Environmental Heat and Salt Stress Induce Transgenerational Phenotypic Changes in Arabidopsis thaliana

Abstract

Plants that can adapt their phenotype may be more likely to survive changing environmental conditions. Heritable epigenetic variation could provide a way to rapidly adapt to such changes. Here we tested whether environmental stress induces heritable, potentially adaptive phenotypic changes independent of genetic variation over few generations in Arabidopsis thaliana. We grew two accessions (Col-0, Sha-0) of A. thaliana for three generations under salt, heat and control conditions and tested for induced heritable phenotypic changes in the fourth generation (G4) and in reciprocal F1 hybrids generated in generation three. Using these crosses we further tested whether phenotypic changes were maternally or paternally transmitted. In generation five (G5), we assessed whether phenotypic effects persisted over two generations in the absence of stress. We found that exposure to heat stress in previous generations accelerated flowering under G4 control conditions in Sha-0, but heritable effects disappeared in G5 after two generations without stress exposure. Previous exposure to salt stress increased salt tolerance in one of two reciprocal F1 hybrids. Transgenerational effects were maternally and paternally inherited. Lacking genetic variability, maternal and paternal inheritance and reversibility of transgenerational effects together indicate that stress can induce heritable, potentially adaptive phenotypic changes, probably through epigenetic mechanisms. These effects were strongly dependent on plant genotype and may not be a general response to stress in A. thaliana.

Genetic control of Eucalyptus globulus seed germination

“…Such changes can be induced by environmental stress (Zhang et al 2013) and result in phenotypic effects that are adaptive (Bräutigam et al 2013;Jablonka 2013). For example, exposure to heat stress has been shown to cause intragenerational epigenetic changes in cork oak (Correia et al 2013), and transgenerational molecular and phenotypic changes in Arabidopsis (Boyko and Kovalchuk 2010;Suter and Widmer 2013). However, while there are exceptions (Grossniklaus et al 2013), the transgenerational epigenetic memory is often relatively transient and only detected in the direct progeny produced following maternal environmental conditioning (Boyko and Kovalchuk 2010;Grossniklaus et al 2013;Holeski et al 2013;Migicovsky and Kovalchuk 2013;Suter and Widmer 2013).…”

Cross generation plasticity in cold hardiness is associated with diapause, but not the non-diapause developmental pathway, in the blowfly, Calliphora vicina

“…Cross-generation responses to environmental stressors are well documented in a broad range of organisms (Marshall, 2008;Castro et al, 2013;Plautz et al, 2013;Suter and Widmer, 2013). Understanding these responses will be critical in determining how different organisms will cope with future climate change (Mondor et al, 2004;Rando and Verstrepen, 2007;Burgess and Marshall, 2011;Salinas and Munch, 2012).…”

“…if adult thermal history influences larval cold tolerance phenotypes. It is already known that higher adult temperatures reduce diapause incidence and duration (McWatters and Saunders, 1998; Hayward and Saunders, 1998), and there is strong evidence in a range of organisms that the physiological history of the parental generation can influence the stress tolerance phenotypes of their progeny (Marshall, 2008;Castro et al, 2013;Plautz et al, 2013;Suter and Widmer, 2013). Such a crossgeneration effect would be of significant ecological relevance and further highlight the importance of including autumn temperature conditions in models of insect overwintering under climate change.…”

Epigenetic responses to heat stress at different time scales and the involvement of small RNAs

“…15 Several groups have reported transgenerational effects of stress exposure at the morphological and epigenetic level (most recently in Ref. 16,17 ). However, the significance and extent of transgenerational stress memory is still far from resolved.…”