Abstract
The Cellulose Synthase gene (CS) superfamily and COBRA-like (COBL) gene family are essential for synthesizing cellulose and hemicellulose, which play a crucial role in cell wall biosynthesis and the hardening of plant tissues. Our study identified 126 ZbCS and 31 ZbCOBL genes from the Zanthoxylum bungeanum (Zb) genome. Phylogenetic analysis and conservative domain analysis unfolded that ZbCS and ZbCOBL genes were divided into seven and two subfamilies, respectively. Gene duplication data suggested that more than 75% of these genes had tandem and fragment duplications. Codon usage patterns analysis indicated that the ZbCS and ZbCOBL genes prefer ending with A/T base, with weak codon preference. Furthermore, seven key ZbCS and five key ZbCOBL genes were identified based on the content of cellulose and hemicellulose and the expression characteristics of ZbCS and ZbCOBL genes in various stages of stipule thorns. Altogether, these results improve the understanding of CS and COBL genes and provide valuable reference data for cultivating Zb with soft thorns.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The data that has been used is confidential.
References
Aouar L, Chebli Y, Geitmann A (2010) Morphogenesis of complex plant cell shapes: the mechanical role of crystalline cellulose in growing pollen tubes. Sex Plant Reprod 23:15–27. https://doi.org/10.1007/s00497-009-0110-7
Betts MJ, Guigo R, Agarwal P, Russell RB (2001) Exon structure conservation despite low sequence similarity: a relic of dramatic events in evolution? EMBO J 20:5354–5360. https://doi.org/10.1093/emboj/20.19.5354
Brady SM, Song S, Dhugga KS, Rafalski JA, Benfey PN (2007) Combining expression and comparative evolutionary analysis. COBRA Gene Family Plant Physiol 143:172–187. https://doi.org/10.1104/pp.106.087262
Cannon SB, Mitra A, Baumgarten A, Young ND, May G (2004) The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol 4:10. https://doi.org/10.1186/1471-2229-4-10
Cao S, Cheng H, Zhang J, Aslam M, Yan M, Hu A, Lin L, Ojolo SP, Zhao H, Priyadarshani S, Yu Y, Cao G, Qin Y (2019) Genome-wide identification, expression pattern analysis and evolution of the Ces/Csl gene superfamily in pineapple (Ananas comosus). Plants (basel). https://doi.org/10.3390/plants8080275
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 13:1194–1202. https://doi.org/10.1016/j.molp.2020.06.009
Cosgrove DJ (2015) Plant expansins: diversity and interactions with plant cell walls. Curr Opin Plant Biol 25:162–172. https://doi.org/10.1016/j.pbi.2015.05.014
Delmer DP, Haigler CH (2002) The regulation of metabolic flux to cellulose, a major sink for carbon in plants. Metab Eng 4:22–28. https://doi.org/10.1006/mben.2001.0206
Fankhauser C, Christie JM (2015) Plant phototropic growth. Curr Biol 25:R384–389. https://doi.org/10.1016/j.cub.2015.03.020
Fei XT, Li JM, Kong LJ, Hu HC, Tian JY, Liu YL, Wei AZ (2020) miRNAs and their target genes regulate the antioxidant system of Zanthoxylum bungeanum under drought stress. Plant Physiol Biochem 150:196–203. https://doi.org/10.1016/j.plaphy.2020.01.040
Feng SJ, Liu ZS, Cheng J, Li ZH, Tian L, Liu M, Yang TX, Liu YL, Liu YH, Dai H, Yang ZJ, Zhang Q, Wang G, Zhang JS, Jiang HF, Wei AZ (2021) Zanthoxylum-specific whole genome duplication and recent activity of transposable elements in the highly repetitive paleotetraploid Z. bungeanum genome. Horticulture Research. https://doi.org/10.1038/s41438-021-00665-1
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. Front Plant Sci 8:2108. https://doi.org/10.3389/fpls.2017.02108
Guo C, Quan S, Zhang Z, Kang C, Liu J, Niu J (2022) Genome-wide identification, characterization and expression profile of TALE gene family in (Juglans regia L.). Sci Hortic 297:110945. https://doi.org/10.1016/j.scienta.2022.110945
Hazen SP, Scott-Craig JS, Walton JD (2002) Cellulose synthase-like genes of rice. Plant Physiol 128:336–340. https://doi.org/10.1104/pp.128.2.336
He L, Chen X, Xu MZ, Liu TT, Zhang TY, Li J, Yang J, Chen JP, Zhong KL (2021) Genome-wide identification and characterization of the cystatin gene family in bread wheat (Triticum aestivum L.). Int J Mol Sci. https://doi.org/10.3390/ijms221910264
