Please wait a minute...
Journal of Integrative Agriculture  2018, Vol. 17 Issue (03): 507-516    DOI: 10.1016/S2095-3119(17)61681-2
Crop Science Advanced Online Publication | Current Issue | Archive | Adv Search |
A wheat gene TaSAP17-D encoding an AN1/AN1 zinc finger protein improves salt stress tolerance in transgenic Arabidopsis
XU Qiao-fang1, 2, MAO Xin-guo2, WANG Yi-xue2, WANG Jing-yi2, XI Ya-jun1, JING Rui-lian  
1 College of Agronomy, Northwest A&F University, Yangling 712100, P.R.China
2 National Key Facility for Crop Gene Resources and Genetic Improvement/Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, P.R.China
Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
Abstract  The stress-associated protein (SAP) multigene family is conserved in both animals and plants.  Its function in some animals and plants are known, but it is yet to be deciphered in wheat (Triticum aestivum L.).  We identified the wheat gene TaSAP17-D, a member of the SAP gene family with an AN1/AN1 conserved domain.  Subcellular localization indicated that TaSAP17-D localized to the nucleus, cytoplasm, and cell membrane.  Expression pattern analyses revealed that TaSAP17-D was highly expressed in seedlings and was involved in NaCl response, polyethylene glycol (PEG), cold, and exogenous abscisic acid (ABA).  Constitutive expression of TaSAP17-D in transgenic Arabidopsis resulted in enhanced tolerance to salt stress, confirmed by improved multiple physiological indices and significantly upregulated marker genes related to salt stress response.  Our results suggest that TaSAP17-D is a candidate gene that can be used to protect crop plants from salt stress.  
Keywords:   SAP        multigene family       TaSAP17-D        salt tolerance        wheat  
Received: 24 February 2017   Accepted:

This work was supported by the National Key Research and Development Program of China (2016YFD0100605), and the Agricultural Science and Technology Innovation Program, China (ASTIP).

Corresponding Authors:  Correspondence XI Ya-jun, Tel: +86-29-87082845, E-mail:; JING Rui-lian, Tel: +86-10-82105829, E-mail:   
About author:  XU Qiao-fang, Mobile: +86-13011216511, E-mail:

Cite this article: 

XU Qiao-fang, MAO Xin-guo, WANG Yi-xue, WANG Jing-yi, XI Ya-jun, JING Rui-lian. 2018. A wheat gene TaSAP17-D encoding an AN1/AN1 zinc finger protein improves salt stress tolerance in transgenic Arabidopsis. Journal of Integrative Agriculture, 17(03): 507-516.

Ali-Rachedi S, Bouinot D, Wagner M H, Bonnet M, Sotta B, Grappin P, Jullien M. 2004. Changes in endogenous abscisic acid levels during dormancy release and maintenance of mature seeds: Studies with the cape verde islands ecotype, the dormant model of Arabidopsis thaliana. Planta, 219, 479–488.

Baek D, Cha J Y, Kang S, Park B, Lee H J, Hong H, Chun H J, Kim D H, Kim M C, Lee S Y, Yun D J. 2015. The Arabidopsis a zinc finger domain protein ARS1 is essential for seed germination and ROS homeostasis in response to ABA and oxidative stress. Frontiers in Plant Science, 6, doi: 10.3389/fpls.2015.00963

Chakraborty N, Singh N, Kaur K, Raghuram N. 2015. G-protein signaling components GCR1 and GPA1 mediate responses to multiple abiotic stresses in Arabidopsis. Frontiers in Plant Science, 6, doi: 10.3389/fpls.2015.01000

Chang J Z, Zhang J N, Mao X G, Li A, Jia J Z, Jing R L. 2013. Polymorphism of TaSAP1-A1 and its association with agronomic traits in wheat. Planta, 237, 1495–1508.

Chien P S, Nam H G, Chen Y R. 2015. A salt-regulated peptide derived from the CAP superfamily protein negatively regulates salt-stress tolerance in Arabidopsis. Journal of Experimental Botany, 66, 5301–5313.

Clough S J, Bent A F. 1998. Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. The Plant Journal, 16, 735–743.

Finch-Savage W E, Leubner-Metzger G. 2006. Seed dormancy and the control of germination. The New Phytologist, 171, 501–523.

Gilles G C, Gervais M L, Planchet E, Satour P, Limami A M, Lelievre E. 2011. A stress-associated protein containing A20/AN1 zing-finger domains expressed in Medicago truncatula seeds. Plant Physiology and Biochemistry, 49, 303–310.

