Reduced fertility caused by meiotic defects and micronuclei formation during microsporogenesis in xBrassicoraphanus

Abstract

Background Hybridization and polyploidization events are important driving forces in plant evolution. Allopolyploids formed between different species can be naturally or artificially created but often suffer from genetic instability and infertility in successive generations. xBrassicoraphanus is an intergeneric allopolyploid obtained from a cross between Brassica rapa and Raphanus sativus, providing a useful resource for genetic and genomic study in hybrid species. Objective The current study aims to understand the cause of hybrid sterility and pollen abnormality in different lines of synthetic xBrassicoraphanus from the cytogenetic perspective. Methods Alexander staining was used to assess the pollen viability. Cytogenetic analysis was employed to monitor meiotic chromosome behaviors in pollen mother cells (PMCs). Origins of parental chromosomes in xBrassicoraphanus meiocytes were determined by genome in situ hybridization analysis. Results The xBrassicoraphanus lines BB#4 and BB#6 showed high rates of seed abortion and pollen deformation. Abnormal chromosome behaviors were observed in their PMCs, frequently forming univalents and inter-chromosomal bridges during meiosis. A positive correlation also exists between meiotic defects and the formation of micronuclei, which is conceivably responsible for unbalanced gamete production and pollen sterility. Conclusion These results suggest that unequal segregation of meiotic chromosomes, due in part to non-homologous interactions, is responsible for micronuclei and unbalanced gamete formation, eventually leading to pollen degeneration and inferior fertility in unstable xBrassicoraphanus lines.

Admixture of divergent genomes facilitates hybridization across species in the family Brassicaceae

“…We previously reported that some genomic regions of Br and Rs share structural similarity, particularly between A8 and R8, although most other regions are fragmented and diversified (Park et al ., 2020). In addition, we recently showed that several x B lines derived from the same intergeneric cross endured chromosome instability and pollen inviability, while occasionally producing tetrads with an extra micronucleus during microsporogenesis (Shin et al ., 2021). This is probably a consequence of homoeologous chromosome exchanges at meiotic prophase I leading to the formation of univalent or multivalent chromosomes (Shin et al ., 2021).…”

“…In addition, we recently showed that several x B lines derived from the same intergeneric cross endured chromosome instability and pollen inviability, while occasionally producing tetrads with an extra micronucleus during microsporogenesis (Shin et al ., 2021). This is probably a consequence of homoeologous chromosome exchanges at meiotic prophase I leading to the formation of univalent or multivalent chromosomes (Shin et al ., 2021). This suggests that chromosome instability persists in successive generations while generating nonfunctional haploid gametes with aberrant karyotypes.…”

“…This may operate as a primary postzygotic barrier, which also appears true for early generations of x B . Most synthetic F 1 individuals of x B , including resynthesized x B plants in this study, display reproductive defects such as pollen inviability and seed abortion (Lee et al ., 2011; Shin et al ., 2021). Underdeveloped embryos must be in vitro rescued, and thus only a handful of progenies can be finally fixed as stable lines.…”

Genomic affinity in hybrids of B-genome Arachis species: new genetic resources toward peanut improvement

“…Meiotic irregularities have been related to the origin of aneuploid gametes (Mursalimov and Deineko 2018), which impose detrimental effects on pollen development (Shin et al 2021). Out-of-plate and out-of-nucleus chromosomes can be caused by unequal tension from the poles (Lampson and Grishchuk 2017).…”

Identification of male-fertility gene AsaNRF1 and molecular marker development in cultivated garlic (Allium sativum L.)

“…Plants with male sterility cannot produce fertile pollen, and this male sterility may be regulated by genes encoded in the nuclear (genic male sterility) or mitochondrial (cytoplasmic male sterility) genomes ( Garcia et al., 2019 ). Abnormalities in the formation of the pollen sac ( Chaban et al., 2020 ; Zheng et al., 2021 ), meiosis ( Qiu et al., 2018 ; Shin et al., 2021 ), callose ( Pu et al., 2019 ; Li et al., 2020 ), tapetum ( Mondol et al., 2020 ; Zhang et al., 2021 ), pollen wall ( Ren et al., 2020 ; Deng et al., 2022 ), and anther dehiscence ( Kim and Kim, 2021 ; Qi et al., 2022 ) during pollen development can lead to pollen abortion and a male-sterile phenotype. Tapetum and meiocytes are primarily affected in most sporophytic male-sterile mutants ( Guo and Liu, 2012 ).…”