Skip to main content
Log in

Identification of a gene involved in the juvenile-to-adult transition (JAT) in cultivated olive trees

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

Abstract

The juvenile-to-adult transition is a complex and poorly understood process in plant development required to reach reproductive competence. For woody plants, knowledge of this transition is even scantier and no genes have been definitively identified as involved in this transition. To search for genes involved in the juvenile-to-adult transition in olive, we constructed juvenile and adult subtractive cDNA gene libraries and identified genes that were differentially expressed in the juvenile and adult phases. In the analysis of theses libraries, we found 13 differentially expressed genes. One of these genes designated as juvenile to adult transition (JAT) was of special interest because it was highly expressed at the mRNA level in the early developmental phases but repressed in the adult phase. The analysis of mutant trees altered in the juvenile-to-adult transition, as well as a segregating progeny of 31 trees from a “Picual” x “Jabaluna” cross, support the contention that its activity might be required for a non-delayed transition. The study of an Arabidopsis thaliana JAT mutant strain confirmed this hypothesis as it showed a delayed flowering phenotype. JAT is expressed in different parts of the plant, showing an unexpectedly high level of mRNA in the roots. However, the JAT expression level is not determined by the distance to the roots, but rather depends on the developmental stage of the branch meristems. JAT is a widely represented gene in plants that appears to be involved in the control of the juvenile-to-adult transition in olive.

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
Fig. 6

Similar content being viewed by others

References

  • Alarcon de la Lastra C, Barranco MD, Motilva V, Herrerias JM (2001) Mediterranean diet and health: biological importance of olive oil. Current Pharmaceutical Design 7:933–950

    Article  CAS  PubMed  Google Scholar 

  • Altschul SF, Gish W, Miller W, Meyers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    CAS  PubMed  Google Scholar 

  • Altschul SF, Madden TL, Schaffer AA et al (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl Acids Res 25:3389–3402

    Article  CAS  PubMed  Google Scholar 

  • Apweiler R, Attwood TK, Bairoch A et al (2001) The InterPro database, an integrated documentation resource for protein families, domains and functional sites. Nucl Acids Res 29:37–40

    Article  CAS  PubMed  Google Scholar 

  • Asai K, Satoh N, Sasaki H, Satoh H, Nagato Y (2002) A rice heterochronic mutant, mori1, is defective in the juvenile-adult phase change. Development 129:265–273

    CAS  PubMed  Google Scholar 

  • Battey NH, Tooke F (2002) Molecular control and variation in the floral transition. Curr Opin Plant Biol 5:62–68

    Article  CAS  PubMed  Google Scholar 

  • Baurens FC, Nicolleau J, Legavre T, Verdeil JL, Monteuuis O (2004) Genomic DNA methylation of juvenile and mature Acacia mangium micropropagated in vitro with reference to leaf morphology as a phase change marker. Tree Physiol 24:401–407

    CAS  PubMed  Google Scholar 

  • Belaj A, Munoz-Diez C, Baldoni L, Porceddu A, Barranco D, Satovic Z (2007) Genetic diversity and population structure of wild olives from North-Western Mediterranean assessed by SSR markers. Annals of Botany 100:449–458

    Article  CAS  PubMed  Google Scholar 

  • Bellini E (1992) Behaviour of some genetic characters in olive seedlings obtained by cross-breeding. Acta Hort 317:197–208

    Google Scholar 

  • Berardini TZ, Bollman K, Sun H, Poethig RS (2001) Regulation of vegetative phase change in Arabidopsis thaliana by cyclophilin 40. Science 291:2405–2407

    Article  CAS  PubMed  Google Scholar 

  • Blazquez MA (1997) Illuminating flowers: CONSTANS induces LEAFY expression. Bioessays 19:277–279

    Article  CAS  PubMed  Google Scholar 

  • Bollman KM, Aukerman MJ, Park MY, Hunter C, Berardini TZ, Poethig RS (2003) HASTY, the Arabidopsis ortholog of exportin 5/MSN5, regulates phase change and morphogenesis. Development 130:1493–1504

    Article  CAS  PubMed  Google Scholar 

  • Carlsbecker A, Tandre K, Johanson U, Englund M, Engstrom P (2004) The MADS-box gene DAL1 is a potential mediator of the juvenile-to-adult transition in Norway spruce (Picea abies). Plant J 40:546–557

