Overexpression of the transcription factor HvSNAC1 improves drought tolerance in barley (Hordeum vulgare L.)
Abstract
NAC proteins constitute a family of plant-specific transcription factors that are involved in many plant cellular processes including responses to abiotic stress. In this study, a cDNA clone encoding the HvSNAC1 transcription factor was isolated from drought-stressed barley using a bioinformatics approach based on amino acid sequence data of the stress-related SNAC1 protein from rice. Phylogenetic analysis of the deduced amino acid sequence of HvSNAC1 showed that this protein belongs to the stress clade of NAC proteins that include SNAC1 and TaNAC2. Expression analysis indicated that the HvSNAC1 gene is strongly induced by different abiotic stresses including drought. Overexpression of HvSNAC1 in barley under the control of a constitutive promoter produced plants that grew normally under well-watered conditions when compared with wild-type plants. Transgenic barley plants overexpressing HvSNAC1 showed higher drought tolerance at different growth stages when compared with wild-type plants. In addition, the constitutive overexpression of HvSNAC1 resulted in improved water status, photosynthetic activity and reduced water loss rate when compared with wild-type plants under drought conditions. Furthermore, the transgenic plants also showed significantly improved productivity, as reflected by the increase in biological yield over the wild-type plants under severe field drought conditions. In conclusion, the HvSNAC1 gene could be a useful tool for improving barley productivity under field drought conditions without impairment in growth under normal field conditions.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Of the material presented in Table 1, only al Abdallat et al. (2014) had examined plant response in a field environment.
“Furthermore, of the material presented in Table 1, only al Abdallat et al. (2014) had examined plant response in a field environment, with many studies focusing only on the seedling stage of growth (Table S2).”
From Genetic resources and precise gene editing for targeted improvement of barley abiotic stress tolerance (2023) · cites this paper as al Abdallat et al. (2014)
Cites
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., & Kumar, S. (2011) · Molecular Biology and Evolution · doi:10.1093/molbev/msr121 · Cited by 39,795 · see citing works
Thompson, J. (1997) · Nucleic Acids Research · doi:10.1093/nar/25.24.4876 · Cited by 39,119 · see citing works
Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A., & Speleman, F. (2002) · Genome Biology · doi:10.1186/gb-2002-3-7-research0034 · Cited by 20,038 · see citing works
Chlorophyll fluorescence—a practical guide
Maxwell, K., & Johnson, G. N. (2000) · Journal of Experimental Botany · doi:10.1093/jexbot/51.345.659 · Cited by 9,347 · see citing works
Lescot, M. (2002) · Nucleic Acids Research · doi:10.1093/nar/30.1.325 · Cited by 8,743 · see citing works
S ALT AND D ROUGHT S TRESS S IGNAL T RANSDUCTION IN P LANTS
Zhu, J. (2002) · Annual Review of Plant Biology · doi:10.1146/annurev.arplant.53.091401.143329 · Cited by 5,808 · see citing works
A Re-Examination of the Relative Turgidity Technique for Estimating Water Deficits in Leaves
Barrs, H., & Weatherley, P. E. (1962) · Australian Journal of Biological Sciences · doi:10.1071/bi9620413 · Cited by 3,691 · see citing works
Plant cis-acting regulatory DNA elements (PLACE) database: 1999
Higo, K., Ugawa, Y., Iwamoto, M., & Korenaga, T. (1999) · Nucleic Acids Research · doi:10.1093/nar/27.1.297 · Cited by 3,387 · see citing works
Yamaguchi‐Shinozaki, K., & Shinozaki, K. (2006) · Annual Review of Plant Biology · doi:10.1146/annurev.arplant.57.032905.105444 · Cited by 2,935 · see citing works
Drought and Salt Tolerance in Plants
Bartels, D., & Sunkar, R. (2005) · Critical Reviews in Plant Sciences · doi:10.1080/07352680590910410 · Cited by 2,611 · see citing works
Hu, H., Dai, M., Yao, J., Xiao, B., Li, X., Zhang, Q., & Xiong, L. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0604882103 · Cited by 1,571 · see citing works
NAC transcription factors: structurally distinct, functionally diverse
Olsen, A. N., Ernst, H. A., Leggio, L. L., & Skriver, K. (2005) · Trends in Plant Science · doi:10.1016/j.tplants.2004.12.010 · Cited by 1,497 · see citing works
Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant.
