Skip to main content
Log in

Genome-wide characterization of the cellulose synthase gene superfamily in Pyrus bretschneideri and reveal its potential role in stone cell formation

  • Original Article
  • Published:
Functional & Integrative Genomics Aims and scope Submit manuscript

A Correction to this article was published on 11 September 2020

This article has been updated

Abstract

Members of the cellulose synthase (CesA) and cellulose synthase–like (Csl) families from the cellulose synthase gene superfamily participate in cellulose and hemicellulose synthesis in the plasma membrane. The members of this superfamily are vital for cell wall construction during plant growth and development. However, little is known about their function in pear fruit, a model for Rosaceae species and for fleshy fruit development. In our research, a total of 36 CesA/Csl family members were identified from the pear and were grouped into six subfamilies (CesA, CslB, CslC, CslD, CslE, and CslG) according to phylogenetic relationships. We performed a protein sequence physicochemical analysis, phylogenetic tree construction, a gene structure, a conserved domain, and chromosomal localization analysis. The results indicated that most of the CesA/Csl genes from pear are closely related to genes in Arabidopsis, but these families have unique characteristics in terms of their gene structure, chromosomal localization, phylogeny, and deduced protein sequences, suggesting that they have evolved through different processes. Tissue expression analysis results showed that most of the CesA/Csl genes were constitutively expressed at different levels in different organs. Furthermore, the expression levels of four genes (Pbr032894.2, Pbr016107.1, Pbr00518.1, and Pbr034218.1) tended to first increase and then decrease during fruit development, implying that these four genes may be involved in the development of stone cells of pear fruit. Our results may help elucidate the evolutionary history and functional differences of the CesA/Csl genes in pear and lay a foundation for further investigation of the CesA/Csl genes in pear and other Rosaceae species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Change history

  • 11 September 2020

    The above article was published online with the same Figures 7 and 8.

References

  • Alan L, Julian G, Schwerdt NJ, Shirley SF, Khor K, Neumann LA, O’Donovan J, Lahnstein HM, Collins MH, Fincher GB, Rachel A (2018) Revised phylogeny of the cellulose synthase gene superfamily: insights into cell wall evolution1[OPEN]. Plant Physiology® 177:1124–1141

    Google Scholar 

  • Bailey TL, Johnson J, Grant CE, Noble WS (2015) The MEME Suite Nucleic acids res gkv416

  • Bernal AJ, Jakob KJ, Harholt J, Sørensen S, Moller I, Blaukopf C, Johansen B, de Lotto R, Pauly M, Scheller HV, Willats WGT (2007) Disruption of atcsld5 results in reduced growth, reduced xylan and homogalacturonan synthase activity and altered xylan occurrence in arabidopsis. Plant J 52:791–802

    PubMed  CAS  Google Scholar 

  • Budak H, Zhang B (2017) MicroRNAs in model and complex organisms. Funct Integr Genomic 17:1–4

    Google Scholar 

  • Burton RA, Shirley NJ, 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • Cai Y, Li G, Nie J, Lin Y, Nie F, Zhang JY, Xu YL (2010) Study of the structure and biosynthetic pathway of lignin in stone cells of pear. Sci Hortic 125:374–379

    CAS  Google Scholar 

  • Cao YP, Han YH, Meng DD, Muhammad A, Li DH, Jin Q, Lin Y, Cai YP (2018) Systematic analysis and comparison of the PHD-finger gene family in Chinese pear (Pyrus bretschneideri) and its role in fruit development. Funct Integr Genomic 18:519–531

    CAS  Google Scholar 

  • Cheng X, Li GH, Muhammad A, Zhang JY, Cheng J, Qiu JX, Jin Q, Cai YP, Lin Y (2019) Family-1 UDP glycosyltransferases in pear (Pyrus bretschneideri): molecular identification, phylogenomic characterization and expression profiling during stone cell formation. Mol Biol Rep 46:2153–2175

    PubMed  CAS  Google Scholar 

  • Cheng X, Li GH, Muhammad A, Li GH, Zhang JY, Jiang TS, Jin Q, Zhao H, Cai YP, Lin Y (2018) Molecular identification, phylogenomic characterization and expression patterns analysis of the LIM (LIN-11, Isl1 and MEC-3 domains) gene family in pear (Pyrus bretschneideri) reveal its potential role in lignin metabolism. Gene 686:237–249

