High temperature-induced production of unreduced pollen and its cytological effects in Populus

Abstract

Temperature change is of potential to trigger the formation of unreduced gametes. In this study, we showed that short periods of high temperature treatment can induce the production of 2n pollen in Populus pseudo-simonii Kitag. The meiotic stage, duration of treatment, and temperature have significant effects on the induction of 2n pollen. Heat stress resulted in meiotic abnormalities, including failure of chromosome separation, chromosome stickiness, laggards and micronuclei. Spindle disorientations in the second meiotic division, such as parallel, fused, and tripolar spindles, either increased in frequency or were induced de novo by high temperature treatment. We found that the high temperature treatment induced depolymerisation of meiotic microtubular cytoskeleton, resulting in the failure of chromosome segregation. New microtubular cytoskeletons were able to repolymerise in some heat-treated cells after transferring them to normal conditions. However, aberrant cytokinesis occurred owing to defects of new radial microtubule systems, leading to production of monads, dyads, triads, and polyads. This suggested that depolymerisation and incomplete restoration of microtubules may be important for high temperature-induction of unreduced gametes. These findings might help us understand how polyploidisation is induced by temperature-related stress and support the potential effects of global climate change on reproductive development of plants.

High temperatures alter cross-over distribution and induce male meiotic restitution in Arabidopsis thaliana

“…Whereas the two MII syncytial spindles normally exhibit a perpendicular orientation, heat-stressed PMCs in rose often display a parallel, fused, or tripolar orientation of MII spindles, yielding restituted dyads and triads instead of regular tetrads at the end of MII 5 . Similar alterations in MII spindle orientation also 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 particularly 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 .…”

“…The male reproductive system has been repeatedly found to be most susceptible to temperature stress 2 . Brief as well as prolonged shifts in the ambient temperature promote 2n gamete formation in a broad range of species, including Lotus tenuis 3 , wheat 4 , rose 5 , Brassica 6 , Arabidopsis 7 , Dianthus caryophyllus 8 , and Populus 9,10 . However, the underlying cellular defect and genetic outcome of meiotic nonreduction greatly varies depending on species and temperature regime.…”

“…In Arabidopsis thaliana, cold stress induces male meiotic restitution by specifically interfering with the RMAs that underpin biogenesis of the second cell wall at the end of MII, and hence yields dyads and triads 7 . Similarly, in wheat and poplar, MII cell wall formation is affected by heat, indicating that the process of male meiotic cytokinesis is highly temperature-sensitive 10,11 . In rose, heat-induced meiotic restitution is caused by alterations in MII spindle organization.…”

Brassinosteroid‐mediated reactive oxygen species are essential for tapetum degradation and pollen fertility in tomato

“…The development of functional pollen is vital for plant reproduction and the expansion of genetic diversity during the spermatophyte life cycle (Deveshwar et al , ). Plants, as immobile organisms, are able to adapt to various environmental conditions; however, the male reproductive tissues are extremely sensitive to changes in environmental factors, such as temperature, moisture and nutrient balance (Nashilevitz et al , ; De Storme and Geelen, ; Arshad et al , ; Wang et al , ). During the stage of early pollen development, meiosis is essential for microspore formation; however, meiosis under high temperature, for example, leads to increased pollen abortion in Populus pseudosimonii (Wang et al , ).…”

“…Plants, as immobile organisms, are able to adapt to various environmental conditions; however, the male reproductive tissues are extremely sensitive to changes in environmental factors, such as temperature, moisture and nutrient balance (Nashilevitz et al , ; De Storme and Geelen, ; Arshad et al , ; Wang et al , ). During the stage of early pollen development, meiosis is essential for microspore formation; however, meiosis under high temperature, for example, leads to increased pollen abortion in Populus pseudosimonii (Wang et al , ). Similarly, the disruption of meiosis and microspore wall formation as a result of chilling stress causes pollen sterility in Oryza sativa (rice) (Arshad et al , ).…”