, Y., Hu, T.: Isolation and characterization of a buffalo grass (Buchloe dactyloides) dehydration responsive element binding transcription factor, BdDREB2. — Gene 536: 123–128, 2014.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, S., Klessig, D.F.: MAPK cascades in plant defense signaling. — Trends Plant Sci. 6: 520–527, 2001.

    Article  CAS  PubMed  Google Scholar 

  • Zhao, J., Fujita, K., Sakai, K.: Reactive oxygen species, nitric oxide, and their interactions play different roles in Cupressus lusitanica cell death and phytoalexin biosynthesis. — New Phytol. 175: 215–229, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Zhao, K., Shen, X., Yuan, H., Liu, Y., Liao, X, Wang, Q., Liu, L., Li, F., Li, T.: Isolation and characterization of dehydration-responsive element-binding factor 2C (MsDREB2C) from Malus sieversii Roem. — Plant Cell Physiol. 54: 1415–1430, 2013.

    Article  CAS  PubMed  Google Scholar 

  • Zhu, J.K.: Salt and drought stress signal transduction in plants. — Annu. Rev. Plant Biol. 53: 247–273, 2002.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. School of Studies in Botany Jiwaji University, Gwalior, MP, 474011, India

    M. A. Ahanger

  2. Department of Botany, Government College University, Faisalabad, 38000, Pakistan

    N. A. Akram

  3. Pakistan Science Foundation, Islamabad, 44000, Pakistan

    M. Ashraf

  4. Department of Botany & Microbiology, King Saud University, Riyadh, 11472, Saudi Arabia

    M. Ashraf, M. N. Alyemeni, L. Wijaya & P. Ahmad

  5. Department of Botany, S.P. College, Srinagar, Jammu and Kashmir, 190001, India

    P. Ahmad

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  1. M. A. Ahanger
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  2. N. A. Akram
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  3. M. Ashraf
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  4. M. N. Alyemeni
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  5. L. Wijaya
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  6. P. Ahmad
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Correspondence to P. Ahmad.

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Acknowledgements: The authors extend their appreciation to the Deanship of Scientific Research, College of Sciences Research Center, King Saud University, Riyadh, Saudi Arabia for supporting the project.

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Ahanger, M.A., Akram, N.A., Ashraf, M. et al. Signal transduction and biotechnology in response to environmental stresses. Biol Plant 61, 401–416 (2017). https://doi.org/10.1007/s10535-016-0683-6

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  • DOI: https://doi.org/10.1007/s10535-016-0683-6

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