Skip to main content
Log in

The sucrose synthase gene family in Populus: structure, expression, and evolution

  • Original Paper
  • Published:
Tree Genetics & Genomes Aims and scope Submit manuscript

Abstract

Sucrose synthase is a key enzyme in sucrose metabolism in plant cells, and it is involved in the synthesis of cell wall cellulose. Although the sucrose synthase gene (SUS) family in the model plants Arabidopsis thaliana has been characterized, little is known about this gene family in trees. This study reports the identification of two novel SUS genes in the economically important poplar tree. These genes were expressed predominantly in mature xylem. Using molecular cloning and bioinformatics analysis of the Populus genome, we demonstrated that SUS is a multigene family with seven members that each exhibit distinct but partially overlapping expression patterns. Of particular interest, three SUS genes were preferentially expressed in the stem xylem, suggesting that poplar SUSs are involved in the formation of the secondary cell wall. Gene structural and phylogenetic analyses revealed that the Populus SUS family is composed of four main subgroups that arose before the separation of monocots and dicots. Phylogenetic analyses associated with the tissue- and organ-specific expression patterns. The high intraspecific nucleotide diversity of two SUS genes was detected in the natural population, and the π nonsyn/π syn ratio was significantly less than 1; therefore, SUS genes appear to be evolving in Populus, primarily under purifying selection. This is the first comprehensive study of the SUS gene family in woody plants; the analysis includes genome organization, gene structure, and phylogeny across land plant lineages, as well as expression profiling in Populus.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Albrecht G, Mustroph A (2003) Localization of sucrose synthase in wheat roots: increased in situ activity of sucrose synthase correlates with cell wall thickening by cellulose deposition under hypoxia. Planta 217:252–260

    PubMed  CAS  Google Scholar 

  • Barratt DHP, Barber L, Kruger NJ, Smith AM, Wang TL, Martin C (2001) Multiple, distinct isoforms of sucrose synthase in pea. Plant Physiol 127:655–664

    Article  PubMed  CAS  Google Scholar 

  • Barratt DHP, Derbyshire P, Findlay K, Pike M, Wellner N, Lunn J, Feil R, Simpson C, Maule AJ, Smith AM (2009) Normal growth of Arabidopsis requires cytosolic invertase but not sucrose synthase. Proc Natl Acad Sci USA 106:13124–13129

    Article  PubMed  CAS  Google Scholar 

  • Baud S, Vaultier MN, Rochat C (2004) Structure and expression profile of the sucrose synthase multigene family in Arabidopsis. J Exp Bot 55:397–409

    Article  PubMed  CAS  Google Scholar 

  • Bieniawska Z, Barratt DHP, Garlick AP, Thole V, Kruger NJ, Martin C, Zrenner R, Smith AM (2007) Analysis of the sucrose synthase gene family in Arabidopsis. Plant J 49:810–828

    Article  PubMed  CAS  Google Scholar 

  • Breen AL, Glenn E, Yeager A, Olson MS (2009) Nucleotide diversity among natural populations of a North American poplar (Populus balsamifera, Salicaceae). New Phytol 182:763–773

    Article  PubMed  CAS  Google Scholar 

  • Chu YG, Su XH, Huang QJ, Zhang XH (2009) Patterns of DNA sequence variation at candidate gene loci in black poplar (Populus nigra L.) as revealed by single nucleotide polymorphisms. Genetica 137:141–150

    Article  PubMed  CAS  Google Scholar 

  • Clancy M, Hannah LC (2002) Splicing of the maize Sh1 first intron is essential for enhancement of gene expression, and a T-rich motif increases expression without affecting splicing. Plant Physiol 130:918–929

    Article  PubMed  CAS  Google Scholar 

  • Coleman HD, Yan J, Mansfield SD (2009) Sucrose synthase affects carbon partitioning to increase cellulose production and altered cell wall ultrastructure. Proc Natl Acad Sci USA 106:13118–13123

    Article  PubMed  CAS  Google Scholar 

  • Demirbas A (2005) Bioethanol from cellulosic materials: a renewable motor fuel from biomass. Energy Sources 27:327–337

