Structure, expression profile, and evolution of the sucrose synthase gene family in peach (Prunus persica)

  • Chunhua Zhang
  • Mingliang Yu
  • Ruijuan Ma
  • Zhijun Shen
  • Binbin Zhang
  • Nicholas Kibet Korir
Original Paper

Abstract

Key message

SUS gene family is comprised of six genes in peach,PpSus1toPpSus6.PpSus1 to PpSus6 were categorized to represent three groups, group I, II, and III. PpSus showed conservative characteristics with Sus in other plants.PpSusexhibited distinct expression patterns in tissues at four development stages.

Abstract

Sucrose synthase (SUS) has been suggested to play a key role in plant sucrose metabolism with recent studies reporting that a small number of genes encoding different isozymes of Sus exist in most plant species. Despite this, information on genes encoding different isozymes of Sus in peach (Prunus persica) is scanty. In this study, we report the prediction, isolation, structural characteristics, phylogenetic connections and expression outline of six Sus genes in peach (PpSus1 to 6). The six PpSus genes were found distributed across scaffolds 1, 3, 5, 7, and 8. Analysis of the exons/introns revealed that PpSus genes contain multiple introns that range from 11 to 13 and displayed a high degree of conservation with corresponding Sus genes in other plant species. The comparative screening of motifs in PpSus proteins indicated high conservation in terms of number, width and order of motifs among PpSus proteins, which indirectly indicates that the six PpSus proteins are indeed members of the SUS family. Phylogenetic analysis revealed that PpSus2 to PpSus4 belonged to group II of the Sus family, PpSus5 and PpSus6 were clustered into group III, and group I contained only one peach gene (PpSus1) together with members from 10 other plant species. Analysis of expression levels of the six PpSus genes revealed that transcripts of PpSus1 were almost undetectable in leaves and in older phloem, while PpSus2 and PpSus4 were almost undetectable in flowers. The other three PpSus genes appeared differentially expressed in all tissues examined and were detected at different stages of tissue development. The results obtained from this study will be useful in selecting candidate PpSus genes for further functional analysis in the pathway of sucrose metabolism in peach and specifically in characterizing the knockout/knockdown mutants of PpSus genes.

Keywords

Peach Sucrose synthase Characteristics Phylogenetic analysis Expression pattern 

Abbreviations

DABF

Days after full bloom

GDR

Genome Database for Rosaceae

GSDS

Gene Structure Display Server

GRAVY

Grand average of hydropathicity

HMM

Hidden Markov model

kDa

Kilodalton

NG

New group

PI

Isoelectric point

qRT-PCR

Quantitative real-time PCR

TAIR

The Arabidopsis Information Resource

Sus

Sucrose synthase

UTR

Untranslated region

Supplementary material

11738_2015_1829_MOESM1_ESM.docx (358 kb)
Supplementary material 1 (DOCX 358 kb)

