Skip to main content
Log in

Sequencing the genomic regions flanking S-linked PvGLO sequences confirms the presence of two GLO loci, one of which lies adjacent to the style-length determinant gene CYP734A50

  • Original Article
  • Published:
Plant Reproduction Aims and scope Submit manuscript

Key message

Primula vulgaris contains two GLOBOSA loci, one located adjacent to the style length determinant gene CYP734A50 which lies within the S -locus.

Abstract

Using a combination of BAC walking and PacBio sequencing, we have sequenced two substantial genomic contigs in and around the S-locus of Primula vulgaris. Using these data, we were able to demonstrate that two alleles of PvGlo P as well as PvGlo T can be present in the genome of a single plant, providing empirical evidence that these two forms of the MADS-box gene GLOBOSA are separate loci and not allelic as previously reported. We propose they should be renamed PvGLO1 and PvGLO2. BAC contigs extending from each GLOBOSA locus were identified and fully sequenced. No homologous genes were found between the contigs other than the GLOBOSA genes themselves, consistent with their identity as separate loci. Exons of the recently identified style-length determinant gene CYP734A50 were identified on one end of the contig containing PvGLO2 and these genes are adjacent in the genome, suggesting that PvGLO2 lies either within or at least very close to the S-locus. Current evidence suggests that both CYP734A50 and GLO2 are specific to the S-morph mating type and are hemizygous rather than heterozygous in the Primula genome. This finding contrasts classical models of the HSI locus, which propose that components of the S-locus are allelic, suggesting that these models may need to be reconsidered.

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
Fig. 7

Similar content being viewed by others

References

  • Aii J, Nagano M, Woo SH, Campbell C (1999) Development of SCAR markers linked to the Sh gene in buckwheat. Fagopyrum 16:19–22

    Google Scholar 

  • Bateson W, Gregory RP (1905) On the inheritance of heterostylism in Primula. Proc R Soc Lond B 76:581–586

    Article  Google Scholar 

  • Burge C, Karlin S (1997) Prediction of complete gene structures in human genomic DNA. J Mol Biol 268:78–94

    Article  CAS  PubMed  Google Scholar 

  • Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL (2009) BLAST+: architecture and applications. BMC Bioinform 15(10):421

    Article  Google Scholar 

  • Darlington CD, Mather K (1949) The elements of genetics. Allen and Unwin Ltd, London

    Google Scholar 

  • Darwin C (1862) On the two forms, or dimorphic conditions, in the species of Primula, and on their remarkable sexual relations. Proc Linn Soc (Botany) 6:105–139

    Google Scholar 

  • Darwin C (1877) The different forms of flowers on plants of the same species. John Murray, London

    Book  Google Scholar 

  • de Folter S, Shchennikova AV, Franken J, Busscher M, Baskar R, Grossniklaus U, Angenent GC, Immink RG (2006) A Bsister MADS-box gene involved in ovule and seed development in petunia and Arabidopsis. Plant J 47(6):934–946

    Article  PubMed  Google Scholar 

  • de Nettancourt D (1977) Incompatibility in angiosperms. Springer, Berlin

    Book  Google Scholar 

  • Dowrick VPJ (1956) Heterosyly and homostyly in Primula obconica. Heredity 10:219–236

    Article  Google Scholar 

  • Ernst A (1955) Self-fertility in monomorphic Primula. Genetica 27:91–146

    Article  Google Scholar 

  • Hildebrand F (1863) De la variation des animeaux et des plantes a l’etat domestique. C Reinwald, Paris

    Google Scholar 

  • Huu CN, Kappel C, Keller B, Sicard A, Takebayashi Y, Breuninger H, Nowak MD, Bäurle I, Himmelbach A, Burkart M, Ebbing-Lohaus T, Sakakibara H, Altschmied L, Conti E, Lenhard M (2016) Presence versus absence of CYP734A50 underlies the style-length dimorphism in primroses. eLife. doi:10.7554/eLife.17956

    PubMed  PubMed Central  Google Scholar 

  • Jones P, Binns D, Chang HY, Fraser M, Li W, McAnulla C, McWilliam H, Maslen J, Mitchell A, Nuka G, Pesseat S, Quinn AF, Sangrador-Vegas A, Scheremetjew M, Yong SY, Lopez R, Hunter S (2014) InterProScan 5: genome-scale protein function classification. Bioinformatics 30(9):1236–1240

