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Identification and Expression Analysis of Cellulose Synthase (CesA/Csl) Gene Superfamily Members in Peach (Prunus persica) |
ZHANG Xing-Zhen, KANG Tong-Yang, BAO Ru, LIU Xin-Li, QIN Rong-Ling, ZHAO Cai-Ping* |
College of Horticulture, Northwest A&F University, Yangling 712100, China |
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Abstract The cellulose synthase (CesA) and cellulose synthase-like (Csl) gene families belonging to the cellulose synthase gene superfamily are responsible for the biosynthesis of cellulose, hemicellulose and pectin polysaccharides of the plant cell wall, and play critical roles in plant development, growth and evolution. In this study, 36 PpCesA/Csl gene family members were identified in the Prunus persica genome, encoding 394 to 1 527 amino acids, respectively. The average molecular weight of the proteins ranged from 44.85 to 171.80 kD, and the number of introns ranged from 4 to 16, containing 20 different motifs. The subcellular localization of PpCesA/ Csl protein was diverse and can be located in chloroplasts, golgi bodies, cell membranes, cytoplasm and mitochondria. Phylogenetic analysis showed that PpCesA/Csl could be divided into 7 subfamilies (CesA, CslA, CslB, CslC, CslD, CslE and CslG). All PpCesA/Csl proteins contained 7 transmembrane domains, of which 27 members contained cellulose synthase domain PF03552 and 9 members contained glycosyltransferase family 2 domain PF00535. In addition, the other 8 PpCesA subgroup members except PpCesA2 contained zinc finger domain zf-UDP, and the other 4 CslD subgroup members except PpCslD1 contained zinc finger domain zf-RING_4. The main conserved active sites of PpCesA/Csl protein were aspartic acid D, D, D residues, followed by QxxRW motif. Most PpCesA/Csl family members contained complete amino acid sequences of this active site. The results indicated that most of the CesA/Csl genes from peach were closely related to genes in Arabidopsis thaliana, but these families had unique characteristics in terms of their gene structure, chromosomal localization, phylogeny, and deduced protein sequences, suggesting that they had evolved through different processes. The transcriptome data of 'Qian Jianbai' peach during storage were used to analyze the expression characteristics of peach CesA/Csl members in mature fruit.The results showed that most peach CesA/Csl members were not expressed or very low expression level during the storage period in 'Qian Jianbai' fruit. Finally, 1 up-regulated member (PpCslE7), 3 down-regulated members (PpCesA6, PpCesA8, PpCslG1) and 1 relatively stable member (PpCslD2) were selected from the members with high expression levels in the transcriptome for analysis of expression characteristics. The qPCR analysis of PpCesA6, PpCesA8, PpCslD2, PpCslE7 and PpCslG1 in different tissues, fruits during different development and storage periods showed that the CesA/Csl genes were constitutively expressed at different levels in different organs. Furthermore, expression analysis of CesA/Csl genes in the fruit development stage showed PpCesA6, PpCesA8 and PpCslD2 all reached the peak expression at 65 d after flowering while PpCslE7 and PpCslG1 peaked at 80 d and 35 d after flowering, respectively. During fruit storage, PpCslD2 and PpCslE7 were up-regulated in both varieties, while PpCesA8 was down-regulated. PpCslG1 was highly expressed in the early storage period of 'Qinwang' fruit, but extremely low in the storage period of 'Shahong' fruit. The family analysis and expression characteristics of CesA/Csl gene in peach provide basic data for further functional study of CesA/Csl gene in peach and other Rosaceae species.
