Plant abiotic stress: a prospective strategy of exploiting promoters as alternative to overcome the escalating burden

Figures & data

Table 1. Constitutive overexpression of stress-responsive genes in transgenic results in growth abnormalities.

Gene	Source	Host	Promoter	Comments	Reference
CBF1	Arabidopsis	cv. umatilla	CaMV35S	Negative phenotypes, including smaller leaves, stunted growth, delayed flower and reduction or lack of tuber production	Pino et al. (2007)
CBF2
CBF3
GUS		Tobacco	AAP2 under influence of CaMV35S	Exhibited twofold to fivefold increase in AAP2 promoter activity and becomes active in all tissue types whereas the AAP2 promoter is active only in the vascular tissue	Zheng et al. (2007)
iaaM			AGL5 under influence of CaMV35S	AGL5:iaa5 showed a wild-type phenotype except seedless fruit whereas CaMV35S:iaa5 showed drastic morphological alternation in non-ovary organs including roots, stem and flowers
Barnase			PAB5under influence of CaMV35S	Drastically reduced transformation efficiency, expression of barnase gene in non-reproductive organ such as calli, shoot primordia whereas PAB5 is the pollen-ovule and early embryo specific promoter
CaXTH	Hot pepper	Arabidopsis	CaMV35S	Exhibited abnormal leaf morphology, twisted and bending edge. Improved tolerance to severe water deficit and lesser extent to high salinity in comparison to wild type	Cho et al. (2006)
DREB1A	Arabidopsis	D. Grandiflorum	CaMV35S	Compared with wild type severe growth retardation was observed	Hong et al. (2006)
DREB1A	O. sativa	Rice	CaMV35S	Improved tolerance to drought, high salt and low temperature. Growth retardation under normal growth conditions	Ito et al. (2006)
DREB1A	Arabidopsis	Tobacco	CaMV35S	Severe growth retardation, tolerance to drought, freezing than control plant	Kasuga et al. (2004)
DREB1A	Oryza sativa	Arabidopsis	CaMV35S	Tolerance to drought, high salt and cold stress, showed mild growth retardation, especially in bolting timing	Dubouzet et al. (2003)
DREB1	T. astivum	Rice	CaMV35S	Suggest that TaDREB1 functions as a DRE-binding transcription factor in wheat and TaDREB1 gene under an unstressed condition causing a dwarf phenotype	Shen et al. (2003)
PIP1b	Arabidopsis	Tobacco	CaMV35S	Significantly increased plant growth under normal conditions, but the plants were more sensitive to drought stress	Aharon et al. (2003)
mltD	E. coli	Wheat	Ubiquitin	had severe abnormalities including sterility, stunted growth, twisted heads and curled leaves	Abebe et al. (2003)
CBF4	Arabidopsis	Arabidopsis	CaMV35S	Plants are more tolerant to freezing and drought stress but CBF4 expression caused the most severe growth phenotype	Haake et al. (2002)
CBF1	Arabidopsis	Tomato	CaMV35S	Exhibited pattern of growth retardation, but resumed the growth after GA3 treatment, also exhibited tolerance against chilling and oxidative stress	Hsieh et al. (2002b)
ABF3		Arabidopsis	CaMV35S	Exhibited mild growth retardation in the arial parts, petioles were slightly shorter and leaves were rounder	Kang et al. (2002)
ABF4				Severe growth retardation, petioles were shorter, leaves were smaller and flowering was delayed
mltD and IMT		N. tabacum	CaMV35S	Had abnormal flower development and reduced sugar content	Sheveleva et al. (2000)
CBF3	Arabidopsis	Arabidopsis	CaMV35S	Increases the freezing tolerance of cold-acclimated plants, had a ‘dwarf’ phenotype	Gilmour et al. (2000)
Adc		Oryza sativa	CaMV35S	High levels of Adc gene expression and inability of callus tissue to develop normally into differentiated plant	Capell et al. (1998)
Stpd1	Apple	Tobacco	CaMV35S	Resulted in necrosis and sterility	Sheveleva et al. (1998)
TPS1	S. cereviaseae	N. tabacum	CaMV35S	Improved drought stress, exhibited stunted growth lancet-shaped leaves, reduced sugar content	Romero et al. (1997)
mtlD		Tobacco	CaMV35S	Transgenics were 20–25% smaller in size and had reduced sucrose compared with wild type	Karakas et al. (1997)
TPS1	S. cereviaseae	Tobacco	CaMV35S	Stunted growth, lancet-shaped leaves, reduced sucrose content and altered stem morphology	Pilon-Smits et al. (1998)
otsA and otsB	E. coli	N. tabacum S. tuberosum	CaMV35S	Results in severely stunted growth	Goddijn et al. (1997)

Table 2. Stress-inducible over expression of stress-responsive genes in transgenic results in stress tolerant with overcoming the problem of growth retardation/abnormalities.

