Inheritance patterns of the response to in vitro doubled haploid induction in perennial ryegrass (Lolium perenne L.)

Plant Cell, Tissue and Organ Culture

Volumn 130, Issue 3, 2017, Pages 667-679

  Begheyn, Rachel F ^a   Roulund, Niels ^b   Vangsgaard, Kirsten ^b   Kopecký, David ^c   Studer, Bruno ^a  

^a ETH ZURICH   (Switzerland)

^b DLF Trifolium AS   (Denmark)

^c INSTITUTE OF EXPERIMENTAL BOTANY   (Czech Republic)

Author keywords

Androgenesis; Androgenic capacity; Anther culture; Doubled haploid (DH); Perennial ryegrass (Lolium perenne L.)

Indexed keywords

CROPS; GENES; GRAIN (AGRICULTURAL PRODUCT);

ANDROGENESIS; ANDROGENIC CAPACITY; ANTHER CULTURE; DOUBLED HAPLOID; LOLIUM PERENNE;

PLANTS (BOTANY);

BREEDING; EMBRYOS; FARM CROPS; PLANTS; TISSUE CULTURE;

EID: 85021061151     PISSN: 01676857     EISSN: 15735044     Source Type: Journal    
DOI: 10.1007/s11240-017-1255-y     Document Type: Article

References (77)

