Functional characterization of ZjPYL8 from sour jujube: enhancing the sensitivity of stomata and roots to ABA in Arabidopsis thaliana

Peiyan Wang

1 Traditional Chinese Medicine Processing Technology Innovation Center of Hebei Province, College of Pharmacy, Shijiazhuang, Hebei 050200, China; 2 College of Pharmacy, Hebei University of Chinese Medicine, Shijiazhuang, Hebei 050200, China
https://orcid.org/0000-0001-9535-4861

Lanting Qi

College of Life and Environment Science, Minzu University of China, Beijing 100081, China
https://orcid.org/0000-0003-4400-2035

Junna Song

1 Traditional Chinese Medicine Processing Technology Innovation Center of Hebei Province, College of Pharmacy, Shijiazhuang, Hebei 050200, China; 2 College of Pharmacy, Hebei University of Chinese Medicine, Shijiazhuang, Hebei 050200, China
https://orcid.org/0009-0001-1165-5964

Ruojia Zhu

1 Traditional Chinese Medicine Processing Technology Innovation Center of Hebei Province, College of Pharmacy, Shijiazhuang, Hebei 050200, China; 2 College of Pharmacy, Hebei University of Chinese Medicine, Shijiazhuang, Hebei 050200, China
https://orcid.org/0009-0009-5029-109X

Xiaowei Han

1 Traditional Chinese Medicine Processing Technology Innovation Center of Hebei Province, College of Pharmacy, Shijiazhuang, Hebei 050200, China; 2 College of Pharmacy, Hebei University of Chinese Medicine, Shijiazhuang, Hebei 050200, China
https://orcid.org/0000-0002-9445-2299

Yu Liu

College of Pharmacy, Hebei University of Chinese Medicine, Shijiazhuang, Hebei 050200, China
https://orcid.org/0009-0008-1754-6954

Xianyun Wang

Cell Therapy Laboratory, The First Hospital of Hebei Medical University, Shijiazhuang, Hebei 050031, China
https://orcid.org/0000-0003-2224-4770

Yuguang Zheng

1 Traditional Chinese Medicine Processing Technology Innovation Center of Hebei Province, College of Pharmacy, Shijiazhuang, Hebei 050200, China; 2 College of Pharmacy, Hebei University of Chinese Medicine, Shijiazhuang, Hebei 050200, China
https://orcid.org/0000-0003-3411-5191

Zhao Liu

1 Traditional Chinese Medicine Processing Technology Innovation Center of Hebei Province, College of Pharmacy, Shijiazhuang, Hebei 050200, China; 2 College of Pharmacy, Hebei University of Chinese Medicine, Shijiazhuang, Hebei 050200, China
https://orcid.org/0009-0001-3408-966X


Abstract

Abscisic acid (ABA) is a plant hormone that plays a crucial role in regulating plant growth, development, and adaptation to stress. The growth of Ziziphus jujuba Mill. var. spinosa (Bunge) Hu ex H. Chou, commonly known as Suanzao in Chinese, is significantly influenced by environmental factors, particularly drought and salt stresses. In this study, we isolated and characterized a putative ABA receptor, ZjPYL8, from Sour jujube. To investigate the effects of ZjPYL8 overexpression on ABA-responsive pathways, we introduced it into Arabidopsis thaliana (A. thaliana) and examined the resulting phenotypes. Our results demonstrated that overexpression of ZjPYL8 in A. thaliana led to a significant reduction in stomatal aperture and root length under ABA treatment, while the wild type (WT) was relatively insensitive to ABA. Moreover, ZjPYL8 transgenic plants exhibited shorter roots under salt treatment than the WT did. These findings suggest that the overexpression of ZjPYL8 in A. thaliana enhances the plant's resistance to stress and support the hypothesis that ZjPYL8 serves as a putative ABA receptor in Sour jujube, which may improve the plant's adaptability to drought and salt stresses. ZjPYL8 appears to mediate plant responses to ABA, similar to most ABA receptors in A. thaliana, such as stomatal closure and root length.

