|
|
|
| Identification and Expression Analysis of the Aquaporin (AQP) Gene Family in Tigernut (Cyperus esculentus) |
| LIU Liu, GAO Huang-Zhi, ZHOU Hou-Ying, ZHOU Qi-Mi LIU, Yun TIAN, Zhi-Hong, HE Yong* |
| College of Life Science, Yangtze University, Jingzhou 434025, China |
|
|
|
|
Abstract Aquaporin (AQP) widely distributes throughout plants, mainly mediates the transmembrane transport of water and small molecule solutes, and plays an important role in plant growth and development in terms of water transport and stress resistance. Tigernut (Cyperus esculentus) is one of the oilseed crops with high oleic and linoleic acid content. In order to identify the AQP gene family and analyze its functions of tigernut, in this study, a total of 33 AQP genes were identified in tigernut using bioinformatics methods, which were analysed mainly in terms of phylogeny, physicochemical properties, gene structure, conserved motifs and promoter cis-acting elements, etc. qPCR was used to detect expression changes in selected members under salt stress. The results showed that members of the oilseed rape AQP gene family exhibited diversity in physicochemical properties such as amino acid content, protein molecular weight, and isoelectric point. Most AQP proteins demonstrated good stability, with subcellular localization studies showing the majority localized to the cell membrane and a minority to the vacuole. Based on phylogenetic relationships, the tigernut AQP gene family could be primarily classified into 4 subfamilies: PIP, TIP, SIP, and NIP, comprising 14, 10, 2 and 7 members, respectively. Genes within the same subfamily shared similar gene structures and conserved motifs, whereas differences existed between members of different subfamilies. Promoter cis-acting elements comprised 4 major categories: Light-responsive elements, plant hormone-responsive elements, growth and development-related elements, and abiotic stress-related elements. Among these, light-responsive elements were the most abundant, while growth and development-related elements were the least numerous. The expression of AQP gene family members in tigernut after salt stress treatment had different trends, suggesting their potential involvement in tigernut's salt stress response mechanisms. This study provides a reference for further functional analyses of water channel proteins.
|
|
Received: 26 May 2025
|
|
|
|
Corresponding Authors:
* warers@yangtzeu.edu.cn
|
|
|
|
[1] 包珠拉太, 高丽, 王锁民. 2017. 植物水通道蛋白及其生理功能[J]. 植物生理学报, 53(7): 1171-1178.
(Bao Z L T, Gao L, Wang S M.2017. Physiological functions of plant aquaporin[J]. Plant Physiology Journal, 53(7): 1171-1178.)
[2] 郝建峰. 2020. 棉花水通道蛋白家族基因鉴定及其渗透胁迫应答功能研究[D]. 硕士学位论文,郑州大学, 导师: 田保明, 师恭曜, pp. 50-58.
(Hao J F.2020. Genome-wide identification of aquaporin gene family in cotton and functional characterization in response to osmotic stresses[D]. Thesis for M.S., Zhengzhou University, Supervisor: Tian B M, Shi G Y, pp. 50-58.)
[3] 李菲, 何小红, 李育柯, 等. 2018. 番茄水通道蛋白基因家族的生物信息学分析[J]. 基因组学与应用生物学, 37(9): 3950-3957.
(Li F, He X H, Li Y K, et al.2018. Bioinformatic analysis of tomato aquaporin gene family[J]. Genomics and Applied Biology, 37(9): 3950-3957.)
[4] 李嵘, 牛向丽, 苗雁文, 等. 2013. 水通道蛋白基因OsPIP2;6的功能分析[J]. 中国农业科学, 46(15): 3079-3086.
(Li R, Niu X L, Miao Y W, et al.2013. Functional characterization of the plasma intrinsic protein gene OsPIP2;6 in rice[J]. Scientia Agricultura Sinica, 46(15): 3079-3086.)
[5] 唐榕. 2022. 油莎豆种子萌发和植株生长对盐碱胁迫的响应[D]. 硕士学位论文, 石河子大学, 导师: 刘建国, 杨相昆, pp. 9-28.
(Tang R.2022. Response of seed germination and plant growth to saline alkali stress of Cyperus esculentus L.[D]. Thesis for M.S., Shihezi University, Supervisor: Liu J G, Yang X K, pp. 9-28.)
[6] 尹延旭. 2014. 辣椒水通道蛋白基因家族分析及CaTIP1-1和CaPIP1-1功能研究[D]. 博士学位论文, 西北农林科技大学, 导师: 巩振辉, pp. 9-21.
(Yin Y X.2014. Genome-wide analysis of aquaporins in pepper and functional characterization of CaTIP1-1 and CaPIP1-1 genes[D]. Thesis for Ph.D., Northwest Agriculture and Forestry University, Supervisor: Gong Z H, pp. 9-21.)
[7] 张琳琳, 于明含, 丁国栋, 等. 2022. 盐碱胁迫对油沙豆生长和生理特性的影响[J]. 中国水土保持科学, 20(2): 65-71.