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Received: 09 August 2021
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Corresponding Authors:
* zhcc@nwsuaf.edu.cn
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[1] 兰晓天, 胡淞, 冯磊, 等. 2019. 铁皮石斛纤维素合成酶超级基因家族生物信息学分析[J]. 河南农业科学, 48(8): 49-55. (Lan X T, Hu S, Feng L, et al.2019. Bioinformatic analysis of the cellulose synthase supergene family in Dendrobium candidum[J]. Journal of Henan Agricultural Sciences, 48(8): 49-55.) [2] 赵云峰, 林瑜, 林河通, 等. 2012. 细胞壁组分变化与果实成熟软化的关系研究进展[J].食品科技, 37(12): 29-33. (Zhao Y F, Lin Y, Lin H T, et al.2012. Change of cell wall component in fruit ripening and softening[J]. Food Science and Technology, 37(12): 29-33.) [3] 朱明月, 沈文涛, 周鹏, 等. 2005.果实成熟软化机理研究进展[J].分子植物育种, 3(3): 421-426. (Zhu M Y, Sheng W T, Zhou P, et al.2005. Research advances on mechanism of fruit ripening and softening[J]. Molecular Plant Breeding, 3(3): 421-426.) [4] Appenzeller L, Doblin M, Barreiro R, et al.2004. Cellulose synthesis in maize: Isolation and expression analysis of the cellulose synthase (CesA) gene family[J]. Cellulose, 11(3): 287-299. [5] Bernal A J, Jensen J K, Harholt J, et al.2007. Disruption of ATCSLD5 results in reduced growth, reduced xylan and homogalacturonan synthase activity and altered xylan occurrence in Arabidopsis[J]. The Plant Journal, 52(5): 791-802. [6] Bernal A J, Yoo C, Mutwil M, et al.2008. Functional analysis of the cellulose synthase-like genes CSLD1, CSLD2, and CSLD4 in tip-growing Arabidopsis cells[J]. Plant Physiology, 148(3): 1238-1253. [7] Burton R A.2006. Cellulose synthase-like CslF genes mediate the synthesis of cell wall (1,3;1,4)--D-glucans[J]. Science, 311(5769): 1940-1942. [8] Cantarel B L, Coutinho P M, Rancurel C, et al.2009. The carbohydrate-active enzymes database (CAZy): An expert resource for glycogenomics[J]. Nucleic Acids Research, 37(SI): D233-D238. [9] Cao S, Cheng H, Zhang J, et al.2019. Genome-wide identification, expression pattern analysis and evolution of the Ces/Csl gene superfamily in pineapple (Ananas comosus)[J]. Plants-Basel, 8(8): 275. [10] Carroll A, Specht C D.2011. Understanding plant cellulose synthases through a comprehensive investigation of the cellulose synthase family sequences[J]. Frontiers in Plant Science, 2: 5. [11] Cocuron J, Lerouxel O, Drakakaki G, et al.2007. A gene from the cellulose synthase-like C family encodes a beta-1,4 glucan synthase[J]. Proceedings of the National Academy of Sciences of the USA, 104(20): 8550-8555. [12] Delmer D P.1999. Cellulose biosynthesis: Exciting times for a difficult field of study[J]. Annual Review of Plant Physiology and Plant Molecular Biology, 50(1): 245-276. [13] Dhugga K S.2012. Biosynthesis of non-cellulosic polysaccharides of plant cell walls[J]. Phytochemistry, 74: 8-19. [14] Djerbi S, Lindskog M, Arvestad L, et al.2005. The genome sequence of black cottonwood (Populus trichocarpa) reveals 18 conserved cellulose synthase (CesA) genes[J]. Planta, 221(5): 739-746. [15] Doblin M S, Kurek I, Jacob-Wilk D, et al.2002. Cellulose biosynthesis in plants: From genes to rosettes[J]. Plant and Cell Physiology, 43(12): 1407-1420. [16] Doblin M S, Pettolino F A, Wilson S M, et al.2009. A barley cellulose synthase-like CSLH gene mediates (1,3;1,4)-D-glucan synthesis in transgenic Arabidopsis[J]. Proceedings of the National Academy of Sciences of the USA, 106(14): 5996-6001. [17] Farrokhi N, Burton R A, Brownfield L, et al.2006. Plant cell wall biosynthesis: Genetic, biochemical and functional genomics approaches to the identification of key genes[J]. Plant Biotechnology Journal, 4(2): 145-167. [18] Gambino G, Perrone I, Gribaudo I.2008. A rapid and effective method for RNA extraction from different tissues of grapevine and other woody plants[J]. Phytochemical Analysis, 19(6): 520-525. [19] Goubet F, Barton C J, Mortimer J C, et al.2009. Cell wall glucomannan in Arabidopsis is synthesised by CSLA glycosyltransferases, and influences the progression of embryogenesis[J]. The Plant Journal, 60(3): 527-538. [20] Hazen S P, Scott-Craig J S, Walton J D.2002. Cellulose synthase-like genes of rice[J]. Plant Physiology, 128(2): 336-340. [21] Holland N, Holland D, Helentjaris T, et al.2000. A comparative analysis of the plant cellulose synthase (CesA) gene family[J]. Plant Physiology, 123(4): 1313-1324. [22] Hu H, Zhang R, Dong S, et al.2018. AtCSLD3 and GhCSLD3 mediate root growth and cell elongation downstream of the ethylene response pathway in Arabidopsis[J]. Journal of Experimental Botany, 69(5): 1065-1080. [23] Kaur S, Dhugga K S, Beech R, et al.2017. Genome-wide analysis of the cellulose synthase-like (Csl) gene family in bread wheat (Triticum aestivum L.)