Proportion of parental genomes in hybrids Allium cepa × A. roylei determines which one becomes dominant

. 2025 Jun ; 18 (2) : e70016.

Jazyk angličtina Země Spojené státy americké Médium print

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid40156203

Grantová podpora
CZ.02.01.01/00/22_008/0004581 ERDF Programme Johannes Amos Comenius
24-10010S Grantová Agentura České Republiky

Interspecific hybridization leads to complex interactions between the parental genomes, often in the form of genome dominance, where one genome prevails over the other. This phenomenon has been attributed to differential chromosome behavior during meiotic division and may involve either female or male meiosis, or both. In hybrids of Allium cepa × A. roylei, only female meiosis is involved, favoring the transmission of A. roylei chromosomes; male meiosis leads to the development of gametes with equal proportion of parental genomes. Female meiotic drive shifts the genome composition from 8R (A. roylei) + 8C (A. cepa) chromosomes in F1 to 9.3R + 6.7C in F2. In this study of two successive backcross generations with A. cepa (BC1 [first backcross generation] and BC1F1 [progeny after intercross of the first backcross generation]), we observed a change in genome dominance: the A. roylei genome, initially dominant during the meiosis in the F1 hybrids, became submissive in BC1, resulting in a genome composition skewed toward A. cepa. Among 23 BC1 and 236 BC1F1 plants, we observed a significant deviating trend of gradual reduction in A. roylei chromosome representation. The reduction was higher in the lineages with more unequal starting proportion of the parental genomes. This study highlights the dynamic nature of genomic interactions in hybrids and raises questions about the underlying molecular mechanisms driving these changes in dominance, as well as the potential for manipulating these interactions for agricultural benefit. Further exploration of the chromosomal behavior during meiosis across various hybrids will deepen our understanding of non-Mendelian inheritance patterns and their implications in plant breeding.

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Akera, T. , Chmátal, L. , Trimm, E. , Yang, K. , Aonbangkhen, C. , Chenoweth, D. M. , Janke, C. , Schultz, R. M. , & Lampson, M. A. (2017). Spindle asymmetry drives non‐Mendelian chromosome segregation. Science, 358, 668–672. 10.1126/science.aan0092 PubMed DOI PMC

Cao, Y. , Zhao, K. , Xu, J. , Wu, L. , Hao, F. , Sun, M. , Dong, J. , Chao, G. , Zhang, H. , Gong, X. , Chen, Y. , Chen, C. , Qian, W. , Pires, J. , Edger, P. , & Xiong, Z. (2023). Genome balance and dosage effect drive allopolyploid formation in Brassica . Proceedings of The National Academy of Sciences of the United States of America, 120, Article e2217672120. PubMed PMC

de Vries, J. N. , Wietsma, W. A. , & de Vries, T. (1992). Introgression of leaf‐blight resistance from Allium roylei Stearn into onion (Allium cepa L.). Euphytica, 62, 127–133.

Ferreira, M. T. M. , Glombik, M. , Perničková, K. , Duchoslav, M. , Scholten, O. , Karafiátová, M. , Techio, V. H. , Doležel, J. , Lukaszewski, A. J. , & Kopecký, D. (2020). Direct evidence for crossover and chromatid interference in meiosis of two plant hybrids (Lolium multiflorum×Festuca pratensis and Allium cepa×A. roylei) . Journal of Experimental Botany, 72(2), 254–267. 10.1093/jxb/eraa455 PubMed DOI PMC

Glombik, M. , Bačovský, V. , Hobza, R. , & Kopecký, D. (2020). Competition of parental genomes in plant hybrids. Frontiers in Plant Science, 11, Article 200. 10.3389/fpls.2020.00200 PubMed DOI PMC

Humphreys, M. , & Thorogood, D. (1993). Disturbed Mendelian segregation at isozyme marker loci in early backcrosses of Lolium multiflorum × Festuca pratensis hybrids to L. multiflorum . Euphytica, 66, 11–18. 10.1007/BF00023503 DOI

Jauhar, P. P. (1993). Cytogenetics of the Festuca‐Lolium complex: Relevance to breeding. Springer.

