Abstract
Lilium produce fritillaria-type embryo sacs and it is easy to obtain aneuploids from 3x × 2x/4x interploidy hybridization. However, there are no reports about introgressive hybridization using aneuploids as male parents because gene imbalance or irregular abnormal meiosis are detrimental to the viability and fertility of aneuploid lilies. In the present study, two partial male fertile aneuploid lines, J1834 and J1859, were selected and crossed with diploid (AA) and tetraploid (AAAA) Asiatic lilies using normal pollination and embryo rescue, and genomic in situ hybridization (GISH) was used to analyze the two aneuploids and their progenies. The GISH results indicated that the formula of genomic composition of J1834 was “LAAA2−”, i.e., 2n = 4x − 2 = 46 = 9 L + 37 A, and that of J1859 was “LAAA5+”, i.e., 2n = 4x + 5 = 53 = 4 L + 48 A + 1 L/A; all the progenies from the “2x/4x × aneuploid” were aneuploid and the alien L-chromosomes in the aneuploid progenies were much less than their aneuploid parents, and three of them, 20085-1, 20085-11 and 20085-12, contained only one small alien L-chromosomal segment. It was concluded that aneuploids could be used as parents to transfer one or a few desirable genes into new cultivars in lily introgression breeding.
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References
Asano Y (1982) Overcoming interspecific hybrid sterility in Lilium. J Japan Soc Hort Sci 51:75–81. https://doi.org/10.2503/jjshs.51.75
Barba-Gonzalez R, Lim KB, Ramanna MS, Visser RGF, van Tuyl JM (2005) Occurrence of 2n gametes in the F1 hybrids of Oriental × Asiatic lilies (Lilium): relevance to intergenomic recombination and backcrossing. Euphytica 143:67–73
Barba-Gonzalez R, Lokker AC, Lim KB, Ramanna MS, Van Tuyl JM (2004) Use of 2n gametes for the production of sexual polyploids from sterile Oriental × Asiatic hybrids of lilies (Lilium). Theor App Genet 109:1125–1132. https://doi.org/10.1007/s00122-004-1739-0
Barba-Gonzalez R, Miller CT, Ramanna MS, Van Tuyl JM (2006a) Nitrous oxide (N2O) induces 2n gametes in sterile F1 hybrids between Oriental × Asiatic lily (Lilium) hybrids and leads to intergenomic recombination. Euphytica 148:303–309. https://doi.org/10.1007/s10681-005-9032-0
Barba-Gonzalez R, Ramanna MS, Visser RGF, Van Tuyl JM (2005b) Intergenomic recombination in F1 lily hybrids (Lilium) and its significance for genetic variation in the BC1 progenies as revealed by GISH and FISH. Genome 48:884–894. https://doi.org/10.1139/g05-057
Barba-Gonzalez R, van Silfhout AA, Visser RGF, Ramanna MS, van Tuyl JM (2006b) Progenies of allotriploids of Oriental × Asiatic lilies (Lilium) examined by GISH analysis. Euphytica 151:243–250. https://doi.org/10.1007/s10681-006-9148-x
Birchler JA, Veitia RA (2007) The gene balance hypothesis: from classical genetics to modern genomics. Plant Cell 19(2):395–402. https://doi.org/10.1105/tpc.106.049338
Birchler JA, Riddle NC, Auger DL, Veitia RA (2005) Dosage balance in gene regulation: biological implications. Trends Genet 21:219–226. https://doi.org/10.1016/j.tig.2005.02.010
Brandham PE (1982) Inter-embryo competition in the progeny of autotriploid Aloineae (Liliaceae). Genetica 59:29–42
Cao Q, Lian Y, Wang L, Zhang Q, Zhao Y, Jia G, He H (2019) Physical mapping of 45S rDNA loci in Lilium OT hybrids and interspecific hybrids with Lilium regale. Sci Hort 252:48–54. https://doi.org/10.1016/j.scienta.2019.03.035
Carputo D, Barone A (2005) Ploidy level manipulations in potato through sexual hybridization. Ann Appl Biol 146:71–79
Chen HF, Wang H, Li ZY (2007) Production and genetic analysis of partial hybrids in intertribal crosses between Brassica species (B. rapa, B. napus) and Capsella bursa-pastoris. Plant Cell Rep 26:1791–1800. https://doi.org/10.1007/s00299-007-0392-x
Chen Y, Wang Y, Wang K, Zhu X, Guo W, Zhang T, Zhou B (2014) Construction of a complete set of alien chromosome addition lines from Gossypium australe in Gossypium hirsutum: morphological, cytological, and genotypic characterization. Theor Appl Genet 127:1105–1121. https://doi.org/10.1007/s00122-014-2283-1
Choi JY, Platts AE, Fuller DQ, Hsing YI, Wing RA, Purugganan MD (2017) The rice paradox: multiple origins but single domestication in Asian rice. Mol Biol Evol 34(4):969–979. https://doi.org/10.1093/molbev/msx049