Gene	Source	Host	Promoter	Comments	Reference
Osmotin	Tobacco	Mulberry	RD29A	More responsive to drought	Das et al. (2010)
DREB1C	M. truncatula	China Rose (R. chinensis)	RD29A	Performance under freezing stress was superior. Transgenic plant phenotypically normal and flowered	Chen et al. (2010)
IDEF1	Rice	Rice	IDS2	Exhibited tolerance to iron deficiency in both hydroponic culture and calcareous soil	Kobayashi et al. (2010)
CBF3		Rice Arabidopsis	HVA22	Significantly higher yield per plant and had higher spikelet fertility than WT, and showed relatively better effect in improving drought resistance of transgenic rice under field conditions	Xiao et al. (2009)
SOS2
NPK1
LOS5
ZAT10
WRKY11	Rice	Rice cultivar Sasanishiki	HSP101	Showed significant heat and drought tolerance, as indicated by the slower leaf-wilting and less-impaired survival rate of green parts of plants	Wu et al. (2009)
DREB1	soybean (Glycine max)f	Alfalfa (Medicago sativa)	RD29A	Significantly higher salt tolerance as measured by ion leakage, chlorophyll fluorescence value, contents of free proline and total soluble sugars; additionally, transcript level of P5CS was up-regulated	Jin et al. (2010)
Bnlea4-1	B. napus	Arabidopsis	RD29A	Enhanced drought tolerance	Dalal et al (2009)
OsLEA3-1	Rice	Rice	OsLEA3-1	Significantly higher relative yield	Xiao et al. (2007)
Rab16A	Rice	Rice	Rab16A	Conferring salt tolerance without affecting growth and yield	RoyChoudhury et al. (2007)
codA	A. globiformis	S. tuberosum	SWPA2	Maintained higher water contents and accumulated higher levels of vegetative biomass	Ahmad et al. (2008)
CBF1	Arabidopsis	cv. Umatilla	RD29A	Restore tuber production to levels similar to wild-type plants and imparting same level of freezing tolerance as the 35S version	Pino et al. (2007)
CBF2
CBF3
DREB1A	Arabidopsis	Peanut (hypogea)	RD29A	No growth retardation or visible phenotypic alternation and achieved higher transpiration efficiency (TE) under water-limiting conditions than the untransformed control	Bhatnagar-Mathur et al. (2008)
DREB1A	Arabidopsis	Bahiagrass (P. notatum)	HVA1	No compromised plant productivity, performance and fertility under non-stress conditions. Enhanced survival and biomass production under severe dehydration and salt stress compared to wild-type plants	James et al. (2008)
OsNAC6	Rice	Rice	OsNAC6	Stress-inducible over expression of OsNAC6 in rice can improve stress tolerance by suppressing the negative effects of OsNAC6 on growth under normal growth conditions	Nakashima et al. (2007)
TPS1	S. cerevisiae	Tobacco	RBCS1A	Enhanced drought tolerance but caused growth aberrations of the green plant and root abnormalities. Shunted growth, slowly growing plants with lancent-shaped leaves	Karim et al. (2007)
DREB1A	Zea mays	A. thaliana	RD29A	Play a dual functional role in mediating the expression of genes responsive to both water and heat stress	Qin et al. (2007)
DREB1A	Arabidopsis	D. Grandiflorum	RD29A	No growth retardation on RD29A:DREB1A plants, exhibited significant stronger tolerance to drought and salt stress than 35S:DREB1A plants. Proline content and SOD activity were increased inductively in RD29A; DREB1A plants	Hong et al. (2006)
DREB1A	Arabidopsis	Potato	RD29A	Improved the dehydration salt and freezing tolerance with overcoming the problem of growth retardation	Behnam et al. (2007)
ERA1 antisense			RD29A	More resistance to water deficit-induced seed abortion during flowering and with adequate water. Transgenic canola produce same amount of seeds as the parental control. Under moderate drought stress at flowering, the seeds yield of transgenic canola was significant higher than the control	Wang et al. (2005)
DREB1A	Arabidopsis	Bread wheat	RD29A	Sustainable resistance to H2O stress in comparison with checks under experimental green house conditions, manifested by a 10-day delay in wilting when water was withheld	Pellegrineschi et al. (2004)
otsA and otsB	E.Coli	Rice	ABRC1	After prolonged exposure to salt stress, almost all of transgenic plants survived and displayed vigorous root and shoot growth	Garg et al. (2002)
P5CS	V. conitifolia	Rice	APIC	Showed significantly higher tolerance to stress produced by high levels of NaCl or water deficiency as judged by faster growth of shoots and roots in comparison with non-transformed plants	Su and Wu (2004)
DREB1A	Arabidopsis	Tobacco	RD29A	Exhibited slightly growth retardation, showed higher tolerance to drought and freezing than the wt plants	Kasuga et al. (2004)
CBF1	Arabidopsis	Tomato	ABRC	Exhibited enhanced tolerance to chilling water deficit and salt stress, minimizing the negative effects in transgenic tomato plants pertaining to growth and yield compared with the use of CaMV35S	Lee et al. (2003)
DREB1A	Arabidopsis	Arabidopsis	RD29A	Exhibited enhanced tolerance to chilling, drought and salt stress. Also solved the problem of growth retardation	Kasuga et al. (1999)