(Zhang L L, Yu M H, Ding G D, et al.2022. Effects of salt and alkali stress on the growth and physiological characteristics of Cyperus esculentus[J]. Science of Soil and Water Conservation, 20(2): 65-71.)
[8] 张璐, 杜相革. 2014. 植物水孔蛋白研究进展[J]. 植物科学学报, 32(3): 304-314.
(Zhang L, Du X G.2014. Recent advances in plant aquaporins[J]. Plant Science Journal, 32(3): 304-314.)
[9] 郑玉皎, 常丽丽, 赵永国, 等. 2024. 油莎豆块茎高水平表达CePIP1;1基因的克隆与分析[J]. 热带作物学报, 45(5): 894-901.
(Zheng Y J, Chang L L, Zhao Y G, et al.2024. Molecular cloning and characterization of CePIP1;1, an aquaporin gene highly abundant in Cyperus esculentus tubers[J]. Chinese Journal of Tropical Crops, 45(5): 894-901.)
[10] 邹智, 郑玉皎, 常丽丽, 等. 2024. 油莎豆CePIP2;1的克隆、亚细胞定位与表达分析[J]. 热带作物学报, 45(7): 1340-1347.
(Zou Z, Zheng Y J, Chang L L, et al.2024. Cloning, subcellular localization, and expression analysis of CePIP2;1, an aquaporin gene from tigernut (Cyperus esculentus L.)[J]. Chinese Journal of Tropical Crops, 45(7): 1340-1347.)
[11] Alexandersson E, Fraysse L, Sjövall-Larsen S, et al.2005. Whole gene family expression and drought stress regulation of aquaporins[J]. Plant Molecular Biology, 59: 469-484.
[12] Anderberg H I, Kjellbom P, Johanson U.2012. Annotation of Selaginella moellendorffii major intrinsic proteins and the evolution of the protein family in terrestrial plants[J]. Frontiers in Plant Science, 3: 33.
[13] Azad A K, Sawa Y, Ishikawa T, et al.2004. Phosphorylation of plasma membrane aquaporin regulates temperature-dependent opening of tulip petals[J]. Plant and Cell Physiology, 45(5): 608-617.
[14] Bhardwaj R, Sharma I, Kanwar M, et al.2013. Ecophysiology and Responses of Plants under Salt Stress[M], Springer, New York, USA, pp. 213-248.
[15] Boursiac Y, Chen S, Luu D T, et al.2005. Early effects of salinity on water transport in Arabidopsis roots. Molecular and cellular features of aquaporin expression[J]. Plant Physiology, 139(2): 790-805.
[16] Chaumont F, Barrieu F, Wojcik E, et al.2001. Aquaporins constitute a large and highly divergent protein family in maize[J]. Plant Physiology, 125(3): 1206-1215.
[17] Codina-Torrella I, Guamis B, Trujillo A J.2015. Characterization and comparison of tiger nuts (Cyperus esculentus L.) from different geographical origin physico-chemical characteristics and protein fractionation[J]. Industrial Crops and Products, 65: 406-414.
[18] Danielson J Å H, Johanson U.2008. Unexpected complexity of the aquaporin gene family in the moss Physcomitrella patens[J]. BMC Plant Biology, 8: 45.
[19] De Castro O, Gargiulo R, Del Guacchio E, et al.2015. A molecular survey concerning the origin of Cyperus esculentus (Cyperaceae, Poales): Two sides of the same coin (weed vs. crop)[J]. Annals of Botany, 115: 733-745.
[20] Defelice M S.2002. Yellow nutsedge Cyperus esculentus L.—snack food of the gods[J]. Weed Technology, 16: 901-907.
[21] Deshmukh R K, Vivancos J, Ramakrishnan G, et al.2015. A precise spacing between the NPA domains of aquaporins is essential for silicon permeability in plants[J]. The Plant Journal, 83: 489-500.
[22] Forrest K L, Bhave M.2008. The PIP and TIP aquaporins in wheat form a large and diverse family with unique gene structures and functionally important features[J]. Functional & Integrative Genomics, 8: 115-133.
[23] Fricke W, Akhiyarova G, Wei W X, et al.2006. The short-term growth response to salt of the developing barley leaf[J]. Journal of Experimental Botany, 57(5): 1079-1095.
[24] Gerbeau P, Güçlü J, Ripoche P, et al.1999. Aquaporin Nt-TIPa can account for the high permeability of tobacco cell vacuolar membrane to small neutral solutes[J]. The Plant Journal, 18(6): 577-587.
[25] Groszmann M, De Rosa A, Ahmed J, et al.2021. A consensus on the aquaporin gene family in the allotetraploid plant, Nicotiana tabacum[J]. Plant Direct, 5(5): e00321.
[26] Gu R L, Chen X L, Zhou Y L, et al.2012. Isolation and characterization of three maize aquaporin genes, ZmNIP2;1, ZmNIP2;4 and ZmTIP4;4 involved in urea transport[J]. BMB Reports, 45(2): 96-101.