Hematy K, Sado PE, Van Tuinen A, Rochange S, Desnos T, Balzergue S, Pelletier S, Renou JP, Hofte H (2007) A receptor-like kinase mediates the response of Arabidopsis cells to the inhibition of cellulose synthesis. Curr Biol 17:922–931. https://doi.org/10.1016/j.cub.2007.05.018
Hu LF, Wang PK, Hao ZD, Lu Y, Xue GX, Cao ZJ, Qu HX, Cheng TL, Shi JS, Chen JH (2021) Gibberellin oxidase gene family in L. chinense: genome-wide identification and gene expression analysis. Int J Mol Sci. https://doi.org/10.3390/ijms22137167
Hu HC, Ma L, Chen X, Fei XT, He BB, Luo YL, Liu YH, Wei AZ (2022) Genome-wide identification of the NAC gene family in Zanthoxylum bungeanum and their transcriptional responses to drought stress. Int J Mol Sci. https://doi.org/10.3390/ijms23094769
Hyles J, Vautrin S, Pettolino F, MacMillan C, Stachurski Z, Breen J, Berges H, Wicker T, Spielmeyer W (2017) Repeat-length variation in a wheat cellulose synthase-like gene is associated with altered tiller number and stem cell wall composition. J Exp Bot 68:1519–1529. https://doi.org/10.1093/jxb/erx051
Kumar S, Tamura K, Nei M (1994) MEGA: molecular evolutionary genetics analysis software for microcomputers. Comput Appl Biosci 10:189–191. https://doi.org/10.1093/bioinformatics/10.2.189
Li YH, Qian O, Zhou YH, Yan MX, Sun L, Zhang M, Fu ZM, Wang YH, Han B, Pang XM, Chen MS, Li JY (2003) BRITTLE CULM1, which encodes a COBRA-like protein, affects the mechanical properties of rice plants. Plant Cell 15:2020–2031. https://doi.org/10.1105/tpc.011775
Li S, Lei L, Gu Y (2013) Functional analysis of complexes with mixed primary and secondary cellulose synthases. Plant Signal Behav 8:e23179. https://doi.org/10.4161/psb.23179
Li GH, Liu X, Liang YX, Zhang Y, Cheng X, Cai YP (2020) Genome-wide characterization of the cellulose synthase gene superfamily in Pyrus bretschneideri and reveal its potential role in stone cell formation. Funct Integr Genom 20:857–858. https://doi.org/10.1007/s10142-020-00748-7
Li Q, Fu CF, Liang CL, Ni XJ, Zhao XH, Chen M, Ou LJ (2022) Crop lodging and the roles of lignin, cellulose, and hemicellulose in lodging resistance. Agron Basel. https://doi.org/10.3390/agronomy12081795
Little A, Schwerdt JG, Shirley NJ, Khor SF, Neumann K, O’Donovan LA, Lahnstein J, Collins HM, Henderson M, Fincher GB, Burton RA (2018) Revised phylogeny of the cellulose synthase gene superfamily: insights into cell wall evolution. Plant Physiol 177:1124–1141. https://doi.org/10.1104/pp.17.01718
Liu L, Shang-Guan K, Zhang B, Liu X, Yan M, Zhang L, Zhou Y (2013) Brittle Culm1, a COBRA-Like protein, functions in cellulose assembly through binding cellulose microfibrils. PLoS Genet 9(8):e1003704. https://doi.org/10.1371/journal.pgen.1003704
Liu D, Li G, Zuo Y (2019) Function determinants of TET proteins: the arrangements of sequence motifs with specific codes. Brief Bioinform 20:1826–1835. https://doi.org/10.1093/bib/bby053
Liu XF, Li SR, Feng XX, Li LL (2021) Study on cell wall composition, fruit quality and tissue structure of hardened “Suli” pears (Pyrus bretschneideri Rehd). J Plant Growth Regul 40:2007–2016. https://doi.org/10.1007/s00344-020-10248-4
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
Meng J, Hu B, Yi GJ, Li XQ, Chen HB, Wang YY, Yuan WN, Xing YQ, Sheng QM, Su ZX, Xu CX (2020) Genome-wide analyses of banana fasciclin-like AGP genes and their differential expression under low-temperature stress in chilling sensitive and tolerant cultivars. Plant Cell Rep 39:693–708. https://doi.org/10.1007/s00299-020-02524-0
Morgan JL, Strumillo J, Zimmer J (2013) Crystallographic snapshot of cellulose synthesis and membrane translocation. Nature 493:181–186. https://doi.org/10.1038/nature11744
Niu YQ, Hu B, Li XQ, Chen HB, Takac T, Samaj J, Xu CX (2018) Comparative digital gene expression analysis of tissue-cultured plantlets of highly resistant and susceptible banana cultivars in response to fusarium oxysporum. Int J Mol Sci. https://doi.org/10.3390/ijms19020350
Panchy N, Lehti-Shiu M, Shiu SH (2016) Evolution of gene duplication in plants. Plant Physiol 171:2294–2316. https://doi.org/10.1104/pp.16.00523
Persson S, Wei HR, Milne J, Page GP, Somerville CR (2005) Identification of genes required for cellulose synthesis by regression analysis of public microarray data sets. Proc Natl Acad Sci USA 102:8633–8638. https://doi.org/10.1073/pnas.0503392102
