Meiotic Chromosome Stability and Suppression of Crossover Between Non-homologous Chromosomes in xBrassicoraphanus, an Intergeneric Allotetraploid Derived From a Cross Between Brassica rapa and Raphanus sativus.

Hye Rang Park,Jeong Eun Park,Hosub Shin,Jin Hoe Huh,Jung Hyo Kim,Hyun Hee Kim,Soo-Seong Lee,Sehyeok Son,Gibum Yi,Seung Hwa Yu

doi:10.3389/fpls.2020.00851

Hye Rang Park, Jeong Eun Park + Show 8 more

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https://doi.org/10.3389/fpls.2020.00851

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Abstract

Hybridization and polyploidization are major driving forces in plant evolution. Allopolyploids can be occasionally formed from a cross between distantly related species but often suffer from chromosome instability and infertility. xBrassicoraphanus is an intergeneric allotetraploid (AARR; 2n = 38) derived from a cross between Brassica rapa (AA; 2n = 20) and Raphanus sativus (RR; 2n = 18). xBrassicoraphanus is fertile and genetically stable, while retaining complete sets of both B. rapa and R. sativus chromosomes. Precise control of meiotic recombination is essential for the production of balanced gametes, and crossovers (COs) must occur exclusively between homologous chromosomes. Many interspecific hybrids have problems with meiotic division at early generations, in which interactions between non-homologous chromosomes often bring about aneuploidy and unbalanced gamete formation. We analyzed meiotic chromosome behaviors in pollen mother cells (PMCs) of allotetraploid and allodiploid F1 individuals of newly synthesized xBrassicoraphanus. Allotetraploid xBrassicoraphanus PMCs showed a normal diploid-like meiotic behavior. By contrast, allodiploid xBrassicoraphanus PMCs displayed abnormal segregation of chromosomes mainly due to the absence of homologous pairs. Notably, during early stages of meiosis I many of allodiploid xBrassicoraphanus chromosomes behave independently with few interactions between B. rapa and R. sativus chromosomes, forming many univalent chromosomes before segregation. Chromosomes were randomly assorted at later stages of meiosis, and tetrads with unequal numbers of chromosomes were formed at completion of meiosis. Immunolocalization of HEI10 protein mediating meiotic recombination revealed that COs were more frequent in synthetic allotetraploid xBrassicoraphanus than in allodiploid, but less than in the stabilized line. These findings suggest that structural dissimilarity between B. rapa and R. sativus chromosomes prevents non-homologous interactions between the parental chromosomes in allotetraploid xBrassicoraphanus, allowing normal diploid-like meiosis when homologous pairing partners are present. This study also suggests that CO suppression between non-homologous chromosomes is required for correct meiotic progression in newly synthesized allopolyploids, which is important for the formation of viable gametes and reproductive success in the hybrid progeny.

Highlights

Hybridization and polyploidization are major driving forces in plant evolution (Van de Peer et al, 2017)
Hybridization barriers exist in nature to prevent a gene flow between different species, and can be divided into pre- and post-zygotic stages according to the timing of fertilization
Pre-zygotic barriers prevent fertilization between species, whereas post-zygotic barriers are mechanisms engaged after fertilization that reduce the viability or fertility of hybrid offspring

Summary

Introduction

Hybridization and polyploidization are major driving forces in plant evolution (Van de Peer et al, 2017). Polyploids can be divided into two classes: ones that undergo the multiplication of a whole set of chromosomes within species (autopolyploids) and the others resulting from hybridization between different species followed by chromosome doubling (allopolyploids). Autopolyploids have random association among four homologous chromosomes (in tetraploids) leading to tetrasomic segregation during meiosis, whereas allopolyploids have two non-pairing sets of homoeologous chromosomes carrying out disomic segregation (Doyle and Egan, 2010). Allopolyploids can be occasionally formed from a cross between genetically divergent species, for instance, between the individuals that belong to different species or even to different genera. Interspecific hybridization and allopolyploidization are likely to contribute to the emergence of many important crop plants such as oilseed rape (Brassica napus), cotton (Gossypium hirsutum), tobacco (Nicotiana tabacum), wheat (Triticum aestivum), sugarcane (Saccharum officinarum), and coffee (Coffea arabica) (Renny-Byfield and Wendel, 2014). Many studies report that most synthetic allopolyploids exhibited genetic instability and sterility, the latter of which is mainly caused by meiotic abnormalities during sexual gamete formation (Madlung et al, 2005; Mestiri et al, 2010; Szadkowski et al, 2010, 2011)

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