Development of Genomic Resources in the Species of Trifolium L. and Its Application in Forage Legume Breeding
Abstract
:1. Introduction
2. White Clover
2.1. Germplasm and Breeding
2.2. Impact of Genomics on Breeding Strategy in White Clover
3. Red Clover (Trifolium pratense L.)
3.1. Traits of Interest
3.2. Genetics and Breeding
3.3. Translational Genomics in Red Clover
4. Genetics and Comparative Genomics in Subterranean Clover (Trifolium ambiguum)
5. Interspecific Hybrids
5.1. T. repens and Its Putative Progenitors
5.2. T. pratense
5.3. T. subterraneum and T. alexandrinum
6. Conclusions and Future Prospects
References and Note
- Suttie, J.M.; Reynolds, S.G.; Batello, C. Grasslands of the world. In Plant Production and Protection Series; FAO: Rome, Italy, 2005; Volume 34, pp. 1–10. [Google Scholar]
- Zohary, M.; Heller, D. The Genus Trifolium; The Israel Academy of Sciences and Humanities: Jerusalem, Israel, 1984; p. 606. [Google Scholar]
- Taylor, N.L. A century of clover breeding developments in the united states. Crop Sci. 2008, 48, 1–13. [Google Scholar]
- Vavilov, N.I. Centers of origin of cultivated plants. Bull. Appl. Bot. Genet. Sel. 1926, 16, 139–248. [Google Scholar]
- Kjaergaard, T. A plant that changed the world: Rise and fall of clover 1000–2000. Landsc. Res. 2003, 28, 41–49. [Google Scholar]
- Laidlaw, A.S.; Teuber, N. Temperate Forage Grass-Legume Mixtures: Advances and Perspectives; Fundacao Estudos Agrarios Luiz Queiroz (Fealq): Piracicaba, Brazil, 2001; pp. 85–92. [Google Scholar]
- Mather, R.D.J.; Melhuish, D.T.; Herlihy, M. Trends in the global marketing of white clover cultivars. In White Clover: New Zealand’s Competitive Edge. Grassland Research and Practice Series; Woodfield, D., Ed.; New Zealand Grassland Association: Palmerston North, New Zealand, 1996; Volume 6, pp. 7–14. [Google Scholar]
- Ellison, N.W.; Liston, A.; Steiner, J.J.; Williams, W.M.; Taylor, N.L. Molecular phylogenetics of the clover genus (Trifolium—Leguminosae). Mol Phylogenet. Evol. 2006, 39, 688–705. [Google Scholar] [CrossRef]
- Abberton, M.T.; Thomas, I. Genetic resources in Trifolium and their utilization in plant breeding. Plant Genet. Res. 2011, 9, 38–44. [Google Scholar] [CrossRef]
- Abberton, M.T.; Marshall, A.H. White Clover. In Crops and Amenity Grasses; Boller, B., Posselt, U.K., Ulrich, K., Veronesi, F., Eds.; Springer: Berlin, Germany, 2010; pp. 457–476. [Google Scholar]
- Michaelson-Yeates, T.P.T.; Marshall, A.; Abberton, M.T.; Rhodes, I. Self-compatibility and heterosis in white clover (Trifolium repens L.). Euphytica 1997, 94, 341–348. [Google Scholar] [CrossRef]
- Jones, E.S.; Hughes, L.J.; Drayton, M.C.; Abberton, M.T.; Michaelson-Yeates, T.P.T.; Bowen, C.; Forster, J.W. An ssr and aflp molecular marker-based genetic map of white clover (Trifolium repens L.). Plant Sci. 2003, 165, 531–539. [Google Scholar] [CrossRef]
- Cogan, N.; Abberton, M.; Smith, K.; Kearney, G.; Marshall, A.; Williams, A.; Michaelson-Yeates, T.; Bowen, C.; Jones, E.; Vecchies, A.;et al. Individual and multi-environment combined analyses identify qtls for morphogenetic and reproductive development traits in white clover (Trifolium repens L.). Theor. Appl. Genet. 2006, 112, 1401–1415. [Google Scholar] [CrossRef]
