Haploid and doubled haploid techniques in perennial ryegrass (lolium perenne l.) to advance research and breeding

Agronomy

Volumn 6, Issue 4, 2016, Pages

  Begheyn, Rachel F ^a   Lübberstedt, Thomas ^b   Studer, Bruno ^a  

^a ETH ZURICH   (Switzerland)

^b IOWA STATE UNIVERSITY   (United States)

Author keywords

Anther culture; Doubled haploid (DH); Forage crops; Microspore culture; Perennial ryegrass (Lolium perenne L.); Plant breeding

Indexed keywords

EID: 85027989487     PISSN: None     EISSN: 20734395     Source Type: Journal    
DOI: 10.3390/agronomy6040060     Document Type: Article

References (135)

1. Tilman, D.; Balzer, C.; Hill, J.; Befort, B.L. Global food demand and the sustainable intensification of agriculture. Proc. Natl. Acad. Sci. USA 2011, 108, 20260–20264. [CrossRef] [PubMed]
2. Fischer, R.A.; Byerlee, D.; Edmeades, G.O. Crop Yields and Global Food Security: Will Yield Increase Continue to Feed the World? ACIAR Monograph No. 158; Australian Centre for International Agricultural Research: Canberra, Australia, 2014.
3. Foley, J.A.; Ramankutty, N.; Brauman, K.A.; Cassidy, E.S.; Gerber, J.S.; Johnston, M.; Mueller, N.D.; O’Connell, C.; Ray, D.K.; West, P.C.; et al. Solutions for a cultivated planet. Nature 2011, 478, 337–342. [CrossRef] [PubMed]
4. Brummer, C.E.; Barber, W.T.; Collier, S.M.; Cox, T.S.; Johnson, R.; Murray, S.C.; Olsen, R.T.; Pratt, R.C.; Thro, A.M. Plant breeding for harmony between agriculture and the environment. Front. Ecol. Environ. 2011, 9, 561–568. [CrossRef]
5. Fischer, R.A.; Edmeades, G.O. Breeding and cereal yield progress. Crop Sci. 2010, 50, S85–S98. [CrossRef]
6. Stamp, P.; Visser, R. The twenty-first century, the century of plant breeding. Euphytica 2012, 186, 585–591. [CrossRef]
7. Fischer, R.A. Definitions and determination of crop yield, yield gaps, and of rates of change. Field Crops Res. 2015, 182, 9–18. [CrossRef]
8. Tester, M.; Langridge, P. Breeding technologies to increase crop production in a changing world. Science 2010, 327, 818–822. [CrossRef] [PubMed]
9. Dawson, I.K.; Russell, J.; Powell, W.; Steffenson, B.; Thomas, W.T.B.; Waugh, R. Barley: A translational model for adaptation to climate change. New Phytol. 2015, 206, 913–931. [CrossRef] [PubMed]
10. Germanà, M.A. Gametic embryogenesis and haploid technology as valuable support to plant breeding. Plant Cell Rep. 2011, 30, 839–857. [CrossRef] [PubMed]
11. Seguí-Simarro, J.M. Androgenesis revisited. Bot. Rev. 2010, 76, 377–404. [CrossRef]
12. Forster, B.P.; Heberle-Bors, E.; Kasha, K.J.; Touraev, A. The resurgence of haploids in higher plants. Trends Plant Sci. 2007, 12, 368–375. [CrossRef] [PubMed]
13. Dunwell, J.M. Haploids in flowering plants: Origins and exploitation. Plant Biotechnol. J. 2010, 8, 377–424. [CrossRef] [PubMed]
14. Dwivedi, S.L.; Britt, A.B.; Tripathi, L.; Sharma, S.; Upadhyaya, H.D.; Ortiz, R. Haploids: Constraints and opportunities in plant breeding. Biotechnol. Adv. 2015, 33, 812–829. [CrossRef] [PubMed]
15. Seguí-Simarro, J.M. Editorial: Doubled haploidy in model and recalcitrant species. Front. Plant Sci. 2015, 6, 1–2. [CrossRef] [PubMed]
16. Geiger, H.H.; Gordillo, G.A. Doubled haploids in hybrid maize breeding. Maydica 2009, 54, 485–499.
17. Smith, K.F.; Spangenberg, G. Forage breeding for changing environments and production systems: An overview. Crop Pasture Sci. 2014, 65. [CrossRef]
18. Reheul, D.; De Cauwer, B.; Cougnon, M. The role of forage crops in multifunctional agriculture. In Fodder Crops and Amenity Grasses; Boller, B., Posselt, U., Veronesi, F., Eds.; Springer: New York, NY, USA, 2010; pp. 457–476.
