Comprehensive identification and expression analysis of the TIFY gene family in cucumber


  • Juncheng HE Jiangxi Agricultural University, College of Bioscience and Bioengineering, Nanchang 330045 (CN)
  • Yikeng CHENG Huazhong Agricultural University, College of Plant Science and Technology, Wuhan 430070 (CN)
  • Lingdi XIAO Jiangxi Agricultural University, College of Bioscience and Bioengineering, Nanchang 330045 (CN)
  • Zhaoyang HU Jiangxi Agricultural University, College of Bioscience and Bioengineering, Nanchang 330045 (CN)
  • Yong ZHOU Jiangxi Agricultural University, College of Bioscience and Bioengineering, Nanchang 330045 (CN)
  • Shiqiang LIU Jiangxi Agricultural University, College of Bioscience and Bioengineering, Nanchang 330045 (CN)



abiotic stress, cucumber, gene expression, root-knot nematode (RKN), TIFY gene family


The TIFY family, a plant-specific gene family with the conserved motif of TIF[F/Y]XG, plays important roles in plant growth, development and abiotic stress response. This family encodes four subfamilies of proteins, including ZIM-like (ZML), TIFY, PPD and JASMONATE ZIM-domain (JAZ). In this study, 17 TIFY family genes were identified in cucumber through genome-wide analysis, including one PPD, two TIFYs, four ZMLs, and 10 JAZs. Phylogenetic analysis revealed that TIFY proteins from cucumber and other plant species can be divided into seven groups, which were designated as TIFY, JAZ I–IV, ZML and PPD. An analysis of conserved domain distribution demonstrated that there are four other domains (Jas, CCT, PPD and GATA domains) in CsTIFY proteins. Tissue expression profiling of the CsTIFY genes revealed that some of them displayed development- and tissue-specific expression patterns. Expression analysis based on transcriptome data and qRT-PCR revealed that the expression levels of some cucumber TIFY genes were altered under multiple abiotic stresses. In addition, several CsJAZ genes were downregulated in cucumber plants under root-knot nematode (RKN) infection, suggesting that they negatively affect the resistance response of cucumber to RKN. Our findings lay a foundation for further functional studies of the TIFY family genes in cucumber.


An XH, Hao YJ, Li EM, Xu K, Cheng CG (2017). Functional identification of apple MdJAZ2 in Arabidopsis with reduced JA-sensitivity and increased stress tolerance. Plant Cell Reports 36(2):255-265.

Bai Y, Meng Y, Huang D, Qi Y, Chen M (2011). Origin and evolutionary analysis of the plant-specific TIFY transcription factor family. Genomics 98(2):128-136.

Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, … Noble WS (2009). MEME SUITE: tools for motif discovery and searching. Nucleic Acids Research 37:W202-208.

Bali S, Kaur P, Sharma A, Ohri P, Bhardwaj R, Alyemeni MN, … Ahmad P (2018). Jasmonic acid-induced tolerance to root-knot nematodes in tomato plants through altered photosynthetic and antioxidative defense mechanisms. Protoplasma 255(2):471-484.

Cai Q, Yuan Z, Chen M, Yin C, Luo Z, Zhao X, … Zhang D (2014). Jasmonic acid regulates spikelet development in rice. Nature Communication 5:3476.

Chen C, Chen X, Han J, Lu W, Ren Z (2020). Genome-wide analysis of the WRKY gene family in the cucumber genome and transcriptome-wide identification of WRKY transcription factors that respond to biotic and abiotic stresses. BMC Plant Biology 20(1):443.

Cheng C, Li Q, Wang X, Li Y, Qian C, Li J, … Chen J (2020). Identification and expression analysis of the CsMYB gene family in root knot nematode-resistant and susceptible cucumbers. Frontiers in Genetics 11:550677.

Cheng Z, Sun L, Qi T, Zhang B, Peng W, Liu Y, Xie D (2011). The bHLH transcription factor MYC3 interacts with the Jasmonate ZIM-domain proteins to mediate jasmonate response in Arabidopsis. Molecular Plant 4(2):279-288.

Chini A, Ben-Romdhane W, Hassairi A, Aboul-Soud MAM (2017). Identification of TIFY/JAZ family genes in Solanum lycopersicum and their regulation in response to abiotic stresses. PLoS One 12(6):e0177381.

