Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Crop and Pasture Science Crop and Pasture Science Society
Plant sciences, sustainable farming systems and food quality
RESEARCH ARTICLE

Transgenic technologies for enhanced molecular breeding of white clover (Trifolium repens L.)

J. W. Forster A B C D , S. Panter A B D , A. Mouradov A B C E , J. Mason A B C and G. C. Spangenberg A B C F
+ Author Affiliations
- Author Affiliations

A Department of Primary Industries, Biosciences Research Division, AgriBio, The Centre for AgriBioscience, 5 Ring Road, Bundoora, Vic. 3083, Australia.

B Dairy Futures Cooperative Research Centre, AgriBio, The Centre for AgriBioscience, 5 Ring Road, Bundoora, Vic. 3083, Australia.

C La Trobe University, Bundoora, Vic. 3086, Australia.

D These authors contributed equally to this review.

E Present address: School of Applied Sciences, RMIT University, Bundoora West Campus, PO Box 71, Bundoora, Vic. 3083, Australia.

F Corresponding author. Email: german.spangenberg@dpi.vic.gov.au

This paper is part of the Legume Research Special Issue (Volume 63, Issues 8&9).

Crop and Pasture Science 64(1) 26-38 https://doi.org/10.1071/CP12184
Submitted: 30 April 2012  Accepted: 22 February 2013   Published: 15 April 2013

Abstract

White clover is an important pasture legume of temperate regions, generally through co-cultivation with a pasture grass in a mixed-sward setting. White clover provides herbage with high nutritional quality to grazing animals, along with the environmental benefit of biological nitrogen fixation. Several key agronomic traits are amenable to modification in white clover through use of transgenic technology. Efficient methods for Agrobacterium-mediated transformation of white clover have been developed. The current status of transgenic research is reviewed for the following traits: resistance to viruses and insect pests; aluminium tolerance and phosphorus acquisition efficiency; control of leaf senescence and seed yield; biosynthesis of flavonoids and rumen bypass proteins for bloat safety and enhanced ruminant nutrition; cyanogenesis; and drought tolerance. Future prospects for transgenic technology in molecular breeding in white clover are also discussed.

Additional keywords: aluminium toxicity, flavonoid, pasture legume, senescence, transformation, virus.


References

Abeynayake S, Panter S, Chapman R, Webster T, Mouradov A, Spangenberg G (2007a) Molecular dissection of flavonoid pathways in developing flowers of white clover (Trifolium repens L.) using CombiMatrix oligonucleotide array expression analysis. In ‘Proceedings of the Fifth International Symposium on the Molecular Breeding of Forage and Turf’. Sapporo, Japan, 1–6 July 2007. (Eds T Yamada, G Spangenberg) p. 61. (Springer: New York)

Abeynayake S, Panter S, Simmonds J, Winkworth A, Rochfort S, Mouradov A, Spangenberg G (2007b) The molecular basis for proanthocyanidin biosynthesis in white clover plants (Trifolium repens L.). In ‘Proceedings of the Fifth International Symposium on the Molecular Breeding of Forage and Turf’. Sapporo, Japan, 1–6 July 2007. (Eds T Yamada, G Spangenberg) p. 63. (Springer: New York)

Abeynayake S, Panter S, Rochfort S, Drayton M, Hand M, Cogan N, Forster JW, Mouradov A, Spangenberg GC (2010a) Spatio-temporal profile of proanthocyanidin biosynthesis in white clover (Trifolium repens L.). In ‘Proceedings of the Sixth International Symposium on the Molecular Breeding of Forage and Turf’. Buenos Aires, Argentina, 15–19 March 2010. (Ed. Raul Rios) p. 207. (Ediciones INTA: Buenos Aires, Argentina)

Abeynayake S, Panter S, Rochfort S, Mouradov A, Spangenberg G (2010b) Cross-talk within the flavonoid pathway in white clover (Trifolium repens L.) flowers. In ‘Proceedings of the Sixth International Symposium on the Molecular Breeding of Forage and Turf’. Buenos Aires, Argentina, 15–19 March 2010. (Ed. Raul Rios) p. 208. (Ediciones INTA: Buenos Aires, Argentina)

Abeynayake SW, Panter S, Chapman R, Webster T, Rochfort S, Mouradov A, Spangenberg G (2012) Biosynthesis of proanthocyanidins in white clover flowers: cross talk within the flavonoid pathway. Plant Physiology 158, 666–678.
Biosynthesis of proanthocyanidins in white clover flowers: cross talk within the flavonoid pathway.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XltVOkt7c%3D&md5=567d0614e2ad16e3e024459784713512CAS | 22167119PubMed |

Abogadallah GM, Nada RM, Malinowski R, Quick P (2011) Overexpression of HARDY, an AP2/ERF gene from Arabidopsis, improves drought and salt tolerance by reducing transpiration and sodium uptake in transgenic Trifolium alexandrinum L. Planta 233, 1265–1276.
Overexpression of HARDY, an AP2/ERF gene from Arabidopsis, improves drought and salt tolerance by reducing transpiration and sodium uptake in transgenic Trifolium alexandrinum L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmsFGgtb0%3D&md5=11592f936f136d577c01d3b100ec7343CAS | 21340699PubMed |

Almeida JR, D’Amico E, Preuss A, Carbone F, de Vos CH, Deiml B, Mourgues F, Perrotta G, Fischer TC, Bovy AG, Martens S, Rosati C (2007) Characterization of major enzymes and genes involved in flavonoid and proanthocyanidin biosynthesis during fruit development in strawberry (Fragaria × ananassa). Archives of Biochemistry and Biophysics 465, 61–71.
Characterization of major enzymes and genes involved in flavonoid and proanthocyanidin biosynthesis during fruit development in strawberry (Fragaria × ananassa).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpsFGhu78%3D&md5=eb481bf43e50bb9264e2d6ae71f80167CAS | 17573033PubMed |

Atwood SS (1940) Genetics of cross-incompatibility among self-incompatible plants of Trifolium repens. Journal - American Society of Agronomy 32, 955–968.
Genetics of cross-incompatibility among self-incompatible plants of Trifolium repens.Crossref | GoogleScholarGoogle Scholar |

Atwood SS (1941) Controlled self- and cross-pollination of Trifolium repens. Journal - American Society of Agronomy 33, 538–545.
Controlled self- and cross-pollination of Trifolium repens.Crossref | GoogleScholarGoogle Scholar |

Atwood SS (1942) Oppositional alleles causing self-incompatibility in Trifolium repens. Genetics 27, 333–338.

Barnett OW, Gibson PB (1975) Identification and prevalence of white clover viruses and the resistance of Trifolium species to these viruses. Crop Science 15, 32–37.
Identification and prevalence of white clover viruses and the resistance of Trifolium species to these viruses.Crossref | GoogleScholarGoogle Scholar |

Barrett B, Griffiths A, Schreiber M, Ellison N, Mercer C, Bouton J, Ong B, Forster J, Sawbridge T, Spangenberg G, Bryan G, Woodfield D (2004) A microsatellite map of white clover (Trifolium repens L.). Theoretical and Applied Genetics 109, 596–608.
A microsatellite map of white clover (Trifolium repens L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmt1Krsr8%3D&md5=0c8e0d8921fa953103c83c3bfe35b5faCAS | 15103407PubMed |

Barrett BA, Baird IJ, Woodfield DR (2005) A QTL analysis of white clover seed production. Crop Science 45, 1844–1850.
A QTL analysis of white clover seed production.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVOrt7bM&md5=018cb4c38531759c417c38f1739f5c6aCAS |

Beck DL, van Dolleweerd CJ, Dudas B, Wite DWR, Forster RLS (1993) Coat protein-mediated protection against White clover mosaic virus and Potato virus X in tobacco. In ‘Proceedings of the XVII International Grasslands Conference’. Palmerston North, New Zealand. (Ed. MJ Baker) pp. 1173–1175. (New Zealand Grassland Association: Palmerston North, New Zealand)