[27] Gupta A B, Sankararamakrishnan R.2009. Genome-wide analysis of major intrinsic proteins in the tree plant Populus trichocarpa: Characterization of XIP subfamily of aquaporins from evolutionary perspective[J]. BMC Plant Biology, 9: 134.
[28] Harries W E C, Akhavan D, Miercke L J W, et al.2004. The channel architecture of aquaporin 0 at a 2.2-Å resolution[J]. Proceedings of the National Academy of Sciences of the USA, 101(39): 14045-14050.
[29] Kumar K, Mosa K A, Chhikara S, et al.2014. Two rice plasma membrane intrinsic proteins, OsPIP2;4 and OsPIP2;7, are involved in transport and providing tolerance to boron toxicity[J]. Planta, 239: 187-198.
[30] Lee J K, Kozono D, Remis J, et al.2005. Structural basis for conductance by the archaeal aquaporin AqpM at 1.68 Å[J]. Proceedings of the National Academy of Sciences of the USA, 102(52): 18932-18937.
[31] Maathuis F J M, Filatov V, Herzyk P, et al.2003. Transcriptome analysis of root transporters reveals participation of multiple gene families in the response to cation stress[J]. The Plant Journal, 35: 675-692.
[32] Madrid-Espinoza J, Brunel-Saldias N, Guerra F P, et al.2018. Genome-wide identification and transcriptional regulation of aquaporin genes in bread wheat (Triticum aestivum L.) under water stress[J]. Genes, 9: 497.
[33] Makareviciene V, Gumbyte M, Yunik A, et al.2013. Opportunities for the use of chufa sedge in biodiesel production[J]. Industrial Crops and Products, 50: 633-637.
[34] Maurel C, Boursiac Y, Luu D T, et al.2015. Aquaporins in plants[J]. Physiological Reviews, 95: 1321-1358.
[35] Maurel C, Reizer J, Schroeder J I, et al.1993. The vacuolar membrane protein γ-TIP creates water specific channels in Xenopus oocytes[J]. The EMBO Journal, 12(6): 2241-2247.
[36] Maurel C, Verdoucq L, Luu D T, et al.2008. Plant aquaporins: Membrane channels with multiple integrated functions[J]. Annual Review of Plant Biology, 59: 595-624.
[37] Nguyen M X, Moon S, Jung K H.2013. Genome-wide expression analysis of rice aquaporin genes and development of a functional gene network mediated by aquaporin expression in roots[J]. Planta, 238(4): 669-681.
[38] Postaire O, Tournaire-Roux C, Grondin A, et al.2010. A PIP1 aquaporin contributes to hydrostatic pressure-induced water transport in both the root and rosette of Arabidopsis[J]. Plant Physiology, 152: 1418-1430.
[39] Reddy P S, Rao T S R B, Sharma K K, et al.2015. Genome-wide identfication and characterization of the aquaporin gene family in Sorghum bicolor (L.)[J]. Plant Gene, 1: 18-28.
[40] Savage D F, Egea P F, Robles-Colmenares Y, et al.2003. Architecture and selectivity in aquaporins 2.5: Å x-ray structure of aquaporin Z[J]. Plos Biology, 1(3): 334-340.
[41] Steudle E.2000. Water uptake by plant roots: an integration of views[J]. Plant and Soil, 226: 45-56.
[42] Su Y C, Liu Z H, Sun J H, et al.2022. Genome-wide identification of maize aquaporin and functional analysis during seed germination and seedling establishment[J]. Frontiers in Plant Science, 13: 831916.
[43] Takano J, Wada M, Ludewig U, et al.2006. The Arabidopsis major intrinsic protein NIP5;1 is essential for efficient boron uptake and plant development under boron limitation[J]. The Plant Cell, 18(6): 1498-1509.
[44] Tournaire-Roux C, Sutka M, Javot H, et al.2003. Cytosolic pH regulates root water transport during anoxic stress through gating of aquaporins[J]. Nature, 425(6956): 393-397.
[45] Xu J, Liu L, Kang F, et al.2024. Abscisic acid-mediated yield gain through reduced oxidative damage caused by salt and water stress in Cyperus esculentus[J]. Frontiers of Agricultural Science and Engineering, 11(4): 561-574.
[46] Zardoya R, Villalba S.2001. A phylogenetic framework for the aquaporin family in eukaryotes[J]. Journal of Molecular Evolution, 52(5): 391-404.
[47] Zhang D Y, Ali Z, Wang C B, et al.2013. Genome-wide sequence characterization and expression analysis of major intrinsic proteins in soybean (Glycine max L.)[J]. PLOS ONE, 8(2): e56312.
[48] Zhang S G, Li P Z, Wei Z M, et al.2022. Cyperus (Cyperus esculentus L.): A review of its compositions, medical efficacy, antibacterial activity and allelopathic potentials[J]. Plants, 11: 1127.
[49] Zou Z, Zheng Y J, Chang L L, et al.2024. TIP aquaporins in Cyperus esculentus: Genome-wide identification, expression profiles, subcellular localizations, and interaction patterns[J]. BMC Plant Biology, 24: 298. |
|
|
|
