Skip to main content
SpringerLink
Log in

Identification of ISSR markers linked to flowering traits in a representative sample of Eucalyptus cladocalyx

  • ORIGINAL PAPER
  • Published:
Journal of Forestry Research Aims and scope Submit manuscript

Abstract

Early flowering and flower abundance have long been considered desirable traits in eucalypt breeding programs. In particular, flowers of Eucalyptus cladocalyx provide a nectar source for the production of honey in arid ecosystems. To identify inter-simple sequence repeat (ISSR) markers that are associated with early flowering and flower abundance in the southern Atacama Desert, we used a sample of 47 trees, representing five Australian provenances of E. cladocalyx. A unified mixed linear model (which considered the effect of genetic structure and the kinship relationship among trees) revealed that three loci were significantly associated with early flowering, which accounted for 10–16 % of the phenotypic variation, while two loci accounted for 11–13 % in flowering intensity. Locus ISO1–500 bp was associated with both flowering traits. This result is consistent with our previous findings indicating that marker-assisted selection on early flowering should have significant and positive impact on flowering intensity. The application of marker-assisted selection to identify trees that flower early and intensively may increase honey production, a resource that generates additional income for the local farmers of the southern Atacama Desert.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Albani MC, Battey NH, Wilkinson MJ (2004) The development of ISSR-derived SCAR markers around the seasonal flowering locus (SFL) in Fragaria vesca. Theor Appl Genet 109:571–579

    Article  CAS  PubMed  Google Scholar 

  • Balasaravanan T, Chezhian P, Kamalakannan R, Yasodha R, Varguese M, Gurumurthi K, Ghosh M (2006) Identification of species-diagnostic ISSR markers for six eucalyptus species. Silvae Genet 55:119–122

    Google Scholar 

  • Ballesta P, Mora F, Ruiz E, Contreras-Soto R (2015) Marker-trait associations for survival, growth, and flowering components in Eucalyptus cladocalyx under arid conditions. Biol Plantarum 59(2):389–392

    Article  CAS  Google Scholar 

  • Bernardo R, Romero-Severson J, Ziegle J, Hauser J, Joe L, Hookstra G, Doerge RW (2000) Parental contribution and coefficient of coancestry among maize inbreds: pedigree, RFLP, and SSR data. Theor Appl Genet 100(3–4):552–556

    CAS  Google Scholar 

  • Bornet B, Branchard M (2001) Non-anchored inter-simple sequence repeat (ISSR) markers: reproducible and specific tools for genome fingerprinting. Plant Mol Biol Rep 19:209–215

    Article  CAS  Google Scholar 

  • Brawner JT, Dillon SK, Lee DJ, Meder AR, Dieters MJ, Southerton SG (2012) The use of genetic correlations to evaluate associations between SNP markers and quantitative traits. Tree Genet Genomes 8:1423–1435

    Article  Google Scholar 

  • Brondani RPV, Williams ER, Brondani C, Grattapaglia D (2006) A microsatellite-based consensus linkage map for species of Eucalyptus and a novel set of 230 microsatellite markers for the genus. BMC Plant Biol 6:20

    Article  PubMed Central  PubMed  Google Scholar 

  • Bush D, Thumma B (2013) Characterizing a Eucalyptus cladocalyx breeding population using SNP markers. Tree Genet Genomes 9:741–752

    Article  Google Scholar 

  • Bush D, McCarthy K, Meder R (2011) Genetic variation of natural durability traits in Eucalyptus cladocalyx (sugar gum). Ann For Sci 68:1057–1066

    Article  Google Scholar 

  • Cané-Retamales C, Mora F, Vargas-Reeve F, Perret S, Contreras-Soto R (2011) Bayesian threshold analysis of breeding values, genetic correlation and heritability of flowering intensity in Eucalyptus cladocalyx under arid conditions. Euphytica 178:177–183

    Article  Google Scholar 

  • Cappa EP, El-Kassaby YA, Garcia MN, Acuña C, Borralho NM, Grattapaglia D, Marcucci Poltri SN (2013) Impacts of population structure and analytical models in genome-wide association studies of complex traits in forest trees: a case study in Eucalyptus globulus. PLoS One 8(11):e81267. doi:10.1371/journal.pone.0081267

