SpringerLink
Log in

Neutral invertases in grapevine and comparative analysis with Arabidopsis, poplar and rice

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Neutral invertases (NIs, EC 3.2.1.26) cleave sucrose to glucose and fructose. They are encoded by a small gene family of 9 members in the Arabidopsis genome, 8 in rice, 16 in poplar and 9 in Vitis vinifera (L.). The grapevine NIs were identified in the 8.4X genome assembly of the quasi-homozygous line PN40024. In addition, alleles of three NIs were sequenced in the heterozygous cultivar ‘Cabernet Sauvignon’. Analyses of sequence variation between alleles, homoeologous and paralogous copies in grapevine and their orthologues in Arabidopsis, poplar and rice are provided. In grapevine, NIs were classified into four α NIs and five β NIs and subsequently grouped into hierarchical clades using a combination of evidence including amino acid identity, exon/intron structure, rate of synonymous substitutions (K s) and chromosomal distribution. Estimation of K s proved the ancient origin of all NIs and the lack of expansion by gene duplication past the event of polyploidisation. We then focused on transcription analysis of five NIs for which evidence of expression was available from expressed sequence tag databases. Among these, four NIs consisted of pairs of homoeologous copies, each pair lying on a pair of chromosomes duplicated by polyploidy. Unequal expression of homoeologous genes was observed by quantitative RT-PCR in leaf, flower, seed and root tissues. Since NIs might play significant roles in fruit and wine quality, NIs expression was monitored in flesh and skin of ‘Merlot’ berries and shown in parallel with the suite of changes that accompany fruit ripening, including glucose and fructose accumulation.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Germany)

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

Abbreviations

BAC:

Bacterial artificial chromosome

Chr:

Chromosome

DAFB:

Days after full bloom

EST:

Expressed sequence tag

FPC:

Fingerprint contig

Indel:

Insertion/deletion

NJ:

Neighbor-joining

NI:

Neutral invertase

SNP:

Single nucleotide polymorphism

SSCP:

Single strand conformational polymorphism

K s :

Substitutions per synonymous site

K a :

Substitutions per non-synonymous site

UTR:

Untranslated region

WGD:

Whole genome duplication

References

  • Adam-Blondon AF, Bernole A, Faes G, Lamoureux D, Pateyron S, Grando MS, Caboche M, Velasco R, Chalhoub B (2005) Construction and characterization of BAC libraries from major grapevine cultivars. Theor Appl Genet 110:1363–1371

    Article  PubMed  CAS  Google Scholar 

  • Adams KL, Wendel JF (2005) Polyploidy and genome evolution in plants. Curr Opin Plant Biol 8:135–141

    Article  PubMed  CAS  Google Scholar 

  • Adams KL, Cronn R, Percifield R, Wendel JF (2003) Genes duplicated by polyploidy show unequal contributions to the transcriptome and organ-specific reciprocal silencing. Proc Natl Acad Sci USA 100:4649–4654

    Article  PubMed  CAS  Google Scholar 

  • Blanc G, Wolfe KH (2004) Functional divergence of duplicated genes formed by polyploidy during Arabidopsis evolution. Plant Cell 16:1679–1691

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Bosch S, Grof CPL, Botha FC (2004) Expression of neutral invertase in sugarcane. Plant Sci 166:1125–1133

    Article  CAS  Google Scholar 

  • Casneuf T, De Bodt S, Raes J, Maere S, Van de Peer Y (2006) Nonrandom divergence of gene expression following gene and genome duplications in the flowering plant Arabidopsis thaliana. Genome Biol 7:13

    Article  CAS  Google Scholar 

  • Castellarin SD, Di Gaspero G, Marconi R, Nonis A, Peterlunger E, Paillard S, Adam-Blondon A-F, Testolin R (2006) Colour variation in red grapevines (Vitis vinifera L.): genomic organisation, expression of flavonoid 3′-hydroxylase, flavonoid 3′, 5′-hydroxylase genes and related metabolite profiling of red cyanidin-/blue delphinidin-based anthocyanins in berry skin. BMC Genomics 7:12

    Article  PubMed  CAS  Google Scholar 

  • Davies C, Robinson SP (1996) Sugar accumulation in grape berries. Cloning of two putative vacuolar invertase cDNAs and their expression in grapevine tissues. Plant Physiol 111:275–283

