Skip to main content
SpringerLink
Log in

Multifunctional genes: the cross-talk among the regulation networks of abiotic stress responses

  • Review
  • Published:
Biologia Plantarum

Abstract

Unfavourable environment brings many kinds of stresses to plants. To survive such stresses, efficient resistance is required for the plants. Multifunctional genes enable the cross-talk among the various abiotic stress resistance systems. This paper reviews the action mechanisms of multifunctional genes. These genes can be classified into three groups: genes encoding diverse proteins through mRNA splicing (e.g. AOX in rice); genes like BADH, P5CS and HAV that control drought, salinity, osmotic and heat stress resistance; and a gene family, for example AQP, controlling transport of many compounds including water and nutrients. These genes participate in signal sensing and transduction, transcriptional regulation and functional gene activation during stress resistance induction. Furthermore, it should be noted that, under abiotic stresses, the regulation cascades are mutually interdependent and there also exists a close correlation between those cascades and normal plant growth and development.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

ABA:

abscisic acid

AOX:

alternative oxidase

APX:

ascorbate peroxidase

AQP:

aquaporins

BADH:

betain aldehyde dehydrogenase

CAT:

catalase

CDPK:

calmodulin binding protein kinase

COR:

cold regulated proteins

DREB:

dehydration-responsive element binding

EREB:

ethylene-responsive element binding

GB:

glycine betaine

GR:

glutathione reductase

HSP:

heat-shock protein

LEA:

late-embryogenesis-abundant

MAPK:

mitogen-activated protein kinase

NUE:

nutrition use efficiency

POX:

peroxidase

ROS:

reactive oxygen species

SOD:

superoxide dismutase

WUE:

water use efficiency

References

  • Aarts, M.G., Keijzer, C.J., Stiekema, W.J., Pereira A.: Molecular characterization of the CER1 gene of Arabidopsis involved in epicuticular wax biosynthesis and pollen fertility. — Plant Cell 7: 2l15–2127, 1995.

    Article  Google Scholar 

  • Abebe, T., Guenzi, A.C., Martin, B., Cushman, J.C.: Tolerance of mannitol-accumulating transgenic wheat to water stress and salinity. — Plant Physiol. 131: 1748–1755, 2003.

    Article  PubMed  CAS  Google Scholar 

  • Aharoni, A., Dixit, S., Jetter, R., Thoenes, E., Van Arkel, G., Pereira A.: The SHINE clade of AP2 domain transcription factors activates wax biosynthesis, alters cuticle properties, and confers drought tolerance when overexpressed in Arabidopsis. — Plant Cell. 16: 2463–2480, 2004.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Aswath, C.R., Kim, S.H., Mo, S.Y., Kim, D.H.: Transgenic plants of creeping bent grass harboring the stress inducible gene, 9-cis-epoxycarotenoid dioxygenase, are highly tolerant to drought and NaCl stress. — Plant Growth Regul. 47: 129–139, 2005.

    Article  CAS  Google Scholar 

  • Babu, R.C., Zhang, J.X., Blum, A., Ho, T.H.D., Wu, R., Nguyen, H.T.: HVA1, a LEA gene from barley confers dehydration tolerance in transgenic rice (Oryza sativa L.) via cell membrane protection. — Plant Sci. 166: 855–862, 2004.

    Article  CAS  Google Scholar 

  • Badawi, G.H., Yamauchi, Y., Shimada, E., Sasaki, R., Kawano, N., Tanaka, K., Tanaka, K.: Enhanced tolerance to salt stress and water deficit by overexpressing superoxide dismutase in tobacco (Nicotiana tabacum) chloroplasts. — Plant Sci. 166: 919–928, 2004.

    Article  CAS  Google Scholar 

  • Bae, H., Herman, E., Bailey, B., Bae, H.J., Sicher, R.: Exogenous trehalose alters Arabidopsis transcripts involved in cell wall modification, abiotic stress, nitrogen metabolism, and plant defense. — Physiol. Plant. 125: 114–126, 2005.

    Article  CAS  Google Scholar 

  • Bahieldin, A., Mahfouz, H.T., Eissa, H.F., Saleh, O.M., Ramadan, A.M., Ahmed, I.A., Dyer, W.E., El-Itriby, H.A., Madkour, M.A.: Field evaluation of transgenic wheat plants stably expressing the HVA1 gene for drought tolerance. — Physiol. Plant. 123: 421–427, 2005.

    Article  CAS  Google Scholar 

  • Bhattacharjee, S.: Calcium-dependent signaling pathway in the heat-induced oxidative injury in Amaranthus lividus. — Biol. Plant. 52: 137–140, 2008.

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Buckley, T.N.: The control of stomata by water balance. — New Phytol. 168: 275–292, 2005.

    Article  PubMed  CAS  Google Scholar 

  • Byzova, M.V., Franken, J., Aarts, M.G., de Almeida-Engler, J., Engler, G., Mariani, C., Van Lookeren Campagne, M.M., Angenent, G.C.: Arabidopsis STERILE APETALA, a multifunctional gene regulating inflorescence, flower, and ovule development. — Genes Dev. 13: 1002–1014, 1999.

    Article  PubMed  CAS  Google Scholar 

  • Caeiro, A.S., Ramos, P.C., Teixeira, A.R., Ferreira, R.B.: The ubiquitin/proteasome pathway from Lemna minor subjected to heat shock. — Biol. Plant. 52: 695–702, 2008.

    Article  CAS  Google Scholar 

  • Chang, W.C., Capite, J.D., Singaravelu, K., Nelson, C., Halse, V., Parekh, A.B.: Local Ca2+ influx through Ca2+ release-activated Ca2+ (CRAC) channels stimulates production of an intracellular messenger and an intercellular proinflammatory signal. — J. biol. Chem. 283: 4622–4631, 2008.

    Article  PubMed  CAS  Google Scholar 

  • Chen, S.Y., Xiao, S., Zhang, M.X., Chen, T., Wang, H.C., An, L.Z.: Antisense and RNAi expression for a chloroplastic superoxide dismutase gene in transgenic plants. — Bot. Bull. Acad. sin. 46: 175–182, 2005.

    CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Cheong, Y.H., Chang, H.S., Gupta, R., Wang, X., Zhu, T., Luan, S.: Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. — Plant Physiol. 129: 1–17, 2002.

    Article  CAS  Google Scholar 

  • Cheong, Y.H., Kim, K.N., Pandey, G.K., Gupta, R., Grant, J.J., Luan, S.: CBL1, a calcium sensor that differentially regulates salt, drought, and cold responses in Arabidopsis. — Plant Cell. 15: 1833–1845, 2003.

    Article  PubMed  CAS  Google Scholar 

  • Chiang, Y.J., Stushnoff, C., McSay, A.E.: Overexpression of mannitol-1-phosphate dehydrogenase increase mannitol accumulation and adds protection against chilling injury in Petunia. — J. amer. Soc. hort. Sci. 130: 605–610, 2005.

    CAS  Google Scholar 

  • Chinnusamy, V., Schumaker, K., Zhu, J.K.: Molecular genetic perspectives on cross-talk and specificity in abiotic stress signalling in plants. — J. exp. Bot. 55: 225–236, 2004.

    Article  PubMed  CAS  Google Scholar 

  • Cho, E.K., Hong, C.B.: Overexpression of tobacco NtHSP70-1 contributes to drought-stress tolerance in plants. — Plant Cell. 25: 349–358, 2006.

    CAS  Google Scholar 

  • Cong, L., Zheng, H.C., Zhang, Y.X., Chai, T.Y.: Arabidopsis DREB1A confers high salinity tolerance and regulates the expression of GA dioxygenases in tobacco. — Plant Sci. 174: 156–164, 2008.

    Article  CAS  Google Scholar 

  • Courtois, C., Besson, A., Dahan, J., Bourque, S., Dobrowolska, G., Pugin, A., Wendehenne, D.: Nitric oxide signalling in plants: interplays with Ca2+ and protein kinases. — J. exp. Bot. 59: 155–163, 2008.

    Article  PubMed  CAS  Google Scholar 

  • Dai, X.Y., Xu, Y.Y., Ma, Q.B., Xu, W.Y., Wang, T., Xue, Y.B., Chong, K.: Overexpression of an R1R2R3 MYB gene, OsMYB3R-2, increases tolerance to freezing, drought, and salt stress in transgenic Arabidopsis. — Plant Physiol. 143: 1739–1751, 2007.

    Article  PubMed  CAS  Google Scholar 

  • De Ronde, J.A., Cress, W.A., Mescht, A.V.D.: Agrobacterium mediated transformation of soybean seed with the GUS-INT marker gene. — South Afr. J. Sci. 97: 421–424, 2001.

    Google Scholar 

  • De Ronde, J.A., Laurie, R.N., Caetano, T., Greyling, M.M., Kerepesi, I.: Comparative study between transgenic and non-transgenic soybean lines proved transgenic lines to be more drought tolerant. — Euphytica 138: 123–132, 2004.

    Article  Google Scholar 

  • Douglas, S.J., Chuck, G., Dengler, R.E., Pelecanda, L., Riggs, C.D.: KNAT1 and ERECTA regulate inflorescence architecture in Arabidopsis. — Plant Cell 14: 547–558, 2002.

    Article  PubMed  CAS  Google Scholar 

  • Dubrovsky, J.G., North, G.B., Nobel, P.S.: Root growth, developmental changes in the apex, and hydraulic conductivity for Opuntia ficus-indica during drough. — New Phytol. 138: 75–82, 1998.

    Article  Google Scholar 

  • Eltayeb, A.E., Kawano, N., Badawi, G.H., Kaminaka, H., Sanekata, T., Shibahara, T., Inanaga, S., Tanaka, K.: Overexpression of monodehydroascorbate reductase in transgenic tobacco confers enhanced tolerance to ozone, salt and polyethylene glycol stresses. — Planta 225: 1255–1264, 2007.

    Article  PubMed  CAS  Google Scholar 

  • Ferreira, A.L., Arrabaca, J.D., Vaz-Pinto, V., Lima-Costa, M.E.: Induction of alternative oxidase chain under salt stress conditions. — Biol. Plant. 52: 66–71, 2008.

    Article  CAS  Google Scholar 

  • Fu, D.L., Huang, B.R., Xiao, Y.M., Muthukrishnan, S., Liang, G.H.: Overexpression of barley hva1 gene in creeping bentgrass for improving drought tolerance. — Plant Cell 26: 467–477, 2007.

    CAS  Google Scholar 

  • Galmés, J., Pou, A., Alsina, M.M., Tomàs, M., Medrano, H., Flexas, J.: Aquaporin expression in response to different water stress intensities and recovery in Richter-110 (Vitis sp.): relationship with ecophysiological status. — Planta 226: 671–681, 2007.

    Article  PubMed  CAS  Google Scholar 

  • Godiard, L., Sauviac, L., Torii, K.U., Grenon, O., Mangin, B., Grimsley, N.H., Marco, Y.: ERECTA, an LRR receptor-like kinase protein controlling development, pleiotropically affects resistance to bacterial wilt. — Plant J. 36: 353–365, 2003.

    Article  PubMed  CAS  Google Scholar 

  • Goodwin, S.B., Sutter, T.R.: Microarray analysis of Arabidopsis genome response to aluminum stress. — Biol. Plant. 53: 85–99, 2009.

    Article  CAS  Google Scholar 

  • Gupta, P., Duplessis, S., White, H., Karnosky, D.F., Martin, F., Podila, G.K.: Gene expression patterns of trembling aspen trees following long-term exposure to interacting elevated CO2 and tropospheric O3. — New Phytol. 167: 129–142, 2005.

    Article  PubMed  CAS  Google Scholar 

  • Hachez, C., Zelazny, E., Chaumont, F.: Modulating the expression of aquaporin genes in plant: a key to understand their physiological functions? — Biochim. biophys. Acta 1758: 1142–1156, 2006.