Pino MT, Skinner JS, Park EJ, Jeknic Z, Hayes PM, Thomashow MF, Chen TH. 2007. Use of a stress inducible promoter to drive ectopic AtCBF expression improves potato freezing tolerance while minimizing negative effects on tuber yield. Plant Biotechnol J. 5:591–604. doi: 10.1111/j.1467-7652.2007.00269.x

 PubMed Web of Science ®Google Scholar

Zheng X, Deng W, Luo K, Duan H, Chen Y, McAvoy R, Song S, Pei Y, Li Y. 2007. The cauliflower mosaic virus (CaMV) 35S promoter sequence alters the level and patterns of activity of adjacent tissue- and organ-specific gene promoters. Plant Cell Rep. 26:1195–1203. doi: 10.1007/s00299-007-0307-x

 PubMed Web of Science ®Google Scholar

Cho SK, Kim JE, Park JA, Eom TJ, Kim WT. 2006. Constitutive expression of abiotic stress-inducible hot pepper CaXTH3, which encodes a xyloglucan endotransglucosylase/hydrolase homolog, improves drought and salt tolerance in transgenic Arabidopsis plants. FEBS Lett. 580:3136–3144. doi: 10.1016/j.febslet.2006.04.062

 PubMed Web of Science ®Google Scholar

Hong B, Tong Z, Ma N, Li J, Kasuga M, Yamaguchi-Shinozaki K, Gao J. 2006. Heterologous expression of the AtDREB1A gene in chrysanthemum increases drought and salt stress tolerance. Sci China C Life Sci. 49:436–445. doi: 10.1007/s11427-006-2014-1

 PubMedGoogle Scholar

Ito Y, Katsura K, Maruyama K, Taji T, Kobayashi M, Seki M, Shinozaki K, Yamaguchi-Shinozaki K. 2006. Functional analysis of rice DREB1/CBF-type transcription factors involved in cold-responsive gene expression in transgenic rice. Plant Cell Physiol. 47:141–153. doi: 10.1093/pcp/pci230

 PubMed Web of Science ®Google Scholar

Kasuga M, Miura S, Shinozaki K, Yamaguchi-Shinozaki K. 2004. A combination of the Arabidopsis DREB1A gene and stress-inducible rd29A promoter improved drought- and low-temperature stress tolerance in tobacco by gene transfer. Plant Cell Physiol. 45:346–350. doi: 10.1093/pcp/pch037

 PubMed Web of Science ®Google Scholar

Dubouzet JG, Sakuma Y, Ito Y, Kasuga M, Dubouzet EG, Miura S, Seki M, Shinozaki K, Yamaguchi-Shinozaki K. 2003. OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high-salt- and cold-responsive gene expression. Plant J. 33:751–763. doi: 10.1046/j.1365-313X.2003.01661.x

 PubMed Web of Science ®Google Scholar

Shen YG, Zhang WK, Yan DQ, Du BX, Zhang JS, Liu Q, Chen SY. 2003. Characterization of a DRE-binding transcription factor from a halophyte Atriplex hortensis. Theor Appl Genet. 107:155–161.