Beck DL, van Dolleweerd CJ, Lough TJ, Balmori E, Voot DM, Anderson MT, O’Brien IEW, Forster RLS (1994) Disruption of virus movement confers broad spectrum resistance against systemic infection by plant viruses with a triple gene block. Proceedings of the National Academy of Sciences of the United States of America 91, 10310–10314.
Disruption of virus movement confers broad spectrum resistance against systemic infection by plant viruses with a triple gene block.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXmslKrurc%3D&md5=f7bccb21a3a3f79cb6de98c949f7526aCAS | 7937946PubMed |

Bogs J, Downey MO, Harvey JS, Ashton AR, Tanner GJ, Robinson SP (2005) Proanthocyanidin synthesis and expression of genes encoding leucoanthocyanidin reductase and anthocyanidin reductase in developing grape berries and grapevine leaves. Plant Physiology 139, 652–663.
Proanthocyanidin synthesis and expression of genes encoding leucoanthocyanidin reductase and anthocyanidin reductase in developing grape berries and grapevine leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFCgsLfP&md5=9510c040576323a63879b78123c2ff58CAS | 16169968PubMed |

Borevitz JO, Xia Y, Blount J, Dixon RA, Lamb C (2000) Activation tagging identifies a conserved MYB regulator of phenylpropanoid biosynthesis. The Plant Cell 12, 2383–2393.

Cai CQ, Doyon Y, Ainley WM, Miller JC, DeKelver RC, Moehle EA, Rock JM, Lee Y-H, Garrison R, Schulenberg L, Blue R, Worden A, Baker L, Faraji F, Zhang L, Holmes MC, Rebar EJ, Collingwood TN, Rubin-Wilson B, Gregory PD, Urnov FD, Petolino JF (2009) Targeted transgene integration in plant cells using designed zinc finger nucleases. Plant Molecular Biology 69, 699–709.
Targeted transgene integration in plant cells using designed zinc finger nucleases.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXis1artLo%3D&md5=41d494e241a0ad7785cd0d9d48cf4ceeCAS | 1:CAS:528:DC%2BD1MXis1artLo%3D&md5=41d494e241a0ad7785cd0d9d48cf4ceeCAS | 19112554PubMed |

Carlsen SCK, Fomsgaard IS (2008) Biologically active secondary metabolites in white clover (Trifolium repens L.) – a review focusing on contents in the plant, plant-pest interactions and transformation. Chemoecology 18, 129–170.
Biologically active secondary metabolites in white clover (Trifolium repens L.) – a review focusing on contents in the plant, plant-pest interactions and transformation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtF2qsr7J&md5=13df9c7a33107a2973d985b63e062f00CAS | 1:CAS:528:DC%2BD1cXhtF2qsr7J&md5=13df9c7a33107a2973d985b63e062f00CAS |

Carroll D (2008) Progress and prospects: zinc-finger nucleases as gene therapy agents. Gene Therapy 15, 1463–1468.
Progress and prospects: zinc-finger nucleases as gene therapy agents.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlais7rF&md5=7673ca332d62a3a3042ff71f92ec3d96CAS | 1:CAS:528:DC%2BD1cXhtlais7rF&md5=7673ca332d62a3a3042ff71f92ec3d96CAS | 18784746PubMed |

Christiansen P, Gibson JM, Moore A, Pedersen C, Tabe L, Larkin PJ (2000) Transgenic Trifolium repens with foliage accumulating the high sulphur protein, sunflower seed albumin. Transgenic Research 9, 103–113.
Transgenic Trifolium repens with foliage accumulating the high sulphur protein, sunflower seed albumin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlvVequ7Y%3D&md5=55d0f75199585a20a7dfd9241ea5e520CAS | 10951694PubMed |

Chu P, Zhao G, Spangenberg GC (2005) Molecular breeding of white clover for transgenic resistance to Alfalfa mosaic virus and natural resistance to Clover yellow vein virus. In ‘Proceedings of the Fourth International Symposium on the Molecular Breeding of Forage and Turf’. Aberystwyth, Wales, UK, July 2005. (Ed. MO Humphreys) p. 224. (Wageningen Academic Publishers: Wageningen)

Cogan NOI, Abberton MT, Smith KF, Kearney G, Marshall AH, Williams A, Michaelson-Yeates TPT, Bowen C, Jones ES, Vecchies AC, Forster JW (2006) Individual and multi-environment combined analyses identify QTLs for morphogenetic and reproductive development traits in white clover (Trifolium repens L.). Theoretical and Applied Genetics 112, 1401–1415.
Individual and multi-environment combined analyses identify QTLs for morphogenetic and reproductive development traits in white clover (Trifolium repens L.).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD283ntVamsw%3D%3D&md5=141a912dc2699c38e4684567329d6e33CAS | 1:STN:280:DC%2BD283ntVamsw%3D%3D&md5=141a912dc2699c38e4684567329d6e33CAS |

Daley M, Knauf VC, Summerfelt KR, Turner JC (1998) Co-transformation with one Agrobacterium tumefaciens strain containing two binary plasmids as a method for producing marker free transgenic plants. Plant Cell Reports 17, 489–496.
Co-transformation with one Agrobacterium tumefaciens strain containing two binary plasmids as a method for producing marker free transgenic plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXisFWkt7s%3D&md5=19b2ee3d24dd345cbed31ef4ff487c7fCAS | 1:CAS:528:DyaK1cXisFWkt7s%3D&md5=19b2ee3d24dd345cbed31ef4ff487c7fCAS |

De Block M, Debrouwer D (1991) Two T-DNAs co-transformed into Brassica napus by a double Agrobacterium tumefaciens infection are rarely integrated at the same locus. Theoretical and Applied Genetics 82, 257–263.
Two T-DNAs co-transformed into Brassica napus by a double Agrobacterium tumefaciens infection are rarely integrated at the same locus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XhtVShu7s%3D&md5=a7594be9d5e1fa76069f5917729231ccCAS | 1:CAS:528:DyaK38XhtVShu7s%3D&md5=a7594be9d5e1fa76069f5917729231ccCAS |

De Lucas JA, Rochfort S, Panter S, Smith KF, Mouradov A, Spangenberg GC (2010) Biosafety studies for the release of Alfalfa mosaic virus resistant transgenic white clover (Trifolium repens L.). In ‘Proceedings of the Sixth International Symposium on the Molecular Breeding of Forage and Turf’. Buenos Aires, Argentina, 15–19 March 2010. (Ed. Raul Rios) p. 234. (Ediciones INTA: Buenos Aires, Argentina)

De Lucas JA, Forster JW, Smith KF, Spangenberg GC (2012) Assessment of gene flow in white clover (Trifolium repens L.) under field conditions in Australia using phenotypic and genetic markers. Crop & Pasture Science 63, 155–163.
Assessment of gene flow in white clover (Trifolium repens L.) under field conditions in Australia using phenotypic and genetic markers.Crossref | GoogleScholarGoogle Scholar |

De Neve M, DeBuck S, Jacobs A, Van Montagu M, Depicker A (1997) T-DNA integration patterns in co-transformed plant cells suggest that T-DNA repeats originate from co-integration of separate T-DNAs. The Plant Journal 11, 15–29.
T-DNA integration patterns in co-transformed plant cells suggest that T-DNA repeats originate from co-integration of separate T-DNAs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXhtFGjs7Y%3D&md5=8000229815b183c2ec9c6efd14c488e4CAS | 1:CAS:528:DyaK2sXhtFGjs7Y%3D&md5=8000229815b183c2ec9c6efd14c488e4CAS | 9025300PubMed |

Delhaize E, Ryan PR, Hebb DM, Yamamoto Y, Sasaki T, Matsumoto H (2004) Engineering high-level aluminum tolerance in barley with the ALMT1 gene. Proceedings of the National Academy of Sciences of the United States of America 101, 15249–15254.
Engineering high-level aluminum tolerance in barley with the ALMT1 gene.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXpsVSgurc%3D&md5=f67e0eadd50b2bc9434449d9e015f113CAS | 1:CAS:528:DC%2BD2cXpsVSgurc%3D&md5=f67e0eadd50b2bc9434449d9e015f113CAS | 15471989PubMed |

