Abstract
While the breeding system known as distyly has been used as a model system in genetics, and evolutionary biology for over a century, the genes determining this system remain unknown. To positionally clone genes determining distyly, a high-resolution map of the S-locus region of Turnera has been constructed using segregation data from 2,013 backcross progeny. We discovered three putative genes tightly linked with the S-locus. An N-acetyltransferase (TkNACE) flanks the S-locus at 0.35 cM while a sulfotransferase (TkST1) and a non-LTR retroelement (TsRETRO) show complete linkage to the S-locus. An assay of population samples of six species revealed that TsRETRO, initially discovered in diploid Turnera subulata, is also associated with the S-allele in tetraploid T. subulata and diploid Turnera scabra. The sulfotransferase gene shows some level of differential expression in long versus short styles, indicating it might be involved in some aspect of distyly. The complete linkage of TkST1 and TsRETRO to the S-locus suggests that both genes may reside within, or in the immediate vicinity of the S-locus. Chromosome walking has been initiated using one of the genes discovered in the present study to identify the genes determining distyly.
Similar content being viewed by others
References
Aii J, Nagano M, Penner GA, Campbell CG, Adachi T (1998) Identification of RAPD markers linked to the homostylar (Ho) gene in buckwheat. Breed Sci 48:59–62
Ananvoranich S, Varin L, Gulick P, Ibrahim R (1994) Cloning and regulation of flavonol 3-sulfotransferase in cell-suspension cultures of Flaveria bidentis. Plant Physio 106:485–491
Arroyo J, Barrett SCH (2000) Discovery of distyly in Narcissus (Amaryllidaceae). Am J Bot 87:748–751
Athanasiou A, Khosravi D, Tamari F, Shore JS (2003) Characterization and localization of short-specific polygalacturonase in distylous Turnera subulata (Turneraceae). Am J Bot 90:675–682
Barrett SCH, Cruzan MB (1994) Incompatibility in heterostylous plants. In: Williams EG, Knox RB, Clarke AG (eds) Genetic control of incompatibility and reproductive development in flowering plants. Kluwer, Boston, pp 189–219
Barrett SCH, Shore JS (1987) Variation and evolution of breeding systems in the Turnera ulmifolia L. complex. Evolution 41:340–354
Barrett SCH, Shore JS (2008) New insights on heterostyly: comparative biology, ecology and genetics. In: Franklin-Tong VE (ed) Self-incompatibility in flowering plants: evolution, diversity and mechanisms. Springer, Berlin, pp 3–32
Barry CS, McQuinn RP, Chung M, Besuden AM, Giovannoni JJ (2008) Amino acid substitutions in homologs of the STAY-GREEN protein are responsible for the green-flesh and chlorophyll retainer mutations of tomato and Pepper. Plant Physiol 147:179–187
Bateson W, Gregory RP (1905) On the inheritance of heterostylism in Primula. Proc R Soc Lond Ser B 76:581–586
Bojarova P, Williams SJ (2008) Sulfotransferases, sulfatases and formylglycine-generating enzymes: a sulfation fascination. Curr opin chem biol 12:1–9
Cui Y, Brugière N, Jackman L, Bi Y, Rothstein SJ (1999) Structural and transcriptional comparative analysis of the S locus regions in two self-incompatible Brassica napus lines. Plant Cell 11:2216–2231
Darwin C (1877) The different forms of flowers on plants of the same species. Murray, London, UK
Dolgin ES, Charlesworth B (2008) The effects of recombination rate on the distribution and abundance of transposable elements. Genetics 178:2169–2177
Dowrick VPJ (1956) Heterostyly and homostyly in Primula obconica. Heredity 10:219–236
Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12:13–15
Dulberger R (1974) Structural dimorphism of stigmatic papillae in distylous Linum species. Am J Bot 61:238–243
Dulberger R (1992) The genetics of heterostyly. In: Barrett SCH (ed) Evolution and function of heterostyly. Springer, Berlin, pp 41–84
Ernst A (1955) Self-fertility in monomorphic Primulas. Genetica 27:391–448
Franklin-Tong VE (2008) Self-incompatibility in flowering plants: evolution, diversity and mechanisms. Springer, Berlin
Ganders FR (1979) The biology of heterostyly. N Z J Bot 17:607–635
Gidda SK, Miersch O, Levitin A, Schmidt J, Wasternack C, Varin L (2003) Biochemical and molecular characterization of a hydroyjasmonate sulfotransferase from Arabidopsis thaliana. J Biol Chem 278:17895–17900
Hall BG (2001) Phylogenetic trees made easy: a how-to manual for molecular biologists. Sinauer, Sunderland, MA