Giri J, Dansana P K, Kothari K S, Sharma G, Vij S, Tyagi A K. 2013. SAPs as novel regulators of abiotic stress response in plants. Bioessays, 35, 639–648.

Hasanuzzaman M, Alam M M, Rahman A, Hasanuzzaman M, Nahar K, Fujita M. 2014. Exogenous proline and glycine betaine mediated upregulation of antioxidant defense and glyoxalase systems provides better protection against salt-induced oxidative stress in two rice (Oryza sativa L.) varieties. BioMed Research International, 2014, 757219.

Hichri I, Muhovski Y, Zizková E, Dobrev P I, Franco-Zorrilla J M, Solano R, Lopez-Vidriero I, Motyka V, Lutts S. 2014. The Solanum lycopersicum zinc finger2 cysteine-2/histidine-2 repressor-like transcription factor regulates development and tolerance to salinity in tomato and Arabidopsis. Plant Physiology, 164, 1967–1990.

Hu C A A, Delauney A J, Verma D P. 1992. A bifunctional enzyme (delta 1-pyrroline-5-carboxylate synthetase) catalyzes the first two steps in proline biosynthesis in plants. Proceedings of the National Academy of Sciences of the United States of America, 89, 9354–9358.

Jan A, Maruyama K, Todaka D, Kidokoro S, Abo M, Yoshimura E, Shinozaki K, Nakashima K, Yamaguchi-Shinozaki K. 2013. OsTZF1, a CCCH-tandem zinc finger protein, confers delayed senescence and stress tolerance in rice by regulating stress-related genes. Plant Physiology, 161, 1202–1216.

Jia J, Zhao S, Kong X, Li Y, Zhao G, He W, Appels R, Pfeifer M, Tao Y, Zhang X, Jing R, Zhang C, Ma Y, Gao L, Gao C, Spannagl M, Mayer K F, Li D, Pan S, Zheng F, et al. 2013. Aegilops tauschii draft genome sequence reveals a gene repertoire for wheat adaptation. Nature, 496, 91–95.

Kang M, Abdelmageed H, Lee S, Reichert A, Mysore K S, Allen R D. 2013. AtMBP-1, an alternative translation product of LOS2, affects abscisic acid responses and is modulated by the E3 ubiquitin ligase AtSAP5. The Plant Journal, 76, 481–493.

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. Nature Biotechnology, 17, 287–291.

Knight H, Knight M R. 2001. Abiotic stress signalling pathways: Specificity and cross-talk. Trends in Plant Science, 6, 262–267.

Li B, Liu D, Li Q R, Mao X G, Li A, Wang J Y, Chang X P, Jing R L. 2016. Overexpression of wheat gene TaMOR improves root system architecture and grain yield in Oryza sativa. Journal of Experimental Botany, 67, 4155–4167.

Ling H Q, Zhao S, Liu D, Wang J, Sun H, Zhang C, Fan H, Li D, Dong L, Tao Y, Gao C, Wu H, Li Y, Cui Y, Guo X, Zheng S, Wang B, Yu K, Liang Q, Yang W, et al. 2013. Draft genome of the wheat A-genome progenitor Triticum urartu. Nature, 496, 87–90.

Mao X G, Zhang H Y, Tian S J, Chang X P, Jing R L. 2010. TaSnRK2.4, an SNF1-type serine/threonine protein kinase of wheat (Triticum aestivum L.), confers enhanced multistress tolerance in Arabidopsis. Journal of Experimental Botany, 61, 683–696.

Mukhopadhyay A, Vij S, Tyagi A K. 2004. Overexpression of a zinc-finger protein gene from rice confers tolerance to cold, dehydration, and salt stress in transgenic tobacco. Proceedings of the National Academy of Sciences of the United States of America, 101, 6309–6314.

Peng Z, Li L, Liu Y P, Liu H M, Jing R L. 2017. Evaluation of salinity tolerance in wheat genotypes at germination and seedling stages. Journal of Plant Genetic Resources, 18, 638–645.

Ren H B, Fan Y J, Gao Z H, Wei K F, Li G F, Liu J, Chen L, Li B B, Hu J F, Jia W S. 2007. Roles of a sustained activation of NCED3 and the synergistic regulation of ABA biosynthesis and catabolism in ABA signal production in Arabidopsis. Chinese Science Bulletin, 52, 484–491.