 PubMed Web of Science ®Google Scholar

Aharon R, Shahak Y, Wininger S, Bendov R, Kapulnik Y, Galili G. 2003. Overexpression of a plasma membrane aquaporin in transgenic tobacco improves plant vigor under favorable growth conditions but not under drought or salt stress. Plant Cell. 15:439–447. doi: 10.1105/tpc.009225

 PubMed Web of Science ®Google Scholar

Abebe T, Guenzi AC, Martin B, Cushman JC. 2003. Tolerance of mannitol-accumulating transgenic wheat to water stress and salinity. Plant Physiol. 131:1748–1755. doi: 10.1104/pp.102.003616

 PubMed Web of Science ®Google Scholar

Haake V, Cook D, Riechmann JL, Pineda O, Thomashow MF, Zhang JZ. 2002. Transcription factor CBF4 is a regulator of drought adaptation in Arabidopsis. Plant Physiol. 130:639–648. doi: 10.1104/pp.006478

 PubMed Web of Science ®Google Scholar

Hsieh TH, Lee JT, Yang PT, Chiu LH, Charng YY, Wang YC, Chan MT. 2002b. 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. doi: 10.1104/pp.003442

 PubMed Web of Science ®Google Scholar

Kang JY, Choi HI, Im MY, Kim SY. 2002. Arabidopsis basic leucine zipper proteins that mediate stress-responsive abscisic acid signaling. Plant Cell. 14:343–357. doi: 10.1105/tpc.010362

 PubMed Web of Science ®Google Scholar

Sheveleva EV, Jensen RG, Bohnert HJ. 2000. Disturbance in the allocation of carbohydrates to regenerative organs in transgenic Nicotiana tabacum L. J Exp Bot. 51:115–122. doi: 10.1093/jexbot/51.342.115

 PubMed Web of Science ®Google Scholar

Gilmour SJ, Sebolt AM, Salazar MP, Everard JD, Thomashow MF. 2000. Over-expression of the Arabidopsis CBF3 transcriptional activator mimics multiple biochemical changes associated with cold acclimation. Plant Physiol. 124:1854–1865. doi: 10.1104/pp.124.4.1854

 PubMed Web of Science ®Google Scholar

Capell T, Escobar C, Liu H, Burtin D, Lepri O, Christou P. 1998. Over-expression of the oat arginine decarboxylase cDNA in transgenic rice (Oryza sativa L.) affects normal development patterns in vitro and results in putrescine accumulation in transgenic plants. Theo Appl Gen. 97:246–254. doi: 10.1007/s001220050892

 Web of Science ®Google Scholar

Sheveleva EV, Marquez S, Chmara W, Zegeer A, Jensen RG, Bohnert HJ. 1998. Sorbitol-6-phosphate dehydrogenase expression in transgenic tobacco. High amounts of sorbitol lead to necrotic lesions. Plant Physiol. 117:831–839. doi: 10.1104/pp.117.3.831

 PubMed Web of Science ®Google Scholar

Romero C, Belles JM, Vaya JL, Serrano R, Culianez-Macia FA. 1997. Expression of the yeast trehalose-6-phosphate synthase gene in transgenic tobacco plants: pleiotropic phenotypes include drought tolerance. Planta. 201:293–297. doi: 10.1007/s004250050069

 PubMed Web of Science ®Google Scholar

Karakas B, Ozias-Akins P, Stushnoff C, Suefferheld M, Rieger M. 1997. Salinity and drought tolerance of mannitol-accumulating transgenic tobacco. Plant Cell Environ. 20:609–616. doi: 10.1111/j.1365-3040.1997.00132.x

 Web of Science ®Google Scholar

Pilon-Smits EAH, Terry N, Sears T, Kim H, Zayed A, Hwang S, VanDun K, Voogd E, Verwoerd TC, Krutwagen RW, Goddijn OJM. 1998. Trehalose-producing transgenic tobacco plants show improved growth performance under drought stress. J Plant Physiol. 152:525–532. doi: 10.1016/S0176-1617(98)80273-3

