Production of Diploid Male Gametes in Arabidopsis by Cold-Induced Destabilization of Postmeiotic Radial Microtubule Arrays      

Abstract

Whole-genome duplication through the formation of diploid gametes is a major route for polyploidization, speciation, and diversification in plants. The prevalence of polyploids in adverse climates led us to hypothesize that abiotic stress conditions can induce or stimulate diploid gamete production. In this study, we show that short periods of cold stress induce the production of diploid and polyploid pollen in Arabidopsis (Arabidopsis thaliana). Using a combination of cytological and genetic analyses, we demonstrate that cold stress alters the formation of radial microtubule arrays at telophase II and consequently leads to defects in postmeiotic cytokinesis and cell wall formation. As a result, cold-stressed male meiosis generates triads, dyads, and monads that contain binuclear and polynuclear microspores. Fusion of nuclei in binuclear and polynuclear microspores occurs spontaneously before pollen mitosis I and eventually leads to the formation of diploid and polyploid pollen grains. Using segregation analyses, we also found that the majority of cold-induced dyads and triads are genetically equivalent to a second division restitution and produce diploid gametes that are highly homozygous. In a broader perspective, these findings offer insights into the fundamental mechanisms that regulate male gametogenesis in plants and demonstrate that their sensitivity to environmental stress has evolutionary significance and agronomic relevance in terms of polyploidization.

Aberrant Classopollis pollen reveals evidence for unreduced (2 n ) pollen in the conifer family Cheirolepidiaceae during the Triassic–Jurassic transition

“…Growth experiments showed that 2n pollen production is stimulated by environmental factors such as temperature, herbivory, wounding, and water and nutrient stress [43,44]. Plants in their natural habitats experience many of the environmental factors that influence 2n gamete rspb.royalsocietypublishing.org Proc R Soc B 280: 20131708 production in growth experiments.…”

Microtubules in Plants

“…Dehydration, high salinity, low temperature, and aluminum are reported to destabilize cortical MTs in plants (Schwarzerová et al 2002;Sivaguru et al 2003;Abdrakhamanova et al 2003;Shoji et al 2006;Krtková et al, 2012;Ban et al 2013). Postmeiotic radial MT arrays in Arabidopsis male gametes are depolymerized in response to cold stress (De Storme et al 2012). Proteasome-dependent degradation of SPR1 protein is stimulated in response to high salinity (Wang et al 2011).…”

Genetic and environmental determinants of unreduced gamete production in Brassica napus, Sinapis arvensis and their hybrids

“…Interestingly, wounding was the only treatment that did not affect silique production, suggesting that our leaf wounding treatment may not have been strong enough, nor applied at the appropriate time or location, to affect meiosis or reproduction in general. It is noteworthy, however, that although wounding and herbivory are frequently listed as an environmental stressor influencing unreduced gamete production (see, for example, Ramsey and Schemske, 1998;De Storme et al, 2012;Mason and Pires, 2015), this observation appears to rest entirely on the early work of Kostoff (Kostoff andKendall, 1929,1930;Kostoff, 1933). All three of these studies involved plants with serious and direct damage to flower buds by mites (Kostoff andKendall, 1929,1930) or a virus (Kostoff, 1933).…”

“…The most frequently cited method of inducing unreduced gametes through alteration of environmental conditions is the cycling of hot and cold temperatures (Mason et al, 2011;De Storme et al, 2012). This approach has been used extensively by potato breeders to produce and introgress desirable genes from diploid into tetraploid lineages (Dewitte et al, 2012).…”