AI Chat Paper
Note: Please note that the following content is generated by AMiner AI. SciOpen does not take any responsibility related to this content.
{{lang === 'zh_CN' ? '文章概述' : 'Summary'}}
{{lang === 'en_US' ? '中' : 'Eng'}}
Chat more with AI
PDF (4.4 MB)
Collect
Submit Manuscript AI Chat Paper
Show Outline
Outline
Show full outline
Hide outline
Outline
Show full outline
Hide outline
Research paper | Open Access

The soybean GmPUB21-interacting protein GmDi19-5 responds to drought and salinity stresses via an ABA-dependent pathway

Yunhua YangaRui RenbAdhimoolam KarthikeyancJinlong YinaTongtong JinaFei FangaHan CaiaMengzhuo LiuaDagang WangaHaijian Zhia( )Kai Lia( )
National Center for Soybean Improvement, National Key Laboratory for Crop Genetics and Germplasm Enhancement, Key Laboratory of Biology and Genetic Improvement of Soybean Ministry of Agriculture, Nanjing Agricultural University, Nanjing 210095, Jiangsu, China
College of Agronomy & Center for Crop Genome Engineering, Henan Agricultural University, Zhengzhou 450046, Henan, China
Subtropical Horticulture Research Institute, Jeju National University, Jeju 63243, Republic of Korea
Show Author Information

Abstract

Drought-induced protein 19 (Di19) is a Cys2/His2 zinc-finger protein that functions in plant growth and development and in tolerance to abiotic stresses. GmPUB21, an E3 ubiquitin ligase, negatively regulates drought and salinity response in soybean. We identified potential interaction target proteins of GmPUB21 by yeast two-hybrid cDNA library screening, GmDi19-5 as a candidate. Bimolecular fluorescence complementation and glutathionine-S-transferase pull-down assays confirmed the interaction between GmDi19-5 and GmPUB21. GmDi19-5 was induced by NaCl, drought, and abscisic acid (ABA) treatments. GmDi19-5 was expressed in the cytoplasm and nucleus. GmDi19-5 overexpression conferred hypersensitivity to drought and high salinity, whereas GmDi19-5 silencing increased drought and salinity tolerance. Transcripts of ABA- and stress response-associated genes including GmRAB18 and GmDREB2A were down-regulated in GmDi19-5-overexpressing plants under drought and salinity stresses. ABA decreased the protein level of GmDi19-5 in vivo, whereas GmPUB21 increased the decrease of GmDi19-5 after exogenous ABA application. The accumulation of GmPUB21 was also inhibited by GmDi19-5. We conclude that GmPUB21 and GmDi19-5 collaborate to regulate drought and salinity tolerance via an ABA-dependent pathway.

References

[1]

J. Kumar, S. Singh, M. Singh, P.K. Srivastava, R.K. Mishra, V.P. Singh, S.M. Prasad, Transcriptional regulation of salinity stress in plants: a short review, Plant Gene 11 (2017) 160–169.

[2]

X. Yang, M. Lu, Y. Wang, Y. Wang, Z. Liu, S. Chen, Response mechanism of plants to drought stress, Horticulturae 7 (2021) 50.

[3]

B. Wang, L. Li, M. Liu, D. Peng, A. Wei, B. Hou, Y. Lei, X. Li, TaFDL2-1A confers drought stress tolerance by promoting ABA biosynthesis, ABA responses, and ROS scavenging in transgenic wheat, Plant J. 112 (2022) 722–737.

[4]

K.B. Singh, R.C. Foley, L. Oñate-Sánchez, Transcription factors in plant defense and stress responses, Curr. Opin. Plant Biol. 5 (2002) 430–436.

[5]

K. Shinozaki, K. Yamaguchi-Shinozaki, M. Seki, Regulatory network of gene expression in the drought and cold stress responses, Curr. Opin. Plant Biol. 6 (2003) 410–417.

[6]

M.A. Rabbani, K. Maruyama, H. Abe, M.A. Khan, K. Katsura, Y. Ito, K. Yoshiwara, M. Seki, K. Shinozaki, K. Yamaguchi-Shinozaki, Monitoring expression profiles of rice genes under cold, drought, and high-salinity stresses and abscisic acid application using cDNA microarray and RNA gel-blot analyses, Plant Physiol. 133 (2003) 1755–1767.

