Abstract
Cellulose synthase A (CESA) is a key enzyme involved in the complex process of plant cell wall biosynthesis, and it remains a productive subject for research. We employed systems biology approaches to explore structural diversity of eudicot CESAs by exon–intron organization, mode of duplication, synteny, and splice site analyses. Using a combined phylogenetics and comparative genomics approach coupled with co-expression networks we reconciled the evolution of cellulose synthase gene family in eudicots and found that the basic forms of CESA proteins are retained in angiosperms. Duplications have played an important role in expansion of CESA gene family members in eudicots. Co-expression networks showed that primary and secondary cell wall modules are duplicated in eudicots. We also identified 230 simple sequence repeat markers in 103 eudicot CESAs. The 13 identified conserved motifs in eudicots will provide a basis for gene identification and functional characterization in other plants. Furthermore, we characterized (in silico) eudicot CESAs against senescence and found that expression levels of CESAs decreased during leaf senescence.
Similar content being viewed by others
References
Appenzeller L et al (2004) Cellulose synthesis in maize: isolation and expression analysis of the cellulose synthase (CesA) gene family. Cellulose 11:287–299
Artimo P (2012) ExPASy: SIB bioinformatics resource portal. Nucl Acids Res 40:W597–W603
Barvkar VT, Pardeshi VC, Kale SM, Kadoo NY, Gupta VS (2012) Phylogenomic analysis of UDP glycosyltransferase 1 multigene family in Linum usitatissimum identified genes with varied expression patterns. BMC Genom 13:175
Betts MJ, Guigó 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
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120
Bolser DM, Staines DM, Perry E, Kersey PJ (2017) Ensembl Plants: integrating tools for visualizing, mining, and analyzing plant genomic data. In: Plant genomics databases. Springer, Berlin, pp 1–31
Brown AV, Hudson KA (2015) Developmental profiling of gene expression in soybean trifoliate leaves and cotyledons. BMC Plant Biol 15:169
Brown AV, Hudson KA (2017) Transcriptional profiling of mechanically and genetically sink-limited soybeans. Plant Cell Environ 40:2307–2318
Brusslan JA, Bonora G, Rus-Canterbury AM, Tariq F, Jaroszewicz A, Pellegrini M (2015) A genome-wide chronological study of gene expression and two histone modifications, H3K4me3 and H3K9ac, during developmental leaf senescence. Plant Physiol 168:1246–1261
Burton RA, Shirley NJ, King BJ, Harvey AJ, Fincher GB (2004) The CesA gene family of barley. Quantitative analysis of transcripts reveals two groups of co-expressed genes. Plant Physiol 134:224–236
Caputi L, Malnoy M, Goremykin V, Nikiforova S, Martens S (2012) A genome-wide phylogenetic reconstruction of family 1 UDP-glycosyltransferases revealed the expansion of the family during the adaptation of plants to life on land. Plant J 69:1030–1042
Carpita NC (2011) Update on mechanisms of plant cell wall biosynthesis: how plants make cellulose and other (1→4)-β-d-glycans. Plant Physiol 155:171–184
Carroll A, Specht CD (2011) Understanding plant cellulose synthases through a comprehensive investigation of the cellulose synthase family sequences. Front Plant Sci 2:5
Darzentas N (2010) Circoletto: visualizing sequence similarity with Circos. Bioinformatics 26:2620–2621
De Vega JJ et al (2015) Red clover (Trifolium pratense L.) draft genome provides a platform for trait improvement. Sci Rep 5:17394
Doblin MS, Kurek I, Jacob-Wilk D, Delmer DP (2002) Cellulose biosynthesis in plants: from genes to rosettes. Plant Cell Physiol 43:1407–1420
Emms DM, Kelly S (2015) OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol 16:157
Ghosh S et al (2013) Induction of senescence and identification of differentially expressed genes in tomato in response to monoterpene. PLoS One 8:e76029
Goodstein DM et al (2011) Phytozome: a comparative platform for green plant genomics. Nucl Acids Res 40:D1178–D1186
He C, Cui K, Duan A, Zeng Y, Zhang J (2012) Genome-wide and molecular evolution analysis of the Poplar KT/HAK/KUP potassium transporter gene family. Ecol Evol 2:1996–2004
Holland N, Holland D, Helentjaris T, Dhugga KS, Xoconostle-Cazares B, Delmer DP (2000) A comparative analysis of the plant cellulose synthase (CesA) gene family. Plant Physiol 123:1313–1324