1. Andersen SB, Madsen S, Roulund N, Halberg N, Olesen A (1997) Haploidy in ryegrass. In: Jain SM, Sopory SK, Veilleux RE (eds) In vitro haploid production in higher plants. Springer, Dordrecht, pp 133–147
2. Arias Aguirre A, Studer B, Frei U, Lübberstedt T (2011) Prospects for hybrid breeding in bioenergy grasses. Bioenergy Res 5:10–19
3. Bante I, Sonke T, Tandler RF, van den Bruel AMR, Meyer EM (1990) Anther culture of Lolium perenne and Lolium multiflorum. In: Sangwan RS, Sangwan-Norreel BS (eds) The impact of biotechnology in agriculture. Springer, Dordrecht, pp 105–127
4. Begheyn RF, Lübberstedt T, Studer B (2016a) Haploid and doubled haploid techniques in perennial ryegrass (Lolium perenne L.) to advance research and breeding. Agronomy 6:60
5. Begheyn RF, Vangsgaard K, Roulund N, Studer B (2016b) Efficient doubled haploid production in perennial ryegrass (Lolium perenne L.). In: Roldán-Ruiz I, Baert J, Reheul D (eds) Breeding in a world of scarcity: proceedings of the 2015 meeting of the section “Forage Crops and Amenity Grasses” of Eucarpia, Ghent, Belgium. Springer, Cham, pp 151–155
6. Birchler JA, Yao H, Chudalayandi S, Vaiman D, Veitia RA (2010) Heterosis. Plant Cell 22:2105–2112
7. Boppenmeier J, Zuchner S, Foroughi-Wehr B (1989) Haploid production from barley yellow dwarf virus resistant clones of Lolium. Plant Breed 103:216–220
8. Cabral AL, Jordan MC, McCartney CA, You RM, Humphreys DG, MacLachlan R, Pozniak CJ (2014) Identification of candidate genes, regions and markers for pre-harvest sprouting resistance in wheat (Triticum aestivum L.). BMC Plant Biol 14:340
9. Castillo AM, Nielsen NH, Jensen A, Vallés MP (2014) Effects of n-butanol on barley microspore embryogenesis. Plant Cell Tissue Organ Cult 117:411–418
10. Chen X-W, Cistué L, Muñoz-Amatriaín M, Sanz M, Romagosa I, Castillo A-M, Vallés M-P (2007) Genetic markers for doubled haploid response in barley. Euphytica 158:287–294
11. Cornish MA, Hayward MD, Lawrence MJ (1979) Self-incompatibility in ryegrass. I. Genetic control in diploid Lolium perenne L. Heredity 43:95–106
12. Devaux P, Kasha KJ (2009) Overview of barley doubled haploid production. In: Touraev A, Forster BP, Jain SM (eds) Advances in haploid production in higher plants. Springer, Dordrecht, pp 47–64
13. Doležel J, Greilhuber J, Suda J (2007) Estimation of nuclear DNA content in plants using flow cytometry. Nat Protoc 2:2233–2244
14. Dunwell JM (2010) Haploids in flowering plants: origins and exploitation. Plant Biotechnol J 8:377–424
15. Dwivedi SL, Britt AB, Tripathi L, Sharma S, Upadhyaya HD, Ortiz R (2015) Haploids: constraints and opportunities in plant breeding. Biotechnol Adv 33:812–829
16. Echávarri B, Cistué L (2016) 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 125:11–22
17. Fábián A, Földesiné Füredi PK, Ambrus H, Jäger K, Barnabás B (2015) Effect of n-butanol and cold pretreatment on the cytoskeleton and the ultrastructure of maize microspores when cultured in vitro. Plant Cell Tissue Organ Cult 123:257–271
18. Ferrie AMR, Caswell KL (2011) Isolated microspore culture techniques and recent progress for haploid and doubled haploid plant production. Plant Cell Tissue Organ Cult 104:301–309
19. Forster BP, Heberle-Bors E, Kasha KJ, Touraev A (2007) The resurgence of haploids in higher plants. Trends Plant Sci 12:368–375
20. Geiger HH, Gordillo GA (2009) Doubled haploids in hybrid maize breeding. Maydica 54:485–499
21. González JM, Muñiz LM, Jouve N (2005) Mapping of QTLs for androgenetic response based on a molecular genetic map of × Triticosecale Wittmack. Genome 48:999–1009
22. Guo Y-D, Hisano H, Shimamoto Y, Yamada T (2009) Transformation of androgenic-derived Festulolium plants (Lolium perenne L. × Festuca pratensis Huds.) by Agrobacterium tumefaciens. Plant Cell Tissue Organ Cult 96:219–227
23. Guo B, Wang D, Guo Z, Beavis WD (2013) Family-based association mapping in crop species. Theor Appl Genet 126:1419–1430
24. Halberg N, Olesen A, Tuvesson IKD, Andersen SB (1990) Genotypes of perennial ryegrass (Lolium perenne L.) with high anther-culture response through hybridization. Plant Breed 105:89–94
25. He P, Shen L, Lu C, Chen Y, Zhu L (1998) Analysis of quantitative trait loci which contribute to anther culturability in rice (Oryza sativa L.). Mol Breed 4:165–172
26. Jacquard C, Asakaviciute R, Hamalian AM, Sangwan RS, Devaux P, Clément C (2006) Barley anther culture: effects of annual cycle and spike position on microspore embryogenesis and albinism. Plant Cell Rep 25:375–381
27. Kindiger B (2016) Generation of paternal dihaploids in tall fescue. Grassl Sci 62:1–5