Aida, M., Ishida, T., Fukaki, H., Fujisawa, H., & Tasaka, M. (1997) · The Plant Cell · doi:10.1105/tpc.9.6.841 · Cited by 1,486 · see citing works
Nakashima, K., Tran, L. P., Nguyen, D. V., Fujita, M., Maruyama, K., Todaka, D., Ito, Y., Hayashi, N., Shinozaki, K., & Yamaguchi‐Shinozaki, K. (2007) · The Plant Journal · doi:10.1111/j.1365-313x.2007.03168.x · Cited by 1,155 · see citing works
NAC proteins: regulation and role in stress tolerance
Puranik, S., Sahu, P. P., Srivastava, P. S., & Prasad, M. (2012) · Trends in Plant Science · doi:10.1016/j.tplants.2012.02.004 · Cited by 1,108 · see citing works
Seki, M., Narusaka, M., Abe, H., Kasuga, M., Yamaguchi‐Shinozaki, K., Carninci, P., Hayashizaki, Y., & Shinozaki, K. (2001) · The Plant Cell · doi:10.1105/tpc.13.1.61 · Cited by 1,105 · see citing works
NAC transcription factors in plant abiotic stress responses
Nakashima, K., Takasaki, H., Mizoi, J., Shinozaki, K., & Yamaguchi‐Shinozaki, K. (2011) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2011.10.005 · Cited by 1,054 · see citing works
Jeong, J. S., Kim, Y. S., Baek, K. H., Jung, H., Ha, S., Choi, Y. D., Kim, M., Reuzeau, C., & Kim, J. (2010) · PLANT PHYSIOLOGY · doi:10.1104/pp.110.154773 · Cited by 832 · see citing works
Engineering drought tolerance in plants: discovering and tailoring genes to unlock the future
Umezawa, T., Fujita, M., Fujita, Y., Yamaguchi-Shinozaki, K., & Shinozaki, K. (2006) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2006.02.002 · Cited by 802 · see citing works
Nakashima, K., Fujita, Y., Kanamori, N., Katagiri, T., Umezawa, T., Kidokoro, S., Maruyama, K., Yoshida, T., Ishiyama, K., Kobayashi, M., et al. (2009) · Plant and Cell Physiology · doi:10.1093/pcp/pcp083 · Cited by 795 · see citing works
Characterization of transcription factor gene SNAC2 conferring cold and salt tolerance in rice
Hu, H., You, J., Fang, Y., Zhu, X., Qi, Z., & Xiong, L. (2008) · Plant Molecular Biology · doi:10.1007/s11103-008-9309-5 · Cited by 652 · see citing works
Fang, Y., You, J., Xie, K., Xie, W., & Xiong, L. (2008) · Molecular Genetics and Genomics · doi:10.1007/s00438-008-0386-6 · Cited by 483 · see citing works
Integrated genomics, physiology and breeding approaches for improving drought tolerance in crops
Mir, R. R., Zaman‐Allah, M., Sreenivasulu, N., Trethowan, R. M., & Varshney, R. K. (2012) · Theoretical and Applied Genetics · doi:10.1007/s00122-012-1904-9 · Cited by 477 · see citing works
Improvement of stress tolerance of wheat and barley by modulation of expression of DREB/CBF factors
Morran, S., Eini, O., Pyvovarenko, T., Parent, B., Singh, R. R., Ismagul, A., Eliby, S., Shirley, N. J., Langridge, P., & Lopato, S. (2010) · Plant Biotechnology Journal · doi:10.1111/j.1467-7652.2010.00547.x · Cited by 466 · see citing works
Drought stress adaptation: metabolic adjustment and regulation of gene expression
Bhargava, S., & Sawant, K. (2012) · Plant Breeding · doi:10.1111/pbr.12004 · Cited by 459 · see citing works
Mao, X., Zhang, H., Qian, X., Li, A., Zhao, G., & Jing, R. (2012) · Journal of Experimental Botany · doi:10.1093/jxb/err462 · Cited by 353 · see citing works
The transcription factor ATAF2 represses the expression of pathogenesis‐related genes in Arabidopsis
Delessert, C., Kazan, K., Wilson, I. W., Straeten, D. V. D., Manners, J. M., Dennis, E. S., & Dolferus, R. (2005) · The Plant Journal · doi:10.1111/j.1365-313x.2005.02488.x · Cited by 321 · see citing works
Hegedus, D. D., Yu, M., Baldwin, D., Gruber, M. Y., Sharpe, A., Parkin, I. A. P., Whitwill, S., & Lydiate, D. J. (2003) · Plant Molecular Biology · doi:10.1023/b:plan.0000006944.61384.11 · Cited by 315 · see citing works
Lu, P.-L., Chen, N.-Z., An, R., Su, Z. Z., Qi, B.-S., Ren, F., Chen, J., & Wang, X.-C. (2006) · Plant Molecular Biology · doi:10.1007/s11103-006-9089-8 · Cited by 311 · see citing works
Collinge, M. A., & Boller, T. (2001) · Plant Molecular Biology · doi:10.1023/a:1010639225091 · Cited by 274 · see citing works
Ren, T., Qu, F., & Morris, T. J. (2000) · The Plant Cell · doi:10.1105/tpc.12.10.1917 · Cited by 270 · see citing works
Xue, G., Way, H. M., Richardson, T. M., Drenth, J., Joyce, P., & McIntyre, C. L. (2011) · Molecular Plant · doi:10.1093/mp/ssr013 · Cited by 267 · see citing works
Barley Cbf3 Gene Identification, Expression Pattern, and Map Location