Ding Y-L, Aldao-Humble G, Ludlow E, Drayton M, Lin Y-H, Nagel J, Dupal M, Zhao G, Pallaghy C, Kalla R, Emmerling M, Spangenberg G (2003) Efficient plant regeneration and Agrobacterium-mediated transformation in Medicago and Trifolium species. Plant Science 165, 1419–1427.
Efficient plant regeneration and Agrobacterium-mediated transformation in Medicago and Trifolium species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXos1Knu74%3D&md5=cacc69bc12d0274db146d4a6833dd0f6CAS | 1:CAS:528:DC%2BD3sXos1Knu74%3D&md5=cacc69bc12d0274db146d4a6833dd0f6CAS |

Doyle JJ, Luckow MA (2003) The rest of the iceberg. Legume diversity and evolution in a phylogenetic context. Plant Physiology 131, 900–910.
The rest of the iceberg. Legume diversity and evolution in a phylogenetic context.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXisFemtbo%3D&md5=bd208894125794995a9e6551b24110b5CAS | 1:CAS:528:DC%2BD3sXisFemtbo%3D&md5=bd208894125794995a9e6551b24110b5CAS | 12644643PubMed |

Dudas B, Woodfield DR, Tong PM, Nicholls MF, Cousins GR, Burgess R, White DWR, Beck DL, Forster TJ, Lough RLS (1998) Estimating the agronomic impact of White clover mosaic virus on white clover performance in the North Island of New Zealand. New Zealand Journal of Agricultural Research 41, 171–178.
Estimating the agronomic impact of White clover mosaic virus on white clover performance in the North Island of New Zealand.Crossref | GoogleScholarGoogle Scholar |

Ealing PM, Hancock KR, White DWR (1994) Expression of the pea albumin 1 gene in transgenic white clover and tobacco. Transgenic Research 3, 344–354.
Expression of the pea albumin 1 gene in transgenic white clover and tobacco.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXitlygt7g%3D&md5=529cf17720204cb4556e358adb390ce3CAS | 1:CAS:528:DyaK2MXitlygt7g%3D&md5=529cf17720204cb4556e358adb390ce3CAS | 8000431PubMed |

Ellison NW, Liston A, Steiner JJ, Williams WM, Taylor NL (2006) Molecular phylogenetics of the clover genus (Trifolium – Leguminosae). Molecular Phylogenetics and Evolution 39, 688–705.
Molecular phylogenetics of the clover genus (Trifolium – Leguminosae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XkslSlt74%3D&md5=a1be2f664949f3f592213b6d58303d77CAS | 1:CAS:528:DC%2BD28XkslSlt74%3D&md5=a1be2f664949f3f592213b6d58303d77CAS | 16483799PubMed |

Emmerling M, Chu P, Smith K, Kalla R, Spangenberg G (2004) Field evaluation of transgenic white clover with AMV immunity and development of elite transgenic germplasm. In ‘Molecular breeding of forage and turf’. (Eds A Hopkins, Z-Y Wang, R Mian, M Sledge, RE Barker) pp. 359–366. (Kluwer Academic Publishers: Dordrecht, The Netherlands)

Emmerling M, Chu P, Smith KF, Binnion C, Ponnampalam M, Measham P, Lin ZY, Bannan N, Wilkinson T, Spangenberg GC (2005) Molecular breeding of transgenic virus-immune white clover (Trifolium repens) cultivars. In ‘Proceedings of the Fourth International Symposium on the Molecular Breeding of Forage and Turf’. Aberystwyth, Wales, UK, July 2005. (Ed. MO Humphreys) p. 225. (Wageningen Academic Publishers: Wageningen)

Foo LY, Lu Y, Molan AL, Woodfield DR, McNabb WC (2000) The phenols and prodelphinidins of white clover flowers. Phytochemistry 54, 539–548.
The phenols and prodelphinidins of white clover flowers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXltlWntrw%3D&md5=40fa7602a79fc6af68e1626009091249CAS | 1:CAS:528:DC%2BD3cXltlWntrw%3D&md5=40fa7602a79fc6af68e1626009091249CAS | 10939359PubMed |

Forster RLS, Bevan MW, Harbison SA, Gardner RC (1988) The complete nucleotide sequence of the potexvirus White clover mosaic virus. Nucleic Acids Research 16, 291–303.
The complete nucleotide sequence of the potexvirus White clover mosaic virus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXktVWmsb8%3D&md5=46924c5bb67dfa26a20fba4ae257b34fCAS | 1:CAS:528:DyaL1cXktVWmsb8%3D&md5=46924c5bb67dfa26a20fba4ae257b34fCAS |

Franzmayr BK, Rasmussen S, Fraser KM, Jameson PE (2012) Expression and functional characterization of a white clover isoflavone synthase in tobacco. Annals of Botany 110, 1291–1301.
Expression and functional characterization of a white clover isoflavone synthase in tobacco.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhs1Sru77I&md5=8fa23514bbee7cc6b1897710eb0ee6a4CAS | 1:CAS:528:DC%2BC38Xhs1Sru77I&md5=8fa23514bbee7cc6b1897710eb0ee6a4CAS | 22915577PubMed |

Gan S, Amasino RM (1995) Inhibition of leaf senescence by autoregulated production of cytokinin. Science 270, 1986–1988.
Inhibition of leaf senescence by autoregulated production of cytokinin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xlt12q&md5=988ac5619a6d817250b58cd5b374037cCAS | 1:CAS:528:DyaK28Xlt12q&md5=988ac5619a6d817250b58cd5b374037cCAS | 8592746PubMed |

Gibson PB, Barnett OW, Skipper HD, McLaughlin MR (1981) Effects of 3 viruses on growth of white clover. Plant Disease 65, 50–51.
Effects of 3 viruses on growth of white clover.Crossref | GoogleScholarGoogle Scholar |

Hackland AF, Rybicki EP, Thomson JA (1994) Coat protein-mediated resistance in transgenic plants. Archives of Virology 139, 1–22.
Coat protein-mediated resistance in transgenic plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXjslWjtLs%3D&md5=9b2286129026e350b4fbec49c79c8865CAS | 1:CAS:528:DyaK2MXjslWjtLs%3D&md5=9b2286129026e350b4fbec49c79c8865CAS | 7826203PubMed |

Hancock KR, Collette V, Fraser K, Grieg M, Xue H, Richardson K, Rasmussen S (2012) Expression of the R2R3-MYB transcription factor TaMYB14 from Trifolium arvense activates proanthocyanidin biosynthesis in the legumes Trifolium repens and Medicago sativa. Plant Physiology 159, 1204–1220.
Expression of the R2R3-MYB transcription factor TaMYB14 from Trifolium arvense activates proanthocyanidin biosynthesis in the legumes Trifolium repens and Medicago sativa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVGlsbnN&md5=fd61f6cddd6d4e54582cda4e7f02599cCAS | 1:CAS:528:DC%2BC38XhtVGlsbnN&md5=fd61f6cddd6d4e54582cda4e7f02599cCAS | 22566493PubMed |

Hand ML, Ponting RC, Drayton MC, Lawless KA, Cogan NOI, Brummer EC, Sawbridge TI, Spangenberg GC, Smith KF, Forster JW (2008) Identification of homologous, homoeologous and paralogous sequence variants in an outbreeding allopolyploid species based on comparison with progenitor taxa. Molecular Genetics and Genomics 280, 293–304.
Identification of homologous, homoeologous and paralogous sequence variants in an outbreeding allopolyploid species based on comparison with progenitor taxa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVGltbfP&md5=63f3b2b472eea0ad4a2477ec5fd20d45CAS | 1:CAS:528:DC%2BD1cXhtVGltbfP&md5=63f3b2b472eea0ad4a2477ec5fd20d45CAS | 18642031PubMed |