19. Ferrie, A.M.R.; Caswell, K.L. Isolated microspore culture techniques and recent progress for haploid and doubled haploid plant production. Plant Cell Tissue Organ Cult. 2011, 104, 301–309. [CrossRef]
20. Seguí-Simarro, J.M.; Nuez, F. How microspores transform into haploid embryos: Changes associated with embryogenesis induction and microspore-derived embryogenesis. Physiol. Plant. 2008, 134, 1–12. [CrossRef] [PubMed]
21. Shariatpanahi, M.E.; Bal, U.; Heberle-Bors, E.; Touraev, A. Stresses applied for the re-programming of plant microspores towards in vitro embryogenesis. Physiol. Plant. 2006, 127, 519–534. [CrossRef]
22. Islam, S.M.S.; Tuteja, N. Enhancement of androgenesis by abiotic stress and other pretreatments in major crop species. Plant Sci. 2012, 182, 134–144. [CrossRef] [PubMed]
23. Kumari, M.; Clarke, H.J.; Small, I.; Siddique, K.H.M. Albinism in plants: A major bottleneck in wide hybridization, androgenesis and doubled haploid culture. CRC. Crit. Rev. Plant Sci. 2009, 28, 393–409. [CrossRef]
24. Maluszynski, M.; Kasha, K.J.; Forster, B.P.; Szarejko, I. Doubled Haploid Production in Crop Plants: A manual; Maluszynski, M., Kasha, K.J., Forster, B.P., Szarejko, I., Eds.; Kluwer Academic Publishers: Dordrecht, The Netherlands, 2003.
25. Touraev, A.; Forster, B.P.; Mohan Jain, S. Advances in Haploid Production in Higher Plants; Touraev, A., Forster, B.P., Jain, S.M., Eds.; Springer: Dordrecht, The Netherlands, 2009.
26. Germanà, M.A.; Lambardi, M. In Vitro Embryogenesis in Higher Plants, 1st ed.; Germanà, M.A., Lambardi, M., Eds.; Humana Press: New York, NY, USA, 2016.
27. Niu, Z.; Jiang, A.; Abu Hammad, W.; Oladzadabbasabadi, A.; Xu, S.S.; Mergoum, M.; Elias, E.M. Review of doubled haploid production in durum and common wheat through wheat × maize hybridization. Plant Breed. 2014, 133, 313–320. [CrossRef]
28. Chen, J.-F.; Cui, L.; Malik, A.A.; Mbira, K.G. In vitro haploid and dihaploid production via unfertilized ovule culture. Plant Cell Tissue Organ Cult. 2010, 104, 311–319. [CrossRef]
29. Pink, D.; Bailey, L.; McClement, S.; Hand, P.; Mathas, E.; Buchanan-Wollaston, V.; Astley, D.; King, G.; Teakle, G. Double haploids, markers and QTL analysis in vegetable brassicas. Euphytica 2008, 164, 509–514. [CrossRef]
30. Tuvesson, S.; Dayteg, C.; Hagberg, P.; Manninen, O.; Tanhuanpää, P.; Tenhola-Roininen, T.; Kiviharju, E.; Weyen, J.; Förster, J.; Schondelmaier, J.; et al. Molecular markers and doubled haploids in European plant breeding programmes. Euphytica 2006, 158, 305–312. [CrossRef]
31. Devaux, P.; Kasha, K.J. Overview of barley doubled haploid production. In Advances in Haploid Production in Higher Plants; Touraev, A., Forster, B.P., Jain, S.M., Eds.; Springer: Dordrecht, The Netherlands, 2009; pp. 47–64.