References

  1. Amor Y, Haigler CH, Johnson S, Wainscott M, Delmer DP (1995) A membrane-associated form of sucrose synthase and its potential role in synthesis of cellulose and callose in plants. Proc Natl Acad Sci USA 92:9353–9357CrossRefPubMedCentralPubMedGoogle Scholar
  2. Anfinsen BC (1973) Principles that govern the folding of protein chains. Science 181(4096):223–230CrossRefPubMedGoogle Scholar
  3. Anfinsen BC, Haber E, Sela M, White F (1961) The kinetics of formation of native ribonuclease during oxidation of the reduced polypeptide chain. Proc Natl Acad Sci 47:1309–1314CrossRefPubMedCentralPubMedGoogle Scholar
  4. Bailey TL, Williams N, Misleh C, Li WW (2006) MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res 34:369–373CrossRefGoogle Scholar
  5. Baud S, Vaultier MN, Rochat C (2004) Structure and expression profile of the sucrose synthase multigene family in Arabidopsis. J Exp Bot 55:397–409CrossRefPubMedGoogle Scholar
  6. Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J, Wittwer CT (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55(4):611–622CrossRefPubMedGoogle Scholar
  7. Cermain V, Ricard B, Raymond P, Saglio PH (1997) The role of sugars, hexokinase, and sucrose synthase in the determination of hypoxically induced tolerance to anoxia in tomato roots. Plant Physiol 14:167–175Google Scholar
  8. Chen AQ, He S, Li FF, Li Z, Ding MQ, Liu QP, Rong JK (2012) Analyses of the sucrose synthase gene family in cotton: structure, phylogeny and expression patterns. BMC Plant Biol 12:85CrossRefPubMedCentralPubMedGoogle Scholar
  9. Cho JI, Kim HB, Kim CY, Hahn TR, Jeon JS (2011) Identification and characterization of the duplicate rice sucrose synthase genes OsSUS5 and OsSUS7 which are associated with the plasma membrane. Mol Cells 31:553–561CrossRefPubMedCentralPubMedGoogle Scholar
  10. 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 106:13118–13123CrossRefPubMedCentralPubMedGoogle Scholar
  11. Cristina BS, Sara HA, Pablo GM, Pilar C (2011) Structure, expression profile and subcellular localisation of four different sucrose synthase genes from barley. Planta 234:391–403CrossRefGoogle Scholar
  12. Duncan KA, Huber SC (2007) Sucrose synthase oligomerization and F-actin association are regulated by sucrose concentration and phosphorylation. Plant Cell Physiol 48(11):1612–1623CrossRefPubMedGoogle Scholar
  13. Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Heger A, Hetherington K, Holm L, Mistry J, Sonnhammer ELL, Tate J, Punta M (2014) The pfam protein families database. Nucleic Acids Res (Database Issue) 42:222–230CrossRefGoogle Scholar
  14. Fu HY, Kim SY, Park WD (1995a) A potato Sus3 sucrose synthase gene contains a context-dependent 3′ element and a leader lntron with both positive and negative tissue-specific effects. Plant Cell 7:1395–1403PubMedCentralPubMedGoogle Scholar
  15. Fu HY, Kim SY, Park WD (1995b) High-leve1 tuber expression and sucrose lnducibility of a potato Sus4 sucrose synthase gene require 5′ and 3′ flanking sequences and the leader intron. Plant Cell 7:1387–1394PubMedCentralPubMedGoogle Scholar
  16. Geigenberger P (2003) Regulation of sucrose to starch conversion in growing potato tubers. J Exp Bot 54(382):457–465CrossRefPubMedGoogle Scholar
  17. HaÈnggi E, Fleming AJ (2001) Sucrose synthase expression pattern in young maize leaves: implications for phloem transport. Planta 214:326–329Google Scholar
  18. Harada T, Satoh S, Yoshioka T, Ishizawa K (2005) Expression of sucrose synthase genes involved in enhanced elongation of pondweed (Potamogeton distinctus) turions under anoxia. Ann Bot 96:683–692CrossRefPubMedCentralPubMedGoogle Scholar