Hand ML, Cogan NOI, Sawbridge TI, Spangenberg GC, Forster JW (2010) Comparison of homoeolocus organisation in paired BAC clones from allotetraploid white clover (Trifolium repens L.) and microcolinearity with model legume species. BMC Plant Biology 10, 94
Comparison of homoeolocus organisation in paired BAC clones from allotetraploid white clover (Trifolium repens L.) and microcolinearity with model legume species.Crossref | GoogleScholarGoogle Scholar | 20492736PubMed |

Hughes MA (1991) The cyanogenic polymorphism in Trifolium repens L. Heredity 66, 105–115.
The cyanogenic polymorphism in Trifolium repens L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXkvV2jt7o%3D&md5=f044cea81fa3b393b3f2a878aaed7bccCAS | 1:CAS:528:DyaK3MXkvV2jt7o%3D&md5=f044cea81fa3b393b3f2a878aaed7bccCAS |

Jiang QZ, Zhang JY, Guo XL, Bedair M, Sumner L, Bouton J, Wang ZY (2010) Improvement of drought tolerance in white clover (Trifolium repens) by transgenic expression of a transcription factor gene WXP1. Functional Plant Biology 37, 157–165.
Improvement of drought tolerance in white clover (Trifolium repens) by transgenic expression of a transcription factor gene WXP1.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlyhsrY%3D&md5=e964a39c1338f6b23346b4202cc66b95CAS | 1:CAS:528:DC%2BC3cXhtlyhsrY%3D&md5=e964a39c1338f6b23346b4202cc66b95CAS |

Jones ES, Hughes LJ, Drayton MC, Abberton MT, Michaelson-Yeates TPT, Bowen C, Forster JW (2003) An SSR and AFLP molecular marker-based genetic map of white clover (Trifolium repens L.). Plant Science 165, 531–539.
An SSR and AFLP molecular marker-based genetic map of white clover (Trifolium repens L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlvVSktLc%3D&md5=1d91d10468b56eb578c3f1409aae5a2eCAS | 1:CAS:528:DC%2BD3sXlvVSktLc%3D&md5=1d91d10468b56eb578c3f1409aae5a2eCAS |

Kakes P (1985) Linamarase and other β-glucosidases are present in the cell wall of Trifolium repens L. leaves. Planta 166, 156–160.
Linamarase and other β-glucosidases are present in the cell wall of Trifolium repens L. leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXmtFWhs70%3D&md5=177ec2d356adf58603eb97ac132b2934CAS | 1:CAS:528:DyaL2MXmtFWhs70%3D&md5=177ec2d356adf58603eb97ac132b2934CAS |

Kalla R, Chu P, Spangenberg G (2001) Molecular breeding of forage legumes for virus resistance. In ‘Molecular breeding of forage crops’. (Ed. G Spangenberg) pp. 219–237. (Kluwer Academic Press: Dordrecht, The Netherlands)

Kim S, Kim J-S (2011) Targeted genome engineering via zinc finger nucleases. Plant Biotechnology Reporter 5, 9–17.
Targeted genome engineering via zinc finger nucleases.Crossref | GoogleScholarGoogle Scholar |

Kölliker R, Jones ES, Drayton MC, Dupal MP, Forster JW (2001) Development and characterisation of simple sequence repeat (SSR) markers for white clover (Trifolium repens L.). Theoretical and Applied Genetics 102, 416–424.
Development and characterisation of simple sequence repeat (SSR) markers for white clover (Trifolium repens L.).Crossref | GoogleScholarGoogle Scholar |

Komari T, Hiei Y, Saito Y, Murai N, Kumashiro T (1996) Vectors carrying two separate T-DNAs for co-transformation of higher plants mediated by Agrobacterium tumefaciens and segregation of transformants free from selection markers. The Plant Journal 10, 165–174.
Vectors carrying two separate T-DNAs for co-transformation of higher plants mediated by Agrobacterium tumefaciens and segregation of transformants free from selection markers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XltVamtrk%3D&md5=6b2a5c77288eb4c0f1ef23e08d52e90cCAS | 1:CAS:528:DyaK28XltVamtrk%3D&md5=6b2a5c77288eb4c0f1ef23e08d52e90cCAS | 8758986PubMed |

Labandera M (2007) Development and evaluation of transgenic white clover (Trifolium repens) for enhanced aluminium tolerance and phosphorus acquisition efficiency. PhD Thesis, Department of Botany, La Trobe University, Bundoora, Vic., Australia.

Labandera CM, Lin YH, Ludlow E, Emmerling M, John U, Sale PW, Pallaghy C, Spangenberg GC (2005) Discovery, isolation and characterisation of promoters in white clover (Trifolium repens L.). In ‘Proceedings of the Fourth International Symposium on the Molecular Breeding of Forage and Turf’. Aberystwyth, Wales, UK, July 2005. (Ed. MO Humphreys) p. 168. (Wageningen Academic Publishers: Wageningen)

Labandera M, Panter S, Winkworth A, Simmonds J, Sale P, John U, Mouradov A, Spangenberg G (2007) Transgenic white clover (Trifolium repens L.) plants with modified organic acid metabolism for aluminium tolerance and phosphorus acquisition efficiency. In ‘Proceedings of the Fifth International Symposium on the Molecular Breeding of Forage and Turf’. Sapporo, Japan, 1–6 July 2007. (Eds T Yamada, G Spangenberg) p. 102. (Springer: New York)

Laidlaw AS, Teuber N (2001). Temperate forage grass-legume mixtures: advances and perspectives. In ‘Proceedings of the XIX International Grassland Congress’. (Eds JA Gomide, WRS Soares, SC da Silva) 11–21 February 2001, Sao Paulo, Brazil. pp. 85–92. (Brazilian Society of Animal Husbandry: Piracicaba, Brazil)

Larkin PJ, Gibson JM, Mathesius U, Weinman JJ, Gartner E, Hall E, Tanner GJ, Rolfe BG, Djordjevic MA (1996) Transgenic white clover. Studies with the auxin-responsive promoter, GH3, in root gravitropism and lateral root development. Transgenic Research 5, 325–335.
Transgenic white clover. Studies with the auxin-responsive promoter, GH3, in root gravitropism and lateral root development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xmt1Wlt7s%3D&md5=e3feecffb18b32a6ac7c2e799eb723dcCAS | 1:CAS:528:DyaK28Xmt1Wlt7s%3D&md5=e3feecffb18b32a6ac7c2e799eb723dcCAS | 11539555PubMed |

Latch GCM, Skipp RA (1987) Diseases. In ‘White clover’. (Eds MJ Baker, WM Williams) pp. 421–446. (CAB International: Wallingford-Oxon, UK)

Li M, Osaki M, Rao IM, Tadano T (1997) Secretion of phytase from the roots of several plant species under phosphorus-deficient conditions. Plant and Soil 195, 161–169.
Secretion of phytase from the roots of several plant species under phosphorus-deficient conditions.Crossref | GoogleScholarGoogle Scholar |

Lin Y-H, Chalmers J, Ludlow E, Pallaghy C, Schrauf G, Rush P, Garcia AM, Mouradov A, Spangenberg GC (2005) LXR™ white clover: development of transgenic white clover (Trifolium repens) with delayed leaf senescence. In ‘Proceedings of the Fourth International Symposium on the Molecular Breeding of Forage and Turf’. Aberystwyth, Wales, UK, July 2005. (Ed. MO Humphreys) p. 229. (Wageningen Academic Publishers: Wageningen)

Lin Y-H, Chalmers J, Ludlow E, Pallaghy C, Schrauf G, Rush P, Garcia A, Panter S, Mouradov A, Garcia J, Spangenberg G (2007) Generation and field-evaluation of LXR™ white clover (Trifolium repens L.) plants with delayed leaf senescence for enhanced seed and herbage yield. In ‘Proceedings of the Fifth International Symposium on the Molecular Breeding of Forage and Turf’. Sapporo, Japan, 1–6 July 2007. (Eds T Yamada, G Spangenberg) p. 66. (Springer: New York)

Lin Y-H, Ludlow EJ, Schrauf G, Rush P, Iannicelli M, Garcia A, Garcia J, Panter S, Mouradov A, Spangenberg GC (2010) LXR™ transgenic white clover plants (Trifolium repens L.) with delayed leaf senescence, increased seed yield and improved stress tolerance. In ‘Proceedings of the Sixth International Symposium on the Molecular Breeding of Forage and Turf’. Buenos Aires, Argentina, 15–19 March 2010. (Ed. Raul Rios) p. 216. (Ediciones INTA: Buenos Aires, Argentina)

Ludlow EJ (2006) RNA silencing as a new tool for antiviral defence and functional genomics in white clover (Trifolium repens L.). PhD Thesis, Department of Botany, La Trobe University, Bundoora, Vic., Australia.