Kamstra, S. A. , Kuipers, A. G. J. , De Jeu, M. J. , Ramanna, M. S. , & Jacobsen, E. (1999). The extent and position of homoeologous recombination in a distant hybrid of Alstroemeria: A molecular cytogenetic assessment of first generation backcross progenies. Chromosoma, 108, 52–63. PubMed

Karlov, G. I. , Khrustaleva, L. I. , Lim, K. B. , & van Tuyl, J. M. (1999). Homoeologous recombination in 2n‐gametes producing interspecific hybrids of Lilium (Liliaceae) studied by genomic in situ hybridization (GISH). Genome, 42, 681–686. 10.1139/g98-167 DOI

Katche, E. , Schierholt, A. , Becker, H. , Batley, J. , & Mason, A. (2023). Fertility, genome stability, and homozygosity in a diverse set of resynthesized rapeseed lines. Crop Journal, 11, 468–477. 10.1016/j.cj.2022.07.022 DOI

Khan, N. , Barba‐Gonzalez, R. , Ramanna, M. S. , Visser, R. G. F. , & Van Tuyl, J. M. (2009). Construction of chromosomal recombination maps of three genomes of lilies (Lilium) based on GISH analysis. Genome, 52, 238–251. 10.1139/G08-122 PubMed DOI

King, I. , Morgan, W. , Harper, J. , & Thomas, H. (1999). Introgression mapping in the grasses. II. Meiotic analysis of the Lolium perenne/Festuca pratensis triploid hybrid. Heredity, 82, 107–112. 10.1038/sj.hdy.6884680 DOI

Kopecký, D. , Bartoš, J. , Zwierzykowski, Z. , & Doležel, J. (2009). Chromosome pairing of individual genomes in tall fescue (Festuca arundinacea Schreb.), its progenitors, and hybrids with Italian ryegrass (Lolium multiflorum Lam.). Cytogenetic and Genome Research, 124, 170–178. 10.1159/000207525 PubMed DOI

Kopecký, D. , Horáková, L. , Duchoslav, M. , & Doležel, J. (2019). Selective elimination of parental chromatin from introgression cultivars of xFestulolium (Festuca × Lolium). Sustainability, 11, Article 3153. 10.3390/su11113153 DOI

Kopecky, D. , Lukaszewski, A. , & Gibeault, V. (2005). Reduction of ploidy level by androgenesis in intergeneric Lolium‐Festuca hybrids for turf grass breeding. Crop Science, 45, 274–281. 10.2135/cropsci2005.0274a DOI

Kopecký, D. , Lukaszewski, A. J. , & Doležel, J. (2008). Cytogenetics of Festulolium (Festuca × Lolium hybrids). Cytogenetic and Genome Research, 120, 370–383. 10.1159/000121086 PubMed DOI

Kopecký, D. , Scholten, O. , Majka, J. , Burger‐Meijer, K. , Duchoslav, M. , & Bartoš, J. (2022). Genome dominance in Allium hybrids (A. cepa × A. roylei). Frontiers in Plant Science, 13, Article 854127. 10.3389/fpls.2022.854127 PubMed DOI PMC

Kopecký, D. , Šimoníková, D. , Ghesquière, M. , & Doležel, J. (2017). Stability of genome composition and recombination between homoeologous chromosomes in Festulolium (Festuca × Lolium) cultivars. Cytogenetic and Genome Research, 151, 106–114. 10.1159/000458746 PubMed DOI

Kosmala, A. , Zwierzykowska, E. , & Zwierzykowski, Z. (2006). Chromosome pairing in triploid intergeneric hybrids of Festuca pratensis with Lolium multiflorum, revealed by GISH. Journal of Applied Genetics, 47, 215–220. 10.1007/BF03194626 PubMed DOI

