Genetic variation of transgenerational plasticity of offspring germination in response to salinity stress and the seed transcriptome of Medicago truncatula

Abstract

BackgroundTransgenerational plasticity provides phenotypic variation that contributes to adaptation. For plants, the timing of seed germination is critical for offspring survival in stressful environments, as germination timing can alter the environmental conditions a seedling experiences. Stored seed transcripts are important determinants of seed germination, but have not previously been linked with transgenerational plasticity of germination behavior. In this study we used RNAseq and growth chamber experiments of the model legume M. trucantula to test whether parental exposure to salinity stress influences the expression of stored seed transcripts and early offspring traits and test for genetic variation.ResultsWe detected genotype-dependent parental environmental effects (transgenerational plasticity) on the expression levels of stored seed transcripts, seed size, and germination behavior of four M. truncatula genotypes. More than 50% of the transcripts detected in the mature, ungerminated seed transcriptome were annotated as regulating seed germination, some of which are involved in abiotic stress response and post-embryonic development. Some genotypes showed increased seed size in response to parental exposure to salinity stress, but no parental environmental influence on germination timing. In contrast, other genotypes showed no seed size differences across contrasting parental conditions but displayed transgenerational plasticity for germimation timing, with significantly delayed germination in saline conditions when parental plants were exposed to salinity. In genotypes that show significant transgenerational plastic germination response, we found significant coexpression networks derived from salt responsive transcripts involved in post-transcriptional regulation of the germination pathway. Consistent with the delayed germination response to saline conditions in these genotypes, we found genes associated with dormancy and up-regulation of abscisic acid (ABA).ConclusionsOur results demonstrate genetic variation in transgenerational plasticity within M. truncatula and show that parental exposure to salinity stress influences the expression of stored seed transcripts, seed weight, and germination behavior. Furthermore, we show that the parental environment influences gene expression to modulate biological pathways that are likely responsible for offspring germination responses to salinity stress.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-015-0322-4) contains supplementary material, which is available to authorized users.

Salt tolerance during germination and seedling growth of wild wheat Aegilops tauschii and its impact on the species range expansion

“…Use of high resolution soil datasets might solve this issue. Refined experimental approaches taking into account complex phenotypic effects, such as transgenerational plasticity, would enable to better assess the degree of salt tolerance providing suitable phenotype data for inferring the genes controlling seedling growth ability under natural salt-stress conditions35. Detailed knowledge on the genetic mechanism(s) underlying the evolution of seedling growth ability would contribute to better understanding of the adaptation of Ae.…”

Adjusting phenotypes via within‐ and across‐generational plasticity

“…temperatures and increased salinity in the offspring environment were only observed when maternal plants were not grown in these environments (Zhang et al, 2012;Vu et al, 2015;Leverett et al, 2016;Moriuchi et al, 2016). This masking can occur when the maternal treatment alone maximized germination or induced such intense dormancy that progeny cues were not able to overcome it.…”

“…Within-generation plasticity can also mask maternal effects on progeny traits. For instance, effects of high maternal salinity on progeny germination time, flowering time and growth were only expressed in offspring grown in low salinity (Vu et al, 2015;Groot et al, 2016;Moriuchi et al, 2016). Within-and trans-generation plasticity may also operate in the same direction.…”

Jasmonic acid‐dependent regulation of seed dormancy following maternal herbivory in Arabidopsis

“…In the case of seed dormancy, maternal experiences of day length and temperature function as seasonal cues to regulate the timing of offspring germination (Fenner, 1991;Donohue, 2009;Kendall & Penfield, 2012). Maternal experiences of nitrate, water status and salinity have also been shown to influence germination behaviour (Fenner, 1991;He et al, 2014;Vu et al, 2015). Hence, maternal effects on seed dormancy in response to the abiotic environment are widespread and well characterized.…”