Ludlow E, Lin YH, Chalmers Y, Kalla R, Pallaghy C, Spangenberg G (2000) Development of transgenic white clover with delayed leaf senescence. In ‘Abstracts 2nd International Symposium on Molecular Breeding of Forage Crops’. Lorne and Hamilton, Victoria, 2000. (Ed. G Spangenberg) p. 84. (Springer: New York)

Ludlow E, Mouradov A, Spangenberg G (2007) Generation of transgenic white clover (Trifolium repens L.) plants resistant to White clover mosaic virus. In ‘Proceedings of the Fifth International Symposium on the Molecular Breeding of Forage and Turf’. Sapporo, Japan, 1–6 July 2007. (Eds T Yamada, G Spangenberg) p.104. (Springer: New York)

Ludlow EJ, Mouradov A, Spangenberg GC (2009) Post-transcriptional gene silencing as an efficient tool for engineering resistance to White clover mosaic virus in white clover (Trifolium repens L.). Journal of Plant Physiology 166, 1557–1567.
Post-transcriptional gene silencing as an efficient tool for engineering resistance to White clover mosaic virus in white clover (Trifolium repens L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlentbrP&md5=c094bb09d2615a49e7c9f32f9c0952b6CAS | 1:CAS:528:DC%2BD1MXhtlentbrP&md5=c094bb09d2615a49e7c9f32f9c0952b6CAS | 19660828PubMed |

Ma JF, Ryan PR, Delhaize E (2001) Aluminium tolerance in plants and the complexing role of organic acids. Trends in Plant Science 6, 273–278.
Aluminium tolerance in plants and the complexing role of organic acids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlsFyjsL0%3D&md5=6bad4233569f820480aa50f73414e09fCAS | 1:CAS:528:DC%2BD3MXlsFyjsL0%3D&md5=6bad4233569f820480aa50f73414e09fCAS | 11378470PubMed |

Ma X-F, Wright E, Ge Y, Bell J, Xi Y, Bouton JH, Wang Z-Y (2009) Improving phosphorus acquisition of white clover (Trifolium repens L.) by transgenic expression of plant-derived phytase and acid phosphatase genes. Plant Science 176, 479–488.
Improving phosphorus acquisition of white clover (Trifolium repens L.) by transgenic expression of plant-derived phytase and acid phosphatase genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXisFGktb0%3D&md5=6e90fcd06f77bd3bbbc1f40584491f55CAS | 1:CAS:528:DC%2BD1MXisFGktb0%3D&md5=6e90fcd06f77bd3bbbc1f40584491f55CAS |

Mather RDJ, Melhuish DT, Herlihy M (1996) Trends in the global marketing of white clover cultivars. In ‘White clover: New Zealand’s competitive edge’. Grassland Research and Practice Series 6. (Ed. DR Woodfield) pp. 7–14. (New Zealand Grassland Association: Palmerston North, New Zealand)

Mathews H, Clendennen SK, Caldwell CG, Liu XL, Connors K, Matheis N, Schuster DK, Menasco DJ, Wagoner W, Lightner J, Wagner DR (2003) Activation tagging in tomato identifies a transcriptional regulator of anthocyanin biosynthesis, modification, and transport. The Plant Cell 15, 1689–1703.
Activation tagging in tomato identifies a transcriptional regulator of anthocyanin biosynthesis, modification, and transport.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXms1WlsL8%3D&md5=d2edd20919c4685c0bb184b330d748bdCAS | 1:CAS:528:DC%2BD3sXms1WlsL8%3D&md5=d2edd20919c4685c0bb184b330d748bdCAS | 12897245PubMed |

McKnight TD, Lillis MT, Simpson RB (1987) Segregation of genes transferred to one plant cell from two separate Agrobacterium strains. Plant Molecular Biology 8, 439–445.
Segregation of genes transferred to one plant cell from two separate Agrobacterium strains.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXktlCisLc%3D&md5=3c1a439cce17f511a20ce090d805be39CAS | 1:CAS:528:DyaL2sXktlCisLc%3D&md5=3c1a439cce17f511a20ce090d805be39CAS |

Meagher LP, Widdup K, Sivakumaran S, Lucas R, Rumball W (2006) Floral Trifolium proanthocyanidins: polyphenol formation and compositional diversity. Journal of Agricultural and Food Chemistry 54, 5482–5488.
Floral Trifolium proanthocyanidins: polyphenol formation and compositional diversity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xmt1Kht70%3D&md5=74db0edd0bf1f46b166f0e942ba95c25CAS | 16848535PubMed |

Meuwissen THE, Hayes BJ, Goddard ME (2001) Prediction of total genetic value using genome-wide dense marker maps. Genetics 157, 1819–1829.

Mitter N, Dietzgen RG (2012) Use of hairpin RNA constructs for engineering plant virus resistance. Methods in Molecular Biology 894, 191–208.
Use of hairpin RNA constructs for engineering plant virus resistance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhslWktb3J&md5=c4d6596ec0e1a431969d2e21ba653292CAS | 22678581PubMed |

Modolo LV, Li L, Pan H, Blount JW, Dixon RA, Wang X (2009) Crystal structures of glycosyltransferase UGT78G1 reveal the molecular basis for glycosylation and deglycosylation of (iso)flavonoids. Journal of Molecular Biology 392, 1292–1302.
Crystal structures of glycosyltransferase UGT78G1 reveal the molecular basis for glycosylation and deglycosylation of (iso)flavonoids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFKnt7%2FN&md5=edc146afba47a8ecfdd9e21e117ae49dCAS | 19683002PubMed |

Mouradov A, Panter S, Abeynayake S, Simmonds J, Winkworth A, Rochfort S, Chapman R, Webster T, Li X, Vardy M, Spangenberg G (2007) Molecular dissection of proanthocyanidin biosynthesis in white clover (Trifolium repens L.): integration of spatial and temporal information. In ‘Proceedings of the Fifth International Symposium on the Molecular Breeding of Forage and Turf’. Sapporo, Japan, 1–6 July 2007. (Eds T Yamada, G Spangenberg) p. 24. (Springer: New York)

Norton MR, Johnstone GR (1998) Occurrence of Alfalfa mosaic, Clover yellow vein, Subterranean clover red leaf, and White clover mosaic viruses in white clover throughout Australia. Australian Journal of Agricultural Research 49, 723–728.
Occurrence of Alfalfa mosaic, Clover yellow vein, Subterranean clover red leaf, and White clover mosaic viruses in white clover throughout Australia.Crossref | GoogleScholarGoogle Scholar |

Olsen KM, Sutherland BL, Small LL (2007) Molecular evolution of the Li/li chemical defence polymorphism in white clover (Trifolium repens L.). Molecular Ecology 16, 4180–4193.
Molecular evolution of the Li/li chemical defence polymorphism in white clover (Trifolium repens L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1yhtL3N&md5=74126365aac1010df0524b2a9e8837aaCAS | 17784921PubMed |