    Article  PubMed Central  PubMed  Google Scholar 

  • Cekic C, Battey NH, Wilkinson MJ (2001) The potential of ISSR-PCR primer-pair combinations for genetic linkage analysis using the seasonal flowering locus in Fragaria as a model. Theor Appl Genet 103:540–546

    Article  CAS  Google Scholar 

  • Chambers PGS, Potts BM, Tilyard PA (1997) The genetic control of flowering precocity in Eucalyptus globulus ssp. globulus. Silvae Genet 46:207–214

    Google Scholar 

  • Chezhian P, Yasodha R, Ghosh M (2010) Genetic diversity analysis in a seed orchard of Eucalyptus tereticornis. New For 40:85–99

    Article  Google Scholar 

  • Contreras-Soto R, Mora F, Perret S, Vargas-Reeve F, Cané-Retamales C (2011) Predicción bayesiana del comportamiento poblacional de Eucalyptus cladocalyx para características binarias de componentes de florecimiento y supervivencia en las zonas áridas de chile. Interciencia 36:644–649

    Google Scholar 

  • Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Photoch Bull 19:11–15

    Google Scholar 

  • El-Lithy ME, Bentsink L, Hanhart CJ, Ruys GJ, Rovito D, Broekhof JLM, van der Poel HJA, van Eijk MJT, Vreugdenhil D, Koornneef M (2006) New arabidopsis recombinant inbred line populations genotyped using SNP wave and their use for mapping flowering-time quantitative trait loci. Genetics 72:1867–1876

    Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    Article  CAS  PubMed  Google Scholar 

  • Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Res 10:564–567

    Article  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multilocus genotype data: dominant markers and null allele. Mol Ecol Notes 7:574–578

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Farro AP, Bortoloto TM, Oda S, Mello E, Marino CL (2013) Identification of molecular marker linked to early flowering in Eucalyptus grandis. Rev Ins Fla 24:149–157

    Google Scholar 

  • Gaut BS, Long AD (2003) The lowdown on linkage disequilibrium. Plan Cell 15:1502–1506

    Article  CAS  Google Scholar 

  • Grillo MA, Li C, Hammond M, Wang L, Schemske DW (2013) Genetic architecture of flowering time differentiation between locally adapted populations of Arabidopsis thaliana. New Phytol 197:1321–1331

    Article  CAS  PubMed  Google Scholar 

  • Hendry AP, Day T (2005) Population structure attributable to reproductive time: isolation by time and adaptation by time. Mol Ecol 14:901–916

    Article  CAS  PubMed  Google Scholar 

  • Izawa T, Takahashi Y, Yano M (2003) Comparative biology comes into bloom: genomic and genetic comparison of flowering pathways in rice and Arabidopsis. Curr Opin Plant Biol 6:113–120

    Article  CAS  PubMed  Google Scholar 

  • Jaya ESKD, Clemens J, Song J, Zhang H, Jameson PE (2010) Quantitative expression analysis of meristem identity genes in Eucalyptus occidentalis: AP1 is an expression marker for flowering. Tree Physiol 30:304–312

    Article  CAS  PubMed  Google Scholar 

  • Keatley MR, Hudson IL (2007) A comparison of long-term flowering patterns of box-Ironbark species in Havelock and Rushworth forests. J Environ Modell Assess 12:279–292

    Article  Google Scholar 

  • Külheim C, Yeoh SH, Wallis RR, Laffan S, Moran GF, Foley WJ (2011) The molecular basis of quantitative variation in foliar secondary metabolites in Eucalyptus globulus. New Phytol 191:1041–1053

    Article  PubMed  Google Scholar 

  • Lepoittevin C, Harvengt L, Plomion C, Garnier-Géré P (2012) Association mapping for growth, straightness and wood chemistry traits in the Pinus pinaster Aquitaine breeding population. Tree Genet Genomes 8:113–126

