Transgenerational epimutations induced by multi-generation drought imposition mediate rice plant’s adaptation to drought condition

Abstract

Epigenetic mechanisms are crucial mediators of appropriate plant reactions to adverse environments, but their involvement in long-term adaptation is less clear. Here, we established two rice epimutation accumulation lines by applying drought conditions to 11 successive generations of two rice varieties. We took advantage of recent technical advances to examine the role of DNA methylation variations on rice adaptation to drought stress. We found that multi-generational drought improved the drought adaptability of offspring in upland fields. At single-base resolution, we discovered non-random appearance of drought-induced epimutations. Moreover, we found that a high proportion of drought-induced epimutations maintained their altered DNA methylation status in advanced generations. In addition, genes related to transgenerational epimutations directly participated in stress-responsive pathways. Analysis based on a cluster of drought-responsive genes revealed that their DNA methylation patterns were affected by multi-generational drought. These results suggested that epigenetic mechanisms play important roles in rice adaptations to upland growth conditions. Epigenetic variations have morphological, physiological and ecological consequences and are heritable across generations, suggesting that epigenetics can be considered an important regulatory mechanism in plant long-term adaptation and evolution under adverse environments.

The Arabidopsis DNA Methylome Is Stable under Transgenerational Drought Stress

“…In particular, DNA methylation is considered a key epigenetic mechanism for which there is now growing evidence (Luo et al, 1996;Boyko and Kovalchuk, 2010;Tricker et al, 2013;Herman and Sultan, 2016;Wibowo et al, 2016;Zheng et al, 2017). The specific contribution of DNA methylation at, or near, protein-coding genes toward basal plant growth and endurance remains unknown, albeit essential for proper development (Finnegan et al, 1996;Henderson and Jacobsen, 2008;Zemach et al, 2013;Yamamuro et al, 2014).…”

“…There is evidence building for the possibility of transgenerational plant stress memory irrespective of chromatin variation (Agrawal, 2002;Rasmann et al, 2012;Murgia et al, 2015;Nosalewicz et al, 2016;Zheng et al, 2017). Indeed, a distinction has been made between transgenerational epigenetic effects, referring to nongenetically determined transgenerational phenotypes, and transgenerational epigenetic inheritance, referring to nongenetically determined transgenerational phenotypes attributable to heritable chromatin modifications (Youngson and Whitelaw, 2008).…”

“…However, root memory phenotypes are not a general occurrence, as demonstrated in studies of phosphate starvation in rice (Secco et al, 2015). Recently, propagation of rice under drought stress led to aboveground differences in generation 11 plants compared with the first generation (Zheng et al, 2017). However, in that study, critically, there were no unstressed lineages incorporated to enable analysis of the phenotypic changes to be considered alongside associated DMRs, as opposed to the stochastic methylome variability observed herein that can arise over such a long-term experiment.…”

“…Furthermore, there are a growing number of conflicting reports of short-term adaptation to abiotic stresses, including salt or drought stress, that occur independently of DNA methylation changes (Cayuela et al, 1996;Jakab et al, 2005;Rossel et al, 2007;Ding et al, 2012Ding et al, , 2013Ding et al, , 2014Gordon et al, 2013;Sani et al, 2013). This is in contrast to the potential for DNA methylationmediated transgenerational memory (Luo et al, 1996;Tricker et al, 2013;Herman and Sultan, 2016;Nosalewicz et al, 2016;Wibowo et al, 2016;Zheng et al, 2017). Thus, the nature of DNA methylation and its contribution to short-term and transgenerational stress adaptation remain enigmatic, which is confounded by the limited identification of causative changes in the DNA methylome correlating with enhanced stress tolerance (Secco et al, 2015;Meng et al, 2016).…”

Epigenomics of Plant’s Responses to Environmental Stress

“…Zheng et al [100] reported that drought adaptability of rice plant improved because of multi-generational drought exposure. They identified appearance of non-random drought-induced epimutations, and a higher proportion of the induced epimutations could maintain the altered DNA methylation level in the subsequent generations.…”