Abstract
Cucumber (Cucumis sativus L.) is a member of the Cucurbitaceae family and can be eaten raw in salads or cooked as a vegetable. The yield of cucumber is limited due to many factors including biotic and abiotic stresses. Tubby-like proteins (TLP) family genes are important regulators of growth and development in plants and are involved in a variety of biotic and abiotic stress responses. The specific function of the TLP family in cucumber has not been thoroughly investigated by a genetic study. Hence, we performed a comparative genomic analysis of cucumber TLP family genes using bioinformatics techniques. Herein, a total of 11 TLP proteins were identified from the cucumber genome and further divided into four different subgroups. Moreover, these CsTLPs were distributed randomly on the five chromosomal positions of cucumber. Motif analysis suggested that motif1 was commonly present in all CsTLPs proteins except CsTLP6. Gene ontology analysis of CsTLPs showed their involvement in the plasma membrane, cellular protein modifications, signal transduction, and stress responses. Similarly, Cis-acting elements showed stress-related elements, validating their role in mitigating various stresses. Expression profiling indicated that CsTLPs expressed dominantly with diverse expression patterns in various organs of the cucumber. The genes CsTLP2, CsTLP5, CsTLP7, and CsTLP10 showed higher expression as compared to the rest of the CsTLPs members under salt stress. The above findings and details can serve as a starting point for further research on TLP function in plants, especially in cucumbers.
Similar content being viewed by others
Data availability
All the relevant data are within the paper and its supporting information file.
References
Altaf A, Zada A, Hussain S, Gull S, Ding Y, Tao R, Zhu M, Zhu X (2022a) Genome-wide identification, characterization, and expression analysis of tubby gene family in wheat (triticum aestivum l.) under biotic and abiotic stresses. Agronomy 12(5):1121
Altaf MA, Shahid R, Ren M-X, Naz S, Altaf MM, Khan LU, Tiwari RK, Lal MK, Shahid MA, Kumar R (2022b) Melatonin improves drought stress tolerance of tomato by modulating plant growth, root architecture, photosynthesis, and antioxidant defense system. Antioxidants 11(2):309
Anderson RJ, Weng Z, Campbell RK, Jiang X (2005) Main-chain conformational tendencies of amino acids. Proteins: Struct, Funct, Bioinform 60(4):679–689
Bano N, Fakhrah S, Mohanty CS, Bag SK (2021) Genome-wide identification and evolutionary analysis of gossypium tubby-like protein (tlp) gene family and expression analyses during salt and drought stress. Front Plant Sci 12:667929
Bano N, Aalam S, Bag SK (2022a) Tubby-like proteins (tlps) transcription factor in different regulatory mechanism in plants: a review. Plant Mol Biol. https://doi.org/10.1007/s11103-022-01301-9
Bano N, Aalam S, Bag SK (2022b) Tubby-like proteins (tlps) transcription factor in different regulatory mechanism in plants: a review. Plant Mol Biol 110(6):455–468
Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, Xia R (2020) Tbtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant 13(8):1194–1202
Elik A, Yanik DK, Istanbullu Y, Guzelsoy NA, Yavuz A, Gogus F (2019) Strategies to reduce post-harvest losses for fruits and vegetables. Strategies 5(3):29–39
Endler A, Kesten C, Schneider R, Zhang Y, Ivakov A, Froehlich A, Funke N, Persson S (2015) A mechanism for sustained cellulose synthesis during salt stress. Cell 162(6):1353–1364
Gasteiger E, Hoogland C, Gattiker A, Wilkins MR, Appel RD, Bairoch A (2005) Protein identification and analysis tools on the ExPASy server. Humana Press
Haider MS, Khan N, Pervaiz T, Zhongjie L, Nasim M, Jogaiah S, Mushtaq N, Jiu S, Jinggui F (2019) Genome-wide identification, evolution, and molecular characterization of the pp2c gene family in woodland strawberry. Gene 702:27–35
Horton P, Park K-J, Obayashi T, Fujita N, Harada H, Adams-Collier C, Nakai K (2007) Wolf PSORT: protein localization predictor. Nucl Acids Res 35:W585–W587