    Article  Google Scholar 

  • McDonald MW, Rawlings M, Butcher PA, Bell JC (2003) Regional divergence and inbreeding in Eucalyptus cladocalyx (Myrtaceae). Aust J Bot 51:393–403

    Article  Google Scholar 

  • McKay JK, Richards JH, Mitchell-Olds T (2003) Genetics of drought adaptation in Arabidopsis thaliana. I. Pleiotropy contributes to genetic correlations among ecological traits. Mol Ecol 12:1137–1151

    Article  CAS  PubMed  Google Scholar 

  • Méndez-Vigo B, Martínez-Zapater JM, Alonso-Blanco C (2013) The flowering repressor SVP underlies a novel Arabidopsis thaliana QTL interacting with the genetic background. PLoS Genet 9:1. doi:10.1371/journal.pgen.1003289

    Article  Google Scholar 

  • Missiaggia AA, Piacezzi AL, Grattapaglia D (2005) Genetic mapping of Eef1, a major effect QTL for early flowering in Eucalyptus grandis. Tree Genet Genomes 1:79–84

    Article  Google Scholar 

  • Montenegro G, Pizarro R, Avila G, Castro R, Ríos C, Muñoz O, Bas F, Gómez M (2003) Origen botánico y propiedades químicas de las mieles de la región mediterránea árida de Chile. Cien Inves Agraria 30:161–174

    Google Scholar 

  • Mora F, Castillo D, Lado B, Matus I, Poland J, Belzile F, Von Zitzewitz J, Del Pozo A (2015) Genome-wide association mapping of agronomic traits and carbon isotope discrimination in a worldwide germplasm collection of spring wheat using SNP markers. Mol Breed 35:69

    Article  Google Scholar 

  • Mora F, Serra N (2014) Bayesian estimation of genetic parameters for growth, stem straightness, and survival in Eucalyptus globulus on an Andean Foothill site. Tree Genet Genomes 10:711–719

    Article  Google Scholar 

  • Mora F, Gleadow R, Perret S, Scapim CA (2009) Genetic variation for early flowering, survival and growth in sugar gum (Eucalyptus cladocalyx F. Muell) in southern Atacama Desert. Euphytica 169:335–344

    Article  Google Scholar 

  • Munguía-Rosas MA, Ollerton J, Parra-Tabla V, De-Nova JA (2011) Meta-analysis of phenotypic selection on flowering phenology suggests that early-flowering plants are favoured. Ecol Lett 14:511–521

    Article  PubMed  Google Scholar 

  • Neale DB, Savolainen O (2004) Association genetics of complex traits in conifers. Trends Plant Sci 9:325–330

    Article  CAS  PubMed  Google Scholar 

  • Neath AA, Cavanaugh JE (2012) The Bayesian information criterion: background, derivation, and applications. Comp Stat 4:199–203

    Google Scholar 

  • Nordborg M (2000) Linkage disequilibrium, gene trees and selfing: an ancestral recombination graph with partial self-fertilization. Genetics 154:923–929

    PubMed Central  CAS  PubMed  Google Scholar 

  • Okun DO, Kenya EU, Oballa PO, Odee DW, Muluvi GM (2008) Analysis of genetic diversity in Eucalyptus grandis (Hill ex Maiden) seed sources using inter simple sequence repeats (ISSR) molecular markers. Afr J Biotechnol 7:2119–2123

    CAS  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    PubMed Central  CAS  PubMed  Google Scholar 

  • Reynolds J, Weir BS, Cockerham CC (1983) Estimation for the coancestry coefficient: basis for a short-term genetic distance. Genetics 105:767–779

    PubMed Central  CAS  PubMed  Google Scholar 

  • Rogiers SY, Smith JP, Holzapfel BP, Nielsen GL (2014) Shifts in biomass and nitrogen allocation of tree seedlings in response to root-zone temperature. Aust J Bot 62:205–216

    Article  CAS  Google Scholar 

  • SAS (2007) Version 9.1.3; SAS Institute Inc.: Cary

  • Stich B, Melchinger AE (2009) Comparison of mixed-model approaches for association mapping in rapeseed, potato, sugar beet, maize, and arabidopsis. BMC Genom 10:1–14

