Heat shock-induced failure of meiosis I to meiosis II transition leads to 2n pollen formation in a woody plant

Abstract

The formation of diploid gametes through chromosome doubling is a major mechanism of polyploidization, diversification, and speciation in plants. Unfavorable climate conditions can induce or stimulate the production of diploid gametes during meiosis. Here, we demonstrated that heat shock stress (38 °C for 3 or 6 h) induced 2n pollen formation, and we generated 42 triploids derived from heat-shock-induced 2n pollen of Populus canescens. Meiotic analysis of treated pollen mother cells (PMCs) revealed that induced 2n pollen originated from the complete loss of meiosis II (MII). Among the 42 triploids, 38 triploids derived from SDR-type 2n pollen and 4 triploids derived from FDR-type 2n pollen were verified using SSR molecular markers. Twenty-two differentially expressed genes related to the cell cycle were identified and characterized by expression profile analysis. Among them was POPTR_0002s08020g (PtCYCA1;2), which encodes a type A Cyclin CYCA1;2 that is required for the MI to MII transition. After male flower buds were exposed to heat shock, a significant reduction was detected in PtCYCA1;2 expression. We inferred that the failure of MI-to-MII transitions might be associated with downregulated expression of PtCYCA1;2, leading to the formation of SDR-type 2n pollen. Our findings provide insights into mechanisms of heat-shock-induced 2n pollen formation in a woody plant and verify that sensitivity to environmental stress has evolutionary importance in terms of polyploidization.

ATM‐mediated double‐strand break repair is required for meiotic genome stability at high temperature

“…Global warming has now become one of the most serious climate factors that influence the living and evolution of land plants, and meiosis and HR in plants are prone to be affected by alterations in environmental temperature (Bomblies et al, 2015; Liu et al, 2019; Modliszewski & Copenhaver, 2017). In Arabidopsis and in tree species, elevated temperatures have been found to induce meiotic restitution, with the resultant formation of unreduced gametes, to interfere with CO formation and/or distribution, and to affect spindle‐dependent chromosome segregation, which results in aneuploid gametes and sterility (De Storme & Geelen, 2020; Lei et al, 2020; Mai et al, 2019; Wang et al, 2017; Zhou et al, 2022). In Arabidopsis, a mildly high temperature within the fertility threshold (28°C) promotes the CO rate by enhancing the activity of the class‐I CO pathway (Lloyd et al, 2018; Modliszewski et al, 2018).…”

Heat stress induces unreduced male gamete formation by targeting the meiotic cyclin TAM/CYCA1;2

“…Rather than a loss of or reduced TAM function, our data show that TAM expression is increased after 24h at 32°C compared to a 20°C control in several high dyad producing accessions, but not in the less sensitive Col-0 background. Remarkably Ning et al (2021) report an increase in TAM expression in Col-0 when temperatures are increased to 36°C and there are indications that a high temperature induced reduction of TAM expression lead to meiotic restitution in poplar (Zhou et al 2022).…”

Ultraviolet attenuates centromere-mediated meiotic genome stability and alters gametophytic ploidy consistency in flowering plants

“…Formation and fusing of unreduced gametes derived from non-reductional meiotic cell division, called meiotic restitution, are considered the main route to WGD (Ramsey and Schemske, 1998). Meiotic restitution can be triggered by either genetic alterations or temperature stresses, which cause loss of meiosis cell cycle, aberrant organization of spindle and/or phragmoplast or irregular cytokinesis (De Storme et al, 2012; De Storme and Geelen, 2011; De Storme and Geelen, 2020; Lei et al, 2020; Ravi et al, 2008; Zhou et al, 2022). However, whether meiotic restitution can be triggered by other environmental factors is less understood.…”