    Article  PubMed  CAS  Google Scholar 

  • Deluc LG, Grimplet J, Wheatley MD, Tillett RL, Quilici DR, Osborne C, Schooley DA, Schlauch KA, Cushman JC, Cramer GR (2007) Transcriptomic and metabolite analyses of Cabernet Sauvignon grape berry development. BMC Genomics 8:429

    Article  PubMed  Google Scholar 

  • Di Gaspero G, Cipriani G, Adam-Blondon AF, Testolin R (2007) Linkage maps of grapevine displaying the chromosomal locations of 420 microsatellite markers and 82 markers for R-gene candidates. Theor Appl Genet 114:1249–1263

    Article  PubMed  CAS  Google Scholar 

  • Emanuelsson O, Nielsen H, von Heijne G (1999) ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. Protein Sci 8:978–984

    Article  PubMed  CAS  Google Scholar 

  • Emanuelsson O, Nielsen H, Brunak S, von Heijne G (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 300:1005–1016

    Article  PubMed  CAS  Google Scholar 

  • Ewing B, Hillier L, Wendl M, Green P (1998) Basecalling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res 8:175–185

    PubMed  CAS  Google Scholar 

  • Francki MG, Walker E, Forster JW, Spangenberg G, Appels R (2006) Fructosyltransferase and invertase genes evolved by gene duplication and rearrangements: rice, perennial ryegrass, and wheat gene families. Genome 49:1081–1091

    Article  PubMed  CAS  Google Scholar 

  • Gallagher JA, Pollock CJ (1998) Isolation and characterization of a cDNA clone from Lolium temulentum L. encoding for a sucrose hydrolytic enzyme which shows alkaline/neutral invertase activity. J Exp Bot 49:789–795

    Article  CAS  Google Scholar 

  • Gibson S (2005) Control of plant development and gene expression by sugar signalling. Curr Opin Plant Biol 8:93–102

    Article  PubMed  CAS  Google Scholar 

  • Haberer G, Hindemitt T, Meyers BC, Mayer KF (2004) Transcriptional similarities, dissimilarities, and conservation of cis-elements in duplicated genes of Arabidopsis. Plant Physiol 136:3009–3022

    Article  PubMed  CAS  Google Scholar 

  • Horton P, Park K-J, Obayashi T, Nakai K (2006) Protein subcellular localization prediction with WoLF PSORT. In: Proceedings of the 4th annual Asia Pacific bioinformatics conference APBC06, Taipei, Taiwan, pp 39–48

  • Iandolino AB, Goes da Silva F, Lim H, Choi H, Williams LE, Cook DR (2004) High-quality RNA, cDNA, and derived EST libraries from grapevine (Vitis vinifera L.). Plant Mol Biol Rep 22:269–278

    Article  CAS  Google Scholar 

  • Jaillon O, Aury JM, Noel B, Policriti A, Clepet C et al (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463–467

    Article  PubMed  CAS  Google Scholar 

  • Ji XM, Van den Ende W, Van Laere A, Cheng SH, Bennett J (2005) Structure, evolution, and expression of the two invertase gene families of rice. J Mol Evol 60:615–634

    Article  PubMed  CAS  Google Scholar 

  • Koch K (2004) Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Curr Opin Plant Biol 7:235–246

    Article  PubMed  CAS  Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163

    Article  PubMed  CAS  Google Scholar 

  • Leon P, Sheen J (2003) Sugar and hormone connections. Trends Plant Sci 8:110–116

    Article  PubMed  CAS  Google Scholar 

  • Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouzé P, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327

    Article  PubMed  CAS  Google Scholar 

  • Lou Y, Gou JY, Xue HW (2007) PIP5K9, an Arabidopsis phosphatidylinositol monophosphate kinase, interacts with a cytosolic invertase to negatively regulate sugar-mediated root growth. Plant Cell 19:163–181

    Article  PubMed  CAS  Google Scholar 

  • Ming R, Hou S, Feng Y, Yu Q, Dionne-Laporte A et al (2008) The draft genome of the transgenic tropical fruit tree papaya (Carica papaya Linnaeus). Nature 452:991–996