    Article  CAS  PubMed  Google Scholar 

  • Corpet F (1988) Multiple sequence alignment with hierarchical clustering. Nucl Acids Res 16:10881–10890

    Article  CAS  PubMed  Google Scholar 

  • De la Rosa R, Kiran AI, Barranco D, Leon L (2006) Seedling vigour as a preselection criterion for short juvenile period in olive breeding. Aust J Agr Res 57:477–481

    Article  Google Scholar 

  • Fraga MF, Canal MJ, Rodriguez R (2002) Phase change related epigenetic and physiological changes in Pinus radiata D. Don Planta 215:672–678

    Article  CAS  Google Scholar 

  • Janick J, Moore JN (1996) Fruit breeding. Wiley, Inc

    Google Scholar 

  • Jones CS (1999) An essay on juvenility, phase change, and heteroblasty in seed plants. Int J Plant Sci 160:S105–S111

    Article  PubMed  Google Scholar 

  • Lavee S, Avidan N, Haskal A, Ogrodovich A (1996) Juvenility period reduction in olive seedlings—a tool for enhancement of breeding. Olivae 60:33–41

    Google Scholar 

  • Letunic I, Copley RR, Pils B, Pinkert S, Schultz J, Bork P (2006) SMART 5: domains in the context of genomes and networks. Nucl Acids Res 34:D257–D260

    Article  CAS  PubMed  Google Scholar 

  • Martin-Trillo M, Martinez-Zapater JM (2002) Growing up fast: manipulating the generation time of trees. Curr Opin Biotechnol 13:151–155

    Article  CAS  PubMed  Google Scholar 

  • Mitaku S, Hirokawa T, Tsuji T (2002) Amphiphilicity index of polar amino acids as an aid in the characterization of amino acid preference at membrane-water interfaces. Bioinformatics 18:608–616

    Article  CAS  PubMed  Google Scholar 

  • Moose SP, Sisco PH (1996) Glossy15, an APETALA2-like gene from maize that regulates leaf epidermal cell identity. Genes Dev 10:3018–3027

    Article  CAS  PubMed  Google Scholar 

  • Moreno-Alías I, Gracia A, León L, De la Rosa R, Rapoport HF. Morphological and histological characteristics related with phase change (juvenile/adult) in olive leaves and its determination by near infrared reflectance spectroscopy. Acta Hort (in press).

  • Nielsen H, Engelbrecht J, Brunak S, Von Heijne G (1997) Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Engineering 10:1–6

    Article  CAS  PubMed  Google Scholar 

  • Nilsson O, Weigel D (1997) Modulating the timing of flowering. Curr Opin Biotechnol 8:195–199

    Article  CAS  PubMed  Google Scholar 

  • Parcy F, Nilsson O, Busch MA, Lee I, Weigel D (1998) A genetic framework for floral patterning. Nature 395:561–566

    Article  CAS  PubMed  Google Scholar 

  • Pena L, Martin-Trillo M, Juarez J, Pina JA, Navarro L, Martinez-Zapater JM (2001) Constitutive expression of Arabidopsis LEAFY or APETALA1 genes in citrus reduces their generation time. Nat Biotechnol 19:263–267

    Article  CAS  PubMed  Google Scholar 

  • Poethig RS (1990) Phase change and the regulation of shoot morphogenesis in plants. Science 250:23–930

    Article  Google Scholar 

  • Poethig RS (2003) Phase change and the regulation of developmental timing in plants. Science 301:334–336

    Article  CAS  PubMed  Google Scholar 

  • Reynolds, S.M., Kall, L., Riffle, M.E., Bilmes, J.A. and Noble, W.S. (2008) Transmembrane topology and signal peptide prediction using dynamic bayesian networks. PLoS Comput Biol 4:e1000213

    Article  CAS  PubMed  Google Scholar 

  • Rosso MG, Li Y, Strizhov N, Reiss B, Dekker K, Weisshaar B (2003) An Arabidopsis thaliana T-DNA mutagenized population (GABI-Kat) for flanking sequence tag-based reverse genetics. Plant Mol Biol 53:247–259

    Article  CAS  PubMed  Google Scholar 

  • Rottmann WH, Meilan R, Sheppard LA et al (2000) Diverse effects of overexpression of LEAFY and PTLF, a poplar (Populus) homolog of LEAFY/FLORICAULA, in transgenic poplar and Arabidopsis. Plant J 22:235–245

