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| Genome-wide identification and characterization of the JAZ gene family and its expression patterns under various abiotic stresses in Sorghum bicolor |
DU Qiao-li1*, FANG Yuan-peng1*, JIANG Jun-mei2, CHEN Mei-qing1, LI Xiang-yang2, XIE Xin1
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1 Key Laboratory of Agricultural Microbiology, College of Agriculture, Guizhou University, Guiyang 550025, P.R.China
2 State Key Laboratory Breeding Base of Green Pesticides and Agricultural Bioengineering/Key Laboratory of Green Pesticides and Agricultural Bioengineering, Ministry of Education, Guizhou University, Guiyang 550025, P.R.China
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摘要
JAZ（The jasmonate ZIM domain）蛋白属于TIFY(TIF[F/Y]XG)家族，它是由植物特异性蛋白组成，在植物生长发育和防御反应中具有十分重要的作用。然而，对于高粱JAZ家族基因在植物响应非生物胁迫的机制尚不清楚。本研究采用隐马尔可夫模型，在高粱中共鉴定到17个JAZ基因。此外，采用实时荧光定量PCR (RT-qPCR) 对高粱JAZ基因在非生物胁迫下的表达模式进行分析。系统发育分析表明，高粱JAZ蛋白主要分为9个亚家族，其启动子区包含多种类型的启动子顺式作用元件，表明JAZ蛋白在植物的胁迫响应中起作用。RT-qPCR结果显示，SbJAZ家族基因的表达具有组织特异性，在冷、热、聚乙二醇、茉莉酸、脱落酸和赤霉素处理下，SbJAZ基因的表达出现明显差异，表明SbJAZ基因参与植物对不同胁迫的响应。此外，在大肠杆菌中表达SbJAZ1可促进重组细胞在非生物胁迫（PEG 6000、NaCl 和 40°C）下的生长。综上所述，本研究结果将有助于更好地了解高粱SbJAZ家族响应非生物胁迫的潜在分子机制。
Abstract
The jasmonate ZIM domain (JAZ) protein belongs to the TIFY ((TIF[F/Y]XG) domain protein) family, which is composed of several plant-specific proteins that play important roles in plant growth, development, and defense responses. However, the mechanism of the sorghum JAZ family in response to abiotic stress remains unclear. In the present study, a total of 17 JAZ genes were identified in sorghum using a Hidden Markov Model search. In addition, real-time quantification polymerase chain reaction (RT-qPCR) was used to analyze the gene expression patterns under abiotic stress. Based on phylogenetic tree analysis, the sorghum JAZ proteins were mainly divided into nine subfamilies. A promoter analysis revealed that the SbJAZ family contains diverse types of promoter cis-acting elements, indicating that JAZ proteins function in multiple pathways upon stress stimulation in plants. According to RT-qPCR, SbJAZ gene expression is tissue-specific. Additionally, under cold, hot, polyethylene glycol, jasmonic acid, abscisic acid, and gibberellin treatments, the expression patterns of SbJAZ genes were distinctly different, indicating that the expression of SbJAZ genes may be coordinated with different stresses. Furthermore, the overexpression of SbJAZ1 in Escherichia coli was found to promote the growth of recombinant cells under abiotic stresses, such as PEG 6000, NaCl, and 40°C treatments. Altogether, our findings help us to better understand the potential molecular mechanisms of the SbJAZ family in sorghum in response to abiotic stresses.
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Received: 09 August 2021
Accepted: 23 November 2021
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Fund: This research was funded by the National Natural Science Foundation of China (32060614 and 32272514), the Guizhou Provincial Science and Technology Project, China ([2022]091), and the China Postdoctoral Science Foundation (2022MD713740).
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| About author: DU Qiao-li, E-mail: abc245425584@163.com; FANG Yuan-peng, E-mail: fyp1290941655@yeah.net; Correspondence XIE Xin, Mobile: +86-17585108412, E-mail: ippxiexin@163.com
* These authors contributed equally to this study. |
Cite this article:
DU Qiao-li, FANG Yuan-peng, JIANG Jun-mei, CHEN Mei-qing, LI Xiang-yang, XIE Xin.
2022.
Genome-wide identification and characterization of the JAZ gene family and its expression patterns under various abiotic stresses in Sorghum bicolor. Journal of Integrative Agriculture, 21(12): 3540-3555.
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Afrin S, Huang J J, Luo Z Y. 2015. JA-mediated transcriptional regulation of secondary metabolism in medicinal plants. Science Bulletin, 60, 1062–1072.
Bailey T L, Boden M, Buske F A, Frith M, Grant C E, Clementi L, Ren J, Li W W, Noble W S. 2009. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Resarch, 37, 202–208.