- Casey, N.; Milbourne, D.; Barth, S.; Febrer, M.; Jenkins, G.; Abberton, M.; Jones, C.; Thorogood, D. The genetic location of the self-incompatibility locus in white clover (Trifolium repens L.). Theor. Appl. Genet. 2010, 121, 567–576. [Google Scholar] [CrossRef]
- Barrett, B.; Griffiths, A.; Schreiber, M.; Ellison, N.; Mercer, C.; Bouton, J.; Ong, B.; Forster, J.; Sawbridge, T.; Spangenberg, G.; et al. A microsatellite map of white clover. Theor. Appl. Genet. 2004, 109, 596–608. [Google Scholar]
- Zhang, Y.; Sledge, M.; Bouton, J. Genome mapping of white clover (Trifolium repens L.) and comparative analysis within the trifolieae using cross-species SSR markers. Theor. Appl. Genet. 2007, 114, 1367–1378. [Google Scholar] [CrossRef]
- Wang, J.; Drayton, M.; George, J.; Cogan, N.; Baillie, R.; Hand, M.; Kearney, G.; Erb, S.; Wilkinson, T.; Bannan, N.; et al. Identification of genetic factors influencing salt stress tolerance in white clover (Trifolium repens L.) by QTL analysis. Theor. Appl. Genet. 2010, 120, 607–619. [Google Scholar] [CrossRef]
- Inostroza, L.; Acuña, H. Water use efficiency and associated physiological traits of nine naturalized white clover populations in chile. Plant Breed. 2010, 129, 700–706. [Google Scholar]
- Abberton, M.; Marshall, A.; Collins, R.P.; Jones, C.M.; Lowe, M. Molecular Breeding of forage and turf, 2009. In QTL Analysis and Gene Expression Studies in White Clover; Yamada, T., Spangenberg, G., Eds.; Springer: Sapporo, Japan, 2009; pp. 163–172. [Google Scholar]
- Jones, C.; Abberton, M.T. Application of Molecular Markers Derived from Medicago Truncatula in White Clover (Trifolium repens L.); Wageningen Academic Publishers: Wageningen, The Netherland, 2005; p. 169. [Google Scholar]
- Young, N.D.; Debelle, F.; Oldroyd, G.E.D.; Geurts, R.; Cannon, S.B.; Udvardi, M.K.; Benedito, V.A.; Mayer, K.F.X.; Gouzy, J.; Schoof, H.; et al. The Medicago genome provides insight into the evolution of rhizobial symbioses. Nature 2011, 480, 520–524. [Google Scholar]
- Kölliker, R.; Jones, E.S.; Drayton, M.C.; Dupal, M.P.; Forster, J.W. Development and characterisation of simple sequence repeat (ssr) markers for white clover (Trifolium repens L.). Theor. Appl. Genet. 2001, 102, 416–424. [Google Scholar] [CrossRef]
- Kοlliker, R.; Jones, E.S.; Jahufer, M.Z.Z.; Forster, J.W. Bulked aflp analysis for the assessment of genetic diversity in white clover (Trifolium repens L.). Euphytica 2001, 121, 305–315. [Google Scholar] [CrossRef]
- Hand, M.; Ponting, R.; Drayton, M.; Lawless, K.; Cogan, N.; Charles Brummer, E.; Sawbridge, T.; Spangenberg, G.; Smith, K.; Forster, J. Identification of homologous, homoeologous and paralogous sequence variants in an outbreeding allopolyploid species based on comparison with progenitor taxa. Mol. Genet. Genom. 2008, 280, 293–304. [Google Scholar]
- Barrett, B.; Baird, I.; Woodfield, D. White clover seed yield: A case study in marker-assisted selection. In Molecular Breeding of Forage and Turf; Yamada, T., Spangenberg, G., Eds.; Springer: Sapporo, Japan, 2009; pp. 241–250. [Google Scholar]
- Flint-Garcia, S.A.; Thornsberry, J.M.; Buckler, E.S. Structure of linkage disequilibrium in plants. Ann. Rev. Plant Biol. 2003, 54, 357–374. [Google Scholar]