[7]

A. Danquah, A. de Zelicourt, J. Colcombet, H. Hirt, The role of ABA and MAPK signaling pathways in plant abiotic stress responses, Biotechnol. Adv. 32 (2014) 40–52.

[8]

H. Zhang, J. Zhu, Z. Gong, J.K. Zhu, Abiotic stress responses in plants, Nat. Rev. Genet. 23 (2022) 104–119.

[9]

P. Jurkiewicz, H. Batoko, Protein degradation mechanisms modulate abscisic acid signaling and responses during abiotic stress, Plant Sci. 267 (2018) 48–54.

[10]

K. Nakashima, K. Yamaguchi-Shinozaki, ABA signaling in stress-response and seed development, Plant Cell Rep. 32 (2013) 959–970.

[11]

F. Hauser, Z. Li, R. Waadt, J.I. Schroeder, SnapShot: abscisic acid signaling, Cell 171 (2017) 1708.

[12]

Y. Ma, I. Szostkiewicz, A. Korte, D. Moes, Y.I. Yang, A. Christmann, E. Grill, Regulators of PP2C phosphatase activity function as abscisic acid sensors, Science 324 (2009) 1064–1068.

[13]

S.Y. Park, P. Fung, N. Nishimura, D.R. Jensen, H. Fujii, Y. Zhao, S. Lumba, J. Santiago, A. Rodrigues, T.F. Chow, S.E. Alfred, D. Bonetta, R. Finkelstein, N.J. Provart, D. Desveaux, P.L. Rodriguez, P. McCourt, J.K. Zhu, J.I. Schroeder, B.F. Volkman, S.R. Cutler, Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins, Science 324 (2009) 1068–1071.

[14]

F. Vlad, S. Rubio, A. Rodrigues, C. Sirichandra, C. Belin, N. Robert, J. Leung, P.L. Rodriguez, C. Laurière, S. Merlot, Protein phosphatases 2C regulate the activation of the Snf1-related kinase OST1 by abscisic acid in Arabidopsis, Plant Cell 21 (2009) 3170–3184.

[15]

W. Yang, W. Zhang, X. Wang, Post-translational control of ABA signalling: the roles of protein phosphorylation and ubiquitination, Plant Biotechnol. J. 15 (2017) 4–14.

[16]

J.M. Barrero, P.L. Rodriguez, VICTOR Quesada, PEDRO Piqueras, M.R. Ponce, J.L. Micol, Both abscisic acid (ABA)-dependent and ABA-independent pathways govern the induction of NCED3, AAO3 and ABA1 in response to salt stress, Plant Cell Environ. 29 (2006) 2000–2008.

[17]

G.P. Hao, X.H. Zhang, Y.Q. Wang, Z.Y. Wu, C.L. Huang, Nucleotide variation in the NCED3 region of Arabidopsis thaliana and its association study with abscisic acid content under drought stress, J. Integr. Plant Biol. 51 (2009) 175–183.

[18]

F.C. Sussmilch, T.J. Brodribb, S.A.M. Mcadam, Up-regulation of NCED3 and ABA biosynthesis occur within minutes of a decrease in leaf turgor but AHK1 is not required, J. Exp. Bot. 68 (2017) 2913–2918.

[19]

L. Zhang, J. Xie, L. Wang, L. Si, S. Zheng, Y. Yang, H. Yang, S. Tian, Wheat TabZIP8, 9, 13 participate in ABA biosynthesis in NaCl-stressed roots regulated by TaCDPK9-1, Plant Physiol. Biochem. 151 (2020) 650–658.

[20]

H. Sakamoto, K. Maruyama, Y. Sakuma, T. Meshi, M. Iwabuchi, K. Shinozaki, K. Yamaguchi-Shinozaki, Arabidopsis Cys2/His2-type zinc-finger proteins function as transcription repressors under drought, cold and high-salinity stress conditions, Plant Physiol. 136 (2004) 2734–2746.

