Brief temperature stress during reproductive stages alters meiotic recombination and somatic mutation rates in the progeny of Arabidopsis

Abstract

BackgroundPlants exposed to environmental stresses draw upon many genetic and epigenetic strategies, with the former sometimes modulated by the latter. This can help the plant, and its immediate progeny, at least, to better endure the stress. Some evidence has led to proposals that (epi) genetic changes can be both selective and sustainably heritable, while other evidence suggests that changes are effectively stochastic, and important only because they induce genetic variation. One type of stress with an arguably high level of stochasticity in its effects is temperature stress. Studies of how heat and cold affect the rates of meiotic recombination (MR) and somatic mutations (SMs, which are potentially heritable in plants) report increases, decreases, or no effect. Collectively, they do not point to any consistent patterns. Some of this variability, however, might arise from the stress being applied for such an extended time, typically days or weeks. Here, we adopted a targeted approach by (1) limiting exposure to one hour; and (2) timing it to coincide with (a) gamete, and early gametophyte, development, a period of high stress sensitivity; and (b) a late stage of vegetative development.ResultsFor plants (Arabidopsis thaliana) otherwise grown at 22 °C, we measured the effects of a 1 h exposure to cold (12 °C) or heat (32 °C) on the rates of MR, and four types of SMs (frameshift mutations; intrachromosomal recombination; base substitutions; transpositions) in the F1 progeny. One parent (wild type) was stressed, the other (unstressed) carried a genetic event detector. When rates were compared to those in progeny of control (both parents unstressed) two patterns emerged. In the progeny of younger plants (stressed at 36 days; pollinated at 40 days) heat and cold either had no effect (on MR) or (for SMs) had effects that were rare and stochastic. In the progeny of older plants (stressed at 41 days; pollinated at 45 days), while effects were also infrequent, those that were seen followed a consistent pattern: rates of all five genetic events were lowest at 12 °C and highest at 32 °C, i.e. they varied in a “dose-response” manner. This pattern was strongest (or, in the case of MR, only apparent) in progeny whose stressed parent was female.ConclusionWhile the infrequency of effects suggests the need for cautious inference, the consistency of responses in the progeny of older plants, indicate that in some circumstances the level of stochasticity in inherited genetic responses to heat or cold stress can be context-dependent, possibly reflecting life-cycle stages in the parental generation that are variably stress sensitive.Electronic supplementary materialThe online version of this article (doi:10.1186/s12870-017-1051-1) contains supplementary material, which is available to authorized users.

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

“…In other genomic regions, however, the meiotic cross-over rate appears unaffected or even increased, indicating that heat does not merely affect the overall genome-wide cross-over level, but instead causes a spatial redistribution of cross-over events along the chromosome. The overall effect of varying temperatures on meiotic crossover rate and distribution in Arabidopsis was recently investigated by several groups 16,18,32 . These studies revealed that heat increases the overall recombination rate in male meiosis, and that the extra crossovers under heat are formed via the class I interference-sensitive pathway.…”

Role of Cis, Trans, and Inbreeding Effects on Meiotic Recombination in Saccharomyces cerevisiae

“…Beyond sequence-related effects, recombination can also be modulated by epigenetic factors, as observed in centromeric regions (N. A. Yelina et al 2012, and by environmental conditions (Phillips et al 2015;Saini et al 2017;Zhang et al 2017).…”

High Temperatures during Flowering Reduce Fruit Set in Rabbiteye Blueberry

“…In flowering plants, environmental factors play an important role in the regulation of plant growth and development, and the reproductive phase is typically highly sensitive to temperature stress (Gao et al, 2014;Ohnishi et al, 2010;Saini et al, 2017;Yang et al, 2015a). Complications can include abnormal meiosis (Bita et al, 2011;Draeger and Moore, 2017;Ohnishi et al, 2010;Yang et al, 2015a); accelerated pollen development and increased pollen abortion (Higuchi et al, 1998;Shen et al, 1999); accelerated flower bud development, resulting in a hastening of flowering time (Rodrigo and Herrero, 2002); reduced pollen germination for underdeveloped pistils (Hedhly et al, 2004;Koubouris et al, 2009;Pham et al, 2015); faster pollen tube growth in the style (Hedhly et al, 2004;Xu and Xu, 2014); inhibition of pollen tube elongation (Zhang et al, 2018); reduction in the number of pollen tubes (Radi cevi c et al, 2016); and reduction in the percentage of the style traversed by the pollen tube (Gao et al, 2014;Koubouris et al, 2009;Pham et al, 2015;Song and Chen, 2018), all of which can result in low fruit set.…”