Huang S et al (2009) The genome of the cucumber, Cucumis sativus L. Nat Genet 41:1275–1282
Hu B, Jin J, Guo A-Y, Zhang H, Luo J, Gao G ((2014)) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31:1296–1297
Jaillon O et al (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449(7161):463–467
Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Bioinformatics 8:275–282
Kaur S, Dhugga KS, Gill K, Singh J (2016) Novel structural and functional motifs in cellulose synthase (CesA) genes of bread wheat (Triticum aestivum, L.). PLoS One 11:e0147046
Kim D, Langmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12:357
Kumar M et al (2009) An update on the nomenclature for the cellulose synthase genes in Populus. Trends Plant Sci 14:248–254
Kumar M, Turner S (2015) Plant cellulose synthesis: CESA proteins crossing kingdoms. Phytochemistry 112:91–99
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874
Le B et al (2016) Genome-wide characterization and expression pattern of auxin response factor (ARF) gene family in soybean and common bean. Genes Genom 38:1165–1178
Lee T-H, Tang H, Wang X, Paterson AH (2012) PGDD: a database of gene and genome duplication in plants. Nucl Acids Res 41:D1152–D1158
Letunic I, Bork P (2006) Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 23:127–128
Li T, Zhang J, Zhu H, Qu H, You S, Duan X, Jiang Y (2016) Proteomic analysis of differentially expressed proteins involved in peel senescence in harvested mandarin fruit. Front Plant Sci 7:725
Little A et al (2018) Revised phylogeny of the Cellulose Synthase gene superfamily: insights into cell wall evolution. Plant Physiol 177:1124–1141
Maleki SS, Mohammadi K, Ji KS (2016) Characterization of cellulose synthesis in plant cells. Sci World J 2016:8641373
Mitchell A et al (2014) The InterPro protein families database: the classification resource after 15 years. Nucl Acids Res 43:D213–D221
Mutwil M et al (2011) PlaNet: combined sequence and expression comparisons across plant networks derived from seven species. Plant Cell 23:895–910
Nadeem MA et al (2018) DNA molecular markers in plant breeding: current status and recent advancements in genomic selection and genome editing. Biotechnol Biotechnol Equip 32:261–285
Nawaz MA, Sadia B, Awan FS, Zia MA, Khan IA (2013) Genetic diversity in hyper glucose oxidase producing Aspergillus niger UAF mutants by using molecular markers. Int J Agri Biol 15:362–366
Nawaz MA et al (2017a) Genome and transcriptome-wide analyses of cellulose synthase gene superfamily in soybean. J Plant Physiol 215:163–175
Nawaz MA et al (2017b) Systems identification and characterization of cell wall reassembly and degradation related genes in Glycine max (L.) Merill, a Bioenergy Legume. Sci Rep 7:10862
Nawaz MA, Yang SH, Rehman HM, Baloch FS, Lee JD, Park JH, Chung G (2017c) Genetic diversity and population structure of Korean wild soybean (Glycine soja Sieb. and Zucc.) inferred from microsatellite markers. Biochem Syst Ecol 71:87–96
Olek AT et al (2014) The structure of the catalytic domain of a plant cellulose synthase and its assembly into dimers. Plant Cell 26:2996–3009
Panchy N, Lehti-Shiu MD, Shiu S-H (2016) Gene Duplicates: from origins to implications for plant evolution. Plant Physiol 171:2294–2316
Persson S et al (2007) Genetic evidence for three unique components in primary cell-wall cellulose synthase complexes in Arabidopsis. Proc Natl Acad Sci 104:15566–15571
Pertea M, Pertea GM, Antonescu CM, Chang T-C, Mendell JT, Salzberg SL (2015) StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat Biotechnol 33:290
Proost S, Mutwil M (2016) Tools of the trade: studying molecular networks in plants. Curr Opin Plant Biol 30:143–150
Rai KM, Thu SW, Balasubramanian VK, Cobos CJ, Disasa T, Mendu V (2016) Identification, characterization, and expression analysis of cell wall-related genes in Sorghum Bicolor (L.) Moench, a food, fodder, and biofuel crop. Front Plant Sci 7:1287
Rehman HM et al (2016) Genome-wide analysis of Family-1 UDP-glycosyltransferases in soybean confirms their abundance and varied expression during seed development. J Plant Physiol 206:87–97
Rehman HM, Nawaz MA, Shah ZH, Daur I, Khatoon S, Yang SH, Chung G (2017) In-depth genomic and transcriptomic analysis of five K+ transporter gene families in soybean confirm their differential expression for nodulation. Front Plant Sci 8:804