Chaurasia N, Mishra Y, Rai L C. 2008. Cloning expression and analysis of phytochelatin synthase (pcs) gene from Anabaena sp. PCC 7120 offering multiple stress tolerance in Escherichia coli. Biochemical and Biophysical Research Communications, 376, 225–230.
Chen C J, Chen H, Zhang Y, Thomas H R, Frank M H, He Y H. 2020. TBtools: An integrative toolkit developed for interactive analyses of big biological data. Molecular Plant, 13, 1194–1202.
Chini A, Fonseca S, Chico J M, Fernandez-Calvo P, Solano R. 2009. The ZIM domain mediates homo- and heteromeric interactions between Arabidopsis JAZ proteins. The Plant Journal, 59, 77–87.
Chung H S, Howe G A. 2009. A critical role for the TIFY motif in repression of jasmonate signaling by a stabilized splice variant of the JASMONATE ZIM-domain protein JAZ10 in Arabidopsis. The Plant Cell, 21, 131–145.
Chen B R, Wang C Y, Wang P, Zhu Z X, Xu N, Shi G S, Yu M, Wang N, Li J H, Hou J M, Li S J, Zhou Y F, Gao S J, Lu X C, Huang R D. 2019. Genome-wide association study for starch content and constitution in sorghum (Sorghum bicolor (L.) Moench). Journal of Integrative Agriculture, 18, 2446–2456.
Bai Y H, Meng Y J, Huang D L, Qi Y H, Chen M. 2011. Origin and evolutionary analysis of the plant-specific TIFY transcription factor family. Genomics, 98, 128–136.
Demianski A J, Chung K M, Kunkel B N. 2017. Analysis of Arabidopsis JAZ gene expression during Pseudomonas syringae pathogenesis. Molecular Plant Pathology, 13, 46–57.
Derelle E, Ferraz C, Rombauts S, Rouze P, Worden A Z, Robbens S, Partensky F S, Degroeve, Echeynie S, Cooke R. 2006. Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features. Proceedings of the National Academy of Sciences of the United States of America, 103, 11647–11652.
Djanaguiraman M, Prasad P V, Murugan M, Perumal R, Reddy U K. 2014. Physiological differences among sorghum (Sorghum bicolor L. Moench) genotypes under high temperature stress. Environmental & Experimental Botany, 100, 43–54.
Farmer E E, Almeras E, Krishnamurthy V. 2003. Jasmonates and related oxylipins in plant responses to pathogenesis and herbivory. Current Opinion in Plant Biology, 6, 372–378.
Fang Y P, Jiang J M, Du Q L, Luo L T, Li X Y, Xie X. 2021. The cytochrome P450 superfamily: Evolutionary and functional divergence in sorghum (Sorghum bicolor) stress resistance. Journal of Agricultural and Food Chemistry, 69, 10952–10961.
Gangappa S N, Prasad V B, Chattopadhyay S. 2010. Functional interconnection of MYC2 and SPA1 in the photomorphogenic seedling development of Arabidopsis. Plant Physiology, 154, 1210–1219.
Gimenez-Ibanez S, Boter M, Ortigosa A, Garcia-Casado G, Chini A, Lewsey M G, Ecker J R, Ntoukakis V, Solano R. 2017. JAZ2 controls stomata dynamics during bacterial invasion. The New Phytologist, 213, 1378–1392.
Guo A Y, Zhu Q H, Chen X, Luo J C. 2007. GSDS: A gene structure display server. Hereditas, 29, 1203–1206.
Hall B G. 2013. Building phylogenetic trees from molecular data with MEGA. Molecular Biology and Evolution, 30, 1229–1235.
He X, Zhu L, Wassan G M, Wang Y, Miao Y, Shaban M, Hu H, Sun H, Zhang X. 2018. GhJAZ2 attenuates cotton resistance to biotic stresses via the inhibition of the transcriptional activity of GhbHLH171. Molecular Plant Pathology, 19, 896–908.
Hou X, Li Y, Xia K, Yan Y, Hao Y. 2010. DELLAs modulate jasmonate signaling via competitive binding to JAZs. Developmental Cell, 19, 884–894.
Hu H Y, He X, Tu L L, Zhu L F, Zhu S T, Ge Z H, Zhang X L. 2016. GhJAZ2 negatively regulates cotton fiber initiation by interacting with the R2R3-MYB transcription factor GhMYB25-like. The Plant Journal, 88, 921–935.
Hudgins J W, Christiansen E, Franceschi V R. 2004. Induction of anatomically based defense responses in stems of diverse conifers by methyl jasmonate: A phylogenetic perspective. Tree Physiology, 24, 251–264.