Ben Saad R, Zouari N, Ben Ramdhan W, Azaza J, Meynard D, Guiderdoni E, Hassairi A. 2010. Improved drought and salt stress tolerance in transgenic tobacco overexpressing a novel A20/AN1 zinc-finger “AlSAP” gene isolated from the halophyte grass Aeluropus littoralis. Plant Molecular Biology, 72, 171–190.

Schmittgen T D, Livak K J. 2008. Analyzing real-time PCR data by the comparative CT method. Nature Protocols, 3, 1101–1108.

Sharma G, Giri J, Tyagi A K. 2015. Rice OsiSAP7 negatively regulates ABA stress signalling and imparts sensitivity to water-deficit stress in Arabidopsis. Plant Science, 237, 80–92.

Shi H, Jiang C, Ye T T, Tan D X, Reiter R J, Zhang H, Liu R Y, Chan Z L. 2015. Comparative physiological, metabolomic, and transcriptomic analyses reveal mechanisms of improved abiotic stress resistance in bermudagrass [Cynodon dactylon (L). Pers.] by exogenous melatonin. Journal of Experimental Botany, 66, 681–694.

Sreedharan S, Shekhawat U K S, Ganapathi T R. 2012. MusaSAP1, a A20/AN1 zinc finger gene from banana functions as a positive regulator in different stress responses. Plant Molecular Biology, 80, 503–517.

Ströher E, Wang X J, Roloff N, Klein P, Husemann A, Dietz K J. 2009. Redox-dependent regulation of the stress-induced zinc-finger protein SAP12 in Arabidopsis thaliana. Molecular Plant, 2, 357–367.

Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28, 2731–2739.

Vij S, Tyagi A K. 2008. A20/AN1 zinc-finger domain-containing proteins in plants and animals represent common elements in stress response. Functional & Integrative Genomics, 8, 301–307.

Wang C X. 2011. Isolation and functional analysis of stressresponse gene TaABC1 and TaSAP1/2 from wheat (Triticum aestivum L.). Ph D thesis, Chinese Academy of Agricultural Sciences, Beijing. (in Chinese)

Wang F, Coe R A, Karki S, Wanchana S, Thakur V, Henry A, Lin H C, Huang J, Peng S, Quick W P. 2016. Overexpression of OsSAP16 regulates photosynthesis and the expression of a broad range of stress response genes in rice (Oryza sativa L.). PLoS ONE, 11, e0157244.

Yu S, Wang W, Wang B. 2012. Recent progress of salinity tolerance research in plants. Russian Journal of Genetics, 48, 497–505.

Zhang H, Liu Y P, Wen F, Yao D M, Wang L, Guo J, Ni L, Zhang A Y, Tan M P, Jiang M Y. 2014. A novel rice C2H2-type zinc finger protein, ZFP36, is a key player involved in abscisic acid-induced antioxidant defence and oxidative stress tolerance in rice. Journal of Experimental Botany, 65, 5795–5809.