Chung MY, Chung JD, Ramanna M, Van Tuyl JM, Lim KB (2013) Production of polyploids and unreduced gametes in Lilium auratum × L. henryi hybrid. Int J Biol Sci 9:693–701. https://doi.org/10.7150/ijbs.6427
Cui L, Sun Y, Xiao K, Wan L, Zhong J, Liu Y, Xie Q, Zhou S (2022) Analysis on the abnormal chromosomal behaviour and the partial female fertility of allotriploid Lilium – ‘Triumphator’ (LLO) is not exceptional to the hypothesis of lily interploid hybridizations. Sci Hort 293:110746. https://doi.org/10.1016/j.scienta.2021.110746
De Jong PC (1974) Some notes on the evolution of lilies. North Am Lily Soc 27:23–28
Flowers JM, Hazzouri KM, Gros-Balthazard M, Mo Z, Koutroumpa K, Perrakis A, Ferrand S, Khierallah HSM, Fuller DQ, Aberlenc F, Fournaraki C, Michael D (2019) Cross-species hybridization and the origin of North African date palms. Proc Natl Acad Sci USA 116(5):1651–1658. https://doi.org/10.1073/pnas.1817453116
Hao M, Zhang L, Ning S, Huang L, Yuan Z, Wu B, Yan Z, Dai S, Jiang B, Zheng Y, Liu D (2020) The resurgence of introgression breeding, as exemplified in wheat improvement. Front Plant Sci 11:252
Hussein S, Spies JJ, Pretorius ZA, Labuschagne MT (2005) Chromosome locations of leaf rust resistance genes in selected tetraploid wheats through substitution lines. Euphytica 141:209–216. https://doi.org/10.1007/s10681-005-7846-4
Jiang J, Friebe B, Gill BS (1993) Recent advances in alien gene transfer in wheat. Euphytica 73:199–212. https://doi.org/10.1007/BF00036700
Khan N, Zhou S, Ramanna MS, Arens P, Herrera J, Visser RGF, Van Tuyl JM (2009) Potential for analytic breeding in allopolyploids: an illustration from Longiflorum × Asiatic hybrid lilies (Lilium). Euphytica 166:399–409. https://doi.org/10.1007/s10681-008-9824-0
Khush GS (2010) Trisomics and alien addition lines in rice. Plant Breed 60:469–474. https://doi.org/10.1270/jsbbs.60.469
Lim KB, Ramanna MS, De Jong JH, Jacobsen E, Van Tuyl JM (2001a) Indeterminate meiotic restitution (IMR): a novel type of meiotic nuclear restitution mechanism detected in interspecific lily hybrids by GISH. Theor Appl Genet 103:219–230. https://doi.org/10.1007/s001220100638
Lim KB, Ramanna MS, Jacobsen E, Van Tuyl JM (2003) Evaluation of BC2 progenies derived from 3x-2x and 3x-4x crosses of Lilium hybrids: a GISH analysis. Theor Appl Genet 106:568–574. https://doi.org/10.1007/s00122-002-1070-6
Lim KB, Ramanna MS, van Tuyl JM (2001b) Comparison of homoeologous recombination frequency between mitotic and meiotic polyploidization in BC1 progeny of interspecific lily hybrids. Acta Hortic 552:65–72. https://doi.org/10.17660/ActaHortic.2001.552.6
Liu Y, Zhang L, Sun Y, Zhou S (2021) The common occurrence of 2n eggs by lily F1 distant hybrids and its significance on lily breeding: a case of analyzing OT hybrids. Euphytica 217:204. https://doi.org/10.1007/s10681-021-02935-4
Luo J, Ramanna MS, Arens P, Niu L, Van Tuyl JM (2012) GISH analyses of backcross progenies of two Lilium species hybrids and their relevance to breeding. J Hortic Sci Biotechnol 87:654–660. https://doi.org/10.1080/14620316.2012.11512926
Maheshwari P (1948) The angiosperm embryo sac. Bot Rev 14:1–56
Mayrose I, Lysak MA (2021) The evolution of chromosome numbers: mechanistic models and experimental approaches. Genome Biol Evol 13(2):evaa220. https://doi.org/10.1093/gbe/evaa220
Natenapit J, Taketa S, Narumi T, Fukai S (2010) Crossing of allotriploid LLO hybrid and Asiatic lilies (Lilium). Hortic Environ Biote 51:426–430
Placido DF, Campbell MT, Folsom JJ, Cui X, Kruger GR, Baenziger PS, Walia H (2013) Introgression of novel traits from a wild wheat relative improves drought adaptation in wheat. Plant Physiol 161:1806–1819. https://doi.org/10.1104/pp.113.214262
Ramsey J, Schemske DW (1998) Pathways, mechanisms, and rates of polyploidy formation in flowering plants. Annu Rev Ecol Syst 29:467–501
Suzuki T, Yamagishi M (2015) Aneuploids without bulbils segregated in F1 hybrids derived from triploid Lilium lancifolium and diploid L. leichtlinii crosses. Hortic J 85:224–231. https://doi.org/10.2503/hortj.MI-089
