Skip to main content
Log in

ABP9, a maize bZIP transcription factor, enhances tolerance to salt and drought in transgenic cotton

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main conclusion

ABP9 , encoding a bZIP transcription factor from maize, enhances tolerance to multiple stresses and may participate in the ABA signaling pathway in transgenic cotton by altering physiological and biochemical processes and stress-related gene expression.

Abiotic stresses, such as soil salinity and drought, negatively affect growth, development, and yield in cotton. Gene ABP9, which encodes a bZIP transcription factor, binds to the abscisic acid (ABA)-responsive-element (ABRE2) motif of the maize catalase1 gene. Its expression significantly improves tolerance in Arabidopsis to multiple abiotic stresses, but little is known about its role in cotton. In the present study, the ABP9 gene was introduced into upland cotton (Gossypium hirsutum L.) cultivar R15 by Agrobacterium tumefaciens-mediated transformation, and 12 independent transgenic cotton lines were obtained. Cotton plants over-expressing ABP9 have enhanced tolerance to salt and osmotic stress. Under stress, they developed better root systems in a greenhouse and higher germination, reduced stomatal aperture, and stomatal density in a growth chamber. Under drought conditions, survival rate and relative water content (RWC) of transgenic cotton were higher than those of R15 plants. Under salt and osmotic stresses, chlorophyll, proline, and soluble sugar contents significantly increased in transgenic cotton leaves and the malondialdehyde (MDA) content was lower than in R15. Overexpression of ABP9 also enhanced oxidative stress tolerance, reduced cellular levels of reactive oxygen species (ROS) through increased activities of antioxidative enzymes, and alleviated oxidative damage to cell. Interestingly, ABP9 over-expressing cotton was more sensitive to exogenous ABA than R15 at seed germination, root growth, stomatal aperture, and stomatal density. Moreover, ABP9 overexpression upregulated significantly the transcription levels of stress-related genes such as GhDBP2, GhNCED2, GhZFP1, GhERF1, GhHB1, and GhSAP1 under salt treatment. Conjointly, these results showed that overexpression of ABP9 conferred enhanced tolerance to multiple abiotic stresses in cotton. The stress-tolerant transgenic lines provide valuable resources for cotton breeding.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

ABA:

Abscisic acid

ABP9:

ABA-responsive-element-binding protein 9

ABRE:

ABA-responsive elements

MDA:

Malondialdehyde

MV:

Methyl viologen

ROS:

Reactive oxygen species

RWC:

Relative water content

SWC:

Soil water content

References

  • Abdurakhmonov IY, Ayubov MS, Ubaydullaeva KA, Buriev ZT, Shermatov SE, Ruziboev HS, Shapulatov UM, Saha S, Ulloa M, Yu JZ, Percy RG, Devor EJ, Sharma GC, Sripathi VR, Kumpatla SP, van der Krol A, Kater HD, Khamidov K, Salikhov SI, Jenkins JN, Abdukarimov A, Pepper AE (2016) RNA interference for functional genomics and improvement of cotton (Gossypium sp.). Front Plant Sci 7:202

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Arnon D (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Bates L, Waldren R, Teare I (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  • Bohnert HJ, Nelson DE, Jensenayb RG (1995) Adaptations to environmental stresses. Plant Cell 7:1099–1111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cao YJ, Wei Q, Liao Y, Song HL, Li X, Xiang CB, Kuai BK (2009) Ectopic overexpression of AtHDG11 in tall fescue resulted in enhanced tolerance todrought and salt stress. Plant Cell Rep 28:579–588

    Article  CAS  PubMed  Google Scholar 

  • Cattivelli L, Rizza F, Badeck FW, Mazzucotelli E, Mastrangelo AM, Francia E, Marè C, Tondelli A, Stanca AM (2008) Drought tolerance improvement in crop plants: an integrated view from breeding to genomics. Field Crop Res 105:1–14