32. Mishra, R.; Jwala, G.; Ao, N.R. In Vitro androgenesis in rice: Advantages, constraints and future prospects. Rice Sci. 2016, 23, 57–68. [CrossRef]
33. Ferrie, A.M.R.; Möllers, C. Haploids and doubled haploids in Brassica spp. for genetic and genomic research. Plant Cell Tissue Organ Cult. 2010, 104, 375–386. [CrossRef]
34. Lippman, Z.B.; Zamir, D. Heterosis: Revisiting the magic. Trends Genet. 2006, 23, 60–66. [CrossRef] [PubMed]
35. Birchler, J.A.; Yao, H.; Chudalayandi, S.; Vaiman, D.; Veitia, R.A. Heterosis. Plant Cell 2010, 22, 2105–2112. [CrossRef] [PubMed]
36. Ferrie, A.M.R. Doubled haploidy as a tool in ornamental breeding. Acta Hortic. 2012, 953, 167–171. [CrossRef]
37. Obsa, B.T.; Eglinton, J.; Coventry, S.; March, T.; Langridge, P.; Fleury, D. Genetic analysis of developmental and adaptive traits in three doubled haploid populations of barley (Hordeum vulgare L.). Theor. Appl. Genet. 2016, 129, 1139–1151. [CrossRef] [PubMed]
38. Brew-Appiah, R.A.T.; Ankrah, N.; Liu, W.; Konzak, C.F.; Von Wettstein, D.; Rustgi, S. Generation of doubled haploid transgenic wheat lines by microspore transformation. PLoS ONE 2013, 8, e80155. [CrossRef] [PubMed]
39. Kumlehn, J.; Serazetdinova, L.; Hensel, G.; Becker, D.; Loerz, H. Genetic transformation of barley (Hordeum vulgare L.) via infection of androgenetic pollen cultures with Agrobacterium tumefaciens. Plant Biotechnol. J. 2006, 4, 251–261. [CrossRef] [PubMed]
40. Kapusi, E.; Hensel, G.; Coronado, M.J.; Broeders, S.; Marthe, C.; Otto, I.; Kumlehn, J. The elimination of a selectable marker gene in the doubled haploid progeny of co-transformed barley plants. Plant Mol. Biol. 2013, 81, 149–160. [CrossRef] [PubMed]
41. Huang, S.; Liu, Z. A new method for generation and screening of Chinese cabbage mutants using isolated microspore culturing and EMS mutagenesis. Euphytica 2016, 207, 23–33. [CrossRef]
42. Shen, Y.; Pan, G.; Lübberstedt, T. Haploid strategies for functional validation of plant genes. Trends Biotechnol. 2015, 33, 611–620. [CrossRef] [PubMed]
43. Ferrie, A.M.R.; Caswell, K.L. Applications of doubled haploidy for improving industrial oilseeds. In Industrial Oil Crops; McKeon, T.A., Hayes, D.G., Hildebrand, D.F., Weselake, R.J., Eds.; Elsevier Inc.: London, UK, 2016; pp. 359–378.
44. Soriano, M.; Li, H.; Boutilier, K. Microspore embryogenesis: Establishment of embryo identity and pattern in culture. Plant Reprod. 2013, 26, 181–196. [CrossRef] [PubMed]
45. Daghma, D.E.S.; Hensel, G.; Rutten, T.; Melzer, M.; Kumlehn, J. Cellular dynamics during early barley pollen embryogenesis revealed by time-lapse imaging. Front. Plant Sci. 2014, 5, 1–14. [CrossRef] [PubMed]
46. Seifert, F.; Bössow, S.; Kumlehn, J.; Gnad, H.; Scholten, S. Analysis of wheat microspore embryogenesis induction by transcriptome and small RNA sequencing using the highly responsive cultivar “Svilena”. BMC Plant Biol. 2016, 16, 97. [CrossRef] [PubMed]
47. Smith, K.F.; Simpson, R.J.; Culvenor, R.A.; Humphreys, M.O.; Prud’Homme, M.P.; Oram, R.N. The effects of ploidy and a phenotype conferring a high water-soluble carbohydrate concentration on carbohydrate accumulation, nutritive value and morphology of perennial ryegrass (Lolium perenne L.). J. Agric. Sci. 2001, 136, 65–74. [CrossRef]
48. Smith, K.F.; McFarlane, N.M.; Croft, V.M.; Trigg, P.J.; Kearney, G.A. The effects of ploidy and seed mass on the emergence and early vigour of perennial ryegrass (Lolium perenne L.) cultivars. Aust. J. Exp. Agric. 2003, 43, 481–486. [CrossRef]