Qaseem MF, Shaheen H, Wu AM (2021) Cell wall hemicellulose for sustainable industrial utilization. Renew Sustain Energy Rev. https://doi.org/10.1016/j.rser.2021.110996
Ren J, Wang JR, Gao MY, Qin L, Wang Y (2021) Decreased cellulose-degrading enzyme activity causes pod hardening of okra (Abelmoschus esculentus L. Moench). Plant Physiol Biochem 162:624–633. https://doi.org/10.1016/j.plaphy.2021.03.035
Richmond TA, Somerville CR (2000) The cellulose synthase superfamily. Plant Physiol 124:495–498. https://doi.org/10.1104/pp.124.2.495
Roudier F, Fernandez AG, Fujita M, Himmelspach R, Borner GHH, Schindelman G, Song S, Baskin TI, Dupree P, Wasteneys GO, Benfey PN (2005) COBRA, an Arabidopsis extracellular glycosyl-phosphatidyl inositol-anchored protein, specifically controls highly anisotropic expansion through its involvement in cellulose microfibril orientation. Plant Cell 17:1749–1763. https://doi.org/10.1105/tpc.105.031732
Sangi S, Araujo PM, Coelho FS, Gazara RK, Almeida-Silva F, Venancio TM, Grativol C (2021) Genome-wide analysis of the COBRA-like gene family supports gene expansion through whole-genome duplication in soybean (Glycine max). Plants (basel). https://doi.org/10.3390/plants10010167
Sheth N, Roca X, Hastings ML, Roeder T, Krainer AR, Sachidanandam R (2006) Comprehensive splice-site analysis using comparative genomics. Nucleic Acids Res 34:3955–3967. https://doi.org/10.1093/nar/gkl556
Song X, Xu L, Yu J, Tian P, Hu X, Wang Q, Pan Y (2019) Genome-wide characterization of the cellulose synthase gene superfamily in Solanum lycopersicum. Gene 688:71–83. https://doi.org/10.1016/j.gene.2018.11.039
Vaahtera L, Schulz J, Hamann T (2019) Cell wall integrity maintenance during plant development and interaction with the environment. Nature Plants 5:924–932. https://doi.org/10.1038/s41477-019-0502-0
Van Soest PJ, Robertson JB, Lewis BA (1991) Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. J Dairy Sci 74:3583–3597. https://doi.org/10.3168/jds.S0022-0302(91)78551-2
Wang X, Cnops G, Vanderhaeghen R, De Block S, Van Montagu M, Van Lijsebettens M (2001) AtCSLD3, a cellulose synthase-like gene important for root hair growth in Arabidopsis. Plant Physiol 126:575–586. https://doi.org/10.1104/pp.126.2.575
Wu R, Duan L, Pruneda-Paz JL, Oh DH, Pound M, Kay S, Dinneny JR (2018) The 6xABRE synthetic promoter enables the spatiotemporal analysis of ABA-mediated transcriptional regulation. Plant Physiol 177:1650–1665. https://doi.org/10.1104/pp.18.00401
Xu G, Guo C, Shan H, Kong H (2012) Divergence of duplicate genes in exon-intron structure. Proc Natl Acad Sci U S A 109:1187–1192. https://doi.org/10.1073/pnas.1109047109
Yuan WN, Liu J, Takac T, Chen HB, Li XQ, Meng J, Tan YH, Ning T, He ZT, Yi GJ, Xu CX (2021) Genome-wide identification of banana csl gene family and their different responses to low temperature between chilling-sensitive and tolerant cultivars. Plants-Basel. https://doi.org/10.3390/plants10010122
Zaheer M, Rehman SU, Khan SH, Shahid S, Rasheed A, Naz R, Sajjad M (2022) Characterization of new COBRA like (COBL) genes in wheat (Triticum aestivum) and their expression analysis under drought stress. Mol Biol Rep 49:1379–1387. https://doi.org/10.1007/s11033-021-06971-0
Zhang JZ (2003) Evolution by gene duplication: an update. Trends Ecol Evol 18:292–298. https://doi.org/10.1016/S0169-5347(03)00033-8
Zhang M, Wang J, Zhu L, Li T, Jiang W, Zhou J, Peng W, Wu C (2017) Zanthoxylum bungeanum Maxim. (Rutaceae): a systematic review of its traditional uses, botany, phytochemistry, pharmacology, pharmacokinetics, and toxicology. Int J Mol Sci. https://doi.org/10.3390/ijms18102172
Zhao DQ, Xu C, Luan YT, Shi WB, Tang YH, Tao J (2021) Silicon enhances stem strength by promoting lignin accumulation in herbaceous peony (Paeonia lactiflora Pall.). Int J Biol Macromol 190:769–779. https://doi.org/10.1016/j.ijbiomac.2021.09.016
Funding
This research was supported by the Natural Science Basic Research Project of Shaanxi Province (2023-JC-YB-197) and Young Breeding Expert Support Program of Yangling Agricultural Hi-tech Industries Demonstration Zone.