 Web of Science ®Google Scholar

Goddijn OJ, Verwoerd TC, Voogd E, Krutwagen RW, de Graaf PT, VanDun K, Poels J, Ponstein AS, Damm B, Pen J. 1997. Inhibition of trehalase activity enhances trehalose accumulation in transgenic plants. Plant Physiol. 113:181–190. doi: 10.1104/pp.113.1.181

 PubMed Web of Science ®Google Scholar

Das M, Chauhan H, Chhibbar A, Haq QMR, Khurana P. 2010. High-efficiency transformation and selective tolerance against biotic and abiotic stress in mulberry, Morus indica cv. K2, by constitutive and inducible expression of tobacco osmotin. Transgenic Res. 20:231–246. doi: 10.1007/s11248-010-9405-6

 PubMed Web of Science ®Google Scholar

Chen JR, Lu JJ, Liu R, Xiong XY, Wang TX, Chen SY, Guo LB, Wang HF. 2010. DREB1C from Medicago truncatula enhances freezing tolerance in transgenic M. truncatula and China Rose (Rosa chinensis Jacq.). Plant Growth Reg. 60:199–211. doi: 10.1007/s10725-009-9434-4

 Web of Science ®Google Scholar

Kobayashi T, Nakanishi H, Nishizawa NK. 2010. Dual regulation of iron deficiency response mediated by the transcription factor IDEF1. Plant Signal Behav. 5:157–159. doi: 10.4161/psb.5.2.10459

 PubMedGoogle Scholar

Xiao BZ, Chen X, Xiang CB, Tang N, Zhang QF, Xiong LZ. 2009. Evaluation of seven function-known candidate genes for their effects on improving drought resistance of transgenic rice under field conditions. Mol Plant. 2: 73–83. doi: 10.1093/mp/ssn068

 PubMed Web of Science ®Google Scholar

Wu X, Shiroto Y, Kishitani S, Ito Y, Toriyama K. 2009. Enhanced heat and drought tolerance in transgenic rice seedlings overexpressing OsWRKY11 under the control of HSP101 promoter. Plant Cell Rep. 28:21–30. doi: 10.1007/s00299-008-0614-x

 PubMed Web of Science ®Google Scholar

Jin T, Chang Q, Li W, Yin D, Li Z, Wang D, Liu B, Liu L. 2010. Stress-inducible expression of GmDREB1 conferred salt tolerance in transgenic alfalfa. Plant Cell, Tissue and Organ Culture. 100:219–227. doi: 10.1007/s11240-009-9628-5

 Web of Science ®Google Scholar

Dalal M, Tayal D, Chinnusamy V, Bansal KC. 2009. Abiotic stress and ABA-inducible Group 4 LEA from Brassica napus plays a key role in salt and drought tolerance. J Biotechnol. 139:137–145. doi: 10.1016/j.jbiotec.2008.09.014

 PubMed Web of Science ®Google Scholar

Xiao B, Huang Y, Tang N, Xiong L. 2007. Over-expression of a LEA gene in rice improves drought resistance under the field conditions. Theo App Gen. 115:35–46. doi: 10.1007/s00122-007-0538-9

 PubMed Web of Science ®Google Scholar

RoyChoudhury A, Roy C, Sengupta DN. 2007. Transgenic tobacco plants overexpressing the heterologous lea gene Rab16A from rice during high salt and water deficit display enhanced tolerance to salinity stress. Plant Cell Rep. 26:1839–1859. doi: 10.1007/s00299-007-0371-2

 PubMed Web of Science ®Google Scholar

Ahmad R, Kim MD, Back KH, Kim HS, Lee HS, Kwon SY, Murata N, Chung WI, Kwak SS. 2008. Stress-induced expression of choline oxidase in potato plant chloroplasts confers enhanced tolerance to oxidative, salt, and drought stresses. Plant Cell Rep. 27:687–698. doi: 10.1007/s00299-007-0479-4

 PubMed Web of Science ®Google Scholar

Bhatnagar-Mathur P, Devi MJ, Reddy DS, Lavanya M, Vadez V, Serraj R, Yamaguchi-Shinozaki K, Sharma KK. 2008. Stress-inducible expression of At DREB1A in transgenic peanut (Arachis hypogaea L.) increases transpiration efficiency under water-limiting conditions. Plant Cell Rep. 26:2071–2082. doi: 10.1007/s00299-007-0406-8