Olsen KM, Hsu SC, Small LL (2008) Evidence on the molecular basis of the Ac/ac adaptive cyanogenesis polymorphism in white clover (Trifolium repens L.). Genetics 179, 517–526.
Evidence on the molecular basis of the Ac/ac adaptive cyanogenesis polymorphism in white clover (Trifolium repens L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXnsl2qtL8%3D&md5=546154dcb842c1ad65602c2c750d09b0CAS | 18458107PubMed |

Oxtoby E, Dunn MA, Pancoro A, Hughes MA (1991) Nucleotide and derived amino acid sequence of the cyanogenic beta-glucosidase (linamarase) from white clover (Trifolium repens L.). Plant Molecular Biology 17, 209–219.
Nucleotide and derived amino acid sequence of the cyanogenic beta-glucosidase (linamarase) from white clover (Trifolium repens L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38Xkt1Wgsrk%3D&md5=d4d3dc7b74f3681e7aff64144c584ffcCAS | 1907511PubMed |

Pang Y, Peel GJ, Wright E, Wang Z, Dixon RA (2007) Early steps in proanthocyanidin biosynthesis in the model legume Medicago truncatula. Plant Physiology 145, 601–615.
Early steps in proanthocyanidin biosynthesis in the model legume Medicago truncatula.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlemsrvE&md5=b495f08f8dfcc65dbc8e253cce480bd7CAS | 17885080PubMed |

Pang Y, Peel GJ, Sharma SB, Tang Y, Dixon RA (2008) A transcript profiling approach reveals an epicatechin-specific glucosyltransferase expressed in the seed coat of Medicago truncatula. Proceedings of the National Academy of Sciences of the United States of America 105, 14210–14215.
A transcript profiling approach reveals an epicatechin-specific glucosyltransferase expressed in the seed coat of Medicago truncatula.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFKjt73O&md5=3d38bd4aaa7290a8d42eef2a14027022CAS | 18772380PubMed |

Panter SN, Simmonds J, Winkworth A, Mouradov A, Spangenberg GC (2005) Foliar expression of candidate genes involved in condensed tannin biosynthesis in white clover (Trifolium repens). In ‘Proceedings of the Fourth International Symposium on the Molecular Breeding of Forage and Turf’. Aberystwyth, Wales, UK, July 2005. (Ed. MO Humphreys) p. 167. (Wageningen Academic Publishers: Wageningen)

Panter S, Chu PG, Ludlow E, Garrett R, Kalla R, Jahufer MZZ, de Lucas Arbiza A, Rochfort S, Mouradov A, Smith KF, Spangenberg G (2012) Molecular breeding of transgenic white clover (Trifolium repens L.) with field resistance to Alfalfa mosaic virus through the expression of its coat protein gene. Transgenic Research 21, 619–632.
Molecular breeding of transgenic white clover (Trifolium repens L.) with field resistance to Alfalfa mosaic virus through the expression of its coat protein gene.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xms12gtrs%3D&md5=40daf7ccbf58b841f3e838a58f99ae5bCAS | 1:CAS:528:DC%2BC38Xms12gtrs%3D&md5=40daf7ccbf58b841f3e838a58f99ae5bCAS | 21947755PubMed |

Paolocci F, Robbins MP, Madeo L, Arcioni S, Martens S, Damiani F (2006) Ectopic expression of a basic helix-loop-helix gene transactivates parallel pathways of proanthocyanidin biosynthesis: structure, expression analysis, and genetic control of leucoanthocyanidin 4-reductase and anthocyanidin reductase genes in Lotus corniculatus. Plant Physiology 143, 504–516.
Ectopic expression of a basic helix-loop-helix gene transactivates parallel pathways of proanthocyanidin biosynthesis: structure, expression analysis, and genetic control of leucoanthocyanidin 4-reductase and anthocyanidin reductase genes in Lotus corniculatus.Crossref | GoogleScholarGoogle Scholar | 17098849PubMed |

Peel GJ, Pang Y, Modolo LV, Dixon RA (2009) The LAP1 MYB transcription factor orchestrates anthocyanidin biosynthesis and glycosylation in Medicago. The Plant Journal 59, 136–149.
The LAP1 MYB transcription factor orchestrates anthocyanidin biosynthesis and glycosylation in Medicago.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXos1GgtLg%3D&md5=09116f3d37be8c30a30b291663d877baCAS | 19368693PubMed |

Pfeiffer J, Kuhnel C, Brandt J, Duy D, Punyasiri PA, Forkmann G, Fischer TC (2006) Biosynthesis of flavan 3-ols by leucoanthocyanidin 4-reductases and anthocyanidin reductases in leaves of grape (Vitis vinifera L.), apple (Malus × domestica Borkh.) and other crops. Plant Physiology and Biochemistry 44, 323–334.
Biosynthesis of flavan 3-ols by leucoanthocyanidin 4-reductases and anthocyanidin reductases in leaves of grape (Vitis vinifera L.), apple (Malus × domestica Borkh.) and other crops.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xosl2js7k%3D&md5=56f514c2429a027c231931701ad5cddcCAS | 1:CAS:528:DC%2BD28Xosl2js7k%3D&md5=56f514c2429a027c231931701ad5cddcCAS | 16806954PubMed |

Poulton JE (1990) Cyanogenesis in plants. Plant Physiology 94, 401–405.
Cyanogenesis in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXmt1Oqtr0%3D&md5=b540dfbc3f707f9072146d87b42150ffCAS | 1:CAS:528:DyaK3cXmt1Oqtr0%3D&md5=b540dfbc3f707f9072146d87b42150ffCAS | 16667728PubMed |

Prins M, Laimer M, Noris E, Schubert J, Wassenegger M, Tepfer M (2008) Strategies for antiviral resistance in transgenic plants. Molecular Plant Pathology 9, 73–83.

Punyasiri PA, Abeysinghe IS, Kumar V, Treutter D, Duy D, Gosch C, Martens S, Forkmann G, Fischer TC (2004) Flavonoid biosynthesis in the tea plant Camellia sinensis: properties of enzymes of the prominent epicatechin and catechin pathways. Archives of Biochemistry and Biophysics 431, 22–30.
Flavonoid biosynthesis in the tea plant Camellia sinensis: properties of enzymes of the prominent epicatechin and catechin pathways.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXotF2gtLo%3D&md5=5e9c225eb2a9eb804f17e9a52ecf9967CAS | 1:CAS:528:DC%2BD2cXotF2gtLo%3D&md5=5e9c225eb2a9eb804f17e9a52ecf9967CAS | 15464723PubMed |

Robbins MP, Morris P (1999) Metabolic engineering of condensed tannins and other phennolic pathways in forage and fodder crops. In ‘Metabolic engineering of plant secondary metabolism’. (Eds R Verpoorte, AW Alfermann) pp. 165–177. (Kluwer: Dordrecht, The Netherlands)

Rogers GE (1990) Improvement of wool production through genetic engineering. Trends in Biotechnology 8, 6–11.
Improvement of wool production through genetic engineering.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXhtlehtrk%3D&md5=9f9b1991762a74bbd3d293e976e6a350CAS | 1:CAS:528:DyaK3cXhtlehtrk%3D&md5=9f9b1991762a74bbd3d293e976e6a350CAS | 1366571PubMed |

Rommens CM, Humara JM, Ye J, Yan H, Richael C, Zhang L, Perry R, Swords K (2004) Crop improvement through modification of the plant’s own genome. Plant Physiology 135, 421–431.
Crop improvement through modification of the plant’s own genome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXkt12msr4%3D&md5=48a7ada609abc2ad0591b203ea6ec194CAS | 1:CAS:528:DC%2BD2cXkt12msr4%3D&md5=48a7ada609abc2ad0591b203ea6ec194CAS | 15133156PubMed |

Rossello F, Vala B, Ludlow EJ, Panter S, Mouradov A, Spangenberg G (2010) Strategies for transgene stacking in white clover (Trifolium repens L.). In ‘Proceedings of the Sixth International Symposium on the Molecular Breeding of Forage and Turf’. Buenos Aires, Argentina, 15–19 March 2010. (Ed. Raul Rios) p. 238. (Ediciones INTA: Buenos Aires, Argentina)

Rudert CP, Lewis AR (1978) The effect of potassium cyanide on the occurrence of nutritional myopathy in lambs. Rhodesian Journal of Agricultural Research 16, 109–116.

