Rye B chromosomes and heat tolerance in microsporogenesis

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Rye supernumerary (B) chromosomes possess an accumulation mechanism involving the subtelomeric domain enriched by B chromosome specific DNA sequence families, D1100 and E3900. Pereira et al. show that presence of rye B chromosomes may protect pollen mother cells at meiosis against heat stress induced damage.

Dynamics of tE3900 (red) and D1100 (green) throughout pre-meiotic interphase and prophase I in 2B plants grown in control conditions.
Dynamics of tE3900 (red) and D1100 (green) throughout pre-meiotic interphase and prophase I in 2B plants grown in control conditions. (A) PMI showing E3900 and D1100 domains partially decondensed in Rabl configuration. (B) (i) Leptotene with D1100 and E3900 B sub-telomeric domains associated with clustered telomeric heterochromatin, (ii) black and white image and (iii) schematic representation showing a striking extension of well-resolved chromosome fibres corresponding to B regions enriched in D1100 and E3900 from the telomeric heterochromatic cluster towards the opposite cell pole. (C) (i) Pachytene with paired B D1100/E3900-enriched regions evident as single extended FISH signals containing two distinct D1100 domains. (ii) High-resolution images of paired pachytene B chromosomes show tE3900 overlapping with the condensed blocks of the proximal D1100 domain and its complete absence in D1100 gaps. The distal D1100 region is highly enriched in both 2·7- and 3·9-kb E3900 variants and is consistently decondensed in a homogeneous manner. (D) Diakinesis with highly condensed D1100 and E3900 signals visible on commonly early resolved B chromosomes. (E) Schematic representation of dynamics in the condensation state of D1100- and E3900-enriched regions in early prophase I. D1100-rich/E3900-poor region is represented in green and D1100/E3900-rich region in red. Condensed mitotic metaphase B chromosome is presented as a reference. (F,G) Pachytene nuclei from a plant with two B chromosomes with a large deletion in the distal extended domain (2B-del). (F) Nucleus showing overlapping of tE3900 (red) and E3900 (yellow). (G) Nucleus showing the proximal condensed D1100 blocks (green) and interstitial regions, which appear intact, together with tE3900 (red). Scale bar = 10 μm.

Heat resulted in equal up-regulation of heat shock protein Hsp101 transcripts in plants with zero or 2B chromosomes. A significant up-regulation of E3900 related transcripts occurred in 2B plants at meiotic prophase I, compared to in 0B plants that showed significantly greater heat induced nuclear anomalies. Bioinformatics revealed a high density of known heat responsive cis-regulatory elements within the E3900 sequence and a truncated variant, supporting stress induced response of transcription and a role for B chromosomes in the protection against heat stress induce damage.

Reference

Pereira, H. S., Delgado, M., Viegas, W., Rato, J. M., Barão, A., & Caperta, A. D. (2016). Rye (Secale cereale) supernumerary (B) chromosomes associated with heat tolerance during early stages of male sporogenesis. Annals of Botany, 119(3), 325–337. https://doi.org/10.1093/aob/mcw206


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