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Keller B, de Vos JM, Conti E (2012) Decrease of sexual organ reciprocity between heterostylous primrose species, with possible functional and evolutionary implications. Ann Bot 110:1233–1244

    Article  PubMed  PubMed Central  Google Scholar 

  • Keller B, Thomson JD, Conti E (2014) Heterostyly promotes disassortative pollination and reduces sexual interference in Darwin’s primroses: evidence from experimental studies. Funct Ecol 28:1413–1425

    Article  Google Scholar 

  • Khosravi D, Siu KWM, Shore JS (2006) A proteomics approach to the study of distyly in Turnera species. In: Teixeira d Silva JA (ed) Floriculture, ornamental and plant biotechnology advances and topical issues, vol 1. Global Science Books, London, pp 51–60

    Google Scholar 

  • Korf I (2004) Gene finding in novel genomes. BMC Bioinform 5:59

    Article  Google Scholar 

  • Kurian V, Richards AJ (1996) A new recombinant in the ‘S’ supergene in Primula. Heredity 78:383–390

    Article  Google Scholar 

  • Labonne JDJ, Shore JS (2011) Positional cloning of the s haplotype determining the floral and incompatibility phenotype of the long-styled morph of distylous Turnera subulata. Mol Genet Genomics 285:101–111

    Article  CAS  PubMed  Google Scholar 

  • Labonne JDJ, Goultiaeva A, Shore JS (2009) High-resolution mapping of the S-locus in Turnera leads to the discovery of three genes tightly associated with the S-alleles. Mol Genet Genomics 281:673–685

    Article  CAS  PubMed  Google Scholar 

  • Lee T, Peace C, Jung S, Zheng P, Main D, Cho I (2011) GenSAS: an online integrated genome sequence annotation pipeline. In: 4th International conference on biomedical engineering and informatics (BMEI), Shanghai, 2011, pp. 1967–1973. doi:10.1109/BMEI.2011.6098712

  • Li J, Webster M, Dudas B, Cook H, Manfield I, Davies B, Gilmartin PM (2008) The S locus-linked Primula homeotic mutant sepaloid shows characteristics of a B-function mutant but does not result from mutation in the B-function gene. Plant J 56:1–12

    Article  CAS  PubMed  Google Scholar 

  • Li J, Dudas B, Webster MA, Cook HE, Davies BH, Gilmartin PM (2010) Hose in Hose, an S locus-linked mutant of Primula vulgaris, is caused by an unstable mutation at the Globosa locus. PNAS 107(12):5664–5668

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li J, Webster MA, Smith MC, Gilmartin PM (2011) Floral heteromorphy in Primula vulgaris: progress towards isolation and characterization of the S locus. Ann Bot 108:715–726

    Article  PubMed  PubMed Central  Google Scholar 

  • Li J, Webster MA, Wright J, Cocker JM, Smith MC, Badakshi F, Heslop-Harrison P, Gilmartin PM (2015) Integration of genetic and physical maps of the Primula vulgaris S locus and localization by chromosome in situ hybridization. New Phytol. doi:10.1111/nph.13373

    Google Scholar 

  • Li J, Cocker JM, Wright J, Webster MA, McCullan M, Dyer S, Swarbreck D, Caccamo M, van Oosterhout C, Gilmartin PM (2016) Genetic architecture and evolution of the S locus supergene in Primula vulgaris. Nat Plants 2:1–7. doi:10.1038/NPLANTS.2016.188

    Article  Google Scholar 

  • Manfield IW, Pavlov VK, Li J, Cook HE, Hummel F, Gilmartin PM (2005) Molecular characterization of DNA sequences from the Primula vulgaris S-locus. J Exp Bot 56:1177–1188

    Article  CAS  PubMed  Google Scholar 

  • Matsui K, Nishio T, Tetsuka T (2004) Genes outside the S supergene suppress S functions in buckwheat (Fagopyrum esculentum). Ann Bot 94:805–809

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McCubbin AG (2008) Heteromorphic self-incompatibility in Primula: 21st century tools promise to unravel a classic 19th century model system. In: Franklin-Tong V (ed) Self-incompatibility in flowering plants: evolution, diversity and mechanisms. Springer, Berlin, pp 286–308