    Article  Google Scholar 

  • de Souza AMS, Batista VGL, Pinheiro MPN, Suassuna JF, de Lima LM, Fernandes PD (2016) Expression of NCED gene in colored cotton genotypes subjected to water stress. Rev Bras Eng Agríc Ambient 20:692–696

    Article  Google Scholar 

  • Ding LY, Zhang W, Wang JC, Tian LL, Li NN, Qi Guo, Yang SM, He ML, Guo WZ (2014) Overexpression of a Gossypium hirsutum stress-associated protein gene (GhSAP1) improves salt stress tolerance in transgenic tobacco. Sci Agric Sin 47:1458–1470 (in Chinese with English abstract)

    CAS  Google Scholar 

  • Dong CJ, Huang B, Liu JY (2010) The cotton dehydration-responsive element binding protein GhDBP1 contains an EAR-motif and is involved in the defense response of Arabidopsis to salinity stress. Funct Plant Biol 37:64–73

    Article  CAS  Google Scholar 

  • Fryer MJ, Oxborough K, Mullineaux PM, Baker NR (2002) Imaging of photo-oxidative stress responses in leaves. J Exp Bot 53:1249–1254

    CAS  PubMed  Google Scholar 

  • Gao SQ, Chen M, Xu ZS, Zhao CP, Li L, Xu HJ, Tang YM, Zhao X, Ma YZ (2011) The soybean GmbZIP1 transcription factor enhances multiple abiotic stress tolerances in transgenic plants. Plant Mol Biol 75(6):537–553

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Guo X, Huang C, Jin S, Liang S, Nie Y, Zhang X (2007) Agrobacterium-mediated transformation of Cry1C, Cry2A and Cry9C genes into Gossypium hirsutum and plant regeneration. Biol Plant 51:242–248

    Article  CAS  Google Scholar 

  • Guo YH, Yu YP, Wang D, Wu CA, Yang GD, Huang JG, Zheng CC (2009) GhZFP1, a novel CCCH-type zinc finger protein from cotton, enhances salt stress tolerance and fungal disease resistance in transgenic tobacco by interacting with GZIRD21A and GZIPR5. New Phytol 183:62–75

    Article  CAS  PubMed  Google Scholar 

  • Guo WQ, Zhang PT, Li CH, Yin JM, Han XY (2015) Recovery of root growth and physiological characters in cotton after salt stress relief. Chil J Agr Res 75:85–91

    Article  Google Scholar 

  • Hirayama T, Shinozaki K (2010) Research on plant abiotic stress responses in the post-genome era: past, present and future. Plant J 61:1041–1052

    Article  CAS  PubMed  Google Scholar 

  • Huang B, Jin L, Liu JY (2008) Identification and characterization of the novel gene GhDBP2 encoding a DRE-binding protein from cotton (Gossypium hirsutum). J Plant Physiol 165:214–223

    Article  CAS  PubMed  Google Scholar 

  • Huang GT, Ma SL, Bai LP, Zhang L, Ma H, Jia P, Liu J, Zhong M, Guo ZF (2012) Signal transduction during cold, salt, and drought stresses in plants. Mol Biol Rep 39:969–987

    Article  PubMed  Google Scholar 

  • Jin SX, Zhang XL, Liang SG, Nie YC, Guo XP, Huang C (2005) Factors affecting transformation efficiency of embryogenic callus of Upland cotton (Gossypium hirsutum) with Agrobacterium tumefaciens. Plant Cell Tiss Org 81:229–237

    Article  CAS  Google Scholar 

  • Keller G, Spatola L, Mccabe D, Martinell B, Swain W, John ME (1997) Transgenic cotton resistant to herbicide bialaphos. Transgenic Res 6:385–392

    Article  CAS  Google Scholar 

  • Kurepa J, Smalle J, Van Montagu M, Inze D (1998) Oxidative stress tolerance and longevity in Arabidopsis: the late-flowering mutant gigantea is tolerant to paraquat. Plant J 14:759–764