[21]

G.H. Yu, L.L. Jiang, X.F. Ma, Z.S. Xu, M.M. Liu, S.G. Shan, X.G. Cheng, F. Chen, A soybean C2H2-type zinc finger gene GmZF1 enhanced cold tolerance in transgenic Arabidopsis, PLoS ONE 9 (2014) e109399.

[22]

J.C. Kim, S.H. Lee, Y.H. Cheong, C.M. Yoo, S.I. Lee, H.J. Chun, D.J. Yun, J.C. Hong, S. Y. Lee, C.O. Lim, M.J. Cho, A novel cold inducible zinc finger protein from soybean, SCOF-1, enhances cold tolerance in transgenic plants, Plant J. 25 (2001) 247–259.

[23]

A. Mukhopadhyay, S. Vij, A.K. Tyagi, Overexpression of a zinc finger protein gene from rice confers tolerance to cold, dehydration, and salt stress in transgenic tobacco, Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 6309–6314.

[24]

S.M. Xu, X.C. Wang, J. Chen, Zinc finger protein 1 (ThZF1) from salt cress (Thellungiella halophila) is a Cys-2/His-2-type transcription factor involved in drought and salt stress, Plant Cell Rep. 26 (2007) 497–506.

[25]

X.Y. Huang, D.Y. Chao, J.P. Gao, M.Z. Zhu, M. Shi, H.X. Lin, A previously unknown zinc finger protein, DST, regulates drought and salt tolerance in rice via stomatal aperture control, Genes Dev. 23 (2009) 1805–1817.

[26]

S.A. Wolfe, L. Nekludova, C.O. Pabo, DNA recognition by Cys2His2 zinc finger proteins, Annu. Rev. Biophys. Biomol. Struct. 29 (2000) 183–212.

[27]

P. Agarwal, R. Arora, S. Ray, A.K. Singh, V.P. Singh, H. Takatsuji, S. Kapoor, A.K. Tyagi, Genome-wide identification of C2H2 zinc-finger gene family in rice and their phylogeny and expression analysis, Plant Mol. Biol. 65 (2007) 467–485.

[28]

S. Ciftci-Yilmaz, R. Mittler, The zinc finger network of plants, Cell Mol. Life Sci. 65 (2008) 1150–1160.

[29]

R. Mittler, Y. Kim, L. Song, J. Coutu, A. Coutu, S. Ciftci-Yilmaz, H. Lee, B. Stevenson, J.K. Zhu, Gain- and loss-of-function mutations in Zat10 enhance the tolerance of plants to abiotic stress, FEBS Lett. 580 (2006) 6537–6542.

[30]

X. Luo, X.i. Bai, D. Zhu, Y. Li, W. Ji, H. Cai, J. Wu, B. Liu, Y. Zhu, GsZFP1, a new Cys2/His2-type zinc-finger protein, is a positive regulator of plant tolerance to cold and drought stress, Planta 235 (2012) 1141–1155.

[31]

M.A.R. Milla, J. Townsend, I.F. Chang, J.C. Cushman, The Arabidopsis AtDi19 gene family encodes a novel type of Cys2/His2 zinc-finger protein implicated in ABA-independent dehydration, high-salinity stress and light signaling pathways, Plant Mol. Biol. 61 (2006) 13–30.

[32]

W.X. Liu, F.C. Zhang, W.Z. Zhang, L.F. Song, W.H. Wu, Y.F. Chen, Arabidopsis Di19 functions as a transcription factor and modulates PR1, PR2, and PR5 expression in response to drought stress, Mol. Plant 6 (2013) 1487–1502.

[33]

L. Wang, C. Yu, C. Chen, C. He, Y. Zhu, W. Huang, Identification of rice Di19 family reveals OsDi19-4 involved in drought resistance, Plant Cell Rep. 33 (2014) 2047–2062.

[34]

G. Li, F.J. Tai, Y. Zheng, J. Luo, S.Y. Gong, Z.T. Zhang, X.B. Li, Two cotton Cys2/His2-type zinc-finger proteins, GhDi19-1 and GhDi19-2, are involved in plant response to salt/drought stress and abscisic acid signaling, Plant Mol. Biol. 74 (4–5) (2010) 437–452.