Hebsgaard SM, Korning PG, Tolstrup N, Engelbreht PR, Rouzé P, Brunak S (1996) Splice site prediction in Arabidopsis thaliana pre-mRNA by combining local and global sequence information. Nucleic Acids Res 24:3439–3459
Kachroo A, Nasrallah ME, Nasrallah JB (2002) Self-incompatibility in the Brassicaceae: receptor-ligand signaling and cell-to-cell communication. Plant Cell 14:227–238
Khosravi D, Yang CC, Siu KWM, Shore JS (2004) High level of α-dioxygenase in short styles of distylous Turnera spp. Int J Plant Sci 165:995–1006
Klein M, Papenbrock J (2004) The multi-protein family of Arabidopsis sulphotransferases and their relatives in other plant species. J Exp Bot 55:1809–1820
Kurian V, Richards AJ (1997) A new recombinant in the heteromorphy ‘S’ supergene in Primula. Heredity 78:383–390
Labonne JDJ, Hilliker AJ, Shore JS (2007) Meiotic recombination in Turnera (Turneraceae): extreme sexual difference in rates, but no evidence for recombination suppression associated with the distyly S-locus. Heredity 98:411–418
Labonne JDJ, Vaisman A, Shore JS (2008) Construction of a first genetic map of distylous Turnera and a fine-scale map of the S-locus region. Genome 51:471–478
Lai Z, Ma W, Han B, Liang L, Zhang Y, Hong G, Xue Y (2002) An F-box gene linked to the self-incompatibility (S) locus of Antirrhinum is expressed specifically in pollen and tapetum. Plant Mol Biol 50:29–42
Lehman A, Black R, Ecker JR (1996) HOOKLESS1, an ethylene response gene is required for differential cell elongation in the Arabidopsis hypocotyl. Cell 85:183–194
Lewis D, Jones DA (1992) The genetics of heterostyly. In: Barrett SCH (ed) Evolution and function of heterostyly. Springer, Berlin, pp 129–150
Li J, Webster M, Furuya M, Gilmartin PM (2007) Identification and characterization of pin and thrum alleles of two genes that co-segregate with the Primula S-locus. Plant J 51:18–31
Maddison DR, Maddison WP (2000) MacClade 4: analysis of phylogeny and character evolution, version 4.05. Sinauer, Sunderland, MA
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
Martin GB, Brommonschenkel SH, Chunwongse J, Frary A, Ganal MW, Spivey R, Wu T, Earle ED, Tanksley SD (1993) Map-based cloning of a protein kinase gene conferring disease resistance in Tomato. Science 262:1432–1436
Mather K, de Winton D (1941) Adaptation and counter-adaptation of the breeding system in Primula. Ann Bot NS 5:297–311
McCubbin AG (2008) Heteromorphic self-incompatibility in Primula: twenty-first century tools promise to unravel a classic nineteeth century model system. In: Franklin-Tong VE (ed) Self-incompatibility in flowering plants: evolution, diversity and mechanisms. Springer, Berlin, pp 289–308
McCubbin AG, Lee C, Hetrick A (2006) Identification of genes showing differential expression between morphs in developing flowers of Primula vulgaris. Sex Plant Reprod 19:63–72
Miljuš-Đukić J, Ninković S, Radović S, Maksimović V, Brkljačić J, Nešković M (2004) Detection of proteins possibly involved in self-incompatibility response in distylous buckwheat. Biol Plant 48:293–296
Nagano M, Aii J, Campbell C, Adachi T, Kawasaki S (2005) Construction of a BAC library for the investigation of the S locus in Buckwheat. Fagopyrum 22:13–20
Richards AJ (1993) Primula. Batsford, London
Rommens MJ, Iannuzzi MC, Kerem BA, Drumm ML, Melmer G, Dean M, Rozmahel R, Cole JL, Kenedy D, Hidaka N, Zsiga M, Buchwald M, Riordan JR, Tsui L, Collins FS (1989) Identification of the cystic fibrosis gene: chromosome walking and jumping. Science 245:1059–1065
Rouleau M, Marsolais F, Richard M, Nicolle L, Voigt B, Adam G, Varin L (1999) Inactivation of Brassinosteroid biological activity by a salicylate-inducible steroid sulfotransferase from Brassica napus. J Biol Chem 274:20925–20930
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Habor Laboratory Press, Cold Spring Habor, NY
Sassa H, Kakui H, Miyamoto M, Suzuki Y, Hanada T, Ushijima K, Kusaba M, Hirano H, Koba T (2007) S locus F-Box Brothers: multiple and pollen-specific F-Box genes with S haplotype-specific polymorphisms in apple and Japanese pear. Genetics 175:1869–1881
Sherman-Broyles S, Nasrallah JB (2008) Self-incompatibility and evolution of mating systems in the Brassicaceae. In: Franklin-Tong VE (ed) Self-incompatibility in flowering plants: evolution, diversity and mechanisms. Springer, Berlin, pp 123–147
Shore JS, Barrett SCH (1986) Genetic modifications of dimorphic incompatibility in the Turnera ulmifolia complex (Turneraceae). Can J Genet Cytol 28:796–807