Leflon, M. , Eber, F. , Letanneur, J. C. , Chelysheva, L. , Coriton, O. , Huteau, V. , Ryder, C. D. , Barker, G. , Jenczewski, E. , & Chèvre, A. M. (2006). Pairing and recombination at meiosis of Brassica rapa (AA) × Brassica napus (AACC) hybrids. Theoretical and Applied Genetics, 113, 1467–1480. 10.1007/s00122-006-0393-0 PubMed DOI

Lopez‐Lavalle, L. A. B. , & Brubaker, C. L. (2007). Frequency and fidelity of alien chromosome transmission in Gossypium hexaploid bridging populations. Genome, 50, 479–491. PubMed

Majka, J. , Glombik, M. , Doležalová, A. , Kneřová, J. , Ferreira, M. T. M. , Zwierzykowski, Z. , Duchoslav, M. , Studer, B. , Doležel, J. , Bartoš, J. , & Kopecký, D. (2023). Both male and female meiosis contribute to non‐Mendelian inheritance of parental chromosomes in interspecific plant hybrids (Lolium × Festuca). New Phytologist, 238, 624–636. 10.1111/nph.18753 PubMed DOI

Masoudi‐Nejad, A. , Nasuda, S. , Mcintosh, R. A. , Endo, T. R. , & Endo, T. R. (2002). Transfer of rye chromosome segments to wheat by a gametocidal system. Chromosome Research, 10, 349–357. 10.1023/A:1016845200960 PubMed DOI

Naganowska, B. , Zwierzykowski, Z. , & Zwierzykowska, E. (2001). Meiosis and fertility of reciprocal triploid hybrids of Lolium multiflorum with Festuca pratensis . Journal of Applied Genetics, 42, 247–255. PubMed

Sandler, L. , Hiraizumi, Y. , & Sandler, I. (1959). Meiotic drive in natural populations of Drosophila melanogaster. 1. The cytogenetic basis of segregation distortion. Genetics, 44, 233–250. 10.1093/genetics/44.2.233 PubMed DOI PMC

Scholten, O. E. , van Kaauwen, M. P. W. , Shahin, A. , Hendrickx, P. M. , Keizer, L. C. P. , Burger, K. , van Heusden, A. W. , van der Linden, C. G. , & Vosman, B. (2016). SNP‐markers in Allium species to facilitate introgression breeding in onion. BMC Plant Biology, 16, Article 187. 10.1186/s12870-016-0879-0 PubMed DOI PMC

Sears, E. R. , & Okamoto, M. (1958). Intergenomic chromosome relationship in hexaploid wheat. In Proceedings of 10th international congress of genetics (pp. 258–259). University of Toronto Press.

Svačina, R. , Sourdille, P. , Kopecký, D. , & Bartoš, J. (2020). Chromosome pairing in polyploid grasses. Frontiers in Plant Science, 11, Article 1056. 10.3389/fpls.2020.01056 PubMed DOI PMC

Takahashi, C. , Leitch, I. J. , Ryan, A. , Bennett, M. D. , & Brandham, P. E. (1997). The use of genomic in situ hybridization (GISH) to show transmission of recombinant chromosomes by a partially fertile bigeneric hybrid, Gasteria lutzii × Aloe aristata (Aloaceae), to its progeny. Chromosoma, 105, 342–348. PubMed

van Heusden, A. W. , van Ooijen, J. W. , Vrielink‐van Ginkel, R. , Verbeek, W. H. J. , Wietsma, W. A. , & Kik, C. (2000). A genetic map of an interspecific cross in Allium based on amplified fragment length polymorphism (AFLPTM) markers. Theoretical and Applied Genetics, 100, 118–126.

Yang, Y. , Wei, X. , Shi, G. , Wei, F. , Braynen, J. , Zhang, J. , Tian, B. , Cao, G. , & Zhang, X. (2017). Molecular and cytological analyses of A and C genomes at meiosis in synthetic allotriploid Brassica hybrids (ACC) between B. napus (AACC) and B. oleracea (CC). Journal of Plant Biology, 60, 181–188. 10.1007/s12374-016-0221-2 DOI

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