    Article  CAS  Google Scholar 

  • Fu YX, Li WH (1993) Statistical tests of neutrality of mutations. Genetics 133:693–709

    PubMed  CAS  Google Scholar 

  • Fu HY, Kim SY, Park WD (1995) A potato Sus3 sucrose synthase gene contains a context-dependent 3′ element and a leader intron with both positive and negative tissue-specific effects. Plant Cell 7:1395–1403

    Article  PubMed  CAS  Google Scholar 

  • Haigler CH, Ivanova-Datcheva M, Hogan PS, Salnikov VV, Hwang S, Martin K, Delmer DP (2001) Carbon partitioning to cellulose synthesis. Plant Mol Biol 47:29–51

    Article  PubMed  CAS  Google Scholar 

  • Hamrick JL, Godt MJW (1996) Effects of life history traits on genetic diversity in plant species. Phil Trans R Soc Lond B 351:1291–1298

    Article  Google Scholar 

  • Hardin SC, Duncan KA, Huber SC (2006) Determination of structural requirements and probable regulatory effectors for membrane association of maize sucrose synthase 1. Plant Physiol 141:1106–1119

    Article  PubMed  CAS  Google Scholar 

  • Hauch S, Magel E (1998) Extractable activities and protein content of sucrose phosphate synthase, sucrose synthase and neutral invertase in trunk tissues of Robinia pseudoacacia L. are related to cambial wood production and heart wood formation. Planta 207:266–274

    Article  CAS  Google Scholar 

  • Hirose T, Scofield GN, Terao T (2008) An expression analysis profile for the entire sucrose synthase gene family in rice. Plant Sci 174:534–543

    CAS  Google Scholar 

  • Huang ZH (1992) The study on the climatic regionalization of the distributional region of Populus tomentosa. Journal of Beijing Forestry University 14:26–32

    CAS  Google Scholar 

  • Ingvarsson PK (2005) Nucleotide polymorphism and linkage disequilibrium within and among natural populations of European aspen (Populus tremula L., Salicaceae). Genetics 169:945–953

    Article  PubMed  CAS  Google Scholar 

  • Ingvarsson PK (2008) Multilocus patterns of nucleotide polymorphism and the demographic history of Populus tremula. Genetics 180:329–340

    Article  PubMed  Google Scholar 

  • Joshi CP, Bhandari S, Ranjan P et al (2004) Genomics of cellulose biosynthesis in poplars. New Phytol 164:53–61

    Article  CAS  Google Scholar 

  • Komatsu OA, Moriguchi T, Koyama K, Omura M, Akihama T (2002) Analysis of sucrose synthase genes in citrus suggests different roles and phylogenetic relationships. J Exp Bot 53:61–71

    Article  PubMed  CAS  Google Scholar 

  • Li X, Weng JK, Chapple C (2008) Improvement of biomass through lignin modification. Plant J 54:569–581

    Article  PubMed  CAS  Google Scholar 

  • Lunn JE (2002) Evolution of sucrose synthesis. Plant Physiol 128:1490–1500

    Article  PubMed  CAS  Google Scholar 

  • Luo XY, Xiao YH, Li DM, Luo M, Hou L, Li XB, Yang X, Pei Y (2005) Cloning and analysis of the upstream regulated sequence of a cotton fiber sucrose synthase gene. Chin J Biochem Mol Biol 21:335–340

    CAS  Google Scholar 

  • Mitchell-Olds T, Clauss MJ (2002) Plant evolutionary genomics. Curr Opin Plant Biol 5:74–79

    Article  PubMed  CAS  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Ross-Ibarra J, Wright SI, Foxe JP, Kawabe A, DeRose-Wilson L, Gos G, Charlesworth D, Gaut BS (2008) Patterns of polymorphism and demographic history in natural populations of Arabidopsis lyrata. PLoSONE3 6:e2411. doi:10.1371/journal.pone.0002411

    Google Scholar 

  • Rozas J, Sánchez-Delbarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497

    Article  PubMed  CAS  Google Scholar 

  • Ruan YL, Llewellyn DJ, Furbank RT (2003) Suppression of sucrose synthase gene expression represses cotton fiber cell initiation, elongation, and seed development. Plant Cell 15:952–964