Jing Y X, Liu J, Liu P, Ming D F, Sun J Q. 2019. Overexpression of TaJAZ1 increases powdery mildew resistance through promoting reactive oxygen species accumulation in bread wheat. Scientific Reports, 9, 5691.
Ju L, Jing Y X, Sh P T, Liu J, Chen J S, Yan J J, Chu J F, Chen K M, Sun J Q. 2019. JAZ proteins modulate seed germination through interaction with ABI5 in bread wheat and Arabidopsis. New Phytologist, 223, 246–260.
Kafi M, Jafari M S, Moayedi A. 2018. The sensitivity of grain sorghum (Sorghum bicolor L.) developmental stages to salinity stress: an integrated approach. Journal of Agricultural Science & Technology, 15, 723–736.
Kazan K, Manners J M. 2012. JAZ repressors and the orchestration of phytohormone crosstalk. Trends in Plant Science, 17, 22–31.
Li W, Xia X C, Han L H, Ni P, Yan J Q, Tao M, Huang G Q, Li X B. 2017. Genome-wide identification and characterization of JAZ gene family in upland cotton (Gossypium hirsutum). Scientific Reports, 7, 2788.
Li X, Yin X, Wang H, Li J, Guo C, Gao H, Zheng Y, Fan C, Wang X. 2014. Genome-wide identification and analysis of the apple (Malus×domestica Borkh.) TIFY gene family. Tree Genetics & Genomes, 11, 1–13.
Liu F, Sun T, Wang L, Su W, Gao S, Su Y, Xu L, Que Y. 2017. Plant jasmonate ZIM domain genes: shedding light on structure and expression patterns of JAZ gene family in sugarcane. BMC Genomics, 18, 771.
Lorenzo O, Chico J M, Sanchez-Serrano J J, Solano R. 2004. JASMONATE-INSENSITIVE1 encodes a MYC transcription factor essential to discriminate between different jasmonate-regulated defense responses in Arabidopsis. The Plant Cell, 16, 1938–1950.
Melotto M C, Mecey Y, Niu H S, Chung L, Katsir J, Yao W, Zeng B, Thines P, Staswick J, Browse G A. 2008. A critical role of two positively charged amino acids in the JAZ motif of Arabidopsis JAZ proteins in mediating coronatine and jasmonoyl isoleucine-dependent interactions with the COI1F-box protein. The Plant Journal, 55, 979–988.
Meng L, Zhang T, Geng S, Scott P B, Li H, Chen S. 2019. Comparative proteomics and metabolomics of JAZ7-mediated drought tolerance in Arabidopsis. Journal of Proteomics, 196, 81–91.
Overmyer K, Tuominen H, Kettunen R, Betz C. 2000. Ozone-sensitive Arabidopsis rcd1 mutant reveals opposite roles for ethylene and jasmonate signaling pathways in regulating superoxide-dependent cell death. The Plant Cell, 12, 1849–1862.
Pauwels L, Barbero G F, Geerinck J, Tilleman S, Grunewald W, Perez A C, Chico J M, Bossche R V, Sewell J, Gil E. 2010. NINJA connects the co-repressor TOPLESS to jasmonate signalling. Nature, 464, 788–791.
Pauwels L, Goossens A. 2011. The JAZ proteins: A crucial interface in the jasmonate signaling cascade. The Plant Cell, 23, 3089–3100.
Pfaffl M W. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research, 29, e45.
Potter S C, Luciani A, Eddy S R, Park Y, Lopez R, Finn R D. 2018. HMMER web server: 2018 update. Nucleic Acids Research, 46, 200–204.
Schmelz E A, Huffaker A, Sims J W, Christensen S A, Lu X, Okada K, Peters R J. 2014. Biosynthesis, elicitation and roles of monocot terpenoid phytoalexins. The Plant Journal, 79, 659–678.
Shen J, Zou Z, Xing H, Duan Y, Zhu X, Ma Y, Wang Y, Fang W. 2020. Genome-wide analysis reveals stress and hormone responsive patterns of JAZ family genes in Camellia Sinensis. International Journal of Molecular Sciences, 21, 2433.
Singh A P, Pandey B K, Mehra P, Chandan R K, Jha G, Giri J. 2020. OsJAZ9 overexpression modulates jasmonic acid biosynthesis and potassium deficiency responses in rice. Plant Molecular Biology, 104, 397–410.
Sreeramaiah N G, Chattopadhyay S. 2010. MYC2, a bHLH transcript factor, modulates the adult phenotype of SPA1. Plant Signaling & Behavior, 5, 1650–1652.
Staswick P E. 2008. JAZing up jasmonate signaling. Trends in Plant Science, 13, 66–71.