  19. Hirose T, Scofield GN, Terao T (2008) An expression analysis profile for the entire sucrose synthase gene family in rice. Plant Sci 174:534–543CrossRefGoogle Scholar
  20. Horst I, Welham T, Kelly S, Kaneko T, Sato S, Tabata S, Parniske M, Wang TL (2007) TILLING mutants of Lotus japonicus reveal that nitrogen assimilation and fixation can occur in the absence of nodule-enhanced sucrose synthase. Plant Physiol 144:806–820CrossRefPubMedCentralPubMedGoogle Scholar
  21. Hu LF, Liu SQ (2011) Genome-wide identification and phylogenetic analysis of the ERF gene family in cucumbers. Genetics Mol Biol 34(4):624–633CrossRefGoogle Scholar
  22. Joshi CP, Bhandari S, Ranjan P, Kalluri UC, Liang XE, Fujino T, Samuga A (2004) Genomics of cellulose biosynthesis in poplars. New Phytol 164:53–61CrossRefGoogle Scholar
  23. Kiefer F, Arnold K, Künzli M, Bordoli L, Schwede T (2009) The SWISS-MODEL repository and associated resources. Nucleic Acids Res 37:D387–D392CrossRefPubMedCentralPubMedGoogle Scholar
  24. Kleczkowski LA, Kunz S, Wilczynska M (2010) Mechanisms of UDP-Glucose synthesis in plants. Crit Rev Plant Sci 29:191–203CrossRefGoogle Scholar
  25. Klotz KL, Finger FL, Shelver WL (2003) Characterization of two sucrose synthase isoforms in sugarbeet root. Plant Physiol Biochem 41:107–115CrossRefGoogle Scholar
  26. Koch KE, Wu Y, Xu J (1996) Sugar and metabolic regulation of genes for sucrose metabolism: potential influence of maize sucrose synthase and soluble invertase responses on carbon partitioning and sugar sensing. J Exp Bot 47:1179–1185CrossRefPubMedGoogle Scholar
  27. Komatsu A, 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 53:61–71CrossRefPubMedGoogle Scholar
  28. Lee JJ, Woodward AW, Chen ZJ (2007) Gene expression changes and early events in cotton fibre development. Ann Bot 100:1391–1401CrossRefPubMedCentralPubMedGoogle Scholar
  29. Lerchl J, Geigenberger P, Stitt M, Sonnewald U (1995) Impaired photoassimilate partitioning caused by phloem-specific removal of phyrophosphate can be complemented by a phloem-specific cytosolic yeast-derived invertase in transgenic plants. Plant Cell 7:259–270CrossRefPubMedCentralPubMedGoogle Scholar
  30. Lingle SE (1999) Sugar metabolism during growth and development in sugarcane internodes. Crop Sci 39(2):480–486CrossRefGoogle Scholar
  31. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the \( 2^{{ - {\Delta \Delta }C_{\text{T}} }} \) method. Methods 25:402–408Google Scholar
  32. Lutfiyya LL, Xu NF, D’Ordine RL, Morrell JA, Miller PW, Duff SMG (2007) Phylogenetic and expression analysis of sucrose phosphate synthase isozymes in plants. J Plant Physiol 164:923–933CrossRefPubMedGoogle Scholar
  33. Marchler-Bauer A, Lu SN, Anderson JB, Chitsaz F, Derbyshire MK, DeWeese-Scott C, Fong JH, Geer LY, Geer RC, Gonzales NR, Gwadz M, Hurwitz DI, Jackson JD, Ke Z, Lanczycki CJ, Lu F, Marchler GH, Mullokandov M, Omelchenko MV, Robertson CL, Song JS, Thanki N, Yamashita RA, Zhang D, Zhang N, Zheng C, Bryant SH (2011) CDD: a conserved domain database for the functional annotation of proteins. Nucleic Acids Res 39:D225–D229CrossRefPubMedCentralPubMedGoogle Scholar
  34. Matic S, Åkerlund HE, Everitt E, Widell S (2004) Sucrose synthase isoforms in cultured tobacco cells. Plant Physiol Biochem 42:299–306CrossRefPubMedGoogle Scholar
  35. Mona S (2001) Predicting protein secondary and supersecondary structure. Princeton University, CRC Press, LLC 29:3–5Google Scholar
  36. Ruan YL, Llewellyn DJ, Furbank RT (2003) Suppression of sucrose synthase gene expression represses cotton fiber cell initiation, elongation, and seed development. Plant Cell 15:952–964CrossRefPubMedCentralPubMedGoogle Scholar