49. Nair, R. Developing tetraploid perennial ryegrass (Lolium perenne L.) populations. N. Z. J. Agric. Res. 2004, 47, 45–49. [CrossRef]
50. Wilkins, P.W. Breeding perennial ryegrass for agriculture. Euphytica 1991, 52, 201–214. [CrossRef]
51. Sampoux, J.P.; Baudouin, P.; Bayle, B.; Béguier, V.; Bourdon, P.; Chosson, J.F.; Deneufbourg, F.; Galbrun, C.; Ghesquière, M.; Noël, D.; et al. Breeding perennial grasses for forage usage: An experimental assessment of trait changes in diploid perennial ryegrass (Lolium perenne L.) cultivars released in the last four decades. Field Crops Res. 2011, 123, 117–129. [CrossRef]
52. Humphreys, M.O. Genetic improvement of forage crops—Past, present and future. J. Agric. Sci. 2005, 143, 441–448. [CrossRef]
53. Cornish, M.A.; Hayward, M.D.; Lawrence, M.J. Self-incompatibility in ryegrass. I. Genetic control in diploid Lolium perenne L. Heredity 1979, 43, 95–106. [CrossRef]
54. Blackmore, T.; Thorogood, D.; Skøt, L.; Mcmahon, R.; Powell, W.; Hegarty, M. Germplasm dynamics: The role of ecotypic diversity in shaping the patterns of genetic variation in Lolium perenne. Sci. Rep. 2016, 6, 22603. [CrossRef] [PubMed]
55. Wang, J.; Pembleton, L.W.; Baillie, R.C.; Drayton, M.C.; Hand, M.L.; Bain, M.; Sawbridge, T.I.; Spangenberg, G.C.; Forster, J.W.; Cogan, N.O.I. Development and implementation of a multiplexed single nucleotide polymorphism genotyping tool for differentiation of ryegrass species and cultivars. Mol. Breed. 2014, 33, 435–451. [CrossRef]
56. Casler, M.D.; Brummer, E.C. Theoretical expected genetic gains for among-and-within-family selection methods in perennial forage crops. Crop Sci. 2008, 48, 890–902. [CrossRef]
57. Stanis, V.A.; Butenko, R.G. Developing viable haploid plants in anther culture of ryegrass. Dokl. Biol. Sci. 1984, 275, 249–251.
58. Boppenmeier, J.; Zuchner, S.; Foroughi-Wehr, B. Haploid production from barley yellow dwarf virus resistant clones of Lolium. Plant Breed. 1989, 103, 216–220. [CrossRef]
59. Olesen, A.; Andersen, S.B.; Due, I.K. Anther culture response in perennial ryegrass (Lolium perenne L.). Plant Breed. 1988, 101, 60–65. [CrossRef]
60. Opsahl-Ferstad, H.-G.; Bjornstad, A.; Rognli, O.A. Influence of medium and cold pretreatment on androgenetic response in Lolium perenne L. Plant Cell Rep. 1994, 13, 594–600. [CrossRef] [PubMed]
61. Bante, I.; Sonke, T.; Tandler, R.F.; van den Bruel, A.M.R.; Meyer, E.M. Anther culture of Lolium perenne and Lolium multiflorum. In The Impact of Biotechnology in Agriculture; Sangwan, R., Sangwan-Norreel, B.S., Eds.; Springer: Dordrecht, The Netherlands, 1990; pp. 105–127.
62. Creemers-Molenaar, J.; Beerepoot, L.J. In Vitro Culture and Micropropagation of Ryegrass (Lolium spp.). In High-Tech and Micropropagation III; Bajaj, Y.P.S., Ed.; Springer: Berlin/Heidelberg, Germany, 1992; Volume 19, pp. 549–575.
63. Madsen, S.; Olesen, A.; Dennis, B.; Andersen, S.B. Inheritance of anther-culture response in perennial ryegrass (Lolium perenne L.). Plant Breed. 1995, 114, 165–168. [CrossRef]
64. Hussain, S.W.; Richardson, K.; Faville, M.; Woodfield, D. Production of haploids and double haploids in annual (Lolium multiflorum) and perennial (L. perenne) ryegrass. In Proceedings of the 13th Australasian Plant Breeding Conference, Christchurch, New Zealand, 18–21 April 2006; Mercer, C.F., Ed.; pp. 531–536.
65. Andersen, S.B.; Madsen, S.; Roulund, N.; Halberg, N.; Olesen, A. Haploidy in ryegrass. In In Vritro Haploid Production in Higher Plants; Jain, S.M., Sopory, S.K., Veilleux, R.E., Eds.; Kluwer Academic Publishers: Dordrecht, The Netherlands, 1997; Volume 4, pp. 133–147.