Keywords:

ZjPYL8, osmotic stress, salt stress, abscisic acid, sour jujube

Aleman, F., Yazaki, J., Lee, M., Takahashi, Y., Kim, A.Y., Li, Z., Kinoshita, T., Ecker, J.R., Schroeder, J.I. (2016). An ABA-increased interaction of the PYL6 ABA receptor with MYC2 transcription factor: a putative link of ABA and JA signaling. Sci. Rep. 6, 1–10. https://doi.org/10.1038/srep28941 DOI: https://doi.org/10.1038/srep28941

Belda, P.B., Gonzalez, G.M.-P., Lozano, J.J., Coego, A., Antoni, R., Julian, J., Peirats, L.M., Rodriguez, L., Berbel, A., Dietrich, D.J. (2018). PYL8 mediates ABA perception in the root through non-cell-autonomous and ligand-stabilization–based mechanisms. Proc. Nat. Acad. Sci., 115, E11857–E11863. https://doi.org/10.1073/pnas.1815410115 DOI: https://doi.org/10.1073/pnas.1815410115

Cutler, S.R., Rodriguez, P.L., Finkelstein, R.R., Abrams, S.R. (2010). Abscisic acid: emergence of a core signaling network. Ann. Rev. Plant Biol., 61, 651–679. https://doi.org/10.1146/annurev-arplant-042809-112122 DOI: https://doi.org/10.1146/annurev-arplant-042809-112122

Deak, K.I., Malamy, J. (2005). Osmotic regulation of root system architecture. Plant J., 43, 17–28. https://doi.org/10.1111/j.1365-313X.2005.02425.x DOI: https://doi.org/10.1111/j.1365-313X.2005.02425.x

Fernando, V.D., Schroeder, D.F. (2016). Role of ABA in Arabidopsis salt, drought, and desiccation tolerance. IntechOpen, 56, 230–239. https://doi.org/10.5772/61957 DOI: https://doi.org/10.5772/61957

Fujii, H., Chinnusamy, V., Rodrigues, A., Rubio, S., Antoni, R., Park, S.-Y., Cutler, S.R., Sheen, J., Rodriguez, P.L., Zhu, J.-K.J.N. (2009). In vitro reconstitution of an abscisic acid signalling pathway. Nature, 462, 660–664. https://doi.org/10.1038/nature08599 DOI: https://doi.org/10.1038/nature08599

He, S., Liang, Z., Yu, L., Zhou, Z.S. (2009). Growth and physiological characteristics of wild sour jujube seedlings from two provenances under soil water stress. Acta Bot. Boreal.-Occid. Sin., 29, 1387–1393. https://kns.cnki.net/kcms/detail/detail.aspx?FileName=DNYX200907020&DbName=CJFQ2009

Jones, H.A. (1920). Physiological study of maple seeds. Bot. Gaz., 69, 127–152. https://www.jstor.org/stable/2469344 DOI: https://doi.org/10.1086/332622

LaRosa, P.C., Hasegawa, P.M., Rhodes, D., Clithero, J.M., Watad, A.-E.A., Bressan, R.A. (1987). Abscisic acid stimulated osmotic adjustment and its involvement in adaptation of tobacco cells to NaCl. Plant Physiol., 85, 174–181. https://doi.org/10.1104/pp.85.1.174 DOI: https://doi.org/10.1104/pp.85.1.174

Lee, H.-N., Lee, K.-H., Kim, C.S. (2015). Abscisic acid receptor PYRABACTIN RESISTANCE-LIKE 8, PYL8, is involved in glucose response and dark-induced leaf senescence in Arabidopsis. Biochem. Biophys. Res. Comm., 463, 24–28. https://doi.org/10.1016/j.bbrc.2015.05.010 DOI: https://doi.org/10.1016/j.bbrc.2015.05.010

Lim, C.W., Baek, W., Han, S.-W., Lee, S.C. (2013). Arabidopsis PYL8 plays an important role for ABA signaling and drought stress responses. Plant Pathol. J., 29, 471. https://doi.org/10.5423/PPJ.NT.07.2013.0071 DOI: https://doi.org/10.5423/PPJ.NT.07.2013.0071