    Article  PubMed  CAS  Google Scholar 

  • Moroldo M, Paillard S, Marconi R, Legeai F, Canaguier A, Cruaud C, De Berardinis V, Guichard C, Brunaud V, Le Clainche I, Scalabrin S, Testolin R, Di Gaspero G, Morgante M, Adam-Blondon AF (2008) A physical map of the heterozygous grapevine ‘Cabernet Sauvignon’ allows map** candidate genes for disease resistance. BMC Plant Biol 8:66

    Article  PubMed  CAS  Google Scholar 

  • Murayama S, Handa H (2007) Genes for alkaline/neutral invertase in rice: alkaline/neutral invertases are located in plant mitochondria and also in plastids. Planta 225:1193–1203

    Article  PubMed  CAS  Google Scholar 

  • Nonis A, Ruperti B, Falchi R, Casatta E, Thamashebi SE, Vizzotto G (2007) Differential expression and regulation of a neutral invertase encoding gene from peach (Prunus persica): evidence for a role in fruit development. Physiol Plant 129:436–446

    Article  CAS  Google Scholar 

  • Olmo HP (1976) Grapes. In: Simmonds NW (ed) Evolution of crop plants. Longman, London, pp 249–298

    Google Scholar 

  • Qi X, Wu Z, Li J, Mo X, Wu S, Chu J, Wu P (2007) AtCYT-INV1, a neutral invertase, is involved in osmotic stress-induced inhibition on lateral root growth in Arabidopsis. Plant Mol Biol 64:575–587

    Article  PubMed  CAS  Google Scholar 

  • Ranwala AP, Iwanami S-S, Masuda H (1991) Acid and neutral invertases in the mesocarp of develo** muskmelon (Cucumis melo L. cv Prince) fruit. Plant Physiol 96:881–886

    PubMed  CAS  Google Scholar 

  • Roitsch T, Gonzalez M-C (2004) Function and regulation of plant invertases: sweet sensations. Trends Plant Sci 9:606–613

    Article  PubMed  CAS  Google Scholar 

  • Rossouw D, Bosch S, Kossmann J, Botha FC, Groenewald J-H (2007) Downregulation of neutral invertase activity in sugarcane cell suspension cultures leads to a reduction in respiration and growth and an increase in sucrose accumulation. Funct Plant Biol 34:490–498

    Article  CAS  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 

  • Sheen J, Zhou L, Jang J-C (1999) Sugars as signalling molecules. Curr Opin Plant Biol 2:410–418

    Article  PubMed  CAS  Google Scholar 

  • Small I, Peeters N, Legeai F, Lurin C (2004) Predotar: a tool for rapidly screening proteomes for N-terminal targeting sequences. Proteomics 4:1581–1590

    Article  PubMed  CAS  Google Scholar 

  • Smeekens S (2000) Sugar-induced signal transduction in plants. Annu Rev Plant Physiol Plant Mol Biol 51:49–81

    Article  PubMed  CAS  Google Scholar 

  • Sturm A, Tang G-Q (1999) The sucrose-cleaving enzymes of planta are crucial for development, growth and carbon partitioning. Trends Plant Sci 4:401–407

    Article  PubMed  Google Scholar 

  • Sturm A, Hess D, Lee HS, Lienhard S (1999) Neutral invertase is a novel type of sucrose-cleaving enzyme. Physiol Plant 107:159–165

    Article  CAS  Google Scholar 

  • Subbaiah CC, Palaniappan A, Duncan K, Rhoads DM, Huber SC, Sachs MM (2006) Mitochondrial localization and putative signaling function of sucrose synthase in maize. J Biol Chem 281:15625–15635

    Article  PubMed  CAS  Google Scholar 

  • Symons GM, Davies C, Shavrukov Y, Dry IB, Reid JB, Thomas MR (2006) Grapes on steroids. Brassinosteroids are involved in grape berry ripening. Plant Physiol 140:150–158

    CAS  Google Scholar 

  • Terrier N, Glissant D, Grimplet J, Barrieu F, Abbal P, Couture C, Ageorges A, Atanassova R, Léon C, Renaudin JP, Dédaldéchamp F, Romieu C, Delrot S, Hamdi S (2005) Isogene specific oligo arrays reveal multifaceted changes in gene expression during grape berry (Vitis vinifera L.) development. Planta 222:832–847

    Article  PubMed  CAS  Google Scholar 

  • Initiative TheArabidopsisGenome (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815