  37. Schafera WE, Rohwerb JM, Bothac FC (2005) Partial purification and characterisation of sucrose synthase in sugarcane. J Plant Physiol 162:11–20CrossRefGoogle Scholar
  38. Schmalstig JG, Hitz WD (1987) Contributions of sucrose synthase and invertase to the metabolism sucrose in developing leaves. Plant Physiol 85:407–412CrossRefPubMedCentralPubMedGoogle Scholar
  39. Schrader S, Sauter JJ (2002) Seasonal changes of sucrose-phosphate synthase and sucrose synthase activities in poplar wood (Populus × Canadensis Moench ‘robusta’) and their possible role in carbohydrate metabolism. J Plant Physiol 159(8):833–843CrossRefGoogle Scholar
  40. Sturm A, Tang GQ (1999) The sucrose-cleaving enzymes of plants are crucial for development, growth and carbon partitioning. Trends Plant Sci 4:401–407CrossRefPubMedGoogle Scholar
  41. 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. doi:10.1093/molbev/msr121 Google Scholar
  42. Tanase K, Yamaki S (2000) Purification and characterization of two sucrose synthase isoforms from Japanese pear fruit. Plant Cell Physiol 41:408–414CrossRefPubMedGoogle Scholar
  43. Tong ZG, Gao ZH, Wang F, Zhou J, Zhang Z (2009) Selection of reliable reference genes for gene expression studies in peach using real-time PCR. BMC Mol Biol 10:1–13CrossRefGoogle Scholar
  44. Tupy J, Primot L (1982) Sucrose synthetase in the latex of Hevea brasiliensis Muell Arg. J Exp Bot 33:988–995CrossRefGoogle Scholar
  45. Wang F, Sanz A, Brenner ML, Smith A (1993) Sucrose synthase, starch accumulation, and tomato fruit sink strength. Plant Physiol 101:321–327PubMedCentralPubMedGoogle Scholar
  46. Wang YJ, Deng DX, Bian YL, Lv YP, Xie Q (2010) Genome-wide analysis of primary auxin-responsive Aux/IAA gene family in maize (Zea mays. L.). Mol Biol Rep 37:3991–4001CrossRefPubMedGoogle Scholar
  47. Xiao XH, Tang CR, Fang YJ, Yang M, Zhou BH, Qi JY, Zhang Y (2013) Structure and expression profile of the sucrose synthase gene family in the rubber tree: indicative of roles in stress response and sucrose utilization in the laticifers. FEBS J 281:291–305CrossRefPubMedGoogle Scholar
  48. Zhang DQ, Xu BH, Yang XH, Zhang ZY, Li BL (2011) The sucrose synthase gene family in Populus: structure, expression, and evolution. Tree Genetics Genomes 7:443–456CrossRefGoogle Scholar
  49. Zhang JS, Arro J, Chen YQ, Ming R (2013a) Haplotype analysis of sucrose synthase gene family in three Saccharum species. BMC Genomics 14:314CrossRefPubMedCentralPubMedGoogle Scholar
  50. Zhang CH, Shen ZJ, Zhang YP, Han J, Ma RJ, Nicholas KK, Yu ML (2013b) Cloning and expression of genes related to the sucrose metabolizing enzymes and carbohydrate changes in peach. Acta Physiol Plant 35:589–602CrossRefGoogle Scholar
  51. Zheng Y, Anderson S, Zhang YF, Garavito RM (2011) The structure of sucrose synthase-1 from Arabidopsis thaliana and its functional implications. J Biol Chem 41:36108–36118CrossRefGoogle Scholar
  52. Zrenner R, Salanoubat M, Willmitzer L, Sonnewald U (1995) Evidence of the crucial role of sucrose synthase for sink strength using transgenic potato plants (Solanum tuberosum L.). Plant J 7:97–107CrossRefPubMedGoogle Scholar

Copyright information

© Franciszek Górski Institute of Plant Physiology, Polish Academy of Sciences, Kraków 2015

Authors and Affiliations

  • Chunhua Zhang
    • 1
  • Mingliang Yu
    • 1
  • Ruijuan Ma
    • 1
  • Zhijun Shen
    • 1
  • Binbin Zhang
    • 1
  • Nicholas Kibet Korir
    • 2
  1. 1.Institute of HorticultureJiangsu Academy of Agricultural Sciences, Jiangsu Key Laboratory for Horticultural Crop Genetic ImprovementNanjingChina
  2. 2.Department of Agricultural Science and TechnologyKenyatta UniversityNairobiKenya

Personalised recommendations