Van Tuyl JM, Arens P (2011) Lilium: breeding history of the modern cultivar assortment. Acta Hortic 900:223–230. https://doi.org/10.17660/ActaHortic.2011.900.27
Van Tuyl JM, Arens P, Shahin A, Marasek-Ciolakowska A, Barba-Gonzalez R, Kim HT, Lim KB (2018) Lilium. In: Van Huylenbroeck J (ed) Ornamental crops. Handbook of plant breeding, vol 11. Springer, Cham, pp 481–512. https://doi.org/10.1007/978-3-319-90698-0_20
Van Tuyl JM, Van Dijken A, Chi HS, Lim KB, Villemoes S, Van Kronenburg BCE (2000) Breakthroughs in interspecific hybridization of lily. Acta Hortic 508:83–90. https://doi.org/10.17660/ActaHortic.2000.508.10
Van Tuyl JM, Van Diën MP, Van Creij MGM, Van Kleinwee TCM, Franken J, Bino RJ (1991) Application of in vitro pollination, ovary culture, ovule culture and embryo rescue for overcoming incongruity barriers in interspecifc Lilium crosses. Plant Sci 74:115–126. https://doi.org/10.1016/0168-9452(91)90262-7
Wang Q, Wang J, Zhang Y, Zhang Y, Xu S, Lu Y (2015) The application of fluorescence in situ hybridization in different ploidy levels cross-breeding of lily. PloS One 10:e0126899. https://doi.org/10.1371/journal.pone.0126899
Wu L, Wan L, Cui L, Xiao K, Zhong J, Liu Y, Zeng J, Sun Y, Zhou S (2021) Analysis of the cross-compatibility of Lilium brownii var. viridulum and L. davidii var. unicolor. Sci Hortic 284:110130
Xi M, Van Tuyl JM, Arens P (2015) GISH analyzed progenies generated from allotriploid lilies as female parent. Sci Hortic 183:130–135. https://doi.org/10.1016/j.scienta.2014.12.022
Xie S, Ramanna MS, Van Tuyl JM (2010) Simultaneous identification of three different genomes in Lilium hybrids through multicolour GISH. Acta Hortic 855:299–304. https://doi.org/10.17660/ActaHortic.2010.855.45
Xuan S, Li M, Zhang C, Shen S, Liu L, Wang D (2002) Plant aneuploids and their use in the genetic studies and breeding. J Agric Univ Hebei 25:47–50 (in Chinese with an English abstract)
Zhou S (2007) Intergenomic recombination and introgression breeding in Longiflorum × Asiatic lilies. In: PhD thesis. Wageningen University, pp 111
Zhou S (2011) The potential of aneuploids for selecting new lily cultivars. In: Helsley, Van Tuyl (eds) The Lily yearbook of the North American Lily society. The North American Lily Society, Inc, pp 100–105
Zhou S, Li K, Zhou G (2012) Analysis of endosperm development of allotriploid × diploid/tetraploid crosses in Lilium. Euphytica 184:401–412. https://doi.org/10.1007/s10681-011-0609-5
Zhou S, Ramanna MS, Visser RGF, Van Tuyl JM (2008b) Genome composition of triploid lily cultivars derived from sexual polyploidization of Longiflorum × Asiatic hybrids (Lilium). Euphytica 160:207–215. https://doi.org/10.1007/s10681-007-9538-8
Zhou S, Ramanna MS, Visser RGF, Van Tuyl JM (2008) Analysis of the meiosis in the F1 hybrids of Longiflorum × Asiatic (LA) of lilies (Lilium) using genomic in situ hybridization. J Genet Genom 35:687–695. https://doi.org/10.1016/S1673-8527(08)60091-0
Zhou S, Yuan G, Xu P, Gong H (2014) Study on lily introgression breeding using allotriploids as maternal parents in interploid hybridizations. Breed Sci 64:97–102. https://doi.org/10.1270/jsbbs.64.97
Zhou S, Zhou G, Li K (2011) Euploid endosperm of triploid × diploid/tetraploid crosses results in aneuploid embryo survival in Lilium. Hort Sci 46:558–562. https://doi.org/10.21273/HORTSCI.46.4.558
Zhu B, Shao Y, Pan Q, Ge X, Li Z (2015) Genome-wide gene expression perturbation induced by loss of C2 chromosome in allotetraploid Brassica napus L. Front Plant Sci 6:763
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The research was supported by the National Natural Science Foundation of China No. 31572154 and 31460527.
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JZ did most of experiments and summarized the results. JC, SL, ZW and DY contributed some parts related with the research. SZ did conceptualization, methodology, and manuscript writing and correction.
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Zhong, J., Cai, J., Liu, S. et al. GISH analysis of introgressive hybridization using aneuploids as male parents in Lilium. Euphytica 218, 167 (2022). https://doi.org/10.1007/s10681-022-03116-7
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DOI: https://doi.org/10.1007/s10681-022-03116-7