    Article  Google Scholar 

  • Thomas TR, Matthews MA, Shackel KA (2006) Direct in situ measurement of cell turgor in grape (Vitis vinifera L.) berries during development and in response to plant water deficits. Plant Cell Environ 29:993–1001

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Tymowska-Lalanne Z, Kreis M (1998) The plant invertases: physiology, biochemistry and molecular biology. Adv Bot Res 28:72–117

    Google Scholar 

  • Vargas W, Cumino A, Salerno GL (2003) Cyanobacterial alkaline/neutral invertases. Origin of sucrose hydrolysis in the plant cytosol? Planta 216:951–960

    PubMed  CAS  Google Scholar 

  • Vargas WA, Pontis HG, Salerno GL (2008) New insights on sucrose metabolism: evidence for an active A/N-Inv in chloroplasts uncovers a novel component of the intracellular carbon trafficking. Planta 227:795–807

    Article  PubMed  CAS  Google Scholar 

  • Velasco R, Zharkikh A, Troggio M, Cartwright DA, Cestaro A et al (2007) A high quality draft consensus sequence of the genome of a heterozygous grapevine variety. PLoS ONE 2(12):e1326

    Article  PubMed  CAS  Google Scholar 

  • Vizzotto G, Pinton R, Varanini Z, Costa G (1996) Sucrose accumulation in develo** peach fruit. Physiol Plant 96:225–230

    Article  CAS  Google Scholar 

  • Wada H, Shackel KA, Matthews MA (2008) Fruit ripening in Vitis vinifera: apoplastic solute accumulation accounts for pre-véraison turgor loss in berries. Planta 227:1351–1361

    Article  PubMed  CAS  Google Scholar 

  • Winter H, Huber SC (2000) Regulation of sucrose metabolism in higher plants: localization and regulation of activity of key enzymes. Crit Rev Plant Sci 19:31–67

    Article  CAS  Google Scholar 

  • Zhang XY, Wang XL, Wang XF, **a GH, Pan QH, Fan RC, Wu FQ, Yu XC, Zhang DP (2006) A shift of phloem unloading from symplasmic to apoplasmic pathway is involved in developmental onset of ripening in grape berry. Plant Physiol 142:220–232

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank S.D. Castellarin (University of Udine) for sampling ‘Merlot’ berries, J.-M. Aury (Genoscope, Paris) for help in the identification of homoeologous regions, R. Marconi (University of Udine) and I. LeClainche (INRA) for help in pooling and screening of BAC clones, A. Fiori (University of Udine) for SSCP analysis, F. Cattonaro and I. Jurman (Istituto di Genomica Applicata, Udine) for sequencing NI alleles in ‘Cabernet Sauvignon’, E. De Paoli (University of Udine) for advice in the use of Phred and Phrap software and C. Coleman for proofreading the manuscript.

Author information

Author notes

  1. Benedetto Ruperti

    Present address: Dipartimento di Agronomia Ambientale e Produzioni Vegetali, University of Padua, viale dell’Università 16, Legnaro, Padua, Italy

Authors and Affiliations

  1. Dipartimento di Scienze Agrarie e Ambientali, University of Udine, via delle Scienze 208, 33100, Udine, Italy

    Alberto Nonis, Benedetto Ruperti, Alessandro Pierasco, Gabriele Di Gaspero & Giannina Vizzotto

  2. UMR de Génomique Végétale, INRA-CNRS-UEVE, 2, Rue Gaston Crémieux, CP5708, 91057, Evry Cedex, France

    Aurelie Canaguier & Anne-Françoise Adam-Blondon

  3. Istituto di Genomica Applicata, Parco Scientifico e Tecnologico Luigi Danieli, via Jacopo Linussio 51, Udine, Italy

    Gabriele Di Gaspero

Authors
  1. Alberto Nonis
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Benedetto Ruperti
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alessandro Pierasco
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Aurelie Canaguier
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Anne-Françoise Adam-Blondon
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Gabriele Di Gaspero
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Giannina Vizzotto
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gabriele Di Gaspero.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Nonis, A., Ruperti, B., Pierasco, A. et al. Neutral invertases in grapevine and comparative analysis with Arabidopsis, poplar and rice. Planta 229, 129–142 (2008). https://doi.org/10.1007/s00425-008-0815-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-008-0815-0

Keywords

Search

Navigation