Liu, M., Cheng, J.R. (1994). A taxonomic study on Chinese jujube and wild jujube. J. Hebei Agric. Univ., 17, 1–10. https://kns.cnki.net/kcms/detail/detail.aspx?FileName=CULT404.000&DbName=CJFQ1994

Ma, Y., Szostkiewicz, I., Korte, A., Moes, D., Yang, Y., Christmann, A., Grill, E. (2009). Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science, 324, 1064–1068. https://doi.org/10.1126/science.1172408 DOI: https://doi.org/10.1126/science.1172408

Ming, W., Yun-wei, S.E. (1986). Fruit trees and vegetables for arid and semi-arid areas in north-west China. J. Arid Environ., 11, 3–16. https://doi.org/10.1016/S0140-1963(18)31305-3 DOI: https://doi.org/10.1016/S0140-1963(18)31305-3

Park, S.-Y., Fung, P., Nishimura, N., Jensen, D.R., Fujii, H., Zhao, Y., Lumba, S., Santiago, J., Rodrigues, A., Tsz-fung, F.C. (2009). Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science, 324, 1068–1071. https://doi.org/10.1126/science.1173041 DOI: https://doi.org/10.1126/science.1173041

Qi, L., Liu, S., Li, C., Fu, J., Jing, Y., Cheng, J., Li, H., Zhang, D., Wang, X., Dong, X.J. (2020a). Phytochrome-interacting factors interact with the ABA receptors PYL8 and PYL9 to orchestrate ABA signaling in darkness. Mol. Plant., 13, 414–430. https://doi.org/10.1016/j.molp.2020.02.001 DOI: https://doi.org/10.1016/j.molp.2020.02.001

Qi, L., Zheng, Y., Wang, P., Song, J., Jing, S., Xu, L., Zhou, X., Hao, Z., Yan, Y., Liu, Z. (2020b). Overexpression of a sour jujube gene ZjPYR1, encoding a putative abscisic acid receptor, increases sensitivity of the stomata and roots to ABA in Arabidopsis thaliana. Gene Exp. Patt., 36, 119117. https://doi.org/10.1016/j.gep.2020.119117 DOI: https://doi.org/10.1016/j.gep.2020.119117

Saavedra, X., Modrego, A., Rodríguez, D., González-García, M.P., Sanz, L., Nicolás, G., Lorenzo, O. (2010). The nuclear interactor PYL8/RCAR3 of Fagus sylvatica FsPP2C1 is a positive regulator of abscisic acid signaling in seeds and stress. Plant Physiol., 152, 133–150. https://doi.org/10.1104/pp.109.146381 DOI: https://doi.org/10.1104/pp.109.146381

Soon, F.-F., Ng, L.-M., Zhou, X.E., West, G.M., Kovach, A., Tan, M.E., Suino-Powell, K.M., He, Y., Xu, Y., Chalmer, M.J. (2012). Molecular mimicry regulates ABA signaling by SnRK2 kinases and PP2C phosphatases. Science, 335, 85–88. https://doi.org/10.1126/science.1215106 DOI: https://doi.org/10.1126/science.1215106

Wang, G., Wei, Z., He, S., Zhou, X., Liang, Z.J. (2011). Effects of drought stress in soil on flavonoids metabolism in leaf and some growth and physiological indexes of Ziziphus jujuba var. spinosa. J. Plant Res. Environ., 20, 1–8. https://kns.cnki.net/kcms/detail/detail.aspx?FileName=ZWZY201103001&DbName=CJFQ2011

Xing, L., Zhao, Y., Gao, J., Xiang C., Zhu, J.-K. (2016). The ABA receptor PYL9 together with PYL8 plays an important role in regulating lateral root growth. Sci. Rep., 6, 1–13. https://doi.org/10.1038/srep27177 DOI: https://doi.org/10.1038/srep27177

Yan, H., Jia, H., Chen, X., Hao, L., An, H., Guo, X.J.P. (2014). The cotton WRKY transcription factor GhWRKY17 functions in drought and salt stress in transgenic Nicotiana benthamiana through ABA signaling and the modulation of reactive oxygen species production. Plant Cell Physiol., 55, 2060–2076. https://doi.org/10.1093/pcp/pcu133 DOI: https://doi.org/10.1093/pcp/pcu133

