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Out-of-position telomeres in meiotic leptotene appear responsible for chiasmate pairing in an inversion heterozygote in wheat (Triticum aestivum L.)

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Abstract

Chromosome pairing in meiosis usually starts in the vicinity of the telomere attachment to the nuclear membrane and congregation of telomeres in the leptotene bouquet is believed responsible for bringing homologue pairs together. In a heterozygote for an inversion of a rye (Secale cereale L.) chromosome arm in wheat, a distal segment of the normal homologue is capable of chiasmate pairing with its counterpart in the inverted arm, located near the centromere. Using 3D imaging confocal microscopy, we observed that some telomeres failed to be incorporated into the bouquet and occupied various positions throughout the entire volume of the nucleus, including the centromere pole. Rye telomeres appeared ca. 21 times more likely to fail to be included in the telomere bouquet than wheat telomeres. The frequency of the out-of-bouquet rye telomere position in leptotene was virtually identical to the frequency of telomeres deviating from Rabl’s orientation in the nuclei of somatic cells, and was similar to the frequency of synapsis of the normal and inverted chromosome arms, but lower than the MI pairing frequency of segments of these two arms normally positioned across the volume of the nucleus. Out-of-position placement of the rye telomeres may be responsible for reduced MI pairing of rye chromosomes in hybrids with wheat and their disproportionate contribution to aneuploidy, but appears responsible for initiating chiasmate pairing of distantly positioned segments of homology in an inversion heterozygote.

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Acknowledgements

The authors thank Drs. David Carter (UCR) and Attila Fabian (MTA, ATK) for assistance with the SP8 confocal laser scanning microscope system.

Funding

This study was done with support from the National Institute of Food and Agriculture (NIFA) Project CA-R-BPS-5411-H to AJL and the National Science Foundation Grants (OTKA K108555) and the Hungarian Academy of Sciences (MTA KEP 2018) to GL. KP and DK were partially supported by the Czech Science Foundation (grant award 17-13853S) and together with OS by a grant award LO1204 from the National Program of Sustainability I.

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Contributions

AJL and GL designed experiments; AJL, EG, and GL performed meiotic experiments; KP, OS, and DK performed mitotic experiments; AJL and GL analyzed data; AJL, GL, and DK wrote the manuscript. All authors read and approved the manuscript.

Corresponding author

Correspondence to Adam J. Lukaszewski.

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This article does not contain any studies with human participants or animals performed by any of the authors.

Conflict of interest

The authors declare that they have no conflict of interest.

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Pernickova, K., Linc, G., Gaal, E. et al. Out-of-position telomeres in meiotic leptotene appear responsible for chiasmate pairing in an inversion heterozygote in wheat (Triticum aestivum L.). Chromosoma 128, 31–39 (2019). https://doi.org/10.1007/s00412-018-0686-5

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