Genome Dominance in Allium Hybrids (A. cepa × A. roylei)

Abstract

Genome dominance is a phenomenon in wide hybrids when one of the parental genomes becomes “dominant,” while the other genome turns to be “submissive.” This dominance may express itself in several ways including homoeologous gene expression bias and modified epigenetic regulation. Moreover, some wide hybrids display unequal retention of parental chromosomes in successive generations. This may hamper employment of wide hybridization in practical breeding due to the potential elimination of introgressed segments from progeny. In onion breeding, Allium roylei (A. roylei) Stearn has been frequently used as a source of resistance to downy mildew for cultivars of bulb onion, Allium cepa (A. cepa) L. This study demonstrates that in A. cepa × A. roylei hybrids, chromosomes of A. cepa are frequently substituted by those of A. roylei and in just one generation, the genomic constitution shifts from 8 A. cepa + 8 A. roylei chromosomes in the F1 generation to the average of 6.7 A. cepa + 9.3 A. roylei chromosomes in the F2 generation. Screening of the backcross generation A. cepa × (A. cepa × A. roylei) revealed that this shift does not appear during male meiosis, which is perfectly regular and results with balanced segregation of parental chromosomes, which are equally transmitted to the next generation. This indicates that female meiotic drive is the key factor underlying A. roylei genome dominance. Single nucleotide polymorphism (SNP) genotyping further suggested that the drive has different strength across the genome, with some chromosome segments displaying Mendelian segregation, while others exhibiting statistically significant deviation from it.

Both male and female meiosis contribute to non‐Mendelian inheritance of parental chromosomes in interspecific plant hybrids (Lolium × Festuca)

“…Similar results were observed in Allium cepa L. × Allium roylei Stearn. hybrids (Kopecký et al ., 2022). Unfortunately, direct observation of chromosome behavior in female meiosis is not feasible; hence, sample sizes are limited.…”

“…In interspecific hybrids, the frequency of such attachments and the ability to be included in the newly formed nuclei may differ between univalents of different parental origin. Indeed, some hybrids show higher elimination rate of chromosomes from the submissive genome (Kopecký et al ., 2022). An extreme case is the instant elimination of one parental chromosome set after hybridization of Hordeum vulgare L. with Hordeum bulbosum L. during first embryo mitoses (Sanei et al ., 2011).…”

Genome composition in Brassica interspecific hybrids affects chromosome inheritance and viability of progeny

“…However, in Lolium × Festuca interspecific hybrids, which show preferential loss of Festuca chromosomes, Majka et al ( 2023 ) were able to attribute this preferential chromosome loss effect to subgenome-specific ( Lolium- only) expression of kinetochore proteins controlling attachment of univalent chromosomes to microtubules, such that Festuca chromosomes were improperly attached and subsequently often lost as micronuclei following meiosis. Similar bias towards inheritance of Allium roylei over A. cepa chromosomes in A. cepa × A. roylei hybrids was attributed to female meiotic drive (Kopecký et al 2022 ). Similar meiotic mechanisms may be operating in our BBAC S 1 hybrids, but further investigation would be required to confirm or refute this hypothesis.…”

Interspecific hybridization and plant breeding: From historical retrospective through work of Mendel to current crops

“…It enables a shift in the genome composition in hybrid progeny. In Allium cepa × A. roylei hybrids, the A. roylei genome appears to predominate: the percentage of roylei alleles in the F 2 population was on average 56% vs. 44% of cepa alleles and the parental chromosome constitution shifted from 8cepa + 8roylei in F 1 gen-https://doi.org/10.17221/19/2022-CJGPB eration to 6.7cepa + 9.3roylei in F 2 generation (van Heusden et al 2000;Kopecký et al 2022). Earlier studies observed chromosomal dominance in all cultivars selected from Lolium multiflorum × Festuca pratensis hybrids.…”

“…This creates an opportunity to direct certain chromosomes preferentially to the egg cell and hence, to the next generation, and eliminates their counterparts. Recent research indicates that the female meiotic drive is the most probable explanation of the Lolium-and A. roylei-genome dominance (Kopecký et al 2022). Female meiotic drive underlying subsequent substitution of one parental genome by the other has been only rarely reported in plant hybrids (Fishman & Saunders 2008).…”