[35]

L.X. Qin, Y. Li, D.D. Li, W.L. Xu, Y. Zheng, X.B. Li, Arabidopsis drought-induced protein Di19-3 participates in plant response to drought and high salinity stresses, Plant Mol. Biol. 86 (2014) 609–625.

[36]

C. Wu, M. Lin, F. Chen, J. Chen, S. Liu, H. Yan, Y. Xiang, Homologous drought-induced 19 proteins, PtDi19-2 and PtDi19-7, enhance drought tolerance in transgenic plants, Int. J. Mol. Sci. 23 (2022) 3371.

[37]

L. Wang, C. Yu, S. Xu, Y. Zhu, W. Huang, OsDi19-4 acts downstream of OsCDPK14 to positively regulate ABA response in rice, Plant Cell Environ. 39 (2016) 2740–2753.

[38]

L.X. Qin, X.Y. Nie, R. Hu, G. Li, W.L. Xu, X.B. Li, Phosphorylation of serine residue modulates cotton Di19-1 and Di19-2 activities for responding to high salinity stress and abscisic acid signaling, Sci. Rep. 6 (2016) 20371.

[39]

M. Chen, Q.Y. Wang, X.G. Cheng, Z.S. Xu, L.C. Li, X.G. Ye, L.Q. Xia, Y.Z. Ma, GmDREB2, a soybean DRE-binding transcription factor, conferred drought and high salt tolerance in transgenic plants, Biochem. Biophys. Res. Commun. 353 (2007) 299–305.

[40]

H. Sobhanian, R. Razavizadeh, Y. Nanjo, A.A. Ehsanpour, F.R. Jazii, N. Motamed, S. Komatsu, Proteome analysis of soybean leaves, hypocotyls and roots under salt stress, Proteome Sci. 8 (2010) 1906e1923.

[41]

P.P. Mohammadi, A. Moieni, S. Hiraga, S. Komatsu, Organ specific proteomic analysis of drought-stressed soybean seedlings, J. Proteom. 75 (2012) 1906e1923.

[42]

Q. Jiang, Z. Hu, H. Zhang, Y. Ma, Overexpression of GmDREB1 improves salt tolerance in transgenic wheat and leaf protein response to high salinity, Crop. J. 2 (2014) 120–131.

[43]

Y. Yang, A. Karthikeyan, J. Yin, T. Jin, R. Ren, F. Fang, H. Cai, M. Liu, D. Wang, K. Li, H. Zhi, The E3 ligase GmPUB21 negatively regulates drought and salinity stress response in soybean, Int. J. Mol. Sci. 23 (2022) 6893.

[44]

F. Chen, L.Q. Li, Q. Xu, Y.H. Kong, H. Wang, W.H. Wu, The WRKY6 transcription factor modulates PHOSPHATE1 expression in response to low Pi stress in Arabidopsis, Plant Cell 21 (2009) 3554–3566.

[45]

J. Wang, B. Qu, S. Dou, L. Li, D. Yin, Z. Pang, Z. Zhou, M. Tian, G. Liu, Q. Xie, D. Tang, X. Chen, L. Zhu, The E3 ligase OsPUB15 interacts with the receptor-like kinase PID2 and regulates plant cell death and innate immunity, BMC Plant Biol. 15 (2015) 49.

[46]

C.Q. Zhang, J.D. Bradshaw, S.A. Whitham, J.H. Hill, The development of an efficient multipurpose bean pod mottle virus viral vector set for foreign gene expression and RNA silencing, Plant Physiol. 153 (2010) 52–65.

[47]

M. Zhang, J. Zhao, L. Li, Y. Gao, L. Zhao, S.B. Patil, J. Fang, W. Zhang, Y. Yang, M. Li, X. Li, The Arabidopsis U-box E3 ubiquitin ligase PUB30 negatively regulates salt tolerance by facilitating BRI1 kinase inhibitor 1 (BKI1) degradation, Plant Cell Environ. 40 (2017) 2831–2843.

