Abstract
Plant fertility is highly sensitive to elevated temperature. Here, we report that hot spells induce the formation of dyads and triads by disrupting the biogenesis or stability of the radial microtubule arrays (RMAs) at telophase II. Heat-induced meiotic restitution in Arabidopsis is predominantly SDR-type (Second Division Restitution) indicating specific interference with RMAs formed between separated sister chromatids. In addition, elevated temperatures caused distinct deviations in cross-over formation in male meiosis. Synapsis at pachytene was impaired and the obligate cross-over per chromosome was discarded, resulting in partial univalency in meiosis I (MI). At diakinesis, interconnections between non-homologous chromosomes tied separate bivalents together, suggesting heat induces ectopic events of non-homologous recombination. Summarized, heat interferes with male meiotic cross-over designation and cell wall formation, providing a mechanistic basis for plant karyotype change and genome evolution under high temperature conditions.
Highlights
Plant fertility is highly sensitive to elevated temperature
The impact of heat on male meiosis was investigated by exposing flowering Arabidopsis plants for 0, 12, 24, 36, and 48 h to mild (26–28 °C) and more extreme temperature (30–32 °C)
Whereas unbalanced dyads can result from a range of different meiotic alterations, balanced dyads typically result from a defect in cytokinesis or cell wall formation
Summary
Plant fertility is highly sensitive to elevated temperature. Here, we report that hot spells induce the formation of dyads and triads by disrupting the biogenesis or stability of the radial microtubule arrays (RMAs) at telophase II. In Arabidopsis thaliana, cold stress induces male meiotic restitution by interfering with the RMAs that underpin biogenesis of the second cell wall at the end of MII, and yields dyads and triads[7]. Similar alterations in MII spindle orientation underpin heat-induced male meiotic restitution and the associated production of 2n gametes in other plant species, such as poplar[10] and Brassica ssp[12]. Overall, these studies bring forward the cytoskeleton, and microtubule (MT)-based arrays, in male MII as temperature-sensitive structures that undergo depolymerization and incomplete restoration upon heat or cold to cause alterations in MII chromosome dynamics and meiotic restitution[7]. With heatinduced meiotic defects leading to the stochastic formation of diand aneuploid spores, we here postulate that meiotic plasticity under temperature stress may constitute a mechanistic basis driving plant genome evolution and karyotype change under environmentally challenging conditions
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