66. Halberg, N.; Olesen, A.; Tuvesson, I.K.D.; Andersen, S.B. Genotypes of perennial ryegrass (Lolium perenne L.) with high anther-culture response through hybridization. Plant Breed. 1990, 105, 89–94. [CrossRef]
67. Opsahl-Ferstad, H.G.; Bjørnstad, N.; Rognli, O.A. Genetic control of androgenetic response in Lolium perenne L. Theor. Appl. Genet. 1994, 89, 133–138. [CrossRef] [PubMed]
68. Wang, Z.-Y.; Ge, Y.; Mian, R.; Baker, J. Development of highly tissue culture responsive lines of Lolium temulentum by anther culture. Plant Sci. 2005, 168, 203–211. [CrossRef]
69. Chen, X.-W.; Cistué, L.; Muñoz-Amatriaín, M.; Sanz, M.; Romagosa, I.; Castillo, A.-M.; Vallés, M.-P. Genetic markers for doubled haploid response in barley. Euphytica 2006, 158, 287–294. [CrossRef]
70. Agache, S.; Bachelier, B.; De Buyser, J.; Henry, Y.; Snape, J. Genetic analysis of anther culture response in wheat using aneuploid, chromosome substitution and translocation lines. Theor. Appl. Genet. 1989, 77, 7–11. [CrossRef] [PubMed]
71. Torp, A.M.; Andersen, S.B. Albinism in microspore culture. In Advances in Haploid Production in Higher Plants; Touraev, A., Forster, B., Jain, S.M., Eds.; Springer: New York, NY, USA, 2009; pp. 155–160.
72. Bolibok, H.; Rakoczy-Trojanowska, M. Genetic mapping of QTLs for tissue-culture response in plants. Euphytica 2006, 149, 73–83. [CrossRef]
73. Nielsen, N.H.; Andersen, S.U.; Stougaard, J.; Jensen, A.; Backes, G.; Jahoor, A. Chromosomal regions associated with the in vitro culture response of wheat (Triticum aestivum L.) microspores. Plant Breed. 2015, 134, 255–263. [CrossRef]
74. Krzewska, M.; Czyczyło-Mysza, I.; Dubas, E.; Gołebiowska-Pikania, G.; Golemiec, E.; Stojałowski, S.; Chrupek, M.; Zur, I. Quantitative trait loci associated with androgenic responsiveness in triticale (×Triticosecale Wittm.) anther culture. Plant Cell Rep. 2012, 31, 2099–2108. [CrossRef] [PubMed]
75. Begheyn, R.F.; Vangsgaard, K.; Roulund, N. Efficient doubled haploid production in perennial ryegrass (Lolium perenne L.). In Breeding in a World of Scarcity, Proceedings of the 2015 Meeting of the Section “Forage Crops and Amenity Grasses” of Eucarpia, Ghent, Belgium, 14 June 2016; Springer: Basel, Switzerland; pp. 151–155.
76. Melchinger, A.E.; Molenaar, W.S.; Mirdita, V.; Schipprack, W. Colchicine alternatives for chromosome doubling in maize haploids for doubled-haploid production. Crop Sci. 2016, 56, 559–569. [CrossRef]
77. Opsahl-Ferstad, H.G. Androgenetic Response in Grasses. I. Anther Culture in Perennial Ryegrass (Lolium perenne L.). II. Molecular Studies of Embryogenesis in Barley (Hordeum vulgare L.). Ph.D. Thesis, Agricultural University of Norway, Ås, Norway, 1993.
78. Madsen, S.; Olesen, A.; Andersen, S.B. Self-fertile doubled haploid plants of perennial ryegrass (Lolium perenne L.). Plant Breed. 1993, 110, 323–327. [CrossRef]
79. Manzanares, C.; Yates, S.; Ruckle, M.; Nay, M.; Studer, B. TILLING in forage grasses for gene discovery and breeding improvement. New Biotechnol. 2016, 33, 594–603. [CrossRef] [PubMed]
80. Conaghan, P.; Casler, M.D. A theoretical and practical analysis of the optimum breeding system for perennial ryegrass. Irish J. Agric. Sci. 2011, 50, 47–63.