[48]

X.Z. Zhang, W.J. Zheng, X.Y. Cao, X.Y. Cui, S.P. Zhao, T.F. Yu, J. Chen, Y.B. Zhou, M. Chen, S.C. Chai, Z.S. Xu, Y.Z. Ma, Genomic analysis of stress associated proteins in soybean and the role of GmSAP16 in abiotic stress responses in Arabidopsis and soybean, Front. Plant Sci. 10 (2019) 1453.

[49]

J. Marcolino-Gomes, F.A. Rodrigues, R. Fuganti-Pagliarini, C. Bendix, T.J. Nakayama, B. Celaya, H.B.C. Molinari, M.C.N. de Oliveira, F.G. Harmon, A. Nepomuceno, N. Cermakian, Diurnal oscillations of soybean circadian clock and drought responsive genes, PLoS ONE 9 (2014) e86402.

[50]

K. Shu, Y. Qi, F. Chen, Y. Meng, X. Luo, H. Shuai, W. Zhou, J. Ding, J. Du, J. Liu, F. Yang, Q. Wang, W. Liu, T. Yong, X. Wang, Y. Feng, W. Yang, Salt stress represses soybean seed germination by negatively regulating GA biosynthesis while positively mediating ABA biosynthesis, Front. Plant Sci. 8 (2017) 1372.

[51]

X. Yang, M.Y. Kim, J. Ha, S.H. Lee, Overexpression of the soybean NAC gene GmNAC109 increases lateral root formation and abiotic stress tolerance in transgenic Arabidopsis plants, Front. Plant Sci. 10 (2019) 1036.

[52]

D. Mukhopadhyay, H. Riezman, Proteasome-independent functions of ubiquitin in endocytosis and signaling, Science 315 (2007) 201–205.

[53]

Y. Kulathu, D. Komander, Atypical ubiquitylation - the unexplored world of polyubiquitin beyond Lys48 and Lys63 linkages, Nat. Rev. Mol. Cell Biol. 13 (2012) 508–523.

[54]

H. Takatsuji, Zinc-finger proteins, the classical zinc finger emerges in contemporary plant science, Plant Mol. Biol. 39 (1999) 1073–1078.

[55]

C.O. Pabo, E. Peisach, R.A. Grant, Design and selection of novel Cys2His2 zinc finger proteins, Annu. Rev. Biochem. 70 (2001) 313–340.

[56]

M.A. Searles, D. Lu, A. Klung, The role of the central zinc fingers of transcription factor ⅢA in binding to 5S RNA, J. Mol. Biol. 301 (2000) 47–60.

[57]

X. Kang, J. Chong, M. Ni, Hypersensitive to red and blue 1, a ZZ-type zinc finger protein, regulates phytochrome B-mediated red and cryptochrome-mediated blue light responses, Plant Cell 17 (2005) 822–835.

[58]

X. Zhang, H. Cai, M. Lu, Q. Wei, L. Xu, C. Bo, Q. Ma, Y. Zhao, B. Cheng, A maize stress-responsive Di19 transcription factor, ZmDi19-1, confers enhanced tolerance to salt in transgenic Arabidopsis, Plant Cell Rep. 38 (2019) 1563–1578.

[59]

Z.J. Feng, X.Y. Cui, X.Y. Cui, M. Chen, G.X. Yang, Y.Z. Ma, G.Y. He, Z.S. Xu, The soybean GmDi19-5 interacts with GmLEA3.1 and increases sensitivity of transgenic plants to abiotic stresses, Front. Plant Sci. 6 (2015) 179.

[60]

X. Zhang, H. Cai, M. Lu, Q. Wei, L. Xu, C. Bo, Q. Ma, Y. Zhao, B. Cheng, A maize stress-responsive Di19 transcription factor, ZmDi19-1, confers enhanced tolerance to salt in transgenic Arabidopsis, Plant Cell Rep. 38 (2019) 1563–1578.

[61]

J.Y. Zhao, J.M. Liu, Z.J. Feng, M. Chen, Y.B. Zhou, J. Chen, Z.S. Xu, C.H. Guo, The response to heat and screening of the interacting proteins of zinc finger protein GmDi19-5 in soybean, Acta Agron. Sin. 50 (2017) 2389–2398 (in Chinese with English abstract).