Chini A, Gimenez-Ibanez S, Goossens A, Solano R (2016). Redundancy and specificity in jasmonate signalling. Current Opinion in Plant Biology 33:147-156.

Chung HS, Niu Y, Browse J, Howe GA (2009). Top hits in contemporary JAZ: an update on jasmonate signaling. Phytochemistry 70(13-14):1547-1559.

de Torres Zabala M, Zhai B, Jayaraman S, Eleftheriadou G, Winsbury R, Yang R, … Grant M (2016). Novel JAZ co-operativity and unexpected JA dynamics underpin Arabidopsis defence responses to Pseudomonas syringae infection. New Phytologist 209(3):1120-1134.

Ebel C, BenFeki A, Hanin M, Solano R, Chini A (2018). Characterization of wheat (Triticum aestivum) TIFY family and role of Triticum durum TdTIFY11a in salt stress tolerance. PLoS One 13(7):e0200566.

Fernández-Calvo P, Chini A, Fernández-Barbero G, Chico JM, Gimenez-Ibanez S, Geerinck J, … Solano R (2011). The Arabidopsis bHLH transcription factors MYC3 and MYC4 are targets of JAZ repressors and act additively with MYC2 in the activation of jasmonate responses. Plant Cell 23(2):701-715.

Fu J, Wu H, Ma S, Xiang D, Liu R, Xiong L (2017). OsJAZ1 attenuates drought resistance by Regulating JA and ABA signaling in rice. Frontiers in Plant Science 8:2108.

Gonzalez N, Pauwels L, Baekelandt A, De Milde L, Van Leene J, Besbrugge N, … Inzé D (2015). A repressor protein complex regulates leaf growth in Arabidopsis. Plant Cell 27(8):2273-2287.

Guang Y, Luo S, Ahammed GJ, Xiao X, Li J, Zhou Y, Yang Y (2021). The OPR gene family in watermelon: Genome-wide identification and expression profiling under hormone treatments and root-knot nematode infection. Plant Biology (Stuttg) 23(1):80-88.

Hakata M, Muramatsu M, Nakamura H, Hara N, Kishimoto M, Iida-Okada K, … Ichikawa H (2017). Overexpression of TIFY genes promotes plant growth in rice through jasmonate signaling. Bioscience, Biotechnology, and Biochemistry 81(5):906-913.

He X, Kang Y, Li W, Liu W, Xie P, Liao L, … Hua W (2020). Genome-wide identification and functional analysis of the TIFY gene family in the response to multiple stresses in Brassica napus L. BMC Genomics 21(1):736.

Heidari P, Faraji S, Ahmadizadeh M, Ahmar S, Mora-Poblete F (2021). New insights into structure and function of TIFY genes in Zea mays and Solanum lycopersicum: A genome-wide comprehensive analysis. Frontiers in Genetics 12:657970.

Huang Z, Jin SH, Guo HD, Zhong XJ, He J, Li X, … Chen QB (2016). Genome-wide identification and characterization of TIFY family genes in Moso Bamboo (Phyllostachys edulis) and expression profiling analysis under dehydration and cold stresses. PeerJ 4:e2620.

Lee IH, Shim D, Jeong JC, Sung YW, Nam KJ, Yang JW, … Kim YH (2019). Transcriptome analysis of root-knot nematode (Meloidogyne incognita)-resistant and susceptible sweetpotato cultivars. Planta 249(2):431-444.

Li L, Liu Y, Huang Y, Li B, Ma W, Wang D, … Wang Z (2021). Genome-wide identification of the TIFY family in Salvia miltiorrhiza reveals that SmJAZ3 interacts with SmWD40-170, a relevant protein that modulates secondary metabolism and development. Frontiers in Plant Science 12:630424.

Li X, Yin X, Wang H, Li J, Guo C, Gao H, … Wang X (2015). Genome-wide identification and analysis of the apple (Malus × domestica Borkh.) TIFY gene family. Tree Genetics & Genomes 11(1):808.

Liu S, Zhang P, Li C, Xia G (2019). The moss jasmonate ZIM-domain protein PnJAZ1 confers salinity tolerance via crosstalk with the abscisic acid signalling pathway. Plant Science 280:1-11.

