Abstract

Plant cytogenetic studies have provided essential knowledge on chromosome behavior during meiosis, contributing to our understanding of this complex process. In this review, we describe in detail the meiotic process in auto- and allopolyploids from the onset of prophase I through pairing, recombination, and bivalent formation, highlighting recent findings on the genetic control and mode of action of specific proteins that lead to diploid-like meiosis behavior in polyploid species. During the meiosis of newly formed polyploids, related chromosomes (homologous in autopolyploids; homologous and homoeologous in allopolyploids) can combine in complex structures called multivalents. These structures occur when multiple chromosomes simultaneously pair, synapse, and recombine. We discuss the effectiveness of crossover frequency in preventing multivalent formation and favoring regular meiosis. Homoeologous recombination in particular can generate new gene (locus) combinations and phenotypes, but it may destabilize the karyotype and lead to aberrant meiotic behavior, reducing fertility. In crop species, understanding the factors that control pairing and recombination has the potential to provide plant breeders with resources to make fuller use of available chromosome variations in number and structure. We focused on wheat and oilseed rape, since there is an abundance of elucidating studies on this subject, including the molecular characterization of the Ph1 (wheat) and PrBn (oilseed rape) loci, which are known to play a crucial role in regulating meiosis. Finally, we exploited the consequences of chromosome pairing and recombination for genetic map construction in polyploids, highlighting two case studies of complex genomes: (i) modern sugarcane, which has a man-made genome harboring two subgenomes with some recombinant chromosomes; and (ii) hexaploid sweet potato, a naturally occurring polyploid. The recent inclusion of allelic dosage information has improved linkage estimation in polyploids, allowing multilocus genetic maps to be constructed.

Highlights

  • The study of meiosis in polyploid species began in the 1920s with the classic report of Newton and Darlington (1929) [1], who studied triploid and pentaploid tulips

  • An autopolyploid has more than two copies of homologous chromosomes that are capable of randomly pairing, synapsing and recombining during prophase I (PI). When these events are observed in more than two homologous chromosomes, a multivalent can be formed at metaphase I (MI), and chromosome missegregation can occur at anaphase I (AI) [27] (Figure 1)

  • Results reported in Arabidopsis support the idea that one CO per chromosome is associated with low multivalent frequency in the natural autotetraploid Arabidopsis arenosa, evidencing the effect of genes on CO rates [13,50]

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Summary

Overview

The study of meiosis in polyploid species began in the 1920s with the classic report of Newton and Darlington (1929) [1], who studied triploid and pentaploid tulips. There are two classes of naturally occurring polyploids: autopolyploids, which have three or more copies of the same genome (e.g., the autotetraploid Solanum tuberosum, 2n = 4x = 48), and allopolyploids, which are the result of interspecific hybridization between related progenitors and genome doubling (e.g., the allotetraploid Nicotiana tabacum, 2n = 4x =24, whose genome composition is AABB). Multivalents or homeologous pairings that reach metaphase I (MI) are related to segregation issues, leading to aneuploid gametes, compromised fertility, and low fitness of offspring [16]

Revisiting Early Meiosis
Meiosis in Autopolyploids
Frequency of Crossovers
Multivalents and Cytological Diploidization
Genetic Control of Meiosis in Autopolyploids
Meiosis in Allopolyploids
Homoeologous Exchanges
Neoallopolyploids
10. Genetic Regulatory Systems in Allopolyploids
12. The Ph1 Locus
13. The ZIP4 Gene
15. Brassica and the Prevalence of Bivalent Pairing
16. PrBn Molecular Characterization and Function
17. BnaPh1
18. Meiotic Proteins and Crossover Formation
19. The Consequences of Meiosis for Genetic Mapping in Auto- and Allopolyploids
Findings
20.2. Sweet Potato
Full Text
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