    Article  CAS  PubMed  Google Scholar 

  • Kwak JM, Mori IC, Pei ZM, Leonhardt N, Torres MA, Dangl JL, Bloom RE, Bodde S, Jones JDG, Schroeder JI (2003) NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J 22:2623–2633

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li YX, Greenberg SM, Liu TX (2007) Effect of Bt cotton expressing Cry1Ac and Cry2Ab, non-Bt cotton and starvation on survival of Trichoplusia ni (Lepidoptera: Noctuidae). Pest Manag Sci 63(5):476–482

    Article  CAS  PubMed  Google Scholar 

  • Liang C, Meng Z, Meng Z, Malik W, Yan R, Lwin KM, Lin F, Wang Y, Sun G, Zhou T, Zhu T, Li J, Jin S, Guo S, Zhang R (2016) GhABF2, a bZIP transcription factor, confers drought and salinity tolerance in cotton (Gossypium hirsutum L.). Sci Rep UK 6:35040

    Article  CAS  Google Scholar 

  • Liu G, Li X, Jin X, Liu X, Zhu L, Nie Y, Zhang X (2014) Overexpression of rice NAC gene SNAC1 improves drought and salt tolerance by enhancing root development and reducing transpiration rate in transgenic cotton. PLoS One 9:e86895

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu X, Song Y, Xing F, Wang N, Wen F, Zhu C (2016) GhWRKY25, a group I WRKY gene from cotton, confers differential tolerance to abiotic and biotic stresses in transgenic Nicotiana benthamiana. Protoplasma 253:1265–1281

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2T-DDC method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Lu G, Gao C, Zheng X, Han B (2009) Identification of OsbZIP72 as a positive regulator of ABA response and drought tolerance in rice. Planta 229(3):605–615

    Article  CAS  PubMed  Google Scholar 

  • Luo Y, Zhao J, Wang J, Pei H, Zhang B, Ye C, Li J, Ou Q, Wang H, Wang W (2015) Characterization of drought resistance in transgenic wheat lines and grey correlation analyses of related traits. Agric Res Arid Areas 33:48–53 (in Chinese with English abstract)

    Google Scholar 

  • Mehrotra R, Bhalothia P, Bansal P, Basantani MK, Bharti V, Mehrotra S (2014) Abscisic acid and abiotic stress tolerance-different tiers of regulation. J Plant Physiol 171:486–496

    Article  CAS  PubMed  Google Scholar 

  • Mei L, Daud MK, Ullah N, Ali S, Khan M, Malik Z, Zhu SJ (2015) Pretreatment with salicylic acid and ascorbic acid significantly mitigate oxidative stress induced by copper in cotton genotypes. Environ Sci Pollut R 22:9922–9931

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Nakashima K, Tran LS, Van Nguyen D, Fujita M, Maruyama K, Todaka D, Ito Y, Hayashi N, Shinozaki K, Yamaguchi-Shinozaki K (2007) Functional analysis of a NAC-type transcription factor OsNAC6 involved in abiotic and biotic stress-responsive gene expression in rice. Plant J 51(4):617–630

    Article  CAS  PubMed  Google Scholar 

  • Nguyen D, Rieu I, Mariani C, van Dam NM (2016) How plants handle multiple stresses: hormonal interactions underlying responses to abiotic stress and insect herbivory. Plant Mol Biol 91:727–740

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ni YX, Wang XL, Li DD, Wu YJ, Xu WL, Li XB (2008) Novel cotton homeobox gene and its expression profiling in root development and in response to stresses and phytohormones. Acta Biochim Biophys Sin 40:78–84

    Article  CAS  PubMed  Google Scholar 

  • Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Safe 60:324–349

    Article  CAS  Google Scholar 

  • Pei ZM, Murata Y, Benning G, Thomine S, Klusener B, Allen GJ, Grill E, Schroeder JI (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406:731–734