Ma Y, Shu S, Bai S, Tao R, Qian M, Teng Y (2018). Genome-wide survey and analysis of the TIFY gene family and its potential role in anthocyanin synthesis in Chinese sand pear (Pyrus pyrifolia). Tree Genetics & Genomes 14:25.

Madeira F, Park YM, Lee J, Buso N, Gur T, Madhusoodanan N, … Lopez R (2019). The EMBL-EBI search and sequence analysis tools APIs in 2019. Nucleic Acids Research 47(W1):W636-w641.

Nahar K, Kyndt T, De Vleesschauwer D, Höfte M, Gheysen G (2011). The jasmonate pathway is a key player in systemically induced defense against root knot nematodes in rice. Plant Physiology 157(1):305-316.

Niu Y, Figueroa P, Browse J (2011). Characterization of JAZ-interacting bHLH transcription factors that regulate jasmonate responses in Arabidopsis. Journal of Experimental Botany 62(6):2143-2154.

Saha G, Park JI, Kayum MA, Nou IS (2016). A genome-wide analysis reveals stress and hormone responsive patterns of TIFY family genes in Brassica rapa. Frontiers in Plant Science 7:936.

Shen J, Zou Z, Xing H, Duan Y, Zhu X, Ma 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(7):2433.

Singh AP, Mani B, Giri J (2021). OsJAZ9 is involved in water-deficit stress tolerance by regulating leaf width and stomatal density in rice. Plant Physiology and Biochemistry 162:161-170.

Singh AP, Pandey BK, Mehra P, Heitz T, Giri J (2020). OsJAZ9 overexpression modulates jasmonic acid biosynthesis and potassium deficiency responses in rice. Plant Molecular Biology 104(4-5):397-410.

Singh P, Mukhopadhyay K (2021). Comprehensive molecular dissection of TIFY transcription factors reveal their dynamic responses to biotic and abiotic stress in wheat (Triticum aestivum L.). Scientific Reports 11(1):9739.

Sirhindi G, Sharma P, Arya P, Goel P, Kumar G, Acharya V, Singh AK (2016). Genome-wide characterization and expression profiling of TIFY gene family in pigeon pea (Cajanus cajan (L.) Millsp.) under copper stress. Journal of Plant Biochemistry and Biotechnology 25(3):301-310.

Song S, Huang H, Wang J, Liu B, Qi T, Xie D (2017). MYC5 is involved in jasmonate-regulated plant growth, leaf senescence and defense responses. Plant and Cell Physiology 58(10):1752-1763.

Song S, Qi T, Huang H, Ren Q, Wu D, Chang C, … Xie D (2011). The Jasmonate-ZIM domain proteins interact with the R2R3-MYB transcription factors MYB21 and MYB24 to affect Jasmonate-regulated stamen development in Arabidopsis. Plant Cell 23(3):1000-1013.

Sun P, Shi Y, Valerio AGO, Borrego EJ, Luo Q, Qin J, … Yan Y (2021). An updated census of the maize TIFY family. PLoS One 16(2):e0247271.

Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G, … Browse J (2007). JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling. Nature 448(7154):661-665.

Thireault C, Shyu C, Yoshida Y, St Aubin B, Campos ML, Howe GA (2015). Repression of jasmonate signaling by a non-TIFY JAZ protein in Arabidopsis. Plant Journal 82(4):669-679.

Um TY, Lee HY, Lee S, Chang SH, Chung PJ, Oh KB, … Choi YD (2018). Jasmonate ZIM-domain protein 9 interacts with slender rice 1 to mediate the antagonistic interaction between jasmonic and gibberellic acid signals in rice. Frontiers in Plant Science 9:1866.

Vanholme B, Grunewald W, Bateman A, Kohchi T, Gheysen G (2007). The tify family previously known as ZIM. Trends in Plant Science 12(6):239-244.

Wang H, Leng X, Xu X, Li C (2020). Comprehensive analysis of the TIFY gene family and its expression profiles under phytohormone treatment and abiotic stresses in roots of Populus trichocarpa. Forests 11(3):315.

Wang X, Cheng C, Zhang K, Tian Z, Xu J, Yang S, … Chen JF (2018). Comparative transcriptomics reveals suppressed expression of genes related to auxin and the cell cycle contributes to the resistance of cucumber against Meloidogyne incognita. BMC Genomics 19(1):583.

