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Expression divergence of cellulose synthase (CesA) genes after a recent whole genome duplication event in Populus

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Abstract

Main conclusion

Secondary cell wall-associated CesA genes in Populus have undergone a functional differentiation in expression pattern that may be attributable to evolutionary alteration of regulatory modules.

Gene duplication is an important mechanism for functional divergence of genes. Secondary cell wall-associated cellulose synthase genes (CesA4, CesA7 and CesA8) are duplicated in Populus plants due to a recent whole genome duplication event. Here, we demonstrate that duplicate CesA genes show tissue-dependent expression divergence in Populus plants. Real-time PCR analysis of Populus CesA genes suggested that Pt × tCesA8-B was more highly expressed than Pt × tCesA8-A in phloem and secondary xylem tissue of mature stem. Histochemical and histological analyses of transformants expressing a GFP-GUS fusion gene driven by Populus CesA promoters revealed that the duplicate CesA genes showed different expression patterns in phloem fibers, secondary xylem, root cap and leaf trichomes. We predicted putative cis-regulatory motifs that regulate expression of secondary cell wall-associated CesA genes, and identified 19 motifs that are highly conserved in the CesA gene family of eudicotyledonous plants. Furthermore, a transient transactivation assay identified candidate transcription factors that affect levels and patterns of expression of Populus CesA genes. The present study reveals that secondary cell wall-associated CesA genes in Populus have undergone a functional differentiation in expression pattern that may be attributable to evolutionary alteration of regulatory modules.

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Abbreviations

CaMV35S:

Cauliflower mosaic virus 35S

CesA:

Cellulose synthase

CSC:

Cellulose synthase complex

GFP:

Green fluorescent protein

EmGFP:

Emerald green fluorescent protein

GUS:

β-Glucuronidase

JTT:

Jones–Taylor–Thornton

LBD:

LOB domain-containing protein

LUC:

Luciferase

M46RE:

MYB46-responsive cis-element

MBSIIG:

MYB binding site IIG

NAC:

NAM, ATAF1/2 and CUC2

NJ:

Neighbor-joining

RLUC:

Renilla reniformis luciferase

UBQ:

Ubiquitin

WGD:

Whole genome duplication

ZF:

Zinc-finger protein

References

  • Betancur L, Singh B, Rapp RA, Wendel JF, Marks MD, Roberts AW, Haigler CH (2010) Phylogenetically distinct cellulose synthase genes support secondary wall thickening in Arabidopsis shoot trichomes and cotton fiber. J Integr Plant Biol 52:205–220

    Article  CAS  PubMed  Google Scholar 

  • Bocock PN, Morse AM, Dervinis C, Davis JM (2008) Evolution and diversity of invertase genes in Populus trichocarpa. Planta 227:565–576

    Article  CAS  PubMed  Google Scholar 

  • Burton RA, Shirley NJ, King BJ, Harvey AJ, Fincher GB (2003) The CesA gene family of barley. Quantitative analysis of transcripts reveals two groups of co-expressed genes. Plant Physiol 134:224–236

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Creux NM, Bossinger G, Myburg AA, Spokevicius AV (2013) Induced somatic sector analysis of cellulose synthase (CesA) promoter regions in woody stem tissues. Planta 237:799–812

    Article  CAS  PubMed  Google Scholar 

  • Dharmawardhana P, Brunner AM, Strauss SH (2010) Genome-wide transcriptome analysis of the transition from primary to secondary stem development in Populus trichocarpa. BMC Genomics 11:150

    Article  PubMed Central  PubMed  Google Scholar 

  • Eriksson ME, Israelsson M, Olsson O, Moritz T (2000) Increased gibberellin biosynthesis in transgenic trees promotes growth, biomass production and xylem fiber length. Nat Biotechnol 18:784–788

    Article  CAS  PubMed  Google Scholar 

  • Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151:1531–1545

    CAS  PubMed Central  PubMed  Google Scholar 

  • Freeling M, Thomas BC (2006) Gene-balanced duplications, like tetraploidy, provide predictable drive to increase morphological complexity. Genome Res 16:805–814