28. Kiviharju E, Moisander S, Tanhuanp P (2017) Oat anther culture and use of DH-lines for genetic mapping. In: Gasparis S (ed) Oat: methods in molecular biology, vol 1536. Springer, New York, pp 71–93
29. Krzewska M, Czyczyło-Mysza I, Dubas E, Gołebiowska-Pikania G, Golemiec E, Stojałowski S, Chrupek M, Żur I (2012) Quantitative trait loci associated with androgenic responsiveness in triticale (× Triticosecale Wittm.) anther culture. Plant Cell Rep 31:2099–2108
30. Krzewska M, Czyczyło-Mysza I, Dubas E, Gołebiowska-Pikania G, Żur I (2015) Identification of QTLs associated with albino plant formation and some new facts concerning green versus albino ratio determinants in triticale (× Triticosecale Wittm.) anther culture. Euphytica 206:263–278
31. Kumari M, Clarke HJ, Small I, Siddique KHM (2009) Albinism in plants: a major bottleneck in wide hybridization, androgenesis and doubled haploid culture. Crit Rev Plant Sci 28:393–409
32. Lantos C, Weyen J, Orsini JM, Gnad H, Schlieter B, Lein V, Kontowski S, Jacobi A, Mihály R, Broughton S, Pauk J (2013) Efficient application of in vitro anther culture for different European winter wheat (Triticum aestivum L.) breeding programmes. Plant Breed 132:149–154
33. Lantos C, Bóna L, Boda K, Pauk J (2014) Comparative analysis of in vitro anther- and isolated microspore culture in hexaploid triticale (× Triticosecale Wittmack) for androgenic parameters. Euphytica 197:27–37
34. Larsen ET, Tuvesson IK, Andersen SB (1991) Nuclear genes affecting percentage of green plants in barley (Hordeum vulgare L.) anther culture. Theor Appl Genet 82:417–420
35. Lazar MD, Baenziger PS, Schaeffer GW (1984) Combining abilities and heritability of callus formation and plantlet regeneration in wheat (Triticum aestivum L.) anther cultures. Theor Appl Genet 68:131–134
36. Madsen S, Olesen A, Dennis B, Andersen SB (1995) Inheritance of anther-culture response in perennial ryegrass (Lolium perenne L.). Plant Breed 114:165–168
37. Makowska K, Oleszczuk S (2014) Albinism in barley androgenesis. Plant Cell Rep 33:385–392
38. Maluszynski M, Kasha KJ, Forster BP, Szarejko I (2003) Doubled haploid production in crop plants: a manual. Kluwer Academic Publishers, Dordrecht
39. Manninen OM (2000) Associations between anther-culture response and molecular markers on chromosomes 2 H, 3 H and 4 H of barley (Hordeum vulgare L.). Theor Appl Genet 100:57–62
40. Manzanares C, Barth S, Thorogood D, Byrne SL, Yates S, Czaban A, Asp T, Yang B, Studer B (2016) A gene encoding a DUF247 domain protein cosegregates with the S self-incompatibility locus in perennial ryegrass. Mol Biol Evol 33:870–884
41. Melchinger AE, Molenaar WS, Mirdita V, Schipprack W (2016) Colchicine alternatives for chromosome doubling in maize haploids for doubled-haploid production. Crop Sci 56:559–569
42. Mishra R, Rao GJN (2016) In-vitro androgenesis in rice: advantages, constraints and future prospects. Rice Sci 23:57–68
43. Moieni A, Lokos-Toth K, Sarrafi A (1997) Evidence for genetic control and media effect on hapioid regeneration in the anther culture of hexaploid wheat (Triticum aestivum L.). Plant Breed 116:502–505
44. Murigneux A, Bentolila S, Hardy T, Baud S, Guitton C, Jullien H, Ben Tahar S, Freyssinet G, Beckert M (1994) Genotypic variation of quantitative trait loci controlling in vitro androgenesis in maize. Genome 37:970–976
45. Niak N, Rout P, Umakanta N, Verma RL, Katara JL, Sahoo KK, Singh ON, Samantaray S (2016) Development of doubled haploids from an elite indica rice hybrid (BS6444G) using anther culture. Plant Cell Tissue Organ Cult 128:679–689
46. Nielsen NH, Andersen SU, Stougaard J, Jensen A, Backes G, Jahoor A (2015) Chromosomal regions associated with the in vitro culture response of wheat (Triticum aestivum L.) microspores. Plant Breed 134:255–263
47. Niu Z, Jiang A, Abu Hammad W, Oladzababbasabadi A, Xu SS, Mergoum M, Elias EM (2014) Review of doubled haploid production in durum and common wheat through wheat × maize hybridization. Plant Breed 133:313–320
48. Obsa BT, Eglinton J, Coventry S, March T, Langridge P, Fleury D (2016) Genetic analysis of developmental and adaptive traits in three doubled haploid populations of barley (Hordeum vulgare L.). Theor Appl Genet 129:1139–1151
49. Olesen A, Andersen SB, Due IK (1988) Anther culture response in perennial ryegrass (Lolium perenne L.). Plant Breed 101:60–65
50. Oleszczuk S, Tyrka M, Zimny J (2014) The origin of clones among androgenic regenerants of hexaploid triticale. Euphytica 198:325–336