    Article  CAS  PubMed  Google Scholar 

  • Qiao ZX, Huang B, Liu JY (2008) Molecular cloning and functional analysis of an ERF gene from cotton (Gossypium hirsutum). Biochim Biophys Acta 1779:122–127

    Article  CAS  PubMed  Google Scholar 

  • Schmugge TJ, Jackson TJ, Mckim HL (1980) Survey of methods for soil moisture determination. Water Resour Res 16:961–979

    Article  Google Scholar 

  • Sirichandra C, Wasilewska A, Vlad F, Valon C, Leung J (2009) The guard cell as a single-cell model towards understanding drought tolerance and abscisic acid action. J Exp Bot 60:1439–1463

    Article  CAS  PubMed  Google Scholar 

  • Sunilkumar G, Rathore KS (2001) Transgenic cotton: factors influencing Agrobacterium-mediated transformation and regeneration. Mol Breed 8:37–52

    Article  CAS  Google Scholar 

  • Tang L, Cai H, Wea Ji (2013) Overexpression of GsZFP1 enhances salt and drought tolerance in transgenic alfalfa (Medicago sativa L.). Plant Physiol Bioch 71:22–30

    Article  CAS  Google Scholar 

  • Trolinder NL, Goodin JR (1988) Somatic embryogenesis in cotton (Gossypium): I. Effects of source of explant and hormone regime. Plant Cell Tissue Organ 2:31–42

    Article  Google Scholar 

  • Tuteja N (2014) Abscisic acid and abiotic stress signaling. Plant Signal Behav 2(3):135–138

    Article  Google Scholar 

  • Umbeck P, Johnson G, Barton K, Swain W (1987) Genetically transformed cotton (Gossypium hirsutum L.) plants. Nat Biotechnol 5:263–266

    Article  CAS  Google Scholar 

  • Wang L, Zhao J, Fan YL (2002) Gene cloning and function analysis of ABP9 protein which specifically binds to ABRE2 motif of maize Cat1 gene. Chin Sci Bull 47:1871–1875

    Article  CAS  Google Scholar 

  • Wang CL, Zhao J, Li YH, Fan YL, Zhang LJ, Liu ZX, Guan RX, Lu SX, Chang RZ, Qiu LJ (2008) Transforming transcription factor ABP9 into soybean and optimization of the transformation system. Sci Agric Sin 41:1908–1916 (in Chinese with English abstract)

    CAS  Google Scholar 

  • Wang W, Luo Y, Wang JH, Pei HD, Chen YL, Ye CL, Luo JJ, Yang SZ (2014) Evaluation of drought resistance in ABP9-transgenic winter wheat lines. J Triticeae Crops 34:1217–1224 (in Chinese with English abstract)

    CAS  Google Scholar 

  • Xiong H, Li J, Liu P, Duan J, Zhao Y, Guo X, Li Y, Zhang H, Ali J, Li Z (2014) Overexpression of OsMYB48-1, a novel MYB-related transcription factor, enhances drought and salinity tolerance in rice. PLoS One 9:e92913

    Article  PubMed  PubMed Central  Google Scholar 

  • Yamaguchi T, Blumwald E (2005) Developing salt-tolerant crop plants: challenges and opportunities. Trends Plant Sci 10:615–620

    Article  CAS  PubMed  Google Scholar 

  • Yu H, Chen X, Hong YY, Wang Y, Xu P, Ke SD, Liu HY, Zhu JK, Oliver DJ, Xiang CB (2008) Activated expression of an Arabidopsis HD-START protein confers drought tolerance with improved root system and reduced stomatal density. Plant Cell 20:1134–1151

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu L, Chen X, Wang Z, Wang S, Wang Y, Zhu Q, Li S, Xiang C (2013) Arabidopsis Enhanced Drought Tolerance1/HOMEODOMAIN GLABROUS11 confers drought tolerance in transgenic rice without yield penalty. Plant Physiol 162:1378–1391