    Article  CAS  PubMed  Google Scholar 

  • Gardiner JC, Taylor NG, Turner SR (2003) Control of cellulose synthase complex localization in developing xylem. Plant Cell 15:1740–1748

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hanada K, Kuromori T, Myouga F, Toyoda T, Shinozaki K (2009) Increased expression and protein divergence in duplicate genes is associated with morphological diversification. PLoS Genet 5:e1000781

    Article  PubMed Central  PubMed  Google Scholar 

  • Handakumbura PP, Matos DA, Osmont KS, Harrington MJ, Heo K, Kafle K, Kim SH, Baskin TI, Hazen SP (2013) Perturbation of Brachypodium distachyon CELLULOSE SYNTHASE A4 or 7 results in abnormal cell walls. BMC Plant Biol 13:131

    Article  PubMed Central  PubMed  Google Scholar 

  • Hao J, Tu L, Hu H, Tan J, Deng F, Tang W, Nie Y, Zhang X (2012) GbTCP, a cotton TCP transcription factor, confers fibre elongation and root hair development by a complex regulating system. J Exp Bot 63:6267–6281

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hsu CY, Adams JP, Kim H, No K, Ma C, Strauss SH, Drnevich J, Vandervelde L, Ellis JD, Rice BM, Wickett N, Gunter LE, Tuskan GA, Brunner AM, Page GP, Barakat A, Carlson JE, DePamphilis CW, Luthe DS, Yuceer C (2011) FLOWERING LOCUS T duplication coordinates reproductive and vegetative growth in perennial poplar. Proc Natl Acad Sci USA 108:10756–10761

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hussey SG, Mizrachi E, Creux NM, Myburg AA (2013) Navigating the transcriptional roadmap regulating plant secondary cell wall deposition. Front Plant Sci 4:325. doi:10.3389/fpls.2013.00325

    Article  PubMed Central  PubMed  Google Scholar 

  • Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jiao Y, Wickett NJ, Ayyampalayam S, Chanderbali AS, Landherr L, Ralph PE, Tomsho LP, Hu Y, Liang H, Soltis PS, Soltis DE, Clifton SW, Schlarbaum SE, Schuster SC, Ma H, Leebens-Mack J, dePamphilis CW (2011) Ancestral polyploidy in seed plants and angiosperms. Nature 473:97–100

    Article  CAS  PubMed  Google Scholar 

  • Jiménez-Delgado S, Pascual-Anaya J, Garcia-Fernàndez J (2009) Implications of duplicated cis-regulatory elements in the evolution of metazoans: the DDI model or how simplicity begets novelty. Brief Funct Genomic Proteomic 8:266–275

    Article  PubMed  Google Scholar 

  • Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8:275–282

    CAS  PubMed  Google Scholar 

  • Kalluri UC, Difazio SP, Brunner AM, Tuskan GA (2007) Genome-wide analysis of Aux/IAA and ARF gene families in Populus trichocarpa. BMC Plant Biol 7:59. doi:10.1186/1471-2229-7-59

    Article  PubMed Central  PubMed  Google Scholar 

  • Kim HJ, Murai N, Fang DD, Triplett BA (2011) Functional analysis of Gossypium hirsutum cellulose synthase catalytic subunit 4 promoter in transgenic Arabidopsis and cotton tissues. Plant Sci 180:323–332

    Article  CAS  PubMed  Google Scholar 

  • Kim WC, Ko JH, Han KH (2012a) Identification of a cis-acting regulatory motif recognized by MYB46, a master transcriptional regulator of secondary wall biosynthesis. Plant Mol Biol 78:489–501

    Article  CAS  PubMed  Google Scholar 

  • Kim WC, Ko JH, Kim JY, Kim JM, Bae HJ, Han KH (2012b) MYB46 directly regulates the gene expression of secondary wall-associated cellulose synthases in Arabidopsis. Plant J 73:26–36

    Google Scholar 

  • Koncz C, Schell J (1986) The promoter of TL-DNA gene 5 controls the tissue-specific expression of chimeric genes carried by a novel type of Agrobacterium binary vector. Mol Gen Genet 204:383–396