Sultan S E. 2010. Plant developmental responses to the environment: eco-devo insights. Current Opinion in Plant Biology, 13, 96–101.
Sun H, Chen L, Li J, Hu M, Ullah A, He X, Yang X, Zhang X. 2017. The JASMONATE ZIM-domain gene family mediates JA signaling and stress response in cotton. Plant & Cell Physiology, 58, 2139–2154.
Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G, Nomura K, He S Y, Howe G A, Browse J. 2007. JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling. Nature, 448, 661–665.
Toda Y, Tanaka M, Ogawa D, Kurata K, Kurotani K, Habu Y, Ando T, Sugimoto K, Mitsuda N, Katoh E, Abe K, Miyao A, Hirochika H, Hattori T, Takeda S. 2013. RICE SALT SENSITIVE3 forms a ternary complex with JAZ and class-C bHLH factors and regulates jasmonate-induced gene expression and root cell elongation. The Plant Cell, 25, 1709–1725.
Vanamala J K P, Massey A R, Pinnamaneni S R, Reddivari L, Reardon K F. 2018. Grain and sweet sorghum (Sorghum bicolor L. Moench) serves as a novel source of bioactive compounds for human health. Critical Reviews in Food Science and Nutrition, 58, 2867–2881.
Vanholme B, Grunewald W, Bateman A, Kohchi T, Gheysen G. 2007. The TIFY family previously known as ZIM. Trends in Plant Science, 12, 239–244.
Wager A, Browse J. 2012. Social network: JAZ protein interactions expand our knowledge of jasmonate signaling. Frontiers in Plant Science, 3, 41.
Wang S K, Bai Y H, Shen C J, Wu Y R, Zhang S N, Jiang D A. 2010. Auxin-related gene families in abiotic stress response in Sorghum bicolor. Functional & Integrative Genomics, 10, 533–546.
Wang Y, Qiao L, Bai J, Wang P, Duan W, Yuan S, Yuan G, Zhang F, Zhang L, Zhao C. 2007. Genome-wide characterization of JASMONATE-ZIM DOMAIN transcription repressors in wheat (Triticum aestivum L.). BMC Genomics, 18, 152.
Wani S H, Kumar V, Shriram V, Sah S K. 2016. Phytohormones and their metabolic engineering for abiotic stress tolerance in crop plants. The Crop Journal, 4, 162–176.
Wu H, Ye H Y, Yao R F, Zhang T, Xiong L Z. 2015. OsJAZ9 acts as a transcriptional regulator in jasmonate signaling and modulates salt stress tolerance in rice. Plant Science, 232, 1–12.
Xu G, Guo C, Shan H, Kong H. 2012. Divergence of duplicate genes in exon-intron structure. Proceedings of the National Academy of Sciences of the United States of America, 109, 1187–1192.
Yan Y X, Christensen S, Isakeit T, Engelberth J. 2012. Disruption of OPR7 and OPR8 reveals the versatile functions of jasmonic acid in maize development and defense. The Plant Cell, 24, 1420–1436.
Ye H, Du H, Tang N, Li X, Xiong L. 2009. Identification and expression profiling analysis of TIFY family genes involved in stress and phytohormone responses in rice. Plant Molecular Biology, 71, 291–305.
Ye M, Luo S M, Xie J F, Li Y F. 2012. Silencing COI1 in rice increases susceptibility to chewing insects and impairs inducible defense. PLoS ONE, 27, e36214.
Zhang Y, Gao M, Singer S D, Fei Z, Wang H, Wang X. 2012. Genome-wide identification and analysis of the TIFY gene family in grape. PLoS ONE, 7, e44465.
Zhang Y H, Wan S Q, Wang W D, Chen J F, Huang L L, Duan M S, Yu Y B. 2018. Genome-wide identification and characterization of the CsSnRK2 family in Camellia sinensis. Plant Physiology and Biochemistry, 132, 287–296.
Zhou X, Yan S, Sun C, Li S, Li J, Xu M, Liu X, Zhang S, Zhao Q, Li Y, Fan Y R, Wang L. 2015. A maize jasmonate Zim-domain protein, ZmJAZ14, associates with the JA, ABA, and GA signaling pathways in transgenic Arabidopsis. PLoS ONE, 10, e0121824.
Zhu D, Cai H, Luo X, Bai X, Deyholos M K, Chen Q, Chen C, Ji W, Zhu Y. 2012. Over-expression of a novel JAZ family gene from Glycine soja, increases salt and alkali stress tolerance. Biochemical and Biophysical Research Communications, 426, 273–279.
Zulak K G, Bohlmann J. 2010. Terpenoid biosynthesis and specialized vascular cells of conifer defense. Journal of Integrative Plant Biology, 52, 86–97.
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