- Breseghello, F.; Sorrells, M.E. Association analysis as a strategy for improvement of quantitative traits in plants. Crop Sci. 2006, 46, 1323–1330. [Google Scholar]
- Skøt, L.; Humphreys, J.; Humphreys, M.O.; Thorogood, D.; Gallagher, J.; Sanderson, R.; Armstead, I.P.; Thomas, I.D. Association of candidate genes with flowering time and water-soluble carbohydrate content in Lolium perenne (L.). Genetics 2007, 177, 535–547. [Google Scholar] [CrossRef]
- Forster, J.W.; Cogan, N.O.I.; Dobrowolski, M.P.; Francki, M.G.; Spangenberg, G.C.; Smith, K.F. Functionally Associated Molecular Genetic Markers for Temperate Pasture Plant Improvement; Cabi Publishing: Wallingford, Oxon, UK, 2008; pp. 154–186. [Google Scholar]
- Brummer, E.C. Capturing heterosis in forage crop cultivar development. Crop Sci. 1999, 39, 943–954. [Google Scholar]
- Li, X.; Brummer, C.E. Inbreeding depression for fertility and biomass in advanced generations of inter- and intrasubspecific hybrids of tetraploid alfalfa. Crop Sci. 2009, 49, 13–19. [Google Scholar]
- Graham, P.H.; Vance, C.P. Legumes: Importance and constraints to greater use. Plant Physiol. 2003, 131, 872–877. [Google Scholar]
- Abberton, M.T.; Marshall, A.H. Progress in breeding perennial clovers for temperate agriculture. J. Agric. Sci. 2005, 143, 117–135. [Google Scholar]
- Taylor, N.L.; Quesenberry, K.H. Red Clover Science; Kluwer Academic Publishers: Dordrecht, The Netherlands, 1996; pp. 1–225. [Google Scholar]
- Hejduk, S.; Knot, P. Effect of provenance and ploidy of red clover varieties on productivity, persistence and growth pattern in mixture with grasses. Plant Soil Environ. 2010, 56, 111–119. [Google Scholar]
- Page, D.; Dulclos, B.; Aubert, G.; Bonavent, J.F.; Mousset-Déclas, C. Sclerotinia rot resistance in red clover: Identification of rapd markers using bulked segregant analysis. Plant Breed. 1997, 116, 73–78. [Google Scholar]
- Smith, R.S.; Bishop, D.J. Astred—A stoloniferous red clover. In Proceedings of the 17th International Grassland Congress, Palmerston North, New Zealand, 8-21 February 1993; pp. 421–423.
- Isobe, S.; Klimenko, I.; Ivashuta, S.; Gau, M.; Kozlov, N.N. First rflp linkage map of red clover (Trifolium pratense L.) based on cdna probes and its transferability to other red clover germplasm. Theor. Appl. Genet. 2003, 108, 105–112. [Google Scholar] [CrossRef]
- Sato, S.; Isobe, S.; Asamizu, E.; Ohmido, N.; Kataoka, R.; Nakamura, Y.; Kaneko, T.; Sakurai, N.; Okumura, K.; Klimenko, I.; et al. Comprehensive structural analysis of the genome of red clover (Trifolium pratense L.). DNA Res. 2005, 12, 301–364. [Google Scholar]
- Herrmann, D.; Boller, B.; Studer, B.; Widmer, F.; Kölliker, R. Qtl analysis of seed yield components in red clover (Trifolium pratense L.). Theor. Appl. Genet. 2006, 112, 536–545. [Google Scholar] [CrossRef]
- Zainol, R. Molecular Genetic Analysis of Key Traits in Red Clover (Trifolium pratense L.). Ph.D. Thesis, Aberystwyth University, Aberystwyth, UK, 2008. [Google Scholar]
- Isobe, S.; Kolliker, R.; Hisano, H.; Sasamoto, S.; Wada, T.; Klimenko, I.; Okumura, K.; Tabata, S. Construction of a consensus linkage map for red clover (Trifolium pratense L.). BMC Plant Biol. 2009, 9, 57. [Google Scholar] [CrossRef]