    Article  CAS  Google Scholar 

  • Kumar M, Thammannagowda S, Bulone V, Chiang V, Han KH, Joshi CP, Mansfield SD, Mellerowicz E, Sundberg B, Teeri T, Ellis BE (2009) An update on the nomenclature for the cellulose synthase genes in Populus. Trends Plant Sci 14:248–254

    Article  CAS  PubMed  Google Scholar 

  • Lee TH, Tang H, Wang X, Paterson AH (2012) PGDD: a database of gene and genome duplication in plants. Nucleic Acids Res 41:D1152–D1158

    Article  PubMed Central  PubMed  Google Scholar 

  • Mitsuda N, Seki M, Shinozaki K, Ohme-Takagi M (2005) The NAC transcription factors NST1 and NST2 of Arabidopsis regulate secondary wall thickenings and are required for anther dehiscence. Plant Cell 17:2993–3006

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nanjo T, Futamura N, Nishiguchi M, Igasaki T, Shinozaki K, Shinohara K (2004) Characterization of full-length enriched expressed sequence tags of stress-treated poplar leaves. Plant Cell Physiol 45:1738–1748

    Article  PubMed  Google Scholar 

  • Oakley RV, Wang YS, Ramakrishna W, Harding SA, Tsai CJ (2007) Differential expansion and expression of α- and β-tubulin gene families in Populus. Plant Physiol 145:961–973

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ohashi-Ito K, Oda Y, Fukuda H (2010) Arabidopsis VASCULAR-RELATED NAC-DOMAIN6 directly regulates the genes that govern programmed cell death and secondary wall formation during xylem differentiation. Plant Cell 22:3461–3473

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ohta T (2003) Evolution by gene duplication revisited: differentiation of regulatory elements versus proteins. Genetica 118:209–216

    Article  CAS  PubMed  Google Scholar 

  • Ohtani M, Nishikubo N, Xu B, Yamaguchi M, Mitsuda N, Goué N, Shi F, Ohme-Takagi M, Demura T (2011) A NAC domain protein family contributing to the regulation of wood formation in poplar. Plant J 67:499–512

    Article  CAS  PubMed  Google Scholar 

  • Rodgers-Melnick E, Mane SP, Dharmawardhana P, Slavov GT, Crasta OR, Strauss SH, Brunner AM, Difazio SP (2012) Contrasting patterns of evolution following whole genome versus tandem duplication events in Populus. Genome Res 22:95–105

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Romero I, Fuertes A, Benito MJ, Malpica JM, Leyva A, Paz-Ares J (1998) More than 80R2R3-MYB regulatory genes in the genome of Arabidopsis thaliana. Plant J 14:273–284

    Article  CAS  PubMed  Google Scholar 

  • Shimada S, Otsuki H, Sakuta M (2007) Transcriptional control of anthocyanin biosynthetic genes in the Caryophyllales. J Exp Bot 58:957–967

    Article  CAS  PubMed  Google Scholar 

  • Song D, Shen J, Li L (2010) Characterization of cellulose synthase complexes in Populus xylem differentiation. New Phytol 187:777–790

    Article  CAS  PubMed  Google Scholar 

  • Suzuki S, Li L, Sun YH, 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Takata N, Saito S, Saito CT, Nanjo T, Shinohara K, Uemura M (2009) Molecular phylogeny and expression of poplar circadian clock genes, LHY1 and LHY2. New Phytol 181:808–819

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tanaka K, Murata K, Yamazaki M, Onosato K, Miyao A, Hirochika H (2003) Three distinct rice cellulose synthase catalytic subunit genes required for cellulose synthesis in the secondary wall. Plant Physiol 133:73–83

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Taylor JS, Raes J (2004) Duplication and divergence: the evolution of new genes and old ideas. Annu Rev Genet 38:615–643

    Article  CAS  PubMed  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 USA 100:1450–1455

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tuskan GA, Difazio S, Jansson S et al (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604