51. Opsahl-Ferstad H-G (1993) Androgenetic response in grasses. I. Anther culture in perennial ryegrass (Lolium perenne L.). II. Molecular studies of embryogenesis in barley (Hordeum vulgare L.). Dissertation, Agricultural University of Norway
52. Opsahl-Ferstad H-G, Bjørnstad Å, Rognli OA (1994a) Influence of medium and cold pretreatment on androgenetic response in Lolium perenne L. Plant Cell Rep 13:594–600
53. Opsahl-Ferstad H-G, Bjørnstad Å, Rognli OA (1994b) Genetic control of androgenetic response in Lolium perenne L. Theor Appl Genet 89:133–138
54. Pembleton LW, Shinozuka H, Wang J, Spangenberg GC, Forster JW, Cogan NOI (2015) Design of an F1 hybrid breeding strategy for ryegrasses based on selection of self-incompatibility locus-specific alleles. Front Plant Sci 6:764
55. R Core Team (2016) R: a language and environment for statistical computing. https://www.r-project.org/. Accessed 1 Feb 2017
56. RStudio Team (2015) RStudio: integrated development for R. http://www.rstudio.com/. Accessed 1 Feb 2017
57. Rubtsova M, Gnad H, Melzer M, Weyen J, Gils M (2013) The auxins centrophenoxine and 2,4-D differ in their effects on non-directly induced chromosome doubling in anther culture of wheat (T. aestivum L.). Plant Biotechnol Rep 7:247–255
58. Sannemann W, Huang BE, Mathew B, Léon J (2015) Multi-parent advanced generation inter-cross in barley: high-resolution quantitative trait locus mapping for flowering time as a proof of concept. Mol Breed 35:86
59. Schedel S, Pencs S, Hensel G et al (2016) RNA-guided Cas9-induced mutagenesis in tobacco followed by efficient genetic fixation in doubled haploid plants. Front Plant Sci 7:1995
60. Seguí-Simarro JM (2010) Androgenesis revisited. Bot Rev 76:377–404
61. Seguí-Simarro JM (2015) Editorial: doubled haploidy in model and recalcitrant species. Front Plant Sci. doi:10.3389/fpls.2015.01175
62. Seguí-Simarro JM, Nuez F (2008) How microspores transform into haploid embryos: changes associated with embryogenesis induction and microspore-derived embryogenesis. Physiol Plant 134:1–12
63. Seldimirova OA, Kruglova NN (2015) Androclinic embryoidogenesis in vitro in cereals. Biol Bull Rev 5:156–165
64. Sinha R, Eudes F (2015) Dimethyl tyrosine conjugated peptide prevents oxidative damage and death of triticale and wheat microspores. Plant Cell Tissue Organ Cult 122:227–237
65. Ślusarkiewicz-Jarzina A, Pudelska H, Woźna J, Pniewski T (2017) Improved production of doubled haploids of winter and spring triticale hybrids via combination of colchicine treatments on anthers and regenerated plants. J Appl Genet. doi:10.1007/s13353-016-0387-9
66. Stanis VA, Butenko RG (1984) Developing viable haploid plants in anther culture of ryegrass. Dokl Biol Sci 275:249–251
67. Studer B, Asp T, Frei U et al (2008) Expressed sequence tag-derived microsatellite markers of perennial ryegrass (Lolium perenne L.). Mol Breed 21:533–548
68. Studer B, Jensen LB, Fiil A, Asp T (2009) “Blind” mapping of genic DNA sequence polymorphisms in Lolium perenne L. by high resolution melting curve analysis. Mol Breed 24:191–199
69. Tenhola-Roininen T, Immonen S, Tanhuanp P (2006) Rye doubled haploids as a research and breeding tool—a practical point of view. Plant Breed 125:584–590
70. Torp AM, Hansen ALA, Andersen SB (2001) Chromosomal regions associated with green plant regeneration in wheat (Triticum aestivum L.) anther culture. Euphytica 119:377–387
71. Tuvesson IK, Pedersen S, Andersen SB (1989) Nuclear genes affecting albinism in wheat (Triticum aestivum L.) anther culture. Theor Appl Genet 78:879–883
72. Wang X, Hu H (1984) The effect of Potato II medium for triticale anther culture. Plant Sci Lett 36(3):237–239
73. Wędzony M, Żur I, Krzewska M, Dubas E, Szechyńska-Hebda M, Wąsek I (2015) Doubled haploids in triticale. In: Eudes F (ed) Triticale. Springer, Cham, pp 111–128
74. Wickham H (2009) ggplot2: elegant graphics for data analysis. https://cran.r-project.org/package=ggplot2. Accessed 1 Feb 2017
75. Wilke CO (2016) cowplot: streamlined plot theme and plot annotations for ‘ggplot2’. https://cran.r-project.org/package=cowplot. Accessed 1 Feb 2017
76. Würschum T, Tucker MR, Maurer HP, Leiser W (2015) Ethylene inhibitors improve efficiency of microspore embryogenesis in hexaploid triticale. Plant Cell Tissue Organ Cult 122:751–757
77. Żur I, Dubas E, Krzewska M, Janowiak F, Hura K, Pociecha E, Bączek-Kwinta R, Płażek A (2014) Antioxidant activity and ROS tolerance in triticale (× Triticosecale Wittm.) anthers affect the efficiency of microspore embryogenesis. Plant Cell Tissue Organ Cult 119:79–94