[J]. BMC Plant Biology, DOI:10.1186/s12870-017-1142-z [24] Liepman A H, Cavalier D M.2012. The cellulose synthase-like A and cellulose synthase-like C families: Recent advances and future perspectives[J]. Frontiers in Plant Science, DOI:10.3389/fpls.2012.00109. [25] Liepman A H, Wilkerson C G, Keegstra K.2005. Expression of cellulose synthase-like (Csl) genes in insect cells reveals that CslA family members encode mannan synthases[J]. Proceedings of the National Academy of Sciences of the USA, 102(6): 2221-2226. [26] Little A, Lahnstein J, Jeffery D W, et al.2019. A novel (1,4)-β-linked glucoxylan is synthesized by members of the cellulose synthase-like F gene family in land plants[J]. ACS Central Science, 5(1): 73-84. [27] Little A, Schwerdt J G, Shirley N J, et al.2018. Revised phylogeny of the cellulose synthase gene superfamily: Insights into cell wall evolution[J]. Plant Physiology, 177(3): 1124-1141. [28] Li G, Liu X, Liang Y, et al.2020. Genome-wide characterization of the cellulose synthase gene superfamily in Pyrus bretschneideri and reveal its potential role in stone cell formation[J]. Functional & Integrative Genomics, 20(5): 723-738. [29] Li Y, Cheng X, Fu Y, et al.2019. A genome-wide analysis of the cellulose synthase-like (Csl) gene family in maize[J]. Biologia Plantarum, 63: 721-732. [30] Li Y, Yang T, Dai D, et al.2017. Evolution, gene expression profiling and 3D modeling of CSLD proteins in cotton[J]. BMC Plant Biology, 17(1): 1-19. [31] Nairn C J, Haselkorn T.2005. Three loblolly pine CesA genes expressed in developing xylem are orthologous to secondary cell wall CesA genes of angiosperms[J]. New Phytologist, 166(3): 907-915. [32] Park S, Szumlanski A L, Gu F, et al.2011. A role for CSLD3 during cell-wall synthesis in apical plasma membranes of tip-growing root-hair cells[J]. Nature Cell Biology, 13(8): 973-980. [33] Pauly M, Gille S, Liu L, et al.2013. Hemicellulose biosynthesis[J]. Planta, 238(4): 627-642. [34] Pear J R, Kawagoe Y, Schreckengost W E, et al.1996. Higher plants contain homologs of the bacterial celA genes encoding the catalytic subunit of cellulose synthase[J]. Proceedings of the National Academy of Sciences of the USA, 93(22): 12637-12642. [35] Persson S, Paredez A, Carroll A, et al.2007. Genetic evidence for three unique components in primary cell-wall cellulose synthase complexes in Arabidopsis[J]. Proceedings of the National Academy of Sciences of the USA, 104(39): 15566-15571. [36] Qian M, Zhang Y, Yan X, et al.2016. Identification and expression analysis of polygalacturonase family members during peach fruit softening[J]. International Journal of Molecular Sciences, 17(11): 1933. [37] Richmond T A, Somerville C R.2000. The cellulose synthase superfamily[J]. Scientific Correspondence, 124(2): 495-498. [38] Sharif R, Liu P, Wang D, et al.2021. Genome-wide characterisation and expression analysis of cellulose synthase genes superfamily under various environmental stresses in Cucumis sativus L.[J]. New Zealand Journal of Crop and Horticultural Science, 49(2-3): 127-150. [39] Song X, Xu L, Yu J, et al.2019. Genome-wide characterization of the cellulose synthase gene superfamily in Solanum lycopersicum[J]. Gene, 688: 71-83. [40] Suzuki S, Li L, Sun Y, et al.2006. The cellulose synthase gene superfamily and biochemical functions of xylem-specific cellulose synthase-like genes in Populus trichocarpa[J]. Plant Physiology, 142(3): 1233-1245. [41] Taylor N G, Gardiner J C, Whiteman R, et al.2004. Cellulose synthesis in the Arabidops is secondary cell wall[J]. Cellulose, 11(3-4): 329-338. [42] Vega-Sánchez M E, Verhertbruggen Y, Christensen U, et al.2012. Loss of cellulose synthase-like F6 function affects mixed-linkage glucan deposition, cell wall mechanical properties, and defense responses in vegetative tissues of rice[J]. Plant Physiology, 159(1): 56-69. [43] Verhertbruggen Y, Yin L, Oikawa A, et al.2011. Mannan synthase activity in the CSLD family[J]. Plant Signaling & Behavior, 6(10): 1620-1623. [44] Yang J, Bak G, Burgin T, et al.2020. Biochemical and genetic analysis identify CSLD3 as a beta-1,4-glucan synthase that functions during plant cell wall synthesis[J]. The Plant Cell, 32(5): 1749-1767. [45] Yin L, Verhertbruggen Y, Oikawa A, et al.2011. The cooperative activities of CSLD2, CSLD3, and CSLD5 are required for normal Arabidopsis development[J]. Molecular Plant, 4(6): 1024-1037. [46] Yin Y, Huang J, Xu Y, et al.2009. The cellulose synthase superfamily in fully sequenced plants and algae[J]. BMC Plant Biology, 9(1): 99. [47] Yin Y, Johns M A, Cao H, et al.2014. A survey of plant and algal genomes and transcriptomes reveals new insights into the evolution and function of the cellulose synthase superfamily[J]. BMC Genomics, 15(1): 260. |
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