    PubMed  Google Scholar 

  • Creux NM, Ranik M, Berger DK, Myburg AA (2008) Comparative analysis of or thologous cellulose synthase promoters from Arabidopsis, Populus and Eucalyptus: evidence of conserved regulatory elements in angiosperms. New Phytol 179:722–737

    PubMed  CAS  Google Scholar 

  • Doblin MS, Kurek I, Jacob-Wilk D, Delmer DP (2002) Cellulose biosynthesis in plants: from genes to rosettes. Plant Cell Physiol 43:1407–1420

    PubMed  CAS  Google Scholar 

  • Doblin MS, Pettolino FA, Wilson SM, Campbell R, Burton RA, Fincher GB, Newbigin E, Antony B (2009) A barley cellulose synthase-like CSLH gene mediates (1,3;1,4)-beta-Dglucan synthesis in transgenic Arabidopsis. Pro Natl Acad Sci USA 106:5996–6001

    CAS  Google Scholar 

  • Douchkov D, Lueck S, Hensel G, Kumlehn J, Rajaraman J, Johrde A, Doblin MS, Beahan CT, Kopischke M, Fuchs R, Lipka V, Niks RE, Bulone V, Chowdhury J, Little A, Burton RA, Bacic A, Fincher GB, Schweizer P (2016) The barley (Hordeum vulgare) cellulose synthase-like D2 gene (HvCslD2) mediates penetration resistance to host-adapted and nonhost isolates of the powdery mildew fungus. New Phytol 212:421–433

    PubMed  CAS  Google Scholar 

  • Fagard M, Desnos T, Desprez T, Goubet F, Refregier G, Mouille G, McCann M, Rayon C, Vernhettes S, Hofte H (2000) PROCUSTE1 encodes a cellulose synthase required for normal cell elongation specifically in roots and dark-grown hypocotyls of Arabidopsis. Plant Cell 12:2409–2423

    PubMed  PubMed Central  CAS  Google Scholar 

  • Farrokhi N, Burton RA, Brownfifield L, Hrmova M, Wilson SM, Bacic A, Fincher GB (2006) Plant cell wall biosynthesis: genetic, biochemical and functional genomics approaches to the identification of key genes. Plant Biotechnol J 4:145–167

    PubMed  CAS  Google Scholar 

  • Fincher GB (2009) Revolutionary times in our understanding of cell wall biosynthesis and remodeling in the grasses. Plant Physiol 149:27–37

    PubMed  PubMed Central  CAS  Google Scholar 

  • Gong JW, Shi YZ, Wang YL, Liu RX, Duan L, Lei K, Zhang Q, Jiang X, Zhang SY, Jia TT, Zhang LP, Shang HH, Yuan YL (2018) Genome-wide identifification and analysis of the evolution and expression patterns of the cellulose synthase gene superfamily in Gossypium species. Gene 646:28–38

    PubMed  Google Scholar 

  • Hamann T, Osborne E, Youngs HL, Misson J, Nussaume L, Somerville C (2004) Global expression analysis of cesa and csl genes in arabidopsis. Cellulose 11:279–286

    CAS  Google Scholar 

  • Hazen SP, Scott-Craig JS, Walton JD (2002) Cellulose synthase-like genes of rice. Plant Physiol 128:336–340

    PubMed  PubMed Central  CAS  Google Scholar 

  • Jin Q, Yan CC, Qiu JX, Zhang N, Lin Y, Cai YP (2013) Structural characterization and deposition of stone cell lignin in Dangshan Su pear. Sci Hortic 155:123–130

    CAS  Google Scholar 

  • Kaur S, Dhugga KS, Beech R, Singh (2017) Genome-wide analysis of the cellulose synthase-like (Csl) gene family in bread wheat (Triticum aestivum L.). BMC Plant Biol 17:193

    PubMed  PubMed Central  Google Scholar 

  • Keegstra K, Walton J (2006) Plant science. Beta-glucans-brewer.’s bane, dietician’s de light. Science 311:1872–1873

    PubMed  CAS  Google Scholar 

  • Kim CM, Park SH, Je BI, Park SH, Park SJ, Piao HL, Eun MY, Dolan L, Han CD (2007) OscslD1 a cellulose synthase-like D1 gene, is required for root hair morphogenesis in rice. Plant Physiol 143:1220–1230

    PubMed  PubMed Central  CAS  Google Scholar 

  • Kim WC, Ko JH, Kim JY, Kim J, Bae HJ, Han KH (2013) MYB46 directly regulates the gene expression of secondary wall-associated cellulose synthases in Arabidopsis. Plant J 73:26–36