    Article  Google Scholar 

  • Thamarus K, Groom K, Murrell J, Byrne M, Moran G (2002) A genetic linkage map for Eucalyptus globulus with candidate loci for wood, fiber, and floral traits. Theor Appl Genet 104:379–387

    Article  CAS  PubMed  Google Scholar 

  • Thornsberry JM, Goodman MM, Doebley J, Kresovich S, Nielsen S, Buckler ES (2001) Dwarf8 polymorphisms associate with variation in flowering time. Nat Genet 28:286–289

    Article  CAS  PubMed  Google Scholar 

  • Thumma BR, Matheson BA, Zhang D, Meeske C, Meder R, Downes GM, Southerton SG (2009) Identification of a cis-acting regulatory polymorphism in a eucalypt COBRA-like gene affecting cellulose content. Genetics 183:1153–1164

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Van-Tassell CP, Van-Vleck LD (1996) Multiple-trait Gibbs sampler for animal models: flexible programs for Bayesian and likelihood-based (co)variance component inference. J Anim Sci 74:2586–2597

    CAS  PubMed  Google Scholar 

  • Vargas-Reeve F, Mora F, Perret S, Scapim CA (2013) Heritability of stem straightness and genetic correlations in Eucalyptus cladocalyx in the semi-arid region of Chile. Crop Breed Appl Biotechnol 13:107–112

    Article  Google Scholar 

  • Woodrow IE, Slocum D, Gleadow RM (2002) Influence of water stress on cyanogenic capacity in Eucalyptus cladocalyx. Aust J Plant Physiol 29:103–110

    CAS  Google Scholar 

  • Yu J, Pressoir G, Briggs WH, Bi IV, Yamasaki M, Doebley JF, McMullen MD, Gaut BS, Nielsen DM, Holland JB, Kresovich S, Buckler ES (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet 38:203–208

    Article  CAS  PubMed  Google Scholar 

  • Zapata-Valenzuela J, Isik F, Maltecca C, Wegrzyn J, Neale D, McKeand S, Whetten R (2012) SNP markers trace familial linkages in a cloned population of Pinus taeda—prospects for genomic selection. Tree Genet Genomes 8:1307–1318

    Article  Google Scholar 

  • Zhao K, Aranzana MJ, Kim S, Lister C, Shindo C, Tang C, Toomajian C, Zheng H, Dean C, Marjoram Z, Nordborg M (2007) An Arabidopsis example of association mapping in structured samples. PLoS Genet 3:e4. doi:10.1371/journal.pgen.0030004

    Article  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

This study was supported by the Chilean National Science and Technology Research Fund (FONDECYT); projects 11090129 and 1130306. We thank Mr. Augusto Gomes, the farmer who allowed the trial to take place on their property.

Author information

Authors and Affiliations

  1. Department of Agronomy, State University of Maringá, Av. Colombo 5790, Maringá, PR, 87020-900, Brazil

    Rodrigo Contreras-Soto

  2. Department of Botany, University of Concepción, Casilla 160-C, Concepción, Chile

    Paulina Ballesta & Eduardo Ruiz

  3. Institute of Biological Sciences, University of Talca, 2 Norte 685, Talca, Chile

    Freddy Mora

Authors
  1. Rodrigo Contreras-Soto
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Paulina Ballesta
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Eduardo Ruiz
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Freddy Mora
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Freddy Mora.

Additional information

Project funding: The study was supported by the Chilean National Science and Technology Research Fund (FONDECYT); projects 11090129 and 1130306.

The online version is available at http://www.springerlink.com

Corresponding editor: Hu Yanbo

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Contreras-Soto, R., Ballesta, P., Ruiz, E. et al. Identification of ISSR markers linked to flowering traits in a representative sample of Eucalyptus cladocalyx . J. For. Res. 27, 239–245 (2016). https://doi.org/10.1007/s11676-015-0149-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11676-015-0149-2

Keywords

Search

Navigation