- Herrmann, D.; Boller, B.; Studer, B.; Widmer, F.; Kölliker, R. Improving persistence in red clover: Insights from qtl analysis and comparative phenotypic evaluation. Crop Sci. 2008, 48, 269–277. [Google Scholar]
- Klimenko, I.; Razgulayeva, N.; Gau, M.; Okumura, K.; Nakaya, A.; Tabata, S.; Kozlov, N.; Isobe, S. Mapping candidate qtls related to plant persistency in red clover. Theor. Appl. Genet. 2010, 120, 1253–1263. [Google Scholar]
- Riday, H. Paternity testing: A non-linkage based marker-assisted selection scheme for outbred forage species. Crop Sci. 2011, 51, 631–641. [Google Scholar]
- Winters, A.; Heywood, S.; Farrar, K.; Donnison, I.; Thomas, A.; Webb, K.J. Identification of an extensive gene cluster among a family of ppos in Trifolium pratense L. (red clover) using a large insert bac library. BMC Plant Biol. 2009, 9, 94. [Google Scholar] [CrossRef]
- Yu, Y.; Collura, K.; Wissotski, M.; Kim, W.; Golser, W.; Braidotti, M.; Zuccola, A.; Wing, R.A.; Kudrna, D.; Skøt, L.; et al. Translational Genomics to Underpin Germplasm Improvement for Complex Traits in Crop Legumes. Genomic Survey Sequences (HR235466-HR298279). 2010. [Google Scholar]
- Wang, L.; Li, P.; Brutnell, T.P. Exploring plant transcriptomes using ultra high-throughput sequencing. Brief. Funct. Genom. 2010, 9, 118–128. [Google Scholar]
- Libault, M.; Farmer, A.; Joshi, T.; Takahashi, K.; Langley, R.J.; Franklin, L.D.; He, J.; Xu, D.; May, G.; Stacey, G. An integrated transcriptome atlas of the crop model glycine max, and its use in comparative analyses in plants. Plant J. 2010, 63, 86–99. [Google Scholar]
- Severin, A.; Woody, J.; Bolon, Y.-T.; Joseph, B.; Diers, B.; Farmer, A.; Muehlbauer, G.; Nelson, R.; Grant, D.; Specht, J.; et al. Rna-seq atlas of glycine max: A guide to the soybean transcriptome. BMC Plant Biol. 2010, 10, 160. [Google Scholar] [CrossRef]
- Yang, S.S.; Tu, Z.; Cheung, F.; Xu, W.; Lamb, J.; Jung, H.-J.; Vance, C.; Gronwald, J. Using rna-seq for gene identification, polymorphism detection and transcript profiling in two alfalfa genotypes with divergent cell wall composition in stems. BMC Genomics 2011, 12, 199. [Google Scholar]
- Garg, R.; Patel, R.K.; Tyagi, A.K.; Jain, M. De novo assembly of chickpea transcriptome using short reads for gene discovery and marker identification. DNA Res. 2011, 18, 53–63. [Google Scholar] [CrossRef]
- Birol, I.; Jackman, S.D.; Nielsen, C.B.; Qian, J.Q.; Varhol, R.; Stazyk, G.; Morin, R.D.; Zhao, Y.; Hirst, M.; Schein, J.E.; et al. De novo transcriptome assembly with abyss. Bioinformatics 2009, 25, 2872–2877. [Google Scholar]
- Zerbino, D.R.; Birney, E. Velvet: Algorithms for de novo short read assembly using de bruijn graphs. Genome Res. 2008, 18, 821–829. [Google Scholar] [CrossRef]
- Katznelson, U.; Morley, H.W. Speciation processes in Trifolium subterraneum L. Israel J. Bot. 1965, 14, 15–35. [Google Scholar]
- Vižintin, L.; Javornik, B.; Bohanec, B. Genetic characterization of selected Trifolium species as revealed by nuclear DNA content and its rDNA region analysis. Plant Sci. 2006, 170, 859–866. [Google Scholar] [CrossRef]