    PubMed  CAS  Google Scholar 

  • Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D (2009) Circos: an information aesthetic for comparative genomics. Genome Res 19:1639–1645

    PubMed  PubMed Central  CAS  Google Scholar 

  • Kumar M, Turner S (2015) Plant cellulose synthesis: CESA proteins crossing kingdoms. Phytochemistry 112:91–99

    PubMed  CAS  Google Scholar 

  • Lee Y, Yoon TH, Lee J, Jeon SY, Lee JH, Lee MK, Chen HZ, Yun J, Oh SY, Wen SH (2018) A lignin molecular brace controls precision processing of cell walls critical for surface integrity in Arabidopsis. Cell 173:1468–1480

    PubMed  CAS  Google Scholar 

  • Letunic I, Doerks T, Bork P (2012) SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Res 40:D302–D305

    PubMed  CAS  Google Scholar 

  • Li SM, Su XQ, Abdullah M, Sun Y, Li GH, Cheng X, Lin Y, Cai Y, Jin Q (2018a) Effects of different pollens on primary metabolism and lignin biosynthesis in pear. Int J Mol Sci 19:2273

    PubMed Central  Google Scholar 

  • Liu F, Xu YJ, Jiang HH, Jiang CS, Du YB, Gong C, Wang W, Zhu SW, Han GM, Cheng BJ (2016) Systematic identification, evolution and expression analysis of the Zea mays PHT1 gene family reveals several new members involved in root colonization by arbuscular mycorrhizal fungi. Int J Mol Sci 17:930

    PubMed Central  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2 -△△ CT method. Methods 25:402–408

    CAS  PubMed  Google Scholar 

  • Li W, Shang H, Ge Q, Zou C, Cai J, Wang D, Fan S, Zhang Z, Deng X, Tan Y, Song W, Li P, Koffiffiffi PK, Jamshed M, Lu Q, Gong W, Li J, Shi Y, Chen T, Gong J, Liu A, Yuan Y (2016) Genome-wide identifification, phylogeny, and expression analysis of pectin methylesterases reveal their major role in cotton fiber development. BMC Genomics 17:1000

    PubMed  PubMed Central  Google Scholar 

  • Li Y, He Y, Hu W, Zhang Y, Wang X, Tang H (2018b) Identification of NADPH oxidase family members associated with cold stress in strawberry. FEBS Open Bio 8:593–605

    PubMed  PubMed Central  Google Scholar 

  • Li Y, Yang T, Dai D, Hu Y, Guo X, Guo H (2017) Evolution, gene expression profifiling and 3D modeling of CSLD proteins in cotton. BMC Plant Biol 17:119

    PubMed  PubMed Central  Google Scholar 

  • Lynch M (2002) Intron evolution as a population-enetic process. Proc Natl Acad Sci U S A 99:6118–6123

    PubMed  PubMed Central  CAS  Google Scholar 

  • Mendu V, Griffiffiffiths JS, Persson S, Stork J, Downie AB, Haughn GW, Debolt S (2011) Subfunctionalization of cellulose synthases in seed coat epidermal cells mediates secondary radial wall synthesis and mucilage attachment. Plant Physiol 157:441–453

    PubMed  PubMed Central  CAS  Google Scholar 

  • Mohnen D (2008) Pectin structure and biosynthesis. Curr Opin Plant Biol 11:266–277

    PubMed  CAS  Google Scholar 

  • Muhammad AN, Hafifiz MR, Faheem SB, Babar I, Muhammad AA, Iqrar AK, Jeong DL, Gyuhwa C, Seung HY (2017) Genome and transcriptome-wide analyses of cellulose synthase gene superfamily in soybean. J Plant Physiol 215:163–175

    Google Scholar 

  • Pauly M, Gille S, Liu L, Mansoori N, Souza A, Schultink A, Xiong G (2013) Hemicellulose biosynthesis. Planta 238:627–642

    PubMed  CAS  Google Scholar 

  • Pauly M, Keegstra K (2008) Cell-wall carbohydrates and their modification as a resource for biofuels. Plant J 54:559–568

    PubMed  CAS  Google Scholar 

  • Pear JR, Kawagoet Y, Schreckengost WE, Delmert DP, Stalker DM (1996) Higher plants contain homologs of the bacterial celA genes encoding the catalytic subunit of cellulose synthase. Proc Natl Acad Sci U S A 93:12637–12642