    Article  CAS  PubMed  Google Scholar 

  • Tzfira T, Tian GW, Lacroix B, Vyas S, Li J, Leitner-Dagan Y, Krichevsky A, Taylor T, Vainstein A, Citovsky V (2005) pSAT vectors: a modular series of plasmids for autofluorescent protein tagging and expression of multiple genes in plants. Plant Mol Biol 57:503–516

    Article  CAS  PubMed  Google Scholar 

  • Wang S, Yin Y, Ma Q, Tang X, Hao D, Xu Y (2012) Genome-scale identification of cell-wall related genes in Arabidopsis based on co-expression network analysis. BMC Plant Biol 12:138

    Article  PubMed Central  PubMed  Google Scholar 

  • Wilkins O, Nahal H, Foong J, Provart NJ, Campbell MM (2009) Expansion and diversification of the Populus R2R3-MYB family of transcription factors. Plant Physiol 149:981–993

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wu AM, Hu JS, Liu JY (2009) Functional analysis of a cotton cellulose synthase A4 gene promoter in transgenic tobacco plants. Plant Cell Rep 28:1539–1548

    Article  CAS  PubMed  Google Scholar 

  • Xiao YL, Redman JC, Monaghan EL, Zhuang J, Underwood BA, Moskal WA, Wang W, Wu HC, Town CD (2010) High throughput generation of promoter reporter (GFP) transgenic lines of low expressing genes in Arabidopsis and analysis of their expression patterns. Plant Methods 6:18

    Article  PubMed Central  PubMed  Google Scholar 

  • Yamaguchi M, Goué N, Igarashi H, Ohtani M, Nakano Y, Mortimer JC, Nishikubo N, Kubo M, Katayama Y, Kakegawa K, Dupree P, Demura T (2010) VASCULAR-RELATED NAC-DOMAIN6 and VASCULAR-RELATED NAC-DOMAIN7 effectively induce transdifferentiation into xylem vessel elements under control of an induction system. Plant Physiol 153:906–914

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yamaguchi M, Mitsuda N, Ohtani M, Ohme-Takagi M, Kato K, Demura T (2011) VASCULAR-RELATED NAC-DOMAIN7 directly regulates the expression of a broad range of genes for xylem vessel formation. Plant J 66:579–590

    Article  CAS  PubMed  Google Scholar 

  • Yin Y, Huang J, Xu Y (2009) The cellulose synthase superfamily in fully sequenced plants and algae. BMC Plant Biol 9:99. doi:10.1186/1471-2229-9-99

    Article  PubMed Central  PubMed  Google Scholar 

  • Zhong R, Lee C, Zhou J, McCarthy RL, Ye ZH (2008) A battery of transcription factors involved in the regulation of secondary cell wall biosynthesis in Arabidopsis. Plant Cell 20:2763–2782

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhong R, McCarthy RL, Lee C, Ye ZH (2011) Dissection of the transcriptional program regulating secondary wall biosynthesis during wood formation in poplar. Plant Physiol 157:1452–1468

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhong R, McCarthy RL, Haghighat M, Ye ZH (2013) The poplar MYB master switches bind to the SMRE site and activate the secondary wall biosynthetic program during wood formation. PLoS One 8:e69219

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zou C, Sun K, Mackaluso JD, Seddon AE, Jin R, Thomashow MF, Shiu SH (2011) Cis-regulatory code of stress-responsive transcription in Arabidopsis thaliana. Proc Natl Acad Sci USA 108:14992–14997

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

We thank Prof. Masaaki Sakuta for a gift of pUC18-CaMV35S::LUC and pUC18-CaMV35S::RLUC constructs. We thank Dr. Misato Ohtani (Nara Institute of Science and Technology) for helpful advice on luciferase transient expression assays. We are grateful to Ms. Maki Konnai and Tomoko Okuyama in our laboratory for their technical assistance. This work was supported in part by a Grant-in-Aid for Young Scientists (Start-up) from the Japan Society for the Promotion of Science (23880029 to NT).

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The authors declare that they have no conflict of interest.

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Takata, N., Taniguchi, T. Expression divergence of cellulose synthase (CesA) genes after a recent whole genome duplication event in Populus . Planta 241, 29–42 (2015). https://doi.org/10.1007/s00425-014-2217-9

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