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu LH, Wu SJ, Peng YS, Liu RN, Chen X, Zhao P, Xu P, Zhu JB, Jiao GL, Pei Y, Xiang CB (2015) Arabidopsis EDT1/HDG11 improves drought and salt tolerance in cotton and poplar and increases cotton yield in the field. Plant Biotechnol J 14:1–13

    Google Scholar 

  • Yuceer SU, Koc NK (2006) Agrobacterium-mediated transformation and regeneration of cotton plants. Russ J Plant Physiol 53:413–417

    Article  CAS  Google Scholar 

  • Zhang X, Wollenweber B, Jiang D, Liu F, Zhao J (2008) Water deficits and heat shock effects on photosynthesis of a transgenic Arabidopsis thaliana constitutively expressing ABP9, a bZIP transcription factor. J Exp Bot 59:839–848

    Article  CAS  PubMed  Google Scholar 

  • Zhang L, Wu J, Dong F, Liang H, Ye X, Lu T, Zhao J (2010) Identification of stress resistant transgenic ryegrass and tall fescue plants expressing ABP9 gene. Pratacult Sci 27:72–77 (in Chinese with English abstract)

    Google Scholar 

  • Zhang X, Wang L, Meng H, Wen H, Fan Y, Zhao J (2011) Maize ABP9 enhances tolerance to multiple stresses in transgenic Arabidopsis by modulating ABA signaling and cellular levels of reactive oxygen species. Plant Mol Biol 75:365–378

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang F, Li S, Yang S, Wang L, Guo W (2015a) Overexpression of a cotton annexin gene, GhAnn1, enhances drought and salt stress tolerance in transgenic cotton. Plant Mol Biol 87:47–67

    Article  CAS  PubMed  Google Scholar 

  • Zhang Z, Zhang X, Hu Z, Wang S, Zhang J, Wang X, Wang Q, Zhang B (2015b) Lack of K-dependent oxidative stress in cotton roots following coronatine-induced ROS accumulation. PLoS One 10:e0126476

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by a Grant from the Key Project for Breeding Genetic Modified Organisms (2015ZX08005-004).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Jun Zhao or Hongmei Cheng.

Electronic supplementary material

Below is the link to the electronic supplementary material.

425_2017_2704_MOESM1_ESM.jpg

Fig. S1 a Phenotypes of R15 and transgenic L24 and L66 plants grown in control conditions (16 h light/8 h dark at 28 ± 2℃) for 2 and 4 weeks. b, c Representative image and seedling length of cotton on 1/2MS medium without NaCl (control) and containing 0.8% NaCl at 2 weeks after germination (JPEG 2026 kb)

425_2017_2704_MOESM2_ESM.jpg

Fig. S2 Root phenotypes (a) and mean (± SD) fresh root biomass (b) of cotton plants after 60-day PEG 6000 treatment. c Physiological variables in cotton leaves after response to 4 weeks of osmotic stress: (1) total chlorophyll content; (2) proline content; (3) soluble sugar content; (4) MDA content. d Representative seedlings. e Length of seedlings 2 weeks after seed germination on 1/2 MS medium without mannitol (control) or with 250 mM mannitol (JPEG 3389 kb)

425_2017_2704_MOESM3_ESM.jpg

Fig. S3 Root phenotypes (a) and mean (± SD) fresh root biomass (b) of cotton plants after 40-day water-withholding (JPEG 1798 kb)

Supplementary material 4 (DOCX 19 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, C., Lu, G., Hao, Y. et al. ABP9, a maize bZIP transcription factor, enhances tolerance to salt and drought in transgenic cotton. Planta 246, 453–469 (2017). https://doi.org/10.1007/s00425-017-2704-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-017-2704-x

Keywords

Navigation