    Article  PubMed  CAS  Google Scholar 

  • Hong, Z.L., Lakkineni, K., Zhang, Z.M., Verma, D.P.S.: Removal of feedback inhibition of D1-pyrroline-5-carboxylate synthetase results in increased praline accumulation and protection of plants from osmotic stress. — Plant Physiol. 122: 1129–1136, 2000.

    Article  PubMed  CAS  Google Scholar 

  • Hooker, T.S., Millar, A.A., Kunst, L.: Significance of the expression of the CER6 coding enzyme for cuticular wax production in Arabidopsis. — Plant Physiol. 129: 1–13, 2002.

    Article  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Hu, X.B., Song, F.M., Zheng, Z.: Molecular characterization and expression analysis of a rice protein phosphatase 2C gene, OsBIPP2C1, and overexpression in transgenic tobacco conferred enhanced disease resistance and abiotic tolerance. — Physiol. Plant. 127: 225–237, 2006.

    Article  CAS  Google Scholar 

  • Huang, L., Zhang, Z.B., Cui, Y.R., Liu, M.Y., Chai, S.X., Chen, Z.B.: [Relationship between wax content and water use efficiency of leaf and yield in wheat.] — J. Triticeae Crops 23: 41–44, 2003. [In Chin.]

    Google Scholar 

  • Ito, Y., Katsura, K., Maruyama, K., Taji, T., Kobayashi, M., Seki, M., Shinozaki, K., Yamaguchi-Shinozaki, K.: Functional analysis of rice DREB1/CBF-type transcription factors involved in cold-responsive gene expression in transgenic rice. — Plant Cell Physiol. 47: 141–153, 2006.

    Article  PubMed  CAS  Google Scholar 

  • Jang, J.Y., Kim, D.G., Kim, Y.O., Kim, J.S., Kang, H.: An expression analysis of a gene family encoding plasma membrane aquaporins in response to abiotic stresses in Arabidopsis thaliana. — Plant mol. Biol. 54: 713–725, 2004.

    Article  PubMed  CAS  Google Scholar 

  • Jang, J.Y., Lee, S.H., Rhee, J.Y., Chung, G.C., Ahn, S.J., Kang, H.S.: Transgenic Arabidopsis and tobacco plants over- expressing an aquaporin respond differently to various abiotic stresses. — Plant mol. Biol. 64: 621–632, 2007.

    Article  PubMed  CAS  Google Scholar 

  • Jyothsnakumari, G., Thippeswamy, M., Veeranagamallaiah, G., Sudhakar, C.: Differential expression of LEA proteins in two genotypes of mulberry under salinity. — Biol. Plant. 53: 145–150, 2009.

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Karaba, A.: Improvement of water use efficiency in rice and tomato using Arabidopsis wax biosynthetic genes and transcription factors. — PhD. Thesis, Wageningen University, Wageningen 2007.

    Google Scholar 

  • Karaba, A., Dixit, S., Greco, R., Aharoni, A., Trijatmiko, K.R., Marsch-Martinez, N., Krishnan, A., Nataraja, K.N., Udayakumar, M., Pereira, A.: Improvement of water use efficiency in rice by expression of HARDY, an Arabidopsis drought and salt tolerance gene. — Proc. nat. Acad. Sci. USA 104: 15270–15275, 2007.

    Article  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Komari, T., Hiei, Y., Saito, Y., Murai, N., Kumashiro, T.: Vectors carrying two separate T-DNAs for co-transformation of higher plants mediated by Agrobacterium tumefaciens and segregation of transformants free from selection markers. — Plant J. 10: 165–174, 1996.

    Article  PubMed  CAS  Google Scholar 

  • Koornneef, A., Pieterse, C.M.J.: Cross talk in defense signaling. — Plant Physiol. 146: 839–844, 2008.

    Article  PubMed  CAS  Google Scholar 

  • Kosová, K., Prášil, I.T., Vítámvás, P.: The relationship between vernalization- and photoperiodically-regulated genes and the development of frost tolerance in wheat and barley. — Biol. Plant. 52: 601–615, 2008.

    Article  Google Scholar 

  • Kumar, S., Dhingra, A., Daniell, H.: Plastid-expressed betaine aldehyde dehydrogenase gene in carrot cultured cells, roots, and leaf confers enhanced salt tolerance. — Plant Physiol. 136: 1–12, 2004.

    Article  CAS  Google Scholar 

  • Kume, S.B., Kobayashi, F., Ishibashi, M., Ohno, R., Nakamura, C., Takumi, S.: Differential and coordinated expression of Cbf and Cor/Lea genes during long-term cold acclimation in two wheat cultivars showing distinct levels of freezing tolerance. — Genes Genet. Syst. 80: 185–197, 2005.

    Article  PubMed  CAS  Google Scholar 

  • Kwon, S.Y., Jeong, Y.J., Lee, H.S., Kim, J.S., Cho, K.Y., Allen, R.D., Kwak, S.S.: Enhanced tolerances of transgenic tobacco plants expressing both superoxide dismutase and ascorbate peroxidase in chloroplasts against methyl viologen-mediated oxidative stress. — Plant Cell Environ. 25: 873–882, 2002.

    Article  Google Scholar 

  • Langridge, P., Paltridge, N., Fincher, G.: Functional genomics of abiotic stress tolerance in cereals. — Brief. Func. Genom. Proteom. 4: 343–354, 2006.

    Article  CAS  Google Scholar 

  • Larkindale, J., Hall, J.D., Knight, M.R., Vierling, E.: Heat stress phenotypes of Arabidopsis mutants implicate multiple signaling pathways in the acquisition of thermotolerance. — Plant Physiol. 138: 882–897, 2005.

    Article  PubMed  CAS  Google Scholar 

  • Lease, K.A., Lau, N.Y., Schuster, R.A., Torii, K.U., Walker, J.C.: Receptor serine/threonine protein kinases in signalling: analysis of the ERECTA receptor-like kinase of Arabidopsis thaliana. — New Phytol. 151: 133–143, 2001.