Iantcheva A, Zhiponova M, Revalska M, Heyman J, Dincheva I, Badjakov I, De Geyter N, Boycheva I, Goormachtig S, De Veylder L (2022) A common f-box gene regulates the leucine homeostasis of medicago truncatula and arabidopsis thaliana. Protoplasma 259(2):277–290
Iqbal I, Tripathi RK, Wilkins O, Singh J (2020) Thaumatin-like protein (tlp) gene family in barley: genome-wide exploration and expression analysis during germination. Genes 11(9):1080
Jain N, Khurana P, Khurana JP (2022) Overexpression of a rice tubby–like protein-encoding gene, OsFBT4, confers tolerance to abiotic stresses. Protoplasma 260(4):1063–1079
Jiu S, Haider MS, Kurjogi MM, Zhang K, Zhu X, Fang J (2018) Genome-wide characterization and expression analysis of sugar transporter family genes in woodland strawberry. The Plant Genome 11(3):170103
Kou Y, Qiu D, Wang L, Li X, Wang S (2009) Molecular analyses of the rice tubby-like protein gene family and their response to bacterial infection. Plant Cell Rep 28:113–121
Li S, Wang Z, Wang F, Lv H, Cao M, Zhang N, Li F, Wang H, Li X, Yuan X (2021a) A tubby-like protein CsTLP8 acts in the aba signaling pathway and negatively regulates osmotic stresses tolerance during seed germination. BMC Plant Biol 21(1):1–14
Li Z, Wang X, Cao X, Chen B, Ma C, Lv J, Sun Z, Qiao K, Zhu L, Zhang C (2021b) GhTULP34, a member of tubby-like proteins, interacts with GhSKP1A to negatively regulate plant osmotic stress. Genomics 113(1):462–474
Li P, Xu Y, Wang K, Guo W, Gu Y, Lyu S, Huang J, Lin H, Huang C, Xu Z (2022a) Genome-wide identification of TLP gene family and their roles in Carya cathayensis sarg in response to Botryosphaeria dothidea. Front Plant Sci 13:849043
Li S, Wang G, Chang L, Sun R, Wu R, Zhong C, Gao Y, Zhang H, Wei L, Wei Y (2022b) Genome-wide identification, characterization, and expression analysis of tubby-like protein (TLP) gene family members in woodland strawberry (Fragaria vesca). Int J Mol Sci 23(19):11961
Liu S, Gao P, Zhu Q, Zhu Z, Liu H, Wang X, Weng Y, Gao M, Luan F (2020) Resequencing of 297 melon accessions reveals the genomic history of improvement and loci related to fruit traits in melon. Plant Biotechnol J 18(12):2545–2558
Musmade A, Desai U (1998) Cucumber and melon. Handbook of vegetable science and technology, CRC Press, pp 263–290
Paes de Melo B, Carpinetti PdA, Fraga OT, Rodrigues-Silva PL, Fioresi VS, de Camargos LF, Ferreira MFdS (2022) Abiotic stresses in plants and their markers: a practice view of plant stress responses and programmed cell death mechanisms. Plants 11(9):1100
Plasterer TN (1997) Mapdraw: sequence data analysis guidebook. Springer, pp 241–256
Rahim AA, Uzair M, Rehman N, Rehman OU, Zahra N, Khan MR (2022) Genome-wide identification and characterization of receptor-like protein kinase 1 (RPK1) gene family in triticum aestivum under drought stress. Front Genet 13:912251
Ram C, Danish S, Kesawat MS, Panwar BS, Verma M, Arya L, Yadav S, Sharma V (2022) Genome-wide comprehensive characterization and expression analysis of TLP gene family revealed its responses to hormonal and abiotic stresses in watermelon (Citrullus lanatus). Gene 844:146818
Rehman OU, Uzair M, Chao H, Fiaz S, Khan MR, Chen M (2022) Role of the type-B authentic response regulator gene family in fragrant rice under alkaline salt stress. Physiol Plant 174(3):e13696
Saleem B, Farooq U, Rehman OU, Aqeel M, Farooq MS, Naeem MK, Inam S, Ajmal W, Rahim AA, Chen M (2022) Genome-wide and molecular characterization of the DNA replication helicase 2 (DNA2) gene family in rice under drought and salt stress. Front Genet 13:1039548
Thompson JD, Gibson TJ, Higgins DG (2003) Multiple sequence alignment using clustalw and clustalx. Curr Protoc Bioinform 1:2–3
Wang T, Hu J, Ma X, Li C, Yang Q, Feng S, Li M, Li N, Song X (2020) Identification, evolution and expression analyses of whole genome-wide TLP gene family in brassica napus. BMC Genomics 21(1):1–14
Wang K, Cheng Y, Yi L, He H, Zhan S, Yang P (2021) Genome-wide identification of the tubby-like protein (TLPs) family in medicinal model plant salvia miltiorrhiza. PeerJ 9:e11403