- Ghamkhar, K.; Isobe, S.; Nichols, P.; Faithfull, T.; Ryan, M.; Snowball, R.; Sato, S.; Appels, R. The first genetic maps for subterranean clover (Trifolium subterraneum L.) and comparative genomics with T. pratense L. and Medicago truncatula Gaertn. To identify new molecular markers for breeding. Mol. Breed. 2011. [Google Scholar]
- Taylor, N.F.; Quarles, R.F.; Anderson, M.K. Methods of overcoming interspecific barriers in Trifolium. Euphytica 1980, 29, 441–450. [Google Scholar]
- Roy, A.K.; Malaviya, D.R.; Kaushal, P. Generation of interspecific hybrids of Trifolium using embryo rescue techniques. Methods Mol. Biol. 2011, 710, 141–151. [Google Scholar] [CrossRef]
- Stebbins, G.L. Chromosomal Evolution in Higher Plants; Edward Arnold: London, UK, 1971. [Google Scholar]
- Mayrose, I.; Barker, M.S.; Otto, S.P. Probabilistic models of chromosome number evolution and the inference of polyploidy. Syst. Biol. 2010, 59, 132–144. [Google Scholar]
- Brewbaker, J.L.; Keim, W.F. A fertile interspecific hybrid in Trifolium (4n T. repens L. × 4n T. nigrescens Viv.). Am. Nat. 1953, 87, 323–326. [Google Scholar]
- Gibson, P.B.; Beinhart, G. Hybridization of Trifolium occidentale with two other species of clover. J. Hered. 1969, 60, 93–96. [Google Scholar]
- Chen, C.C.; Gibson, P.B. Chromosome pairing in two interspecific hybrids of Trifolium. Can. J. Genet. Cytol. 1970, 12, 790–794. [Google Scholar]
- Chen, C.C.; Gibson, P.B. Karyotypes of 15 Trifolium species in section amoria. Crop Sci. 1971, 11, 441–445. [Google Scholar] [CrossRef]
- Badr, A.; El-Shazly, H.; Mekki, L. Genetic diversity in white clover and its progenitors as revealed by DNA fingerprinting. Biol. Plant. 2012, 56, 283–291. [Google Scholar]
- Kakes, P.; Chardonnens, A.N. Cyanotypic frequencies in adjacent and mixed populations of Trifolium occidentale coombe and Trifolium repens L. are regulated by different mechanisms. Biochem. Syst. Ecol. 2000, 28, 633–649. [Google Scholar] [CrossRef]
- Olsen, K.M.; Sutherland, B.L.; Small, L.L. Molecular evolution of the li/li chemical defence polymorphism in white clover (Trifolium repens L.). Mol. Ecol. 2007, 16, 4180–4193. [Google Scholar] [CrossRef]
- Chou, M.C.; Gibson, P.B. Cross-compatibility of Trifolium nigrescens with diploid and tetraploid Trifolium occidentale. Crop Sci. 1968, 8, 266–267. [Google Scholar] [CrossRef]
- Chen, C.C.; Gibson, P.B. Seed development following matings of Trifolium nigrescens × Trifolium occidentale at different ploidy levels. Crop Sci. 1974, 14, 72–77. [Google Scholar] [CrossRef]
- Williams, W.M.; Ansari, H.A.; Hussain, S.W.; Ellison, N.W.; Williamson, M.L.; Verry, I.M. Hybridization and introgression between two diploid wild relatives of white clover, Trifolium nigrescens viv. And T. occidentale Coombe. Crop Sci. 2008, 48, 139–148. [Google Scholar] [CrossRef]
- Hirst, M.; Marra, M.A. Next generation sequencing based approaches to epigenomics. Brief. Funct. Genom. 2010, 9, 455–465. [Google Scholar]
- Song, K.M.; Lu, P.; Tang, K.L.; Osborn, T.C. Rapid genome change in synthetic polyploids ofbrassica and its implications for polyploid evolution. Proc. Natl. Acad. Sci. USA 1995, 92, 7719–7723. [Google Scholar]