    Article  CAS  Google Scholar 

  • Lee, Y.P., Kim, S.H., Bang, J.W., Lee, H.S., Kwak, S.S., Kwon, S.Y.: Enhanced tolerance to oxidative stress in transgenic tobacco plants expressing three antioxidant enzymes in chloroplasts. — Plant Cell 26: 591–598, 2007.

    CAS  Google Scholar 

  • Lefebvre, V., North, H., Frey, A., Sotta, B., Seo, M., Okamoto, M., Nambara, E., Marion-Poll, A.: Functional analysis of Arabidopsis NCED6 and NCED9 genes indicates that ABA synthesized in the endosperm is involved in the induction of seed dormancy. — Plant J. 45: 309–319, 2006.

    Article  PubMed  CAS  Google Scholar 

  • Leide, J., Hildebrandt, U., Reussing, K., Riederer, M., Vogg, G.: The developmental pattern of tomato fruit wax accumulation and its impact on cuticular transpiration barrier properties: effects of a deficiency in a β-ketoacyl-coenzyme A synthase (LeCER6). — Plant Physiol. 144: 1667–1679, 2007.

    Article  PubMed  CAS  Google Scholar 

  • Lin, P.C., Hwang, S.G., Endo, A., Okamoto, M., Koshiba, T., Cheng, W.H.: Ectopic expression of abscisic acid 2/glucose insensitive 1 in Arabidopsis promotes seed dormancy and stress tolerance. — Plant Physiol. 143: 745–758, 2007.

    Article  PubMed  CAS  Google Scholar 

  • Liu, J.G., Yao, Q.H., Zhang, Z., Peng, R.H., Xiong, A.S., Xu, F., Zhu, H.: Isolation and characterization of a cDNA encoding two novel heat-shock factor OsHSF6 and OsHSF12 in Oryza sativa L. — J. Biochem. mol. Biol. 38: 602–608, 2005.

    PubMed  CAS  Google Scholar 

  • Lopez-Carrion, A.I., Castellano, R., Rosales, M.A., Ruiz, J.M., Romero, L.: Role of nitric oxide under saline stress: implications on proline metabolism. — Biol. Plant. 52: 587–591, 2008.

    Article  CAS  Google Scholar 

  • Luan, S., Kudla, J., Rodriguez-Concepcion, M., Yalovsky, S., Gruissem, W.: Calmodulins and calcineurin B-like proteins, calcium sensors for specific signal response coupling in plants. — Plant Cell 14(Suppl.): s389–s400, 2002.

    PubMed  CAS  Google Scholar 

  • Ma, Z., Bielenberg, D.G., Brown, K.M., Lynch, J.P.: Regulation of root hair density by phosphorus availability in Arabidopsis thaliana. — Plant Cell Environ. 24: 459–467, 2001.

    Article  CAS  Google Scholar 

  • Manfre, A.J., Lanni, L.M., Marcotte, W.R.: The Arabidopsis group 1 late embryogenesis abundant protein ATEM6 is required for normal seed development. — Plant Physiol. 140: 140–149, 2006.

    Article  PubMed  CAS  Google Scholar 

  • Maqbool, S.B., Zhong, H., El-Maghraby, Y., Ahmad, A., Chai, B., Wang, W., Sticklen, M.: Competence of oat (Avena sativa L.) shoot apical meristems for integrative transformation, inherited expression, and osmotic tolerance of transgenic lines containing hva1. — Theor. appl. Genet. 105: 201–208, 2002.

    Article  PubMed  CAS  Google Scholar 

  • Masle, J., Gilmore, S.R., Farquhar, G.D.: The ERECTA gene regulates plant transpiration efficiency in Arabidopsis. — Nature 436: 866–879, 2005.

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • McCabe, T.C., Finnegan, P.M., Millar, A.H., Day, D.A., Whelan, J.: Differential expression of alternative oxidase genes in soybean cotyledons during postgerminative development. — Plant Physiol. 118: 675–682, 1998.

    Article  PubMed  CAS  Google Scholar 

  • Mittler, R.: Abiotic stress, the field environmentand stress combination. — Trends Plant Sci. 11: 15–19, 2006.

    Article  PubMed  CAS  Google Scholar 

  • Moghaieb, R.E.A., Tanaka, N., Saneoka, H., Hussein, H.A., Yousef, S.S., Ewada, M.A.F., Mohamed, A.M.A., Kounosuke, F.: Expression of Betaine Aldehyde Dehydrogenase gene in transgenic tomato hairy roots leads to the accumulation of glycine betaine and contributes to the maintenance of the osmotic potential under salt stress. — Soil Sci. Plant Nutr. 46: 873–883, 2000.

    CAS  Google Scholar 

  • Mohanty, A., Kathuria, H., Ferjani, A., Sakamoto, A., Mohanty, P., Murata, N., Tyagi, A.: Transgenics of an elite indica rice variety Pusa Basmati 1 harbouring the codA gene are highly tolerant to salt stress. — Theor. appl. Genet. 106: 51–57, 2002.

    PubMed  CAS  Google Scholar 

  • Mohanpuria, P., Rana, N.K., Yadav, S.K.: Transient RNAi based gene silencing of glutathione synthetase reduces glutathione content in Camellia sinensis (L.) O. Kuntze somatic embryos. — Biol. Plant. 52: 361–364, 2008.

    Article  Google Scholar 

  • Niu, C.F., Tian, A.G., Zhang, Z.B., Zhang, J.S., Chen, S.Y.: Molecular cloning and characterization of the WRKY genes induced by water deficit in wheat (Triticum aestivum L.). — In: The First International Conference on the Theory and Practices in Bio-Water-Saving. Vol. 1. Pp. 4–78, Beijing 2006.

    Google Scholar 

  • Oraby, H.F., Ransom, C.B., Kravchenko, A.N., Sticklen, M.B.: Barley HVA1 gene confers salt tolerance in R3 transgenic oat. — Crop Sci. 45: 2218–2227, 2005.