Wang J, Wu R, Shangguan T, Chen G, Zheng Y, Tao X, Li S, Wang Y, Xu S (2022) NDR1/HIN1-like genes may regulate glycine max seed germination under chilling stress through the aba pathway. Plant Growth Regul 98(3):613–624
Wehner TC, Naegele RP, Myers JR, Narinder P, Crosby K (2020) Cucurbits. CABI
Xu J-N, Xing S-S, Zhang Z-R, Chen X-S, Wang X-Y (2016a) Genome-wide identification and expression analysis of the tubby-like protein family in the Malus domestica genome. Front Plant Sci 7:1693
Xu JN, Xing SS, Zhang ZR, Chen XS, Wang XY (2016b) Genome-wide identification and expression analysis of the tubby-like protein family in the malus domestica genome. Front Plant Sci. https://doi.org/10.3389/fpls.2016.01693
Xu K, Wu N, Yao W, Li X, Zhou Y, Li H (2021) The biological function and roles in phytohormone signaling of the f-box protein in plants. Agronomy 11(11):2360
Xu H, Liu Y, Yu T, Hou Z, Zheng J, Chen J, Zhou Y, Chen M, Fu J, Ma Y (2022) Comprehensive profiling of tubby-like proteins in soybean and roles of the GmTLP8 gene in abiotic stress responses. Front Plant Sci 13:844545
Yadav BG, Aakanksha KR, Yadava SK, Kumar A, Ramchiary N (2023) Understanding the proteomes of plant development and stress responses in Brassica crops. J Proteome Res 22(3):660–680
Yang L, Sagar V (2022) Genome evaluation of cucumber in relation to cucurbit family: the cucumber genome. Springer, pp 105–119
Yang H, Tao Y, Zheng Z, Zhang Q, Zhou G, Sweetingham MW, Howieson JG, Li C (2013) Draft genome sequence, and a sequence-defined genetic linkage map of the legume crop species Lupinus angustifolius L. PLoS ONE 8(5):e64799
Yu J, Wu S, Sun H, Wang X, Tang X, Guo S, Zhang Z, Huang S, Xu Y, Weng Y (2022) CuGenDBv2: an updated database for cucurbit genomics. Nucl Acids Res 51(D1):D1457–D1464
Zeng Y, Fu J, Geng H, Dan Z, Zhao W, Xu W, Huang W (2022) Genome-wide identification and comprehensive analysis of tubby-like protein gene family in multiple crops. Front Plant Sci 13:1093944
Zhang Y, He X, Su D, Feng Y, Zhao H, Deng H, Liu M (2020) Comprehensive profiling of tubby-like protein expression uncovers ripening-related TLP genes in tomato (Solanum lycopersicum). Int J Mol Sci 21(3):1000
Acknowledgements
The authors extend their appreciation to the Researchers Supporting Project number (RSP-2024R369), King Saud University, Riyadh, Saudi Arabia. We acknowledge the Chinese Government for providing scholarships to I.U. for completing his M.Sc. degree research. We are thankful to National Institute for Genomics and Advanced Biotechnology (NIGAB), Pakistan, and Hongzhi’s Lab, China for providing the research facilities.
Funding
This research was conducted with the funds of the Science and Technology Program of Yunnan Province (Grant No. 202102AE090051) and the Yunnan Provincial Science and Technology Talent and Platform Project (202205AF150017).
Author information
Authors and Affiliations
Contributions
Conceptualization, IU, MU, JL, and HW; methodology, software, and validation, OR, MS, SA, HA, MARR, SF, and IU; formal analysis and investigation, IU, OR, and MU; writing—original draft preparation, review, and editing, IU, MU, SA, SJS, KAA, AMA, IK, MARR, and HW; visualization, MU; supervision, HW, RC, and JL; funding acquisition, HW. All authors have read and agreed to the published version of the manuscript.
Corresponding authors
Ethics declarations
Conflicts of interest
The authors declare no conflict of interest.
Ethical approval and consent to participate
Not applicable.
Consent for publication
Not applicable.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Ullah, I., Uzair, M., Rehman, O.U. et al. Characterization of the tubby-like proteins (TLPs) gene family in Cucumis sativus L.: insights into the evolution, structure, and expression patterns under salt stress. Genet Resour Crop Evol 71, 2019–2036 (2024). https://doi.org/10.1007/s10722-023-01722-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10722-023-01722-5