 Web of Science ®Google Scholar

James VA, Neibaur I, Altpeter F. 2008. Stress inducible expression of the DREB1A transcription factor from xeric, Hordeum spontaneum L. in turf and forage grass (Paspalum notatum Flugge) enhances abiotic stress tolerance. Trans Res. 17:93–104. doi: 10.1007/s11248-007-9086-y

 PubMed Web of Science ®Google Scholar

Nakashima K, Tran LS, Van Nguyen D, Fujita M, Maruyama K, Todaka D, Ito Y, Hayashi N, Shinozaki K, Yamaguchi-Shinozaki K. 2007. Functional analysis of a NAC-type transcription factor OsNAC6 involved in abiotic and biotic stress-responsive gene expression in rice. Plant J. 51:617–630. doi: 10.1111/j.1365-313X.2007.03168.x

 PubMed Web of Science ®Google Scholar

Karim S, Aronsson H, Ericson H, Pirhonen M, Leyman B, Welin B, Mantyla E, Palva ET, VanDijck P, Holmstrom KO. 2007. Improved drought tolerance without undesired side effects in transgenic plants producing trehalose. Plant Mol Biol. 64:371–386. doi: 10.1007/s11103-007-9159-6

 PubMed Web of Science ®Google Scholar

Qin F, Kakimoto M, Sakuma Y, Maruyama K, Osakabe Y, Tran LSP, Shinozaki K, Yamaguchi-Shinozaki K. 2007. Regulation and functional analysis of ZmDREB2A in response to drought and heat stresses in Zea mays L. Plant J. 50:54–69. doi: 10.1111/j.1365-313X.2007.03034.x

 PubMed Web of Science ®Google Scholar

Behnam B, Kikuchi A, Celebi-Toprak F, Kasuga M, Yamaguchi-Shinozaki K, Watanabe KN. 2007. Arabidopsis rd29A: DREB1A enhances freezing tolerance in transgenic potato. Plant Cell Rep. 26:1275–1282. doi: 10.1007/s00299-007-0360-5

 PubMed Web of Science ®Google Scholar

Wang Y, Ying J, Kuzma M, Chalifoux M, Sample A, McArthur C, Uchacz T, Sarvas C, Wan J, Dennis DT, et al. 2005. Molecular tailoring of farnesylation for plant drought tolerance and yield protection. Plant J. 43:413–424. doi: 10.1111/j.1365-313X.2005.02463.x

 PubMed Web of Science ®Google Scholar

Pellegrineschi A, Reynolds M, Pacheco M, Brito RM, Almeraya R, Yamaguchi-Shinozaki K, Hoisington D. 2004. Stress-induced expression in wheat of the Arabidopsis thaliana DREB1A gene delays water stress symptoms under greenhouse conditions. Genome. 47:493–500. doi: 10.1139/g03-140

 PubMed Web of Science ®Google Scholar

Garg AK, Kim JK, Owens TG, Ranwala AP, Choi YD, Kochian LV, Wu J. 2002. Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses. Proc Natl Acad Sci USA. 99:15898–15903. doi: 10.1073/pnas.252637799

 PubMed Web of Science ®Google Scholar

Su J, Wu R. 2004. Stress-inducible synthesis of proline in transgenic rice confers faster growth under stress conditions than that with constitutive synthesis. Plant Sci. 166: 941–948. doi: 10.1016/j.plantsci.2003.12.004

 Web of Science ®Google Scholar

Lee JT, Prasad V, Yang PT, Wu JF, Ho THD, Charng YY, Chan MT. 2003. Expression of Arabidopsis CBF1 regulated by an ABA/stress inducible promoter in transgenic tomato confers stress tolerance without affecting yield. Plant Cell Environ. 26:1181–1190. doi: 10.1046/j.1365-3040.2003.01048.x

 Web of Science ®Google Scholar

Kasuga M, Liu Q, Miura S, Yamaguchi-Shinozaki K, Shinozaki K. 1999. Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat Biotechnol. 17:287–291. doi: 10.1038/7036

 PubMed Web of Science ®Google Scholar