    Article  CAS  Google Scholar 

  • Pandey, G.K., Grant, J.J., Cheong, Y.H., Kim, B.G., Li, L.G., Luan, S.: Calcineurin-B-Like protein CBL9 interacts with target kinase CIPK3 in the regulation of ABA response in seed germination. — Mol. Plant 1: 238–248, 2008.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Park, E.J., Jeknić, Z., Sakamoto, A., DeNoma, J., Yuwansiri, R., Murata, N.: Genetic engineering of glycine betaine synthesis in tomato protects seeds, plants, and flowers from chilling damage. — Plant J. 40: 474–487, 2004.

    Article  PubMed  CAS  Google Scholar 

  • Parvanova, D., Ivanov, S., Konstantinova, T., Karanov, E., Atanassov, A., Tsvetkov, T., Alexieva, V., Djilianov, D.: Transgenic tobacco plants accumulating osmolytes show reduced oxidative damage under freezing stress. — Plant Physiol. Biochem. 42: 57–63, 2004a.

    Article  PubMed  CAS  Google Scholar 

  • Parvanova, D., Popova, A., Zaharieva, I., Lambrev, P., Konstantinova, T., Taneva, S., Atanassov, A., Goltsev, V., Djilianov, D.: Low temperature tolerance of tobacco plants transformed to accumulate proline, fructans, or glycine betaine, variable chlorophyll fluorescence evidence. — Photosynthetica 42: 175–185, 2004b.

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Porcel, R., Aroca, R., Azcón, R., Ruiz-Lozano, J.M.: PIP aquaporin gene expression in arbuscular mycorrhizal Glycine max and Lactuca sativa plants in relation to drought stress tolerance. — Plant mol. Biol. 60: 389–404, 2006.

    Article  PubMed  CAS  Google Scholar 

  • Qin, X.Q., Zeevaart, J.A.D.: The 9-cis-epoxycarotenoid cleavage reaction is the key regulatory step of abscisic acid biosynthesis in water-stressed bean. — Plant Biol. 96: 15354–15361, 1999.

    CAS  Google Scholar 

  • Qiu, Q.S., Guo, Y., Quintero, F.J., Pardo, J.M., Schumaker, K.S., Zhu, J.K.: Regulation of vacuolar Na+/H+ exchange in Arabidopsis thaliana by the salt-overly-sensitive (SOS) pathway. — J. biol. Chem. 279: 207–215, 2004.

    Article  PubMed  CAS  Google Scholar 

  • Quan, L.J., Zhang, B., Shi, W.W., Li, H.Y.: Hydrogen peroxide in plants: a versatile molecule of the reactive oxygen species network. — J. intergr. Plant Biol. 50: 2–18, 2008.

    Article  CAS  Google Scholar 

  • Quresh, M.I., Qadir, S., Zolla, L.: Proteomics-based dissection of stress-responsive pathways in plants. — J. Plant Physiol. 164: 1239–1260, 2007.

    Article  CAS  Google Scholar 

  • Rácz, I., Páldi, E., Szalai, G., Janda, T., Pál, M., Lásztity, D.: S-methylmethionine reduces cell membrane damage in higher plants exposed to low-temperature stress. — J. Plant Physiol. 165: 1483–1490, 2008.

    Article  PubMed  CAS  Google Scholar 

  • Rana, N.K., Mohanpuria, P., Yadav, S.K.: Expression of tea cytosolic glutamine synthetase is tissue specific and induced by cadmium and salt stress. — Biol. Plant. 52: 361–364, 2008.

    Article  CAS  Google Scholar 

  • Ren, D., Liu, Y., Yang, K.Y., Han, L., Mao, G., Glazebrook, J., Zhang, S.: A fungal-responsive MAPK cascade regulates phytoalexin biosynthesis in Arabidopsis. — PNAS 105: 5638–5643, 2008.

    Article  PubMed  Google Scholar 

  • Río, L.A.D., Sandalio, L.M., Corpas, F.J., Palma, J.M., Barroso, J.B.: Reactive oxygen species and reactive nitrogen species in peroxisomes, production, scavenging, and role in cell signaling. — Plant Physiol. 141: 330–335, 2006.

    Article  PubMed  CAS  Google Scholar 

  • Ross, C.A., Liu, Y., Shen, Q.X.: The WRKY gene family in rice. J. intergr. Plant Biol. 49: 827–842, 2007.

    Article  CAS  Google Scholar 

  • Roxas, V.P., Lodhi, S.A., Garrett, D.K., Mahan, J.R., Allen, R.D.: Stress tolerance in transgenic tobacco seedlings that over-express glutathione-S-transferase/glutathione peroxidase. — Plant Cell Physiol. 41: 1229–1234, 2000.

    Article  PubMed  CAS  Google Scholar 

  • Rubio, M.C., González, E.M., Minchin, F.R., Webb, K.J., Arrese-Igor, C., Ramos, J., Becana, M.: Effects of water stress on antioxidant enzymes of leaves and nodules of transgenic alfalfa overexpressing superoxide dismutases. — Physiol. Plant. 115: 531–540, 2002.

    Article  PubMed  CAS  Google Scholar 

  • Saez, A., Robert, N., Maktabi, M.H., Schroeder, J.I., Serrano, R., Rodriguez, P.L.: Enhancement of abscisic acid sensitivity and reduction of water consumption in Arabidopsis by combined inactivation of the protein phosphatases type 2C ABI1 and HAB1. — Plant Physiol. 141: 1389–1399, 2006.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Sakamoto, A., Murata, A.N.: Metabolic engineering of rice leading to biosynthesis of glycine betaine and tolerance to salt and cold. — Plant mol. Biol. 38: 1011–1019, 1998.

    Article  PubMed  CAS  Google Scholar 

  • Sakamoto, A., Murata, A.N.: The role of glycine betaine in the protection of plants from stress: clues from transgenic plants. — Plant Cell Environ. 25: 163–170, 2002.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Salcedo, G., Sánchez-Monge, R., Barber, D., Díaz-Perales, A.: Plant non-specific lipid transfer proteins: an interface between plant defence and human allergy. — Biochim. biophys. Acta. 1171: 781–791, 2007.