81. Wang, Z.Y.; Brummer, E.C. Is genetic engineering ever going to take off in forage, turf and bioenergy crop breeding? Ann. Bot. 2012, 110, 1317–1325. [CrossRef] [PubMed]
82. Arias Aguirre, A.; Studer, B.; Frei, U.; Lübberstedt, T. Prospects for hybrid breeding in bioenergy grasses. BioEnergy Res. 2011, 5, 10–19. [CrossRef]
83. Langridge, P.; Fleury, D. Making the most of “omics” for crop breeding. Trends Biotechnol. 2011, 29, 33–40. [CrossRef] [PubMed]
84. Sinha, R.K.; Eudes, F. Dimethyl tyrosine conjugated peptide prevents oxidative damage and death of triticale and wheat microspores. Plant Cell Tissue Organ Cult. 2015, 122, 227–237. [CrossRef]
85. Sriskandarajah, S.; Sameri, M.; Lerceteau-Köhler, E.; Westerbergh, A. Increased recovery of green doubled haploid plants from barley anther culture. Crop Sci. 2015, 55, 2806–2812. [CrossRef]
86. Echavarri, B.; Cistue, L. Enhancement in androgenesis efficiency in barley (Hordeum vulgare L.) and bread wheat (Triticum aestivum L.) by the addition of dimethyl sulfoxide to the mannitol pretreatment medium. Plant Cell Tissue Organ Cult. 2016, 125, 11–22. [CrossRef]
87. Devaux, P.; Zivy, M. Protein markers for anther culturability in barley. Theor. Appl. Genet. 1994, 88, 701–706. [CrossRef] [PubMed]
88. Zhang, L.; Zhang, L.; Luo, J.; Chen, W.; Hao, M.; Liu, B.; Yan, Z.; Zhang, B.; Zhang, H.; Zheng, Y.; et al. Synthesizing double haploid hexaploid wheat populations based on a spontaneous alloploidization process. J. Genet. Genom. 2011, 38, 89–94. [CrossRef] [PubMed]
89. Muñoz-Amatriaín, M.; Castillo, A.M.; Chen, X.W.; Cistué, L.; Vallés, M.P. Identification and validation of QTLs for green plant percentage in barley (Hordeum vulgare L.) anther culture. Mol. Breed. 2008, 22, 119–129. [CrossRef]
90. Bélanger, S.; Esteves, P.; Clermont, I.; Jean, M.; Belzile, F. Genotyping-by-sequencing on pooled samples and its use in measuring segregation bias during the course of androgenesis in barley. Plant Genome 2016, 9, 1–13. [CrossRef]
91. Hayward, M.D.; Olesen, A.; Due, I.K.; Jenkins, R.; Morris, P. Segregation of isozyme marker loci amongst androgenetic plants of Lolium perenne L. Plant Breed. 1990, 104, 68–71. [CrossRef]
92. Kindiger, B. Generation of paternal dihaploids in tall fescue. Grassl. Sci. 2016, 62, 1–5. [CrossRef]
93. Kindiger, B. Sampling the genetic diversity of tall fescue utilizing gamete selection. In Genetic Diversity in Plants; Caliskan, M., Ed.; InTech: Rijeka, Croatia, 2012; pp. 271–284.
94. Ravi, M.; Chan, S.W. Centromere-mediated generation of haploid plants. In Plant Centromere Biology; Jiang, J., Birchler, J.A., Eds.; John Wiley & Sons, Inc.: Hoboken, NJ, USA, 2013; pp. 169–181.
95. Kelliher, T.; Starr, D.; Wang, W.; Mccuiston, J.; Zhong, H.; Nuccio, M.L.; Martin, B. Maternal haploids are preferentially induced by CENH3-tailswap transgenic complementation in maize. Front. Plant Sci. 2016, 7, 1–11. [CrossRef] [PubMed]
96. Karimi-Ashtiyani, R.; Ishii, T.; Niessen, M.; Stein, N.; Heckmann, S.; Gurushidze, M.; Banaei-Moghaddam, A.M.; Fuchs, J.; Schubert, V.; Koch, K.; et al. Point mutation impairs centromeric CENH3 loading and induces haploid plants. Proc. Natl. Acad. Sci. USA 2015, 112, 11211–11216. [CrossRef] [PubMed]
97. Charlesworth, D.; Willis, J.H. The genetics of inbreeding depression. Nat. Rev. Genet. 2009, 10, 783–796. [CrossRef] [PubMed]
98. Wilde, K.; Burger, H.; Prigge, V.; Presterl, T.; Schmidt, W.; Ouzunova, M.; Geiger, H.H. Testcross performance of doubled-haploid lines developed from European flint maize landraces. Plant Breed. 2010, 129, 181–185. [CrossRef]
99. Strigens, A.; Schipprack, W.; Reif, J.C.; Melchinger, A.E. Unlocking the genetic diversity of maize landraces with doubled haploids opens new avenues for breeding. PLoS ONE 2013, 8, e57234. [CrossRef] [PubMed]