Shore JS, Barrett SCH (1987) Inheritance of floral and isozyme polymorphisms in Turnera ulmifolia L. J Hered 78:44–48
Shore JS, Arbo MM, Fernandez A (2006) Breeding system variation, genetics and evolution in the Turneraceae. New Phytol 171:539–551
Sijacic P, Wang X, Skirpan AL, Wang Y, Dowd PE, McCubbin AG, Huang S, Kao T (2004) Identification of the pollen determinant of S-RNase mediated self-incompatibility. Nature 429:302–305
Stein JC, Howlett H, Boyes DC, Nasrallah ME, Nasrallah JB (1991) Molecular cloning of a putative receptor protein kinase gene encoded at the self-incompatibility locus of Brassica oleraceae. Proc Natl Acad Sci USA 88:8816–8820
Suzuki G, Kai N, Hirose T, Fukui K, Nishio T, Takayama S, Isogai A, Watanabe M, Hinata K (1999) Genomic organization of the S locus: identification and characterization of genes in SLG/SRK region of S9 haplotype of Brassica campestris (syn. rapa). Genetics 153:391–400
Swofford DL (2001) PAUP* version 4.0b10: phylogenetic analysis using parsimony (*and other methods). Sinauer, Sunderland, MA
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 176:125–133
Tamari F, Khosravi D, Hilliker AJ, Shore JS (2005) Inheritance of spontaneous mutant homostyles in Turnera subulata × krapovickasii and in autotetraploid T. scabra (Turneraceae). Heredity 94:207–216
Tanksley SD, Ganal MW, Martin GB (1995) Chromosome landing: a paradigm for map-based cloning in plants with large genomes. TIG 11:63–68
Thomas SG, Franklin-Tong VE (2004) Self-incompatibility triggers programmed cell-death in Papaver pollen. Nature 429:305–309
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The Clustal_X Windows interface: flexible strategies for multiple sequences alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882
Truyens S, Arbo MM, Shore JS (2005) Phylogenetic relationships, chromosome and breeding system evolution in Turnera (Turneraceae): inferences from ITS sequence data. Am J Bot 92:1749–1758
Varin L, Marsolais F, Richard M, Rouleau M (1997a) Biochemistry and molecular biology of plant sulfotransferases. FASEB J 11:517–525
Varin L, Chamberland H, Lafontaine JG, Richard M (1997b) The enzyme involved in sulfation of the turgorin, gallic acid 4-O-(β-D-glucopyranosyl-6’-sulfate) is pulvini-localized in Mimosa pudica. Plant J 12:831–837
Wang Y, Wang X, McCubbin AG, Kao T (2003) Genetic mapping and molecular characterization of the self-incompatibility (S) locus in Petunia inflata. Plant Mol Biol 53:565–580
Wang Y, Tsukamoto T, Yi K, Wang X, Huang S, McCubbin AG, Kao T (2004) Chromosome walking in the Petunia inflata self-incompatibility (S-) locus and gene identification in an 881-kb contig containing S2-RNase. Plant Mol Biol 54:727–742
Wedderburn FM, Richards AJ (1990) Variation in within-morph incompatibility inhibition sites in heteromorphic Primula. New Phytol 116:149–162
Weinshilboum RM, Otterness DM, Aksoy IA, Wood TC, Her C, Raftogianis RB (1997) Sulfotransferase molecular biology: cDNAs and genes. FASEB J 11:3–14
Wheeler MJ, Armstrong SA, Franklin-Tong VE, Franklin FCH (2003) Genomic organization of the Papaver rhoeas self-incompatibility S 1 locus. J Exp Bot 54:131–139
Wong KC, Watanabe M, Hinata K (1994) Protein profiles in pin and thrum floral organs of distylous Averrhoa carambola L. Sex Plant Reprod 7:107–115
Wright SI, Agrawal N, Bureau TE (2003) Effects of recombination rate and gene density on transposable element distributions in Arabidopsis thaliana. Genome Res 13:1897–1903
Yasui Y, Mori M, Matsumoto D, Ohnishi O, Campbell CG, Ota T (2008) Construction of a BAC library for buckwheat genome research—an application to positional cloning of agriculturally valuable traits. Genes Genet Syst 83:393–401
Acknowledgments
We would like to thank Dr. Stephen Wright and Dr. Arthur Hilliker for advice, Ruth Haile-Meskale, Jessica Tavone and Mohammad Mokhtari for technical assistance, and Paul Chafe for providing the Piriqueta samples. We also thank Lee Wong of the Molecular Core Facility at York University for sequencing of samples. This work was funded by a Natural Sciences and Engineering Research Council grant to J.S. Shore.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by R. Hagemann.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Labonne, J.J.D., Goultiaeva, A. & Shore, J.S. 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 (2009). https://doi.org/10.1007/s00438-009-0439-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00438-009-0439-5