    Google Scholar 

  • Samis, K., Bowley, S., McKersie, B.: Pyramiding Mn-superoxide dismutase transgenes to improve persistence and biomass production in alfalfa. — J. exp. Bot. 53: 1343–1350, 2002.

    Article  PubMed  CAS  Google Scholar 

  • Secchi, F., Lovisolo, C., Uehlein, N., Kaldenhoff, R., Schubert, A.: Isolation and functional characterization of three aquaporins from olive (Olea europaea L.). — Planta 225: 381–392, 2007.

    Article  PubMed  CAS  Google Scholar 

  • Serrot, P.H., Sabater, B., Martin, M.: Expression of the ndhCKJ operon of barley and editing at the 13th base of the mRNA of the ndhC gene. — Biol. Plant. 52: 347–350, 2008.

    Article  CAS  Google Scholar 

  • Shao, H.B., Guo, Q.J., Chu, L.Y., Zhao, X.N., Su, Z.L., Hu, Y.C., Cheng, J.F.: Understanding molecular mechanism of higher plant plasticity under abiotic stress. — Colloid Surface Biointerfaces 54: 37–45, 2007.

    Article  CAS  Google Scholar 

  • Sharma, S.S., Dietz, K.J.: The significance of amino acids and amino acid-derived molecules in plant responses and adaptation to heavy metal stress. — J. exp. Bot. 57: 711–726, 2006.

    Article  PubMed  CAS  Google Scholar 

  • Shamsi, I.H., Wei, K., Zhang, G.P., Jilani G.H., Hassan, M.J.: Interactive effects of cadmium and aluminum on growth and antioxidative enzymes in soybean. — Biol. Plant. 52: 165–169, 2008.

    Article  CAS  Google Scholar 

  • Sheen, J.: Ca2+-dependent protein kinases and stress signal transduction in plants. — Science 274: 1900–1902, 1996.

    Article  PubMed  CAS  Google Scholar 

  • Shen, Y.G., He, S.J., Zhang, W.K., Zhang, J.S., Liu, Q., Chen, S.Y.: An EREBP/AP2-type protein in Triticum aestivum was a DRE-binding transcription factor induced by cold, dehydration and ABA stress. — Theor. appl. Genet. 106: 923–930, 2003.

    PubMed  CAS  Google Scholar 

  • Shen, Y.Y., Wang, X.F., Wu, F.Q., Du, S.Y., Cao, Z., Shang, Y., Wang, X.L., Peng, C.C., Yu, X.C., Zhu, S.Y., Fan, R.C., Xu, Y.H., Zhang, D.P.: The Mg-chelatase H subunit is an abscisic acid receptor. — Nature 443: 823–826, 2006.

    Article  PubMed  CAS  Google Scholar 

  • Shepherd, T., Griffiths, D.W.: The effects of stress on plant cuticular waxes. — New Phytol. 171: 469–499, 2006.

    PubMed  CAS  Google Scholar 

  • Shi, H.Z., Xiong, L.M., Stevenson, B., Lu, T.G., Zhu, J.K.: The Arabidopsis salt overly sensitive 4 mutants uncover a critical role for vitamin B6 in plant salt tolerance. — Plant Cell 14: 575–588, 2002.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Silva, C., Martinez, V., Carvajal, M.: Osmotic versus toxic effects of NaCl on pepper plants. — Biol. Plant. 52: 72–79, 2008.

    Article  CAS  Google Scholar 

  • Sivamani, E., Bahieldinb, A., Wraith, J.M., Al-Niemi, T., Dyer, W.E., David Ho, T.H., Qu, R.D.: Improved biomass productivity and water use efficiency under water deficit conditions in transgenic wheat constitutively expressing the barley HVA1 gene. — Plant Sci. 155: 1–9, 2000.

    Article  PubMed  CAS  Google Scholar 

  • Sokhansanj, A., Sadat, Noori, S.A., Niknam, V.: Comparison of bacterial and plant genes participating in proline biosynthesis with osmotin gene, with respect to enhancing salinity tolerance of transgenic tobacco plants. — Rus. J. Plant Physiol. 53: 110–115, 2006.

    Article  CAS  Google Scholar 

  • Su, J., Wu, R.: Stress-inducible synthesis of proline in transgenic rice confers faster growth under stress conditions than that with constitutive synthesis. — Plant Sci. 166: 941–948, 2004.

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Tarantino, D., Vannini, C., Bracale, M., Campa, M., Soave, C., Murgia, I.: Antisense reduction of thylakoidal ascorbate peroxidase in Arabidopsis enhances Paraquat-induced photooxidative stress and Nitric Oxide-induced cell death. — Planta 221: 757–765, 2005.

    Article  PubMed  CAS  Google Scholar 

  • Taylor, I.B., Sonneveld, T., Bugg, T.D.H., Thompson, A.J.: Regulation and manipulation of the biosynthesis of abscisic acid, including the supply of xanthophyll precursors. — Plant Growth Regul. 24: 253–273, 2005.

    CAS  Google Scholar 

  • Thompson, A.J., Andrews, J., Mulholland, B.J., McKee, J.M.T., Hilton, H.W., Horridge, J.S., Farquhar, G.D., Smeeton, R.C., Smillie, I.R.A., Black, C.R., Taylor, I.B.: Overproduction of abscisic acid in tomato increases transpiration efficiency and root hydraulic conductivity and influences leaf expansion. — Plant Physiol. 143: 1905–1917, 2007.

    Article  PubMed  CAS  Google Scholar 

  • Thompson, A.J., Jackson, A.C., Parker, R.A., Morpeth, D.R., Burbidge, A., Taylor, I.B.: Abscisic acid biosynthesis in tomato: regulation of zeaxanthin epoxidase and 9-cis-epoxycarotenoid dioxygenase mRNAs by light/dark cycles, water stress and abscisic acid. — Plant mol. Biol. 42: 833–845, 2000.