100. Jacquard, C.; Nolin, F.; Hécart, C.; Grauda, D.; Rashal, I.; Dhondt-Cordelier, S.; Sangwan, R.S.; Devaux, P.; Mazeyrat-Gourbeyre, F.; Clément, C. Microspore embryogenesis and programmed cell death in barley: Effects of copper on albinism in recalcitrant cultivars. Plant Cell Rep. 2009, 28, 1329–1339. [CrossRef] [PubMed]
101. Larsen, E.T.; Tuvesson, I.K.; Andersen, S.B. Nuclear genes affecting percentage of green plants in barley (Hordeum vulgare L.) anther culture. Theor. Appl. Genet. 1991, 82, 417–420. [CrossRef] [PubMed]
102. Gurushidze, M.; Hensel, G.; Hiekel, S.; Schedel, S.; Valkov, V.; Kumlehn, J. True-breeding targeted gene knock-out in barley using designer TALE-nuclease in haploid cells. PLoS ONE 2014, 9, 1–9. [CrossRef] [PubMed]
103. Giri, C.C.; Praveena, M. In vitro regeneration, somatic hybridization and genetic transformation studies: An appraisal on biotechnological interventions in grasses. Plant Cell Tissue Organ Cult. 2014, 120, 843–860. [CrossRef]
104. Eudes, F.; Shim, Y.S.; Jiang, F. Engineering the haploid genome of microspores. Biocatal. Agric. Biotechnol. 2014, 3, 20–23. [CrossRef]
105. Chugh, A.; Amundsen, E.; Eudes, F. Translocation of cell-penetrating peptides and delivery of their cargoes in triticale microspores. Plant Cell Rep. 2009, 28, 801–810. [CrossRef] [PubMed]
106. Bilichak, A.; Luu, J.; Eudes, F. Intracellular delivery of fluorescent protein into viable wheat microspores using cationic peptides. Front. Plant Sci. 2015, 6, 666. [CrossRef] [PubMed]
107. Kumar, V.; Jain, M. The CRISPR-Cas system for plant genome editing: Advances and opportunities. J. Exp. Bot. 2015, 66, 47–57. [CrossRef] [PubMed]
108. Maluszynski, M.; Ahloowalia, B.S.; Sigurbjörnsson, B. Application of in vivo and in vitro mutation techniques for crop improvement. Euphytica 1995, 85, 303–315. [CrossRef]
109. Szarejko, I.; Forster, B.P. Doubled haploidy and induced mutation. Euphytica 2007, 158, 359–370. [CrossRef]
110. Kurowska, M.; Labocha-Pawłowska, A.; Gnizda, D.; Maluszynski, M.; Szarejko, I. Molecular analysis of point mutations in a barley genome exposed to MNU and Gamma rays. Mutat. Res. 2012, 738–739, 52–70. [CrossRef] [PubMed]
111. Lübberstedt, T.; Frei, U.K. Application of doubled haploids for target gene fixation in backcross programmes of maize. Plant Breed. 2012, 131, 449–452. [CrossRef]
112. Delourme, R.; Falentin, C.; Fomeju, B.F.; Boillot, M.; Lassalle, G.; André, I.; Duarte, J.; Gauthier, V.; Lucante, N.; Marty, A.; et al. High-density SNP-based genetic map development and linkage disequilibrium assessment in Brassica napus L. BMC Genom. 2013, 14, 120. [CrossRef] [PubMed]
113. Cabral, A.L.; Jordan, M.C.; McCartney, C.A.; You, F.M.; Humphreys, D.G.; MacLachlan, R.; Pozniak, C.J. Identification of candidate genes, regions and markers for pre-harvest sprouting resistance in wheat (Triticum aestivum L.). BMC Plant Biol. 2014, 14, 340. [CrossRef] [PubMed]
114. Sannemann, W.; Huang, B.E.; Mathew, B.; Léon, J. Multi-parent advanced generation inter-cross in barley: High-resolution quantitative trait locus mapping for flowering time as a proof of concept. Mol. Breed. 2015, 35, 86. [CrossRef]
115. Bert, P.F.; Charmet, G.; Sourdille, P.; Hayward, M.D.; Balfourier, F. A high-density molecular map for ryegrass (Lolium perenne) using AFLP markers. Theor. Appl. Genet. 1999, 99, 445–452. [CrossRef] [PubMed]
116. Jones, E.S.; Mahoney, N.L.; Hayward, M.D.; Armstead, I.P.; Jones, J.G.; Humphreys, M.O.; King, I.P.; Kishida, T.; Yamada, T.; Balfourier, F.; et al. An enhanced molecular marker based genetic map of perennial ryegrass (Lolium perenne) reveals comparative relationships with other Poaceae genomes. Genome 2002, 45, 282–295. [CrossRef] [PubMed]