- Feldman, M.; Liu, B.; Segal, G.; Abbo, S.; Levy, A.A.; Vega, J.M. Rapid elimination of low-copy DNA sequences in polyploid wheat: A possible mechanism for differentiation of homoeologous chromosomes. Genetics 1997, 147, 1381–1387. [Google Scholar]
- Zou, J.; Fu, D.; Gong, H.; Qian, W.; Xia, W.; Pires, J.C.; Li, R.; Long, Y.; Mason, A.S.; Yang, T.-J.; et al. De novo genetic variation associated with retrotransposon activation, genomic rearrangements and trait variation in a recombinant inbred line population of brassica napus derived from interspecific hybridization with Brassica rapa. Plant J. 2011, 68, 212–224. [Google Scholar] [CrossRef]
- Pederson, G.A.; Windham, G.L. Resistance to meloidogyne incognita in Trifolium interspecific hybrids and species related to white clover. Plant Dis. 1989, 73, 567–569. [Google Scholar] [CrossRef]
- Hussain, S.W.; Williams, W.M.; Mercer, C.F.; White, D.W.R. Transfer of clover cyst nematode resistance from Trifolium nigrescens Viv to T. repens L. by interspecific hybridisation. Theor. Appl. Genet. 1997, 95, 1274–1281. [Google Scholar] [CrossRef]
- Marshall, A.H.; Michaelsonyeates, T.P.T.; Aluka, P.; Meredith, M. Reproductive characters of interspecific hybrids between Trifolium repens L. and T. nigrescens Viv. Heredity 1995, 74, 136–145. [Google Scholar] [CrossRef]
- bberton, M.T.; Michaelson-Yeates, T.P.T.; Marshall, A.H.; Holdbrook-Smith, K.; Rhodes, I. Morphological characteristics of hybrids between white clover, Trifolium repens L., and caucasian clover, Trifolium ambiguum m Bieb. Plant Breed. 1998, 117, 494–496. [Google Scholar]
- Pederson, G.A.; Mclaughlin, M.R. Resistance to viruses in Trifolium interspecific hybrids related to white clover. Plant Dis. 1989, 73, 997–999. [Google Scholar] [CrossRef]
- Taylor, N.L.; Stroube, W.H.; Collins, G.B.; Kendall, W.A. Interspecific hybridization of red clover (Trifolium pratense L.). Crop Sci. 1963, 3, 549–552. [Google Scholar] [CrossRef]
- Dabkeviciene, G.; Paplauskiene, V.; Pasakinskiene, I. Assessment of the agronomic utility of interspecific hybrids Trifolium pratense L. × T. diffusum Ehrh. and confirmation of their hybridity with ISSR markers. J. Food Agric. Environ. 2008, 6, 187–190. [Google Scholar]
- Armstrong, K.C.; Cleveland, R.W. Hybrids of Trifolium pratense × Trifolium pallidum. Crop Sci. 1970, 10, 354–357. [Google Scholar] [CrossRef]
- Schwer, J.F.; Cleveland, R.W. Tetraploid and triploid interspecific hybrids of Trifolium pratense L., T. diffusum Ehrh, and some related species. Crop Sci. 1972, 12, 321–324. [Google Scholar] [CrossRef]
- Merker, A. Amphidiploids between Trifolium alpestre and Trifolium pratense. Hereditas 1988, 108, 267–267. [Google Scholar] [CrossRef]
- Phillips, G.C.; Grosser, J.W.; Berger, S.; Taylor, N.L.; Collins, G.B. Interspecific hybridization between red clover and Trifolium alpestre using in vitro embryo rescue. Crop Sci. 1992, 32, 1113–1115. [Google Scholar] [CrossRef]
- Phillips, G.C.; Collins, G.B.; Taylor, N.L. Interspecific hybridization of red clover (Trifolium pratense L.) with Trifolium sarosiense Hazsl. using in vitro embryo rescue. Theor. Appl. Genet. 1982, 62, 17–24. [Google Scholar]
- Merker, A. Hybrids between Trifolium medium and Trifolium pratense. Hereditas 1984, 101, 267–268. [Google Scholar]
