Review
Transgenerational epigenetic inheritance in plants

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Abstract

Interest in transgenerational epigenetic inheritance has intensified with the boosting of knowledge on epigenetic mechanisms regulating gene expression during development and in response to internal and external signals such as biotic and abiotic stresses. Starting with an historical background of scantily documented anecdotes and their consequences, we recapitulate the information gathered during the last 60 years on naturally occurring and induced epialleles and paramutations in plants. We present the major players of epigenetic regulation and their importance in controlling stress responses. The effect of diverse stressors on the epigenetic status and its transgenerational inheritance is summarized from a mechanistic viewpoint. The consequences of transgenerational epigenetic inheritance are presented, focusing on the knowledge about its stability, and in relation to genetically fixed mutations, recombination, and genomic rearrangement. We conclude with an outlook on the importance of transgenerational inheritance for adaptation to changing environments and for practical applications. This article is part of a Special Issue entitled “Epigenetic control of cellular and developmental processes in plants”.

Research highlights

► The relevance of plant adaptation for coping with adverse environments ► Insights into mechanisms by which biotic and abiotic stress might impinge on the epigenome of plants ► The potential role of inherited epigenetic adjustments for plant adaptation

Introduction

Generations of life scientists have contributed to our current view that selection, acting on randomly generated genetic variations or polymorphisms, is the driving force for adaptive responses and organismal evolution. Accordingly, the fact that some genotypes perform better than others under defined environmental conditions, could be seen as being the result of sheer luck.

This dogma of genetic inheritance and evolution has been challenged repeatedly by Lamarckian viewpoints, which also occurred for ideological reasons in the Soviet Union and countries of the former Eastern Block [1], [2], [3], [4]. One could start with the enigmatic character Paul Kammerer, an Austrian biologist trying to make a strong case for Lamarckism at the beginning of the 20th century. This involved experiments on regenerative capacities of Ciona (a tunicate) as well as his infamous attempts to prove heritable environmental effects on the anatomy of midwife toads (Alytes obstetricans) [5]. Given that some of these experiments appear to have been fabricated, which might have contributed to Kammerer's decision to put an end to his life, it is astounding to note that his legacy still causes some dispute in the scientific community [5], [6], [7], [8], [9]. Somewhat more far-reaching consequences arose from the doctrines represented by the agronomist Trofim Lysenko and his followers. Based on experiments addressing vernalization in wheat, he came up with a concept aiming to substantially improve crop qualities via inheritance of acquired phenotypic traits [10]. The resulting denial of Mendelian genetics also ruined the careers of numerous brilliant scientists in the Soviet Union, which makes it perhaps understandable that any attempt to rehabilitate such Lamarckian positions is considered, at the very least, problematic [11]. Even today, when viewing arguments of proponents of ‘Intelligent Design’ we are confronted with attempts to challenge well-established evolutionary concepts without offering any scientifically valid support for such divergent hypotheses [12], [13]. Thus, when it comes to transgenerational inheritance of acquired characteristics, a skeptical viewpoint appears justified.

Epigenetic responses are caused by variations in epigenetic marks, that is, reversible enzyme-mediated modifications of DNA or associated histones that control transcriptional activity of genes, repetitive sequences, and transposable elements and thus, are important regulators of genome integrity in higher eukaryotes [14].

Here, it is important to discriminate between inheritance of established epigenetic marks upon formation of specialized cell files in multicellular organisms, and the inheritance of such epigenetic marks across generations. Intraorganismal inheritance of epigenetic marks can be traced back to Conrad Waddington who originally postulated the concept as a means of explaining the fact that diverse cell types that constitute a multicellular organism can arise from only a single genome [15], [16], [17], [18]. In contrast, transgenerational epigenetic inheritance requires the passage of epigenetic marks, such as DNA methylation, through the germline without being erased by surveillance mechanisms that ensure establishment of cellular totipotency at the onset of ontogenesis [19], [20]. Erasure of epigenetic marks, in early developmental stages, is well documented in mammals, but its relevance for developmental decisions made during plant embryogenesis is less well understood [21]. Nevertheless, the observation that epigenetic alleles (i.e., epialleles) are stably inherited over several generations in a wide range of organisms, including plants indicates that the resetting to an epigenetic ‘default-state’ is seemingly a leaky process (Table 1).

For a long time, only limited genetic and molecular evidence pointed towards transgenerational epigenetic inheritance mechanisms. Some important early experiments were undertaken in higher plants, such as those addressing the mechanisms underlying pigment variations in corn lines that could not be explained by conventional Mendelian segregation [22]. These early studies involved analyses of the maize r1 and b1 loci that can switch between distinct epiallelic states that, in turn, heritably affect kernel pigmentation [23], [24], [25]. This phenomenon, known as paramutation, depends on regulatory crosstalk between distinct alleles in a heterozygous state, causing inherited alterations in the expression status of one of the alleles involved (also called paramutable allele). The switch to a then-paramutagenic allele is stably inherited through meiosis and furthermore, efficiently triggers conversion of naïve paramutable alleles into the paramutagenic state in subsequent generations, which accounts for the non-Mendelian inheritance of such traits [26], [27], [28]. With the development of molecular biology tools, some insights into the mechanisms underlying paramutation have become available, and suggest a role for locus-specific DNA repeats and their methylation status, as well as activity of small RNAs, highlighting the epigenetic nature underlying this phenomenon [29], [30], [31], [32], [33], [34]. Another well-known plant example for transgenerational epigenetic inheritance relates to a symmetry change in flowers of Linaria vulgaris (toadflax) [35]. A change from bilateral to radial symmetry has been associated with increased DNA methylation in the upstream promoter region of the Lcyc locus, whereas somatic reversion to bilateral flower symmetry correlates with diminished DNA methylation [36]. Whether or not it is actually inheritance of the