117. Guo, B.; Wang, D.; Guo, Z.; Beavis, W.D. Family-based association mapping in crop species. Theor. Appl. Genet. 2013, 126, 1419–1430. [CrossRef] [PubMed]
118. King, J.; Armstead, I.P.; Donnison, I.S.; Harper, J.A.; Roberts, L.A.; Thomas, H.; Ougham, H.; Thomas, A.; Huang, L.; King, I.P. Introgression mapping in the grasses. Chromosom. Res. 2007, 15, 105–113. [CrossRef] [PubMed]
119. Humphreys, M.W.; Gasior, D.; Lesniewska-Bocianowska, A.; Zwierzykowski, Z.; Rapacz, M. Androgenesis as a means of dissecting complex genetic and physiological controls: Selecting useful gene combinations for breeding freezing tolerant grasses. Euphytica 2007, 158, 337–345. [CrossRef]
120. Petersen, G.; Johansen, B.; Seberg, O. PCR and sequencing from a single pollen grain. Plant Mol. Biol. 1996, 31, 189–191. [CrossRef] [PubMed]
121. Dreissig, S.; Fuchs, J.; Cápal, P.; Kettles, N.; Byrne, E.; Houben, A. Measuring meiotic crossovers via multi-locus genotyping of single pollen grains in barley. PLoS ONE 2015, 10, 1–10. [CrossRef] [PubMed]
122. Chen, P.H.; Pan, Y.B.; Chen, R.K. High-throughput procedure for single pollen grain collection and polymerase chain reaction in plants. J. Integr. Plant Biol. 2008, 50, 375–383. [CrossRef] [PubMed]
123. Goff, S.A. Tansley review—A unifying theory for general multigenic heterosis: Energy efficiency, protein metabolism, and implications for molecular breeding. New Phytol. 2011, 189, 923–937. [CrossRef] [PubMed]
124. Hallauer, A.R.; Carena, M.J.; Filho, J.B.M. Inbreeding. In Quantitative Genetics in Maize Breeding; Hallauer, A.R., Carena, M.J., Filho, J.B.M., Eds.; Springer: New York, NY, USA, 2010; pp. 425–475.
125. Geiger, H.H.; Miedaner, T. Rye breeding. In Cereals; Carena, M.J., Ed.; Springer: New York, NY, USA, 2009; pp. 157–181.
126. Brummer, E.C. Capturing heterosis in forage crop cultivar development. Crop Sci. 1999, 39, 943–954. [CrossRef]
127. Riddle, N.C.; Birchler, J.A. Comparative analysis of inbred and hybrid maize at the diploid and tetraploid levels. Theor. Appl. Genet. 2008, 116, 563–576. [CrossRef] [PubMed]
128. Kopecky, D.; Lukaszewski, A.J.; Gibeault, V. Reduction of ploidy level by androgenesis in intergenic Lolium—Festuca hybrids for turf grass breeding. Crop Sci. 2005, 45, 274–281.
129. Yang, B.; Thorogood, D.; Armstead, I.P.; Franklin, F.C.H.; Barth, S. Identification of genes expressed during the self-incompatibility response in perennial ryegrass (Lolium perenne L.). Plant Mol. Biol. 2009, 70, 709–723. [CrossRef] [PubMed]
130. Klaas, M.; Yang, B.; Bosch, M.; Thorogood, D.; Manzanares, C.; Armstead, I.P.; Franklin, F.C.H.; Barth, S. Progress towards elucidating the mechanisms of self-incompatibility in the grasses: Further insights from studies in Lolium. Ann. Bot. 2011, 108, 677–685. [CrossRef] [PubMed]
131. Manzanares, C.; Barth, S.; Thorogood, D.; Byrne, S.L.; Yates, S.; Czaban, A.; Asp, T.; Yang, B.; Studer, B. A gene encoding a DUF247 domain protein cosegregates with the S self-incompatibility locus in perennial ryegrass. Mol. Biol. Evol. 2016, 33, 870–884. [CrossRef] [PubMed]
132. Islam, M.S.; Studer, B.; Møller, I.M.; Asp, T. Genetics and biology of cytoplasmic male sterility and its applications in forage and turf grass breeding. Plant Breed. 2014, 133, 299–312. [CrossRef]
133. Pembleton, L.W.; Shinozuka, H.; Wang, J.; Spangenberg, G.C.; Forster, J.W.; Cogan, N.O.I. Design of an F1 hybrid breeding strategy for ryegrasses based on selection of self-incompatibility locus-specific alleles. Front. Plant Sci. 2015, 6, 764. [CrossRef] [PubMed]
134. Do Canto, J.; Studer, B.; Lubberstedt, T. Overcoming self-incompatibility in grasses: A pathway to hybrid breeding. Theor. Appl. Genet. 2016, 129, 1815–1829. [CrossRef] [PubMed]
135. Posselt, U.K. Heterosis in grasses. Czech J. Genet. Plant Breed. 2003, 39, 48–53.