Zhao, Y., Chan, Z., Gao, J., Xing, L., Cao, M., Yu, C., Hu, Y., You, J., Shi, H., Zhum J.K. (2016). ABA receptor PYL9 promotes drought resistance and leaf senescence. Proc. Nat. Acad. Sci., 113, 1949–1954. https://doi.org/10.1073/pnas.1522840113 DOI: https://doi.org/10.1073/pnas.1522840113

Zhao, Y., Xing, L., Wang, X., Hou, Y.-J., Ga, J., Wang, P., Duan, C.-G., Zhu, X., Zhu J.-K. (2014). The ABA receptor PYL8 promotes lateral root growth by enhancing MYB77-dependent transcription of auxin-responsive genes. Sci. Signal., 7, ra53-ra53. https://doi.org/10.1126/scisignal.2005051 DOI: https://doi.org/10.1126/scisignal.2005051

Zhu, J.-K. (2002). Salt and drought stress signal transduction in plants. Ann. Rev. Plant Biol., 53, 247–273. https://doi.org/10.1146/annurev.arplant.53.091401.143329 DOI: https://doi.org/10.1146/annurev.arplant.53.091401.143329

Download

Published
2023-12-22



Peiyan Wang 
1 Traditional Chinese Medicine Processing Technology Innovation Center of Hebei Province, College of Pharmacy, Shijiazhuang, Hebei 050200, China; 2 College of Pharmacy, Hebei University of Chinese Medicine, Shijiazhuang, Hebei 050200, China https://orcid.org/0000-0001-9535-4861
Lanting Qi 
College of Life and Environment Science, Minzu University of China, Beijing 100081, China https://orcid.org/0000-0003-4400-2035
Junna Song 
1 Traditional Chinese Medicine Processing Technology Innovation Center of Hebei Province, College of Pharmacy, Shijiazhuang, Hebei 050200, China; 2 College of Pharmacy, Hebei University of Chinese Medicine, Shijiazhuang, Hebei 050200, China https://orcid.org/0009-0001-1165-5964
Ruojia Zhu 
1 Traditional Chinese Medicine Processing Technology Innovation Center of Hebei Province, College of Pharmacy, Shijiazhuang, Hebei 050200, China; 2 College of Pharmacy, Hebei University of Chinese Medicine, Shijiazhuang, Hebei 050200, China https://orcid.org/0009-0009-5029-109X
Xiaowei Han 
1 Traditional Chinese Medicine Processing Technology Innovation Center of Hebei Province, College of Pharmacy, Shijiazhuang, Hebei 050200, China; 2 College of Pharmacy, Hebei University of Chinese Medicine, Shijiazhuang, Hebei 050200, China https://orcid.org/0000-0002-9445-2299
Yu Liu 
College of Pharmacy, Hebei University of Chinese Medicine, Shijiazhuang, Hebei 050200, China https://orcid.org/0009-0008-1754-6954
Xianyun Wang 
Cell Therapy Laboratory, The First Hospital of Hebei Medical University, Shijiazhuang, Hebei 050031, China https://orcid.org/0000-0003-2224-4770
Yuguang Zheng 
1 Traditional Chinese Medicine Processing Technology Innovation Center of Hebei Province, College of Pharmacy, Shijiazhuang, Hebei 050200, China; 2 College of Pharmacy, Hebei University of Chinese Medicine, Shijiazhuang, Hebei 050200, China https://orcid.org/0000-0003-3411-5191
Zhao Liu 
1 Traditional Chinese Medicine Processing Technology Innovation Center of Hebei Province, College of Pharmacy, Shijiazhuang, Hebei 050200, China; 2 College of Pharmacy, Hebei University of Chinese Medicine, Shijiazhuang, Hebei 050200, China https://orcid.org/0009-0001-3408-966X



License

Creative Commons License

This work is licensed under a Creative Commons Attribution 4.0 International License.

 

Articles are made available under the conditions CC BY 4.0 (until 2020 under the conditions CC BY-NC-ND 4.0).
Submission of the paper implies that it has not been published previously, that it is not under consideration for publication elsewhere.

The author signs a statement of the originality of the work, the contribution of individuals, and source of funding.