Richmond TA, Somerville CR (2000) The cellulose synthase superfamily. Plant Physiol 124:495–498
Roberts AW, Roberts E (2004) Cellulose synthase (CesA) genes in algae and seedless plants. Cellulose 11:419–435
Römling U, Galperin MY (2015) Bacterial cellulose biosynthesis: diversity of operons, subunits, products, and functions. Trends Microbiol 23:545–557
Ruprecht C et al (2016) FamNet: A framework to identify multiplied modules driving pathway diversification in plants. Plant Physiol 170:1878–1894
Ruprecht C et al (2017) Phylogenomic analysis of gene co-expression networks reveals the evolution of functional modules. Plant J 90:447–465
Schmutz J et al (2010) Genome sequence of the palaeopolyploid soybean. Nature 463:178
Schmutz J et al (2014) A reference genome for common bean and genome-wide analysis of dual domestications. Nat Genet 46:707
Schranz ME, Lysak MA, Mitchell-Olds T (2006) The ABC's of comparative genomics in the Brassicaceae: building blocks of crucifer genomes. Trends Plant Sci 11:535–542
Schwerdt JG et al (2015) Evolutionary dynamics of the cellulose synthase gene superfamily in grasses. Plant Physiol 168:968–983
Sheth N, Roca X, Hastings ML, Roeder T, Krainer AR, Sachidanandam R (2006) Comprehensive splice-site analysis using comparative genomics. Nucl Acids Res 34:3955–3967
Sievers F et al (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7:539
Somerville C (2006) Cellulose synthesis in higher plants. Annu Rev Cell Dev Biol 22:53–78
Suzuki S, Li L, Sun Y-H, Chiang VL (2006) The cellulose synthase gene superfamily and biochemical functions of xylem-specific cellulose synthase-like genes in Populus trichocarpa. Plant Physiol 142:1233–1245
Taylor NG, Gardiner JC, Whiteman R, Turner SR (2004) Cellulose synthesis in the Arabidopsis secondary cell wall. Cellulose 11:329–338
The Arabidopsis Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815
Turner SR, Somerville CR (1997) Collapsed xylem phenotype of Arabidopsis identifies mutants deficient in cellulose deposition in the secondary cell wall. Plant Cell 9:689–701
Tuskan GA et al (2006) The genome of black cottonwood Populus trichocarpa (Torr. & Gray). Science 313(5793):1596–1604
Wang X et al (2011) The genome of the mesopolyploid crop species Brassica rapa. Nat Genet 43:1035
Wang K et al (2012a) The draft genome of a diploid cotton Gossypium raimondii. Nat Genet 44:1098–1103
Wang Y et al (2012b) PIECE: a database for plant gene structure comparison and evolution. Nucl Acids Res 41:D1159–D1166
Wang N, Xia E-H, Gao L-Z (2016) Genome-wide analysis of WRKY family of transcription factors in common bean, Phaseolus vulgaris: chromosomal localization, structure, evolution and expression divergence. Plant Gene 5:22–30
Woo HR, Kim HJ, Nam HG, Lim PO (2013) Plant leaf senescence and death—regulation by multiple layers of control and implications for aging in general. J Cell Sci 126:4823–4833
Worberg A, Quandt D, Barniske A-M, Löhne C, Hilu KW, Borsch T (2007) Phylogeny of basal eudicots: insights from non-coding and rapidly evolving DNA. Org Divers Evol 7:55–77
Yin Y, Huang J, Xu Y (2009) The cellulose synthase superfamily in fully sequenced plants and algae. BMC Plant Biol 9:99
Yin Y, Johns MA, Cao H, Rupani M (2014) A survey of plant and algal genomes and transcriptomes reveals new insights into the evolution and function of the cellulose synthase superfamily. BMC Genom 15:260
You FM et al (2008) BatchPrimer3: a high throughput web application for PCR and sequencing primer design. BMC Bioinform 9:253
Young ND et al (2011) The Medicago genome provides insight into the evolution of rhizobial symbioses. Nature 480:520
Acknowledgements
This work was carried out with the support of ‘‘Cooperative Research Program for Agriculture Science and Technology Development (Project No. PJ01133402)’’ Rural Development Administration, Republic of Korea.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
We claim that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Nawaz, M.A., Lin, X., Chan, TF. et al. Characterization of Cellulose Synthase A (CESA) Gene Family in Eudicots. Biochem Genet 57, 248–272 (2019). https://doi.org/10.1007/s10528-018-9888-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10528-018-9888-z