    PubMed  PubMed Central  CAS  Google Scholar 

  • Persson S, Paredez A, Carroll A, Palsdottir H, Doblin M, Poindexter P, Natalie K, Manfred A, Somervill CR (2007) Genetic evidence for three unique components in primary cell-wall cellulose synthase complexes in Arabidopsis. Proc Natl Acad Sci U S A 104:15566–15571

    PubMed  PubMed Central  CAS  Google Scholar 

  • Punta M (2015) The Pfam protein families database. Nucleic Acids Res:gkr1065

  • 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 1287

  • Richmond TA, Somerville CR (2000) The cellulose synthase superfamily. Plant Physiol 124:495–498

    PubMed  PubMed Central  CAS  Google Scholar 

  • Sandhu APS, Randhawa GS, Dhugga KS (2009) Plant cell wall matrix polysaccharide biosynthesis. Mol Plant 2:840–850

    PubMed  CAS  Google Scholar 

  • Schmutz J, Cannon SB, Schlueter J, Ma J, Mitors J, Nelson W (2010) Genome sequence of the palaeopolyploid soybean. Nature 463:178–183

    PubMed  CAS  Google Scholar 

  • Schwerdt JG, MacKenzie K, Wright F, Oehme D, Wagner JM, Harvey AJ, Shirley NJ, Burton RA, Schreiber M, Halpin C (2015) Evolutionary dynamics of the cellulose synthase gene superfamily in grasses. Plant Physiol 168:968–983

    PubMed  PubMed Central  Google Scholar 

  • Shu O, Wei Z, John H, Lin H, Matthew C, Kevin C, Franoise TN, Malek RL, Yuandan L, Li Z, Joshua O, Brian H, Jennifer W, Buellet CR (2007) The TIGR rice genome annotation resource: improvements and new features. Nucleic Acids Res 35:D883–D887

    Google Scholar 

  • Soliman ERS, Meyer P (2019) Responsiveness and adaptation to salt stress of the redox-responsive transcription factor 1 (RRTF1) gene are controlled by its promoter. Mol Biotechnol 61:254–260

    PubMed  CAS  Google Scholar 

  • Song XM, Xu L, Yu JW, Tian P, Hu X, Wang QJ, Pan Y (2019) Genome-wide characterization of the cellulose synthase gene superfamily in Solanum lycopersicum. Gene 688:71–83

    PubMed  CAS  Google Scholar 

  • Sorek N, Yeats TH, Szemenyei H, Youngs H, Somerville CR (2014) The implications of Lignocellulosic biomass chemical composition for the production of advanced biofuels. Bioscience 64:192–201

    Google Scholar 

  • Takata N, Taniguchi T (2015) Expression divergence of cellulose synthase (CesA) genes after a recent whole genome duplication event in Populus. Planta 241:29–42

    PubMed  CAS  Google Scholar 

  • Tamura K, Peterson D, Steche G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analys is using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    PubMed  PubMed Central  CAS  Google Scholar 

  • Taylor NG, Howells RM, Huttly AK, Vickers K, Turner SR (2003) Interactions among three distinct CesA proteins essential for cellulose synthesis. Proc Natl Acad Sci U S A 100:1450–1455

    PubMed  PubMed Central  CAS  Google Scholar 

  • Taylor NG, Laurie S, Turner SR (2000) Multiple cellulose synthase catalytic subunits are required for cellulose synthesis in Arabidopsis. Plant Cell 12:2529–2540

    PubMed  PubMed Central  CAS  Google Scholar 

  • Thomas J, Bowman MJ, Vega A, Kim HR, Mukherjee A (2018) Comparative transcriptome analysis provides key insights into gene expression pattern during the formation of nodule-like structures in Brachypodium. Funct Integr Genomic 8:315–326

    Google Scholar 

  • Wang DP, Zhang YB, Zhang Z, Zhu J, Yu J (2010) KaKs_Calculator 2.0: a toolkit incorporating gamma-series methods and sliding window strategies. Genom Proteom Bioinf 8:77–80

    CAS  Google Scholar 

  • Worberg A, Quandt D, Barniske AM, 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

    Google Scholar 

  • Wu J, Wang ZW, Shi ZB, Zhang S, Ming R, Zhu SL, Khan MA, Zhang SL (2013) The genome of the pear (Pyrus bretschneideri Rehd.). Genome Res 23:396–408