- Sawai, A.; Ueda, S.; Gau, M.; Uchiyama, K. Interspecific hybrids of Trifolium medium L. × 4x T. pratense L. obtained through embryo culture. Nippon Sochi Gakkaishi J. Jpn. Soc. Grassl. Sci. 1990, 35, 267–272. [Google Scholar]
- Repkova, J.; Nedbalkova, B.; Holub, J. Regeneration of plants from zygotic embryos after interspecific hybridization within the genus Trifolium and electrophoretic evaluation of hybrids. In Scientific Studies—OSEVA Research Institute for Fodder Plants, OSEVA Breeding Institute for Fodder Plants; Research Institute for Fodder Plants: Troubsko, Czech Republic, 1991; Volume 12, pp. 7–14. [Google Scholar]
- Sawai, A.; Yamaguchi, H.; Uchiyama, K. Fertility and morphology of the chromosome-doubled hybrid T. medium × T. pratense (red clover) and backcross progeny. Nippon Sochi Gakkaishi J. Jpn. Soc. Grassl. Sci. 1995, 41, 122–127. [Google Scholar]
- Isobe, S.; Sawai, A.; Yamaguchi, H.; Gau, M.; Uchiyama, K. Breeding potential of the backcross progenies of a hybrid between Trifolium medium × T. pratense to T. pratense. Can. J. Plant Sci. 2002, 82, 395–399. [Google Scholar]
- Katznelson, J. Interspecific hybridization in Trifolium. Crop Sci. 1967, 7, 307–310. [Google Scholar]
- Putiyevsky, E.; Katznelson, J. Cytogenetic studies in Trifolium spp. related to berseem. Theor. Appl. Genet. 1973, 43, 351–358. [Google Scholar]
- Selim, A.K.A.; Abdel-Tawab, F.M.; Fahmy, E.M. Phylogenetic relationships in genus Trifolium L. Egypt. J. Genet. Cytol. 1977, 6, 274–283. [Google Scholar]
- Malaviya, D.R.; Roy, A.K.; Kaushal, P.; Kumar, B.; Tiwari, A. Development and characterization of interspecific hybrids of Trifolium alexandrinum × T. apertum using embryo rescue. Plant Breed. 2004, 123, 536–542. [Google Scholar]
- Roy, A.K.; Malaviya, D.R.; Kaushal, P.; Kumar, B.; Tiwari, A. Interspecific hybridization of Trifolium alexandrinum with T. constantinopolitanum using embryo rescue. Plant Cell Rep. 2004, 22, 705–710. [Google Scholar]
- Kaushal, P.; Malaviya, D.R.; Roy, A.K.; Kumar, B.; Tiwari, A. Trifolium alexandrinum × T. resupinatum—Interspecific hybrids developed through embryo rescue. Plant Cell Tiss. Org. Cult. 2005, 83, 137–144. [Google Scholar]
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Ravagnani, A.; Abberton, M.T.; Skøt, L. Development of Genomic Resources in the Species of Trifolium L. and Its Application in Forage Legume Breeding. Agronomy 2012, 2, 116-131. https://doi.org/10.3390/agronomy2020116
Ravagnani A, Abberton MT, Skøt L. Development of Genomic Resources in the Species of Trifolium L. and Its Application in Forage Legume Breeding. Agronomy. 2012; 2(2):116-131. https://doi.org/10.3390/agronomy2020116
Chicago/Turabian StyleRavagnani, Adriana, Michael T. Abberton, and Leif Skøt. 2012. "Development of Genomic Resources in the Species of Trifolium L. and Its Application in Forage Legume Breeding" Agronomy 2, no. 2: 116-131. https://doi.org/10.3390/agronomy2020116
APA StyleRavagnani, A., Abberton, M. T., & Skøt, L. (2012). Development of Genomic Resources in the Species of Trifolium L. and Its Application in Forage Legume Breeding. Agronomy, 2(2), 116-131. https://doi.org/10.3390/agronomy2020116