Abstract
Key messageUnreduced gametes.The absence of a strict pachytene checkpoint in plants presents an opportunity to study meiosis in polyhaploid organisms. In the present study, we demonstrate that meiosis is coordinated in hybrids between disomic wheat–rye substitution lines 1Rv(1A), 2R(2D), 5R(5D), 6R(6A) and rye (Triticum aestivum L. × Secale cereale L., 4x = 28, ABDR). By using in situ hybridization with a centromere pAet6-09 probe and immunostaining with H3Ser10ph-, CENH3-, and α-tubulin-specific antibodies, we distinguished four chromosome behaviour types. The first one is a mitotic-like division that is characterized by mitotic centromere architecture, robust bipolar spindle, one-step loss of arm and centromere cohesion, and sister chromatid separation in the first and only meiotic division. The second type involves a monopolar spindle formation, which appears as a hat-shaped group of chromosomes moving in one direction, wherein MT bundles are co-oriented polewards. It prevents chromosome segregation in meiosis I, with a bipolar spindle distributing sister chromatids to the poles in meiosis II. These events subsequently result in the formation of unreduced microspores. The other two meiotic-like chromosome segregation patterns known as reductional and equational plus reductional represent stand-alone types of cell division rather than intermediate steps of meiosis I. Only sterile pollen is produced as a result of such meiotic-like chromosome behaviours. Slightly variable meiotic phenotypes are reproducibly observed in hybrids under different growth conditions. The 2R(2D)xR genotype tends to promote reductional division. In contrast, the genotypes 1Rv(1A)xR, 5R(5D)xR, and 6R(6A)xR promote equational chromosome segregation and monopolar spindle formation in addition to reductional and equational plus reductional division types.Electronic supplementary materialThe online version of this article (doi:10.1007/s00497-016-0279-5) contains supplementary material, which is available to authorized users.
Highlights
Polyploidy is widespread among flowering plants, and allopolyploidy is one of the major speciation pathways in plant evolution (Adams and Wendel 2005; Otto 2007; Soltis et al 2009; Soltis and Soltis 2009; Feldman and Levy 2012; Tayale and Parisod 2013; Estep et al 2014)
By directly visualizing the pattern of chromosome segregation and the dynamics of centromere behaviour, we provide evidence arguing in favour of the idea that four distinct chromosome behaviour types exist in the meiosis of wheat–rye amphihaploids
In 2R(2D)xR F1 hybrids, univalents were observed to be randomly scattered between the poles at metaphase I (MI) (Fig. 1A, b), with 2R2R bivalents segregating as is typical for meiosis
Summary
Polyploidy is widespread among flowering plants, and allopolyploidy is one of the major speciation pathways in plant evolution (Adams and Wendel 2005; Otto 2007; Soltis et al 2009; Soltis and Soltis 2009; Feldman and Levy 2012; Tayale and Parisod 2013; Estep et al 2014). The bread wheat subgenomes A, B, and D were originally derived from three diploid (2x; 2n = 14) species within tribe Triticeae: Triticum urartu (AA), an extinct or yet undiscovered species from Aegilops speltoides (BB) lineage, and Ae. tauschii (DD) (IGWSC 2014). An alternative evolutionary scenario was proposed for the bread wheat (Marcussen et al 2014) According to this scenario, the very first hybridization event between the ancestral A and B genome lineages occurred about 5.5 MYA and led to the origin of the D genome lineage by homoploid hybrid speciation. The second hybridization event (less than 0.8 MYA) between a close relative (BB) of Ae. speltoides and T. urartu (AA) gave rise to the allotetraploid emmer wheat (T. turgidum; AABB) by polyploidization. Bread wheat originated by allopolyploidization from a third hybridization (less than 0.8 MYA), between emmer wheat and Ae. tauschii (DD). Bread wheat displays diploid-like meiotic behaviour (exclusive bivalent pairing of homologues), which leads to full fertility and disomic inheritance (Feldman and Levy 2005; Griffiths et al 2006)
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