Choi, D., Rodriguez, E. M., & Close, T. J. (2002) · PLANT PHYSIOLOGY · doi:10.1104/pp.003046 · Cited by 216 · see citing works
High-throughput Agrobacterium-mediated barley transformation
Bartlett, J. G., Alves, S. C., Smedley, M. A., et al. (2008) · Plant Methods · doi:10.1186/1746-4811-4-22 · Cited by 213 · see citing works
Ning, X., Zhang, G., Liu, X., Deng, L., Cai, G., Zhang, Y., Wang, X., Zhao, J., Huang, L., & Kang, Z. (2010) · Molecular Biology Reports · doi:10.1007/s11033-010-0023-4 · Cited by 194 · see citing works
Gramene database in 2010: updates and extensions
Youens‐Clark, K., Buckler, E. S., Casstevens, T. M., Chen, C., DeClerck, G., Derwent, P., Dharmawardhana, P. D., Jaiswal, P., Kersey, P. J., Karthikeyan, A. S., et al. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkq1148 · Cited by 176 · see citing works
Saad, A. S. I., Li, X., Li, H., Huang, T., Gao, C.-S., Guo, M., Cheng, W., Zhao, G., & Liao, Y. (2013) · Plant Science · doi:10.1016/j.plantsci.2012.12.016 · Cited by 170 · see citing works
Jensen, M. K., Rung, J. H., Gregersen, P. L., Gjetting, T., Fuglsang, A. T., Hansen, M., Jøhnk, N., Lyngkjær, M. F., & Collinge, D. B. (2007) · Plant Molecular Biology · doi:10.1007/s11103-007-9204-5 · Cited by 169 · see citing works
The development and application of molecular markers for abiotic stress tolerance in barley
Forster, B. P., Ellis, R. P., Thomas, W. T. B., Newton, A. C., Tuberosa, R., This, D., El‐Enein, R. A., Bahri, M., & Salem, M. B. (2000) · Journal of Experimental Botany · doi:10.1093/jexbot/51.342.19 · Cited by 162 · see citing works
Mapping regulatory genes as candidates for cold and drought stress tolerance in barley
Tondelli, A., Francia, E., Barabaschi, D., et al. (2005) · Theoretical and Applied Genetics · doi:10.1007/s00122-005-0144-7 · Cited by 142 · see citing works
Mysore, K. S., Crasta, O. R., Tuori, R. P., Folkerts, O., Swirsky, P. B., & Martin, G. B. (2002) · The Plant Journal · doi:10.1046/j.1365-313x.2002.01424.x · Cited by 131 · see citing works
Genomic approaches for designing durum wheat ready for climate change with a focus on drought
Habash, D. Z., Kehel, Z., & Nachit, M. M. (2009) · Journal of Experimental Botany · doi:10.1093/jxb/erp211 · Cited by 129 · see citing works
Zimmermann, P., Laule, O., Schmitz, J., et al. (2008) · Molecular Plant · doi:10.1093/mp/ssn048 · Cited by 101 · see citing works
Christiansen, M. W., Holm, P. B., & Gregersen, P. L. (2011) · BMC Research Notes · doi:10.1186/1756-0500-4-302 · Cited by 100 · see citing works
A Rapid and Simple Method of Assaying Plants Transformed with Hygromycin or PPT Resistance Genes
Wang, M., & Waterhouse, P. M. (1997) · Plant Molecular Biology Reporter · doi:10.1023/a:1007446721394 · Cited by 46 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Barley Genes as Tools to Confer Abiotic Stress Tolerance in Crops
Gürel, F., Öztürk, Z. N., Uçarlı, C., & Rosellini, D. (2016) · Frontiers in Plant Science · doi:10.3389/fpls.2016.01137 · Cited by 130 · see citing works
Karunarathne, S., Walker, E., Sharma, D., Li, C., & Han, Y. (2023) · Journal of Zhejiang University-SCIENCE B · doi:10.1631/jzus.b2200552 · Cited by 18 · see citing works
- Authors
- Al Abdallat, A. M., Ayad, J. Y., Abu Elenein, J. M., Al Ajlouni, Z., & Harwood, W. A.
- Affiliations
- University of Jordan (JO)
- John Innes Centre (GB)
- Venue
- Molecular Breeding
- Published
- 2013-09-20
- Volume
- 33
- Issue
- 2
- Pages
- 401-414
- ISSN
- 1380-3743 (ISSN-L)
- 1572-9788
- OpenAlex
- W2082247810
- Cited by
- 64
- References
- 45
- Citations by year
- 2026: 3 · 2025: 4 · 2024: 4 · 2023: 4 · 2022: 9 · 2021: 10 · 2020: 2 · 2019: 8 · 2018: 4 · 2017: 2 · 2016: 8 · 2015: 4 · 2014: 2
- FWCI
- 5.63
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Molecular Breeding (publishedVersion)
- MELSpace (ICARDA (The International Center for Agricultural Research in Dry Areas)) (submittedVersion)
- Funders
- Biotechnology and Biological Sciences Research Council (BBS/E/J/000CA410)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Stress Responses and Tolerance
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Molecular Biology Research
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Genetics and Plant Breeding
- Keywords
- NAC transcription factors, drought tolerance, barley, transgenic overexpression, abiotic stress response, water status, photosynthesis, water loss, grain yield
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