    Google Scholar 

  • McCubbin AG, Roalson EH (2005) Construction of bacterial artificial chromosome libraries for use in phylogenetic studies. Methods Enzymol 395:384–400

    Article  CAS  PubMed  Google Scholar 

  • McCubbin AG, Lee C, Hetrick A (2006) Identification of genes showing differential expression between morphs in developing flowers of Primula vulgaris. Sex Plt Reprod 19:63–72

    Article  CAS  Google Scholar 

  • Mizzotti C, Mendes MA, Caporali E, Schnittger A, Kater MM, Battaglia R, Colombo L (2012) The MADS box genes SEEDSTICK and ARABIDOPSIS Bsister play a maternal role in fertilization and seed development. Plant J 70(3):409–420

    Article  CAS  PubMed  Google Scholar 

  • Nowak MD, Russo G, Schlapbach R, Huu CN, Lenhard M, Conti E (2015) The draft genome of Primula veris yields insights into the molecular basis of heterostyly. Genome Biol 16:12. doi:10.1186/s13059-014-0567-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Salzberg SL, Pertea M, Delcher AL, Gardner MJ, Tettelin H (1999) Interpolated Markov models for eukaryotic gene finding. Genomics 59(1):24–31

    Article  CAS  PubMed  Google Scholar 

  • Shore JS, Arbo MM, Fernandez A (2006) Breeding system variation, genetics and evolution in the Turneraceae. New Phytol 171:539–551

    CAS  PubMed  Google Scholar 

  • Sonnhammer ELL, Eddy SR, Durbin R (1997) Pfam: a comprehensive database of protein families based on seed alignments. Proteins 28:405–420

    Article  CAS  PubMed  Google Scholar 

  • Stanke M, Steinkamp R, Waack S, Morgenstern B (2004) AUGUSTUS: a web server for gene finding in eukaryotes. Nucleic Acids Res 32:W309–W312

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Steinbiss S, Gremme G, Schärfer C, Mader M, Kurtz S (2009) AnnotationSketch: a genome annotation drawing library. Bioinformatics 25(4):533–534

    Article  CAS  PubMed  Google Scholar 

  • Tamari F, Shore JS (2004) Distribution of style and pollen polygalacturonases among distylous and homostylous Turnera and Piriqueta spp. (Turneraceae). Heredity 92(5):380–385

    Article  CAS  PubMed  Google Scholar 

  • Tamari F, Shore JS (2006) Allelic variation for a short-specific polygalacturonase in Turnera subulata: is it associated with the degree of self-compatibility? Int J Plant Sci 167:125–133

    Article  CAS  Google Scholar 

  • Tan G, Gao Y, Shi M, Zhang X, He S, Chen Z, An C (2005) SiteFinding-PCR: a simple and efficient PCR method for chromosome walking. Nucleic Acids Res 33(13):e122

    Article  PubMed  PubMed Central  Google Scholar 

  • Yasui Y, Mori M, Aii J, Abe T, Matsumoto D (2012) S-LOCUS EARLY FLOWERING 3 is exclusively present in the genomes of short-styled buckwheat plants that exhibit heteromorphic self-incompatibility. PLoS ONE 7(2):e31264

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zimmer R, Verrinder Gibbins AM (1997) Construction and characterization of a large-fragment chicken bacterial artificial chromosome library. Genetics 42:217–226

    CAS  Google Scholar 

Download references

Acknowledgements

The authors thank Chuck Cody for greenhouse support, Dave Dutton for technical assistance and Derek Pouchnik and Mark Wildung of the WSU Genomic Core Lab for BAC sequencing and assembly.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Andrew G. McCubbin.

Additional information

Communicated by Teh-hui Kao.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 255 kb)

Supplementary material 2 (XLSX 15 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Burrows, B.A., McCubbin, A.G. Sequencing the genomic regions flanking S-linked PvGLO sequences confirms the presence of two GLO loci, one of which lies adjacent to the style-length determinant gene CYP734A50 . Plant Reprod 30, 53–67 (2017). https://doi.org/10.1007/s00497-017-0299-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00497-017-0299-9

Keywords

Navigation