Wang Y, Pan F, Chen D, Chu W, Liu H, Xiang Y (2017). Genome-wide identification and analysis of the Populus trichocarpa TIFY gene family. Plant Physiology and Biochemistry 115:360-371.

White DW (2006). PEAPOD regulates lamina size and curvature in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 103(35):13238-13243.

Wu H, Ye H, Yao R, Zhang T, Xiong L (2015). OsJAZ9 acts as a transcriptional regulator in jasmonate signaling and modulates salt stress tolerance in rice. Plant Science 232:1-12.

Xie DX, Feys BF, James S, Nieto-Rostro M, Turner JG (1998). COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility. Science 280(5366):1091-1094.

Yang Y, Ahammed GJ, Wan C, Liu H, Chen R, Zhou Y (2019). Comprehensive analysis of TIFY transcription factors and their expression profiles under jasmonic acid and abiotic stresses in watermelon. International Journal of Genomics 2019:6813086.

Yang YX, Wu C, Ahammed GJ, Wu C, Yang Z, Wan C, Chen J (2018). Red light-induced systemic resistance against root-knot nematode is mediated by a coordinated regulation of salicylic acid, jasmonic acid and redox signaling in watermelon. Frontiers in Plant Science 9:899.

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(3):291-305.

Yu Y, Wan Y, Jiao Z, Bian L, Yu K, Zhang G, Guo D (2019). Functional characterization of resistance to powdery mildew of VvTIFY9 from Vitis vinifera. International Journal of Molecular Sciences 20(17):4286.

Zhang G, Yan X, Zhang S, Zhu Y, Zhang X, Qiao H, … Wang X (2019). The jasmonate-ZIM domain gene VqJAZ4 from the Chinese wild grape Vitis quinquangularis improves resistance to powdery mildew in Arabidopsis thaliana. Plant Physiology and Biochemistry 143:329-339.

Zhang L, You J, Chan Z (2015a). Identification and characterization of TIFY family genes in Brachypodium distachyon. Journal of Plant Research 128(6):995-1005.

Zhang X, Ran W, Zhang J, Ye M, Lin S, Li X, … Sun X (2020). Genome-wide identification of the Tify gene family and their expression profiles in response to biotic and abiotic stresses in tea plants (Camellia sinensis). International Journal of Molecular Sciences 21(21):8316.

Zhang Z, Li X, Yu R, Han M, Wu Z (2015b). Isolation, structural analysis, and expression characteristics of the maize TIFY gene family. Molecular Genetics and Genomics 290(5):1849-1858.

Zhou J, Jia F, Shao S, Zhang H, Li G, Xia X, … Shi K (2015a). Involvement of nitric oxide in the jasmonate-dependent basal defense against root-knot nematode in tomato plants. Frontiers in Plant Science 6:193.

Zhou X, Yan S, Sun C, Li S, Li J, Xu M, … Wang L (2015b). A maize jasmonate Zim-domain protein, ZmJAZ14, associates with the JA, ABA, and GA signaling pathways in transgenic Arabidopsis. PLoS One 10(3):e0121824.

Zhou Y, Li G, Zhang L, Xu J, Hu L, Jiang L, Liu S (2020). Comprehensive genomic analysis and expression profiling of the BTB and TAZ (BT) genes in cucumber (Cucumis sativus L.). Czech Journal of Genetics and Plant Breeding 56(1):15-23.

Zhou Y, Ouyang L, Zhou D, Cai Y, He H (2021). Superoxide dismutase family genes in watermelon and their responses to different abiotic stresses. Frontiers of Agricultural Science and Engineering 8(4):645-658.

Zhu Y, Luo X, Liu X, Wu W, Cui X, He Y, Huang J (2020). Arabidopsis PEAPODs function with LIKE HETEROCHROMATIN PROTEIN1 to regulate lateral organ growth. Journal of Integrative Plant Biology 62(6):812-831.



How to Cite

HE, J., CHENG, Y., XIAO, L., HU, Z., ZHOU, Y., & LIU, S. (2022). Comprehensive identification and expression analysis of the TIFY gene family in cucumber. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 50(2), 12703.



Research Articles
DOI: 10.15835/nbha50212703