Author information
Authors and Affiliations
Contributions
WG, JN, JY, and JW performed the experiments. WG, SW, and XZ analyzed the data and prepared Figs and tables. WG, YL, and YL wrote the paper and reviewed the draft. All authors have read and agreed to the published version of the manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Fig. S1
Conserved domains of ZbCS and ZbCOBL gene families. (a) ZbCS superfamily. (b) ZbCOBL gene family (TIF 3162 kb)
Fig. S2
Gene structure of the ZbCS and ZbCOBL gene families. (a) ZbCS superfamily. (b) ZbCOBL gene family (TIF 4499 kb)
Fig. S3
Conserved motif of the ZbCS and ZbCOBL gene families. (a) ZbCS superfamily. (b) ZbCOBL gene family (TIF 4751 kb)
Fig. S4
The structure of 10 motif logos in ZbCS genes. The downscale represents the position of the corresponding amino acid in the motif. The size of amino acids represents the degree of conservation. The red line box indicates the specific motif of the gene family (TIF 9762 kb)
Fig. S5
The structure of 10 motif logos in ZbCOBL genes. The downscale represents the position of the corresponding amino acid in the motif. The size of amino acids represents the degree of conservation. The red line box indicates the specific motif of the gene family (TIF 7933 kb)
Fig. S6
Cis-element of the ZbCS and ZbCOBL gene family. (a) ZbCS superfamily. (b) ZbCOBL gene family (TIF 7094 kb)
Fig. S7
Statistics of cis-elements of the ZbCS and ZbCOBL gene families. (a) Statistics of cis-elements of the ZbCS genes. (b) Statistics of cis-elements of the ZbCOBL genes. The top ten cis-elements were displayed (TIF 95 kb)
Fig. S8
Genomic distribution of ZbCS and ZbCOBL genes on the chromosome. The red gene in the same chromosome indicates tandem duplication. The gene id and the black line on the bars show the approximate location of the ZbCS and ZbCOBL. The scale illustrates the length of chromosomes (TIF 10902 kb)
Fig. S9
Analysis of codon preference in ZbCS and ZbCOBL genes. (a) Neutral plot analysis. (b) PR2 plot analysis. (c) ENC map analysis (TIF 24642 kb)
Fig. S10
Optimal codon analysis of CS and COBL gene family in Zanthoxylum bungeanum (Zb). The bar chart above represents the number of italicized codons below. The black dots in the graph below indicate that the corresponding codon is the optimal codon of the corresponding subfamily. The measured color bands and numbers on the left represent the number of optimal codons in the corresponding subfamily (TIF 3557 kb)
Table S1
Primers for real-time quantitative PCR (XLSX 22 kb)
Table S2
Classification and characterization of the putative CS and COBL gene families in Zanthoxylum bungeanum (Zb) (XLSX 23 kb)
Table S3
Duplications of ZbCS and ZbCOBL genes in Zanthoxylum bungeanum (Zb) (XLSX 17 kb)
Table S4
Correlation analysis between cellulose/hemicellulose and related gene expression in Zanthoxylum bungeanum (Zb) (XLSX 13 kb)
Table S5
The key genes of ZbCS and ZbCOBL genes (XLSX 8 kb)
Table S6
Homologous genes and functions of key genes in Arabidopsis thaliana (At) (XLSX 10 kb)
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
Gao, W., Nie, J., Yao, J. et al. Genomic survey and expression analysis of cellulose synthase superfamily and COBRA-like gene family in Zanthoxylum bungeanum stipule thorns. Physiol Mol Biol Plants 30, 369–382 (2024). https://doi.org/10.1007/s12298-024-01432-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12298-024-01432-x