    Article  PubMed  CAS  Google Scholar 

  • Savard L, Li P, Strauss SH, Chase MW, Michaud M, Bousquet J (1994) Chloroplast and nuclear gene sequences indicate late Pennsylvanian time for the last common ancestor of extant seed plants. Proc Natl Acad Sci USA 91:5163–5167

    Article  PubMed  CAS  Google Scholar 

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    PubMed  CAS  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  PubMed  CAS  Google Scholar 

  • Tang GQ, Strum A (1999) Antisense repression of sucrose synthase in carrot (Daucus carota L.) affects growth rather than sucrose partitioning. Plant Mol Biol 41:465–479

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Watterson GA (1975) On the number of segregating sites in genetical models without recombination. Theor Popul Biol 7:188–193

    Article  Google Scholar 

  • Zhang DQ, Zhang ZY, Yang K (2007) Identification of AFLP markers associated with embryonic root development in Populus tomentosa. Silvae Genet 56:27–32

    Google Scholar 

  • Zhang DQ, Du QZ, Xu BH, Zhang ZY, Li B (2010a) The actin multigene family in Populus: organization, expression and phylogenetic analysis. Mol Genet Genomics 284:105–119

    Article  CAS  Google Scholar 

  • Zhang DQ, Yang XH, Zhang ZY, Li B (2010b) Expression and nucleotide diversity of the poplar COBL gene. Tree Genet Genomes 6:331–344

    Article  Google Scholar 

Download references

Acknowledgments

This work was supported by grants from the Fundamental Research Funds for the Central Universities (No. BLJC200906), the project of National Natural Science Foundation of China (No. 30600479, 30872042), Major Science Foundation of Ministry of Education of China (No. 307006), Foundation for the Author of National Excellent Doctoral Dissertation of PR China (No. 200770), Program for New Century Excellent Talents in University (No. NCET-07-0084), and Introduction of Foreign Advanced Agricultural Science and Technology into China (No. 2009-4-22).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Deqiang Zhang or Bailian Li.

Additional information

Communicated by W. Boerjan

Sequence data from this article have been deposited with the GenBank Data Library under accession numbers GU559727–GU559735 (PtSUS1, PtSUS2, PtrSUS1 to PtrSUS7 cDNA) and HM026865–HM026944 for the population sequences of PtSUS1 and PtSUS2 genes.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Fig. S1

Geographic location of each individual P. tomentosa tree used for nucleotide diversity analysis. The relevant Chinese provinces are shown. Each tree is indicated by a red dot (DOC 1411 kb)

Fig. S2

Nucleotide and deduced amino acid sequences of PtSUS1 (a) and PtSUS2 (b). Numbers on the left refer to the positions of nucleotides or amino acid residues (DOC 52 kb)

Fig. S3

Spatiotemporal expression patterns of PtSUS1 and PtSUS2 in poplar. a Relative transcript levels of PtSUS1 and PtSUS2 in various poplar tissues. b The spatial expression of PtSUS1 and PtSUS2 in the mature xylem of poplar (DOC 29 kb)

Fig. S4

Protein sequence alignment of PtrSUS family members. The numbers on the left are the positions of the amino acids in each protein, with gaps (dashes) included to maximize alignments. Identical and similar amino acids are shaded in pink and blue, respectively (DOC 189 kb)

Table S1

Primers used for sucrose synthase cDNA amplification (DOC 30 kb)

Table S2

Primers used for sucrose synthase gene amplification (DOC 42 kb)

Table S3

List of sucrose synthase gene sequences used in this study (DOC 59 kb)

Table S4

Lengths of gene regions analyzed in this study (DOC 36 kb)

Table S5

The frequencies of nucleotide substitution types in PtSUS1 and PtSUS2 (DOC 35 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhang, D., Xu, B., Yang, X. et al. The sucrose synthase gene family in Populus: structure, expression, and evolution. Tree Genetics & Genomes 7, 443–456 (2011). https://doi.org/10.1007/s11295-010-0346-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11295-010-0346-2

Keywords

Navigation