    Article  PubMed  CAS  Google Scholar 

  • Torii, K.U., Mitsukawa, N., Oosmul, T., Matsuura, Y., Yokoyama, R., Whittier, R.F., Komeda, Y.: The Arabidopsis ERECTA gene encodes a putative receptor protein kinase with extracellular leucine-rich repeats. — Plant Cell 8: 735–746, 1996.

    Article  PubMed  CAS  Google Scholar 

  • Tran, L.S.P., 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  PubMed  CAS  Google Scholar 

  • Tseng, M.J., Liu, C.W., Yiu, J.C.: Enhanced tolerance to sulfur dioxide and salt stress of transgenic Chinese cabbage plants expressing both superoxide dismutase and catalase in chloroplasts. — Plant Physiol. Biochem. 45: 822–833, 2007.

    Article  PubMed  CAS  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. Biotechnol. 17: 113–122, 2006.

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Vendruscolo, E.C.G., Schuster, I., Pileggi, M., Scapim, C.A., Molinari, H.B.C., Marur, C.J., Vieira, L.G.E.: Stress-induced synthesis of proline confers tolerance to water deficit in transgenic wheat. — J. Plant Physiol. 164: 1367–1376, 2007.

    Article  PubMed  CAS  Google Scholar 

  • Vij, S., Tyagi, A.K.: Emerging trends in the functional genomics of the abiotic stress response in crop plants. — Plant Biotechnol. J. 5: 361–380, 2007.

    Article  PubMed  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  PubMed  CAS  Google Scholar 

  • Wang, F., Jiang, Y., Feng, X.C., Xu, L.N., Li, M.T., Liang, H.T., Li, Y.M., Zhu, N., Liu, Y.L., Ma, T.H.: Molecular cloning of a Glycyrrhiza uralensis F. aquaporin GuPIP1 up-regulated in response to drought, salt and ABA stress. — Chem. Res. Chin. Univ. 23: 52–57, 2007a.

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Wang, Y.J., Yu, J.N., Chen, T., Zhang, Z.G., Hao, Y.J., Zhang, J.S., Chen, S.Y.: Functional analysis of a putative Ca2+ channel gene TaTPC1 from wheat. — J. exp. Bot. 56: 3051–3060, 2005.

    Article  PubMed  CAS  Google Scholar 

  • Wang, Y.L., Wang, X.D., Zhao, B., Wang, Y.C.: Reduction of hyperhydricity in the culture of Lepidium meyenii shoots by the addition of rare earth elements. — Plant Growth Regul. 52: 151–159, 2007b.

    Article  CAS  Google Scholar 

  • Wang, Y.N., Liu, C., Li, K.X., Sun, F.F., Hu, H.Z., Li, X., Zhao, Y.K., Han, C.Y., Zhang, W.S., Duan, Y.F., Liu, M.Y.: Arabidopsis EIN2 modulates stress response through abscisic acid response pathway. — Plant Mol. Biol. 64: 633–644, 2007c.

    Article  PubMed  CAS  Google Scholar 

  • Watari, A., Yutsudo, M.: Multi-functional gene ASY/Nogo/RTN-X/RTN4: Apoptosis, tumor suppression, and inhibition of neuronal regeneration. — Apoptosis 8: 5–9, 2003.

    Article  PubMed  CAS  Google Scholar 

  • Wu, C.A., Yang, G.D., Meng, Q.W., Zheng, C.C.: The cotton GhNHX1 gene encoding a novel putative tonoplast Na+/H+ antiporter plays an important role in salt stress. — Plant Cell Physiol. 45: 600–607, 2004.

    Article  PubMed  CAS  Google Scholar 

  • Wu, W., Su, Q., Xia, X.Y., Wang, Y., Luan, Y.S., An, L.J.: The Suaeda liaotungensis kitag betaine aldehyde dehydrogenase gene improves salt tolerance of transgenic maize mediated with minimum linear length of DNA fragment. — Euphytica 159: 17–25, 2008.

    Article  CAS  Google Scholar 

  • Xiong, L., Zhu, J.K.: Molecular and genetic aspects of plant responses to osmotic stress. — Plant Cell Environ. 25: 131–139, 2002.

    Article  PubMed  CAS  Google Scholar 

  • Xiong, L.M., Zhu, J.K.: Abiotic stress signal transduction in plants: molecular and genetic perspectives. — Physiol. Plant. 112: 152–157, 2001.

    Article  PubMed  CAS  Google Scholar 

  • Xu, D.P., Duan, X., Wang, B.: Expression of a late embryo- genesis abundant protein gene, HAV1, from barley confers tolerance to water deficit and salt stress in transgenic rice. — Plant Physiol. 110: 249–257, 1996.

    PubMed  CAS  Google Scholar 

  • Xu, L., Xu, Y., Dong, A., Sun, Y., Pi, L., Xu, Y., Huang, H.: Novel as1 and as2 defects in leaf adaxial-abaxial polarity reveal the requirement for ASYMMETRIC LEAVES1 and 2 and ERECTA functions in specifying leaf adaxial identity. — Development 130: 4097–4107, 2003.

    Article  PubMed  CAS  Google Scholar 

  • Xue, Z.Y., Zhi, D.Y., Xue, G.P., Zhang, H., Zhao, Y.X., Xia, G.M.: Enhanced salt tolerance of transgenic wheat (Triticum aestivum L.) expressing a vacuolar Na+/H+ antiporter gene with improved grain yields in saline soils in the field and a reduced level of leaf Na+. — Plant Sci. 167: 849–859, 2004.

    Article  CAS  Google Scholar 

  • Yadav, R., Courtois, B., Huang, N., McLaren, G.: Mapping genes controlling root morphology and root distribution in a doubled-haploid population of rice. — Theor. appl. Genet. 94: 619–632, 1997.

    Article  CAS  Google Scholar 

  • Yang, C.Y., Chen, Y.C., Jauh, G.Y., Wang, C.S.: A lily ASR protein involves abscisic acid signaling and confers drought and salt resistance in Arabidopsis. — Plant Physiol. 139: 836–846, 2005a.