    PubMed  PubMed Central  CAS  Google Scholar 

  • Xu G, Guo C, Shan H, Kong H (2012) Divergence of duplicate genes in exon-intron structure. Proc. Natl Acad Sci USA 109:1187–1192

    PubMed  CAS  PubMed Central  Google Scholar 

  • Xu LL, Qiao X, Zhang MY, Zhang SL (2018) Genome-wide analysis of aluminum-activated malate transporter family genes in six rosaceae species, and expression analysis and functional characterization on malate accumulation in Chinese white pear. Plant Sci 24:451–456

    Google Scholar 

  • Yang SL, Zhang XN, Lu GL, Wang CR, Wang R (2015) Regulation of gibberellin on gene expressions related with the lignin biosynthesis in ‘Wangkumbae’ pear (Pyrus pyrifolia Nakai) fruit. Plant Growth Regultion 76:127–134

    CAS  Google Scholar 

  • 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 Genomics 15:260

    PubMed  PubMed Central  Google Scholar 

  • Yuo T, Shiotani K, Shitsukawa N, Miyao A, Hirochika H, Ichii M, Taketa S (2011) Root hairless 2 (rth2) mutant represents a loss-of-function allele of the cellulose synthase-like gene OsCSLD1 in rice (Oryza Sativa L.). Breed Sci 61:225–233

    CAS  Google Scholar 

  • Zhang MY, Xue C, Xu LL, Sun HH, Qin MF, Zhang SL, Wu J (2016) Distinct transcriptome profiles reveal gene expression patterns during fruit development and maturation in five main cultivated species of pear (Pyrus L.). Sci Rep 6:28130

    PubMed  PubMed Central  CAS  Google Scholar 

  • Zou X, Zhen Z, Ge Q, Fan S, Liu A, Gong W (2018) Genome-wide identififi-cation and analysis of the evolution and expression patterns of the cellulose synthase gene superfamily in Gossypium species. Gene 646:28–38

    PubMed  CAS  Google Scholar 

Download references

Funding

This work was financially supported by the China Postdoctoral Science Foundation (2019M662135), Anhui Provincial Natural Science Foundation (2008085QC100), Anhui Provincial Postdoctoral Science Foundation (2019B319), Scientific Research Foundation of Anhui Agricultural University (2019zd01 and yj2019-17), Medjaden Academy & Research Foundation for Young Scientists (MJR20201119).

Author information

Authors and Affiliations

Authors

Contributions

Conception or design of the work: Guohui Li, Xin Liu, Xi Cheng; software: Guohui Li, Xin Liu, Yuxuan Liang, Ynag Zhang; writing-review and editing: Guohui Li, Xin Liu, Yuxuan Liang; funding acquisition: Yongping Cai, Xi Cheng

Corresponding authors

Correspondence to Xi Cheng or Yongping Cai.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

The original version of this article was revised: The above article was published online with the same Figures 7 and 8.

Guohui Li and Xin Liu are the co-first authors

Electronic supplementary material

Figure S1

Phylogenetic analysis of cellulose synthase families. Neighbor-Joining (NJ) tree of 36 Ces/Csl gene was constructed by MEGA 5.0. 41 genes in Arabidopsis, 32 genes in rice, 33 genes in Populus euphratica and 36 CesA/Csl genes in pear. According to their classification in Arabidopsis, all Ces/Csl genes were divided into different subfamilies (I-V). (JPG 2796 kb)

Figure S2

Sequence logos for the motifs of PbCesA/Csl domains using the MEME program. MEME motifs are displayed by stacks of letters at each site. The overall height of the stack indicates the sequence conservation at that position, while the height of symbols within the stack indicates the relative frequency of each amino acid at that position. The x-axis represents the width of the motif, and the y-axis represents the bits of each letter. (JPG 857 kb)

Figure S3

Sliding window plots of duplicated PbCesA/Csl members of pear species families. The x-axis represents the Ka/Ks value, and the y-axis represents the nucleotide position. (JPG 451 kb)

Table S1

(DOC 15 kb)

Table S2

(DOC 26 kb)

Table S3

(DOC 84 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, G., Liu, X., Liang, Y. et al. Genome-wide characterization of the cellulose synthase gene superfamily in Pyrus bretschneideri and reveal its potential role in stone cell formation. Funct Integr Genomics 20, 723–738 (2020). https://doi.org/10.1007/s10142-020-00747-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10142-020-00747-8

Keywords

Navigation