Zhang L, Li Y Z, Lu W J, Meng F, Wu C A, Guo X Q. 2012. Cotton GhMKK5 affects disease resistance, induces HR-like cell death, and reduces the tolerance to salt and drought stress in transgenic Nicotiana benthamiana. Journal of Experimental Botany, 63, 3935–3951.
[1] DU Dan, HU Xin, SONG Xiao-mei, XIA Xiao-jiao, SUN Zhen-yu, LANG Min, PAN Yang-lu, ZHENG Yu, PAN Yu. SlTPP4 participates in ABA-mediated salt tolerance by enhancing root architecture in tomato[J]. >Journal of Integrative Agriculture, 2023, 22(8): 2384-2396.
[2] TU Ke-ling, YIN Yu-lin, YANG Li-ming, WANG Jian-hua, SUN Qun. Discrimination of individual seed viability by using the oxygen consumption technique and headspace-gas chromatography-ion mobility spectrometry[J]. >Journal of Integrative Agriculture, 2023, 22(3): 727-737.
[3] HU Wen-jing, FU Lu-ping, GAO De-rong, LI Dong-sheng, LIAO Sen, LU Cheng-bin. Marker-assisted selection to pyramid Fusarium head blight resistance loci Fhb1 and Fhb2 in a high-quality soft wheat cultivar Yangmai 15[J]. >Journal of Integrative Agriculture, 2023, 22(2): 360-370.
[4] LI Si-ping, ZENG Lu-sheng, SU Zhong-liang. Wheat growth, photosynthesis and physiological characteristics under different soil Zn levels[J]. >Journal of Integrative Agriculture, 2022, 21(7): 1927-1940.
[5] ZHANG Hai-feng, Tofazzal ISLAM, LIU Wen-de. Integrated pest management programme for cereal blast fungus Magnaporthe oryza[J]. >Journal of Integrative Agriculture, 2022, 21(12): 3420-3433.
[6] ZHAO Lai-bin, XIE Die, HUANG Lei, ZHANG Shu-jie, LUO Jiang-tao, JIANG Bo, NING Shun-zong, ZHANG Lian-quan, YUAN Zhong-wei, WANG Ji-rui, ZHENG You-liang, LIU Deng-cai, HAO Ming. Integrating the physical and genetic map of bread wheat facilitates the detection of chromosomal rearrangements[J]. >Journal of Integrative Agriculture, 2021, 20(9): 2333-2342.
[7] LI Si-nan, CHEN Wen, MA Xin-yao, TIAN Xia-xia, LIU Yao, HUANG Li-li, KANG Zhen-sheng, ZHAO Jie. Identification of eight Berberis species from the Yunnan-Guizhou plateau as aecial hosts for Puccinia striiformis f. sp. tritici, the wheat stripe rust pathogen[J]. >Journal of Integrative Agriculture, 2021, 20(6): 1563-1569.
[8] LIU Yang, LI Yu-xiang, LI Yi-xiang, TIAN Zhong-wei, HU Jin-ling, Steve ADKINS, DAI Ting-bo. Changes of oxidative metabolism in the roots of wheat (Triticum aestivum L.) seedlings in response to elevated ammonium concentrations[J]. >Journal of Integrative Agriculture, 2021, 20(5): 1216-1228.
[9] LIU Hang, TANG Hua-ping, LUO Wei, MU Yang, JIANG Qian-tao, LIU Ya-xi, CHEN Guo-yue, WANG Ji-rui, ZHENG Zhi, QI Peng-fei, JIANG Yun-feng, CUI Fa, SONG Yin-ming, YAN Gui-jun, WEI Yuming, LAN Xiu-jin, ZHENG You-liang, MA Jian. Genetic dissection of wheat uppermost-internode diameter and its association with agronomic traits in five recombinant inbred line populations at various field environments[J]. >Journal of Integrative Agriculture, 2021, 20(11): 2849-2861.
[10] LIU Da-zhong, YANG Fei-fei, LIU Sheng-ping. Estimating wheat fractional vegetation cover using a density peak k-means algorithm based on hyperspectral image data[J]. >Journal of Integrative Agriculture, 2021, 20(11): 2880-2891.
[11] XIAO Jing-xiu, ZHU Ying-an, BAI Wen-lian, LIU Zhen-yang, TANG Li, ZHENG Yi. Yield performance and optimal nitrogen and phosphorus application rates in wheat and faba bean intercropping[J]. >Journal of Integrative Agriculture, 2021, 20(11): 3012-3025.
[12] PAN Li-jun, LU Lin, LIU Yu-ping, WEN Sheng-xian, ZHANG Zeng-yan. The M43 domain-containing metalloprotease RcMEP1 in Rhizoctonia cerealis is a pathogenicity factor during the fungus infection to wheat[J]. >Journal of Integrative Agriculture, 2020, 19(8): 2044-2055.
[13] ZHOU Chun-yun, XIONG Hong-chun, LI Yu-ting, GUO Hui-jun, XIE Yong-dun, ZHAO Lin-shu, GU Jiayu, ZHAO Shi-rong, DING Yu-ping, SONG Xi-yun, LIU Lu-xiang. Genetic analysis and QTL mapping of a novel reduced height gene in common wheat (Triticum aestivum L.)[J]. >Journal of Integrative Agriculture, 2020, 19(7): 1721-1730.
[14] FANG Zheng-wu, HE Yi-qin, LIU Yi-ke, JIANG Wen-qiang, SONG Jing-han, WANG Shu-ping, MA Dong-fang, YIN Jun-liang. Bioinformatic identification and analyses of the non-specific lipid transfer proteins in wheat[J]. >Journal of Integrative Agriculture, 2020, 19(5): 1170-1185.
[15] LIANG Pan-pan, ZHAO Chen, LIN Yuan, GENG Ji-jia, CHEN Yuan, CHEN De-hua, ZHANG Xiang. Effects of sodium benzoate on growth and physiological characteristics of wheat seedlings under compound heavy metal stress[J]. >Journal of Integrative Agriculture, 2020, 19(4): 1010-1018.
No Suggested Reading articles found!