Rudert CP, Oliver J (1976) The effect of thiocyanate on the occurrence of goitre in new-born lambs. Rhodesian Journal of Agricultural Research 14, 67–72.

Saito K, Kobayashi M, Gong ZZ, Tanaka Y, Yamazaki M (1999) Direct evidence for anthocyanidin synthase as a 2-oxoglutarate-dependent oxygenase: molecular cloning and functional expression of cDNA from a red forma of Perilla frutescens. The Plant Journal 17, 181–189.
Direct evidence for anthocyanidin synthase as a 2-oxoglutarate-dependent oxygenase: molecular cloning and functional expression of cDNA from a red forma of Perilla frutescens.Crossref | GoogleScholarGoogle Scholar | 10074715PubMed |

Sasaki T, Yamamoto Y, Ezaki B, Katsuhara M, Ahn SJ, Ryan PR, Delhaize E, Matsumoto H (2004) A wheat gene encoding an aluminum-activated malate transporter. The Plant Journal 37, 645–653.
A wheat gene encoding an aluminum-activated malate transporter.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXislyltr4%3D&md5=c30dacbb7d19b59d716bdbae4ff00475CAS | 14871306PubMed |

Sawbridge T, Ong E-K, Binnion C, Emmerling M, Meath K, Nunan K, O’Neill M, O’Toole F, Simmonds J, Wearne K, Winkworth A, Spangenberg G (2003) Generation and analysis of expressed sequence tags in white clover (Trifolium repens L.). Plant Science 165, 1077–1087.
Generation and analysis of expressed sequence tags in white clover (Trifolium repens L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXnsVagtrc%3D&md5=b2bb6c261dcaee9a968ba24ecdfdc9bfCAS |

Sharma SB, Dixon RA (2005) Metabolic engineering of proanthocyanidins by ectopic expression of transcription factors in Arabidopsis thaliana. The Plant Journal 44, 62–75.
Metabolic engineering of proanthocyanidins by ectopic expression of transcription factors in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFeksrjK&md5=7a7a4747e8b1cbeec5196aaae1fe4463CAS | 16167896PubMed |

Sharma SB, Hancock KR, Ealing PM, White DWR (1998) Expression of a sulfur-rich maize seed storage protein δ-zein, in white clover (Trifolium repens) to improve forage quality. Molecular Breeding 4, 435–448.
Expression of a sulfur-rich maize seed storage protein δ-zein, in white clover (Trifolium repens) to improve forage quality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXntlOmt7c%3D&md5=98658f74baf45ddcc2f231d9265968b5CAS |

Smith KF, Forster JW, Dobrowolski MP, Cogan NOI, Bannan NR, van Zijll de Jong E, Emmerling M, Spangenberg GC (2005) Application of molecular technologies in forage plant breeding. In ‘Molecular breeding for the genetic improvement of forage crops and turf’. (Ed. MO Humphreys) pp. 63–73. (Academic Publishers: Wageningen, The Netherlands)

Spangenberg G, Kalla R, Lidgett A, Sawbridge T, Ong EK, John U (2001) Breeding forage plants in the genome era. In ‘Molecular breeding of forage crops’. (Ed. G Spangenberg) pp. 1–39. (Kluwer Academic Publishers: Dordrecht, The Netherlands)

Spangenberg G, Smith K, Chu P, Bannan N, Binnion C, Ponnampalam M, Trigg P, Wilkinson T, Ludlow E, de Lucas Arbiza A, Winkworth A, Sivakumaran A, Mahesawaran G, Walkiewicz M, Rochfort S, Elkins A, Ezemieks V, Emmerling M, Panter S, Mouradov A (2007) Generation of transgenic white clover (Trifolium repens L.) cultivars resistant to Alfalfa mosaic virus. In ‘Proceedings of the Fifth International Symposium on the Molecular Breeding of Forage and Turf’. Sapporo, Japan, 1–6 July 2007. (Eds T Yamada, G Spangenberg) p. 103. (Springer: New York)

Tanner GJ (2004) Condensed tannins. In ‘Plant pigments and their manipulation. Annual plant reviews, Vol. 14’. (Ed. K Davies) pp. 150–184. (Blackwell Publishing Ltd: Oxford, UK)

Tanner GJ, Francki KT, Abrahams S, Watson JM, Larkin PJ, Ashton AR (2003) Proanthocyanidin biosynthesis in plants: purification of legume leucoanthocyanidin reductase and molecular cloning of its cDNA. The Journal of Biological Chemistry 278, 31647–31656.
Proanthocyanidin biosynthesis in plants: purification of legume leucoanthocyanidin reductase and molecular cloning of its cDNA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmsVOnt7g%3D&md5=583c4cd04aa1aca808ef3fa164579c25CAS | 12788945PubMed |

Tashiro RM, Han Y, Monteros MJ, Bouton JH, Parrott WA (2010) Leaf trait coloration in white clover and molecular mapping of the red midrib and leaflet number traits. Crop Science 50, 1260–1268.
Leaf trait coloration in white clover and molecular mapping of the red midrib and leaflet number traits.Crossref | GoogleScholarGoogle Scholar |

Tesfaye M, Temple SJ, Allan DL, Vance CP, Samac DA (2001) Overexpression of malate dehydrogenase in transgenic alfalfa enhances organic acid synthesis and confers tolerance to aluminium. Plant Physiology 127, 1836–1844.
Overexpression of malate dehydrogenase in transgenic alfalfa enhances organic acid synthesis and confers tolerance to aluminium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjtVWksA%3D%3D&md5=5cc1b42e2192923a7c8420f91f6473f4CAS | 1:CAS:528:DC%2BD38XjtVWksA%3D%3D&md5=5cc1b42e2192923a7c8420f91f6473f4CAS | 11743127PubMed |

Verdier J, Zhao J, Torres-Jerez I, Ge S, Liu C, He X, Mysore KS, Dixon RA, Udvardi MK (2012) MtPAR MYB transcription factor acts as an on switch for proanthocyanidin biosynthesis in Medicago truncatula. Proceedings of the National Academy of Sciences of the United States of America 109, 1766–1771.
MtPAR MYB transcription factor acts as an on switch for proanthocyanidin biosynthesis in Medicago truncatula.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XitlKltL4%3D&md5=ad589a8c23fe836e0ed856ef145db64cCAS | 1:CAS:528:DC%2BC38XitlKltL4%3D&md5=ad589a8c23fe836e0ed856ef145db64cCAS | 22307644PubMed |

Voisey CR, White DWR, Dudas B, Appleby RD, Ealing PM, Scott AG (1994a) Agrobacterium-mediated transformation of white clover using direct shoot organogenesis. Plant Cell Reports 13, 309–314.
Agrobacterium-mediated transformation of white clover using direct shoot organogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXhtlGisQ%3D%3D&md5=558a2b2f8c7577b8dde54c71ae0c0f10CAS | 1:CAS:528:DyaK2MXhtlGisQ%3D%3D&md5=558a2b2f8c7577b8dde54c71ae0c0f10CAS |

Voisey CR, White DWR, Wigley PJ, Chilcott CN, McGregor PG, Woodfield DR (1994b) Release of transgenic white clover plants expressing Bacillus thuringiensis genes – an ecological perspective. Biocontrol Science and Technology 4, 475–481.
Release of transgenic white clover plants expressing Bacillus thuringiensis genes – an ecological perspective.Crossref | GoogleScholarGoogle Scholar |

Voisey CR, Dudas B, Biggs R, Burgess EPJ, Wigley PJ, McGregor PG, Lough TJ, Beck DL, Forster RLS, White DWR (2001) Development and implementation of molecular markers for forage crop improvement. In ‘Molecular breeding of forage crops’. (Ed. G Spangenberg) pp. 239–250. (Kluwer Academic Press: Dordrecht, The Netherlands)