    Article  CAS  PubMed  Google Scholar 

  • Santos-Antunes F, León L, de la Rosa R, Alvarado J, Mohedo A, Trujillo I, Rallo L (2005) The length of the juvenile period in olive as influenced by vigor of the seedlings and the precocity of the parents. HortScience 40:1213–1215

    Google Scholar 

  • Schwarz S, Grande AV, Bujdoso N, Saedler H, Huijser P (2009) The microRNA regulated SBP-box genes SPL9 and SPL15 control shoot maturation in Arabidopsis. Plant Mol Biol 67:183–195

    Article  Google Scholar 

  • Valderrama R, Corpas FJ, Carreras A et al (2006) The dehydrogenase-mediated recycling of NADPH is a key antioxidant system against salt-induced oxidative stress in olive plants. Plant Cell Environ 29:1449–1459

    Article  CAS  PubMed  Google Scholar 

  • Valderrama R, Corpas FJ, Carreras A et al (2007) Nitrosative stress in plants. FEBS Lett 581:453–461

    Article  CAS  PubMed  Google Scholar 

  • Van der Linden CG, Vosman B, Smulders MJ (2002) Cloning and characterization of four apple MADS box genes isolated from vegetative tissue. J Exp Bot 53:1025–1036

    Article  PubMed  Google Scholar 

  • von Aderkas, P. and Bonga, J.M. (2000) Influencing micropropagation and somatic embryogenesis in mature trees by manipulation of phase change, stress and culture environment. Tree Physiol 20:921-928.

    Google Scholar 

  • Weigel D, Nilsson O (1995) A developmental switch sufficient for flower initiation in diverse plants. Nature 377:495–500

    Article  CAS  PubMed  Google Scholar 

  • Wu G, Park MY, Conway SR, Wang JW, Weigel D, Poethig RS (2009) The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell 138:750–759

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

Two-month-old olive plants were kindly provided by Dr Araceli Barceló, from Centro IFAPA “Churriana” Málaga. DNA sequencing was carried out and supported by the Servicios Técnicos de Investigación, Universidad de Jaén. This work was financed by the Universidad de Jaén project OA/3/2004 and Junta de Andalucía support to Groups CVI258 and CVI286.

Ethical standards

The experiments performed in this work comply with the laws of Spain and the European Union.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Francisco Luque.

Additional information

Communicated by A. Dandekar

Electronic supplementary material

Below is the link to the electronic supplementary material.

Figure s1

Fast minimum evolution tree of the closest to O. europaea JAT peptide sequences present in GenBank database: Phylogenetic tree of the closest peptide sequences to the O. europaea JAT peptide. The sequences inside the closed line are probable JAT orthologs (PPT 402 kb)

Figure s2

Multiple alignment of JAT amino acid sequence and the five more similar proteins present in GenBank database: Amino acids identical to the upper sequence are shown as dots. When a position has the same amino acid for at least three of the six sequences, they are shown with black shadows while similar amino acids are indicated by grey shadows (PPT 146 kb)

Figure s3

JAT hydrophobicity and transmembrane-prediction diagrams and putative domains: The bar below the hydrophobicity diagram represents the amino acid position. The putative phosphorylase family domain is shown. TMD means putative transmembrane domains; black box for high probability of the predicted transmembrane domain and light grey for moderate probability. PNP_UDP_1, means phosphorylase superfamily; Pfs, means nucleoside phosphorylase [nucleotide transport and metabolism]; PRK05584, means 5&apos,-methylthioadenosine/S-adenosylhomocysteine nucleosidase; PRK06714, means S-adenosylhomocysteine nucleosidase; DeoD, means Purine-nucleoside phosphorylase [nucleotide transport and metabolism]; PRK07077, hypothetical protein (provisional); PRK06698, means bifunctional 5'-methylthioadenosine/S-adenosylhomocysteine nucleosidase (PPT 69 kb)

Figure s4

JAT signal peptide prediction by Philius algorithm: Result of the prediction Philius algorithm for the JAT deduced protein (PPT 70 kb)

Table s1

XXX (DOC 131 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fernández-Ocaña, A., Carmen García-López, M., Jiménez-Ruiz, J. et al. Identification of a gene involved in the juvenile-to-adult transition (JAT) in cultivated olive trees. Tree Genetics & Genomes 6, 891–903 (2010). https://doi.org/10.1007/s11295-010-0299-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11295-010-0299-5

Keywords

Navigation