    Article  PubMed  CAS  Google Scholar 

  • Yang, X.H., Liang, Z., Lu, C.M.: Genetic engineering of the biosynthesis of glycinebetaine enhances photosynthesis against high temperature stress in transgenic tobacco plants. — Plant Physiol. 138: 2299–2309, 2005b.

    Article  PubMed  CAS  Google Scholar 

  • Yang, X.H., Liang, Z., Wen, X.G., Lu, C.M.: Genetic engineering of the biosynthesis of glycine betaine leads to increased tolerance of photosynthesis to salt stress in transgenic tobacco plants. — Plant mol. Biol. 66: 73–86, 2008.

    Article  PubMed  CAS  Google Scholar 

  • Ying, N., Tachiiri, Y., Tsuchiya, H., Hua, Y.: Responses of tiller growth and related genes expression in rice to red and blue radiation. — Biol. Plant. 53: 188–190, 2009.

    Article  CAS  Google Scholar 

  • Yu, Q.J., Hu, Y.L., Li, J.F., Wu, Q., Lin, Z.P.: Sense and antisense expression of plasma membrane aquaporin BnPIP1 from Brassica napus in tobacco and its effects on plant drought resistance. — Plant Sci. 169: 647–656, 2005.

    Article  CAS  Google Scholar 

  • Zhang, J.Y., Broeckling, C.D., Blancaflor, E.B., Sledge, M.K., Sumner, L.W., Wang, Z.Y.: Overexpression of WXP1, a putative Medicago truncatula AP2 domain-containing transcription factor gene, increases cuticular wax accumulation and enhances drought tolerance in transgenic alfalfa (Medicago sativa). — Plant J. 42: 689–707, 2005a.

    Article  PubMed  CAS  Google Scholar 

  • Zhang, J.Y., Broeckling, C.D., Blancaflor, E.B., Sledge, M.K., Sumner, L.W., Wang, Z.Y.: Heterologous expression of two Medicago truncatula putative ERF transcription factor genes, WXP1 and WXP2, in Arabidopsis led to increased leaf wax accumulation and improved drought tolerance, but differential response in freezing tolerance. — Plant mol. Biol. 64: 265–278, 2007a.

    Article  PubMed  CAS  Google Scholar 

  • Zhang, W.X., Ruan, J.H., Ho, T.H.D., You, Y.S., Yu, T.T., Quatrano, R.S.: Cis-regulatory element based targeted gene finding: genome-wide identification of abscisic acid- and abiotic stress-responsive genes in Arabidopsis thaliana. — Bioinformatics. 21: 3074–3081, 2005b.

    Article  PubMed  CAS  Google Scholar 

  • Zhang, Z.B., Shao, H.B., Xu, P., Chu, L.Y., Lu, Z.H., Tian, J.Y.: On evolution and perspectives of bio-water-saving. — Colloid Surface Biointerfaces 55: 1–7, 2007b.

    Article  CAS  Google Scholar 

  • Zhang, Z.B., Shan, L.: [Studies on relationship between drought resistance physiological traits and leaf curl degree and wax of wheat.] — Acta agron. sin. 24: 608–612, 1998. [In Chin.]

    CAS  Google Scholar 

  • Zhang, Z.B., Xu, P., Zhang, J.H., Wang, J.: [Advance on study of molecular marker and gene cloning and transgenes in drought resistance and water saving in crops.] — Acta bot. boreali-occid. sin. 22: 1537–1544, 2002. [In Chin.]

    CAS  Google Scholar 

  • Zhao, F.Y., Wang, Z.L., Zhang, Q., Zhao, Y.X., Zhang, H.: Analysis of the physiological mechanism of salt-tolerant transgenic rice carrying a vacuolar Na +/H + antiporter gene from Suaeda salsa. — J. Plant Res. 119: 95–104, 2006.

    Article  PubMed  CAS  Google Scholar 

  • Zhu, B., Su, J., Chang, M., Verma, D.P.S., Fan, Y.L., Wu, R.: Overexpression of a D1-pyrroline-5- carboxylate synthetase gene and analysis of tolerance to water- and salt-stress in transgenic rice. — Plant Sci. 139: 41–48, 1998.

    Article  CAS  Google Scholar 

  • Zhuang, Y.L., Ren, G.J., Zhu, Y., Hou, G.H., Qu, X., Li, Z.X., Yue, G.D., Zhang, J.R.: Transcriptional profiles of immature ears and tassels in maize at early stage of water stress. — Biol. Plant. 52: 754–758, 2008.

    Article  CAS  Google Scholar 

Download references

Acknowledgement

This work is supported by the High-Tech Research and Development Program of China (Grant No. 2006AA100201), the National Key Technology R&D Program of China (Grant No. 2006BAD29B02, 2009BADA3B01), the Excellent Middle-aged or Young Scientists from Shandong Province (BS2009DX028) and the College Foundation from Shandong Province (J09LG82).

Author information

Authors and Affiliations

  1. Center for Agricultural Resources Research, Institute of Genetic and Developmental Biology, CAS, Shijiazhuang, 050021, P.R. China

    X. J. Hu, Z. B. Zhang, P. Xu, Z. Y. Fu & W. Y. Song

  2. Linyi Normal University, Linyi, 276005, P.R. China

    X. J. Hu & S. B. Hu

  3. Graduate University of the Chinese Academy of Sciences, Beijing, 100049, P.R. China

    X. J. Hu, Z. Y. Fu & W. Y. Song

  4. Xinjiang Institute of Physics and Chemistry Technology, CAS, Wulumuqi, 830011, P.R. China

    Z. Y. Fu

  5. Shangqiu Normal University, Shangqiu, 476000, P.R. China

    W. Y. Song

Authors
  1. X. J. Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Z. B. Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. P. Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Z. Y. Fu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. S. B. Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. W. Y. Song
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to X. J. Hu or Z. B. Zhang.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hu, X.J., Zhang, Z.B., Xu, P. et al. Multifunctional genes: the cross-talk among the regulation networks of abiotic stress responses. Biol Plant 54, 213–223 (2010). https://doi.org/10.1007/s10535-010-0039-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10535-010-0039-6

Additional key words

Search

Navigation