Wang Y, Douglas GB, Waghorn GC, Barry TN, Foote AG, Purchas RW (1996) Effect of condensed tannins upon the performance of lambs grazing Lotus corniculatus and lucerne (Medicago sativa). The Journal of Agricultural Science 126, 87–98.
Effect of condensed tannins upon the performance of lambs grazing Lotus corniculatus and lucerne (Medicago sativa).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xit12mtbc%3D&md5=ca7c3e3eacec5106f47d520da2174fbdCAS |

Wang J, Drayton MC, George J, Cogan NOI, Baillie RC, Hand ML, Kearney G, Trigg P, Erb S, Wilkinson T, Bannan N, Forster JW, Smith KF (2010) QTL analysis of salt stress tolerance in white clover (Trifolium repens L.). Theoretical and Applied Genetics 120, 607–619.
QTL analysis of salt stress tolerance in white clover (Trifolium repens L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXotV2itQ%3D%3D&md5=a86fc758c08f9826e13db57766dfe9a4CAS | 1:CAS:528:DC%2BC3cXotV2itQ%3D%3D&md5=a86fc758c08f9826e13db57766dfe9a4CAS | 19865805PubMed |

White DWR, Greenwood D (1987) Transformation of the forage legume Trifolium repens L. using binary Agrobacterium vectors. Plant Molecular Biology 8, 461–469.
Transformation of the forage legume Trifolium repens L. using binary Agrobacterium vectors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXktlChtrk%3D&md5=dbc72a7d9a275702a9fabdaf6f90a29eCAS | 1:CAS:528:DyaL2sXktlChtrk%3D&md5=dbc72a7d9a275702a9fabdaf6f90a29eCAS |

White DWR, Voisey CR (1994) Prolific direct plant regeneration from cotyledons of white clover. Plant Cell Reports 13, 303–308.
Prolific direct plant regeneration from cotyledons of white clover.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXltVCgsbY%3D&md5=3bd136ff73c897d0f097e7526622d63cCAS | 1:CAS:528:DyaK2cXltVCgsbY%3D&md5=3bd136ff73c897d0f097e7526622d63cCAS |

Williams WM, Ellison NW, Ansari HA, Verry IM, Hussain SW (2012) Experimental evidence for the ancestry of allotetraploid Trifolium repens and creation of synthetic forms with value for plant breeding. BMC Plant Biology 12, 55
Experimental evidence for the ancestry of allotetraploid Trifolium repens and creation of synthetic forms with value for plant breeding.Crossref | GoogleScholarGoogle Scholar | 22530692PubMed |

Xie DY, Sharma SB, Paiva NL, Ferreira D, Dixon RA (2003) Role of anthocyanidin reductase, encoded by BANYULS in plant flavonoid biosynthesis. Science 299, 396–399.
Role of anthocyanidin reductase, encoded by BANYULS in plant flavonoid biosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjsF2rsw%3D%3D&md5=2d004ef45d1d1d5232bcaedd5de8a63dCAS | 1:CAS:528:DC%2BD3sXjsF2rsw%3D%3D&md5=2d004ef45d1d1d5232bcaedd5de8a63dCAS | 12532018PubMed |

Xie DY, Sharma SB, Dixon RA (2004) Anthocyanidin reductases from Medicago truncatula and Arabidopsis thaliana. Archives of Biochemistry and Biophysics 422, 91–102.
Anthocyanidin reductases from Medicago truncatula and Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjtVamtg%3D%3D&md5=3f21162054e38d88a2432cc83203dd44CAS | 1:CAS:528:DC%2BD2cXjtVamtg%3D%3D&md5=3f21162054e38d88a2432cc83203dd44CAS | 14725861PubMed |

Xie DY, Sharma SB, Wright E, Wang ZY, Dixon RA (2006) Metabolic engineering of proanthocyanidins through co-expression of anthocyanidin reductase and the PAP1 MYB transcription factor. The Plant Journal 45, 895–907.
Metabolic engineering of proanthocyanidins through co-expression of anthocyanidin reductase and the PAP1 MYB transcription factor.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xjs1Sms7Y%3D&md5=603261252432b1874a37195db83b35b6CAS | 1:CAS:528:DC%2BD28Xjs1Sms7Y%3D&md5=603261252432b1874a37195db83b35b6CAS | 16507081PubMed |

Yamaguchi M, Sasaki T, Sivaguru M, Yamamoto Y, Osawa H, Ahn SJ, Matsumoto H (2005) Evidence for the plasma membrane localization of Al-activated malate transporter (ALMT1). Plant & Cell Physiology 46, 812–816.
Evidence for the plasma membrane localization of Al-activated malate transporter (ALMT1).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXkvVWqu7o%3D&md5=04989d86404f582dab6be26df49b7e33CAS | 1:CAS:528:DC%2BD2MXkvVWqu7o%3D&md5=04989d86404f582dab6be26df49b7e33CAS |

Young H, Paterson VJ (1980) Condensed tannins from white clover seed diffusate. Phytochemistry 19, 159–160.
Condensed tannins from white clover seed diffusate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXktVertLY%3D&md5=4cb5ad66fe37b98221ad2d079761527dCAS | 1:CAS:528:DyaL3cXktVertLY%3D&md5=4cb5ad66fe37b98221ad2d079761527dCAS |

Zhang JY, Broeckling CD, Blancaflor EB, Sledge MK, Sumner LW, Wang ZY (2005) Overexpression of WXP1, a putative Medicago truncatula AP2 domain-containing transcription factor gene, increases cuticular wax accumulation and enhances drought tolerance in transgenic alfalfa (Medicago sativa). The Plant Journal 42, 689–707.
Overexpression of WXP1, a putative Medicago truncatula AP2 domain-containing transcription factor gene, increases cuticular wax accumulation and enhances drought tolerance in transgenic alfalfa (Medicago sativa).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXlt1yns7w%3D&md5=3f4d8e90926c8ca07d2b547632e3a6b1CAS | 1:CAS:528:DC%2BD2MXlt1yns7w%3D&md5=3f4d8e90926c8ca07d2b547632e3a6b1CAS | 15918883PubMed |

Zhang Y, Sledge M, Bouton J (2007) Genome mapping of white clover (Trifolium repens L.) and comparative analysis within the Trifolieae using cross-species SSR markers. Theoretical and Applied Genetics 114, 1367–1378.
Genome mapping of white clover (Trifolium repens L.) and comparative analysis within the Trifolieae using cross-species SSR markers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXltVWgtbc%3D&md5=39cb23c1efd3f4313c11213175a0a399CAS | 1:CAS:528:DC%2BD2sXltVWgtbc%3D&md5=39cb23c1efd3f4313c11213175a0a399CAS | 17356868PubMed |

Zhang X, Sato S, Ye X, Dorrance AE, Morris TJ, Clemente TE, Qu F (2011) Robust RNAi-based resistance to mixed infection of three viruses in soybean plants expressing separate short hairpins from a single transgene. Phytopathology 101, 1264–1269.
Robust RNAi-based resistance to mixed infection of three viruses in soybean plants expressing separate short hairpins from a single transgene.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsVOlurbM&md5=8555ce96b14669149f5f2dd03e1fabbeCAS | 1:CAS:528:DC%2BC3MXhsVOlurbM&md5=8555ce96b14669149f5f2dd03e1fabbeCAS | 21999157PubMed |

Zhao J, Pang Y, Dixon RA (2010) The mysteries of proanthocyanidin transport and polymerization. Plant Physiology 153, 437–443.
The mysteries of proanthocyanidin transport and polymerization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXnvVamsLc%3D&md5=c2c3d2c9f83f624a23c0ed0ede84588cCAS | 1:CAS:528:DC%2BC3cXnvVamsLc%3D&md5=c2c3d2c9f83f624a23c0ed0ede84588cCAS | 20388668PubMed |