[62]

F. Qin, Y. Sakuma, L.S. Tran, K. Maruyama, S. Kidokoro, Y. Fujita, M. Fujita, T. Umezawa, Y. Sawano, K. Miyazono, M. Tanokura, K. Shinozaki, K. YamaguchiShinozaki, Arabidopsis DREB2A-interacting proteins function as RING E3 ligases and negatively regulate plant drought stress-responsive gene expression, Plant Cell 20 (2008) 1693–1707.

[63]

N. Zhang, Y. Yin, X. Liu, S. Tong, J. Xing, Y. Zhang, R.N. Pudake, E.M. Izquierdo, H. Peng, M. Xin, Z. Hu, Z. Ni, Q. Sun, Y. Yao, The E3 ligase TaSAP5 alters drought stress responses by promoting the degradation of DRIP proteins, Plant Physiol. 175 (2017) 1878–1892.

[64]

M.Y. Ahn, D.H. Seo, W.T. Kim, PUB22 and PUB23 U-box E3 ubiquitin ligases negatively regulate 26S proteasome activity under proteotoxic stress conditions, J. Integr. Plant Biol. 64 (2022) 625–631.

[65]

N. Wang, Y. Liu, Y. Cong, T. Wang, X. Zhong, S. Yang, Y. Li, J, Gai., Genome-wide identification of soybean U-Box E3 ubiquitin ligases and roles of GmPUB8 in negative regulation of drought stress response in Arabidopsis, Plant Cell Physiol. 57 (2016) 1189–1209.

[66]

Y. Jiang, S. Tong, N. Chen, B. Liu, Q. Bai, Y. Chen, H. Bi, Z. Zhang, S. Lou, H.u. Tang, J. Liu, T. Ma, H. Liu, The PalWRKY77 transcription factor negatively regulates salt tolerance and abscisic acid signaling in Populus, Plant J. 105 (2021) 1258–1273.

[67]

S. Tong, N. Chen, D. Wang, F. Ai, B. Liu, L. Ren, Y. Chen, J. Zhang, S. Lou, H. Liu, J. Liu, T. Ma, Y. Jiang, The U-box E3 ubiquitin ligase PalPUB79 positively regulates ABA-dependent drought tolerance via ubiquitination of PalWRKY77 in Populus, Plant Biotechnol. J. 19 (2021) 2561–2575.

[68]

T. Yoshida, J. Mogami, K. Yamaguchi-Shinozaki, ABA-dependent and ABA-independent signaling in response to osmotic stress in plants, Curr. Opin. Plant Biol. 21 (2014) 133–139.

[69]

S. Li, C. Xu, Y. Yang, G. Xia, Functional analysis of TaDi19A, a salt-responsive gene in wheat, Plant Cell Environ. 33 (2010) 117–129.

[70]

L. Wang, C. Yu, C. Chen, C. He, Y. Zhu, W. Huang, Identifification of rice Di19 family reveals OsDi19-4 involved in drought resistance, Plant Cell Rep. 33 (2014) 2047–2062.

[71]

M.A. Milla, Y. Uno, I.F. Chang, J. Townsend, E.A. Maher, D. Quilici, J.C. Cushman, A novel yeast two-hybrid approach to identify CDPK substrates: Characterization of the interaction between AtCPK11 and AtDi19, a nuclear zinc finger protein, FEBS Lett. 580 (2006) 904–911.

The Crop Journal
Pages 1152-1162
Cite this article:
Yang Y, Ren R, Karthikeyan A, et al. The soybean GmPUB21-interacting protein GmDi19-5 responds to drought and salinity stresses via an ABA-dependent pathway. The Crop Journal, 2023, 11(4): 1152-1162. https://doi.org/10.1016/j.cj.2023.05.005

293

Views

6

Downloads

5

Crossref

4

Web of Science

4

Scopus

0

CSCD

Altmetrics

Received: 04 October 2022
Revised: 28 November 2022
Accepted: 15 June 2023
Published: 28 June 2023
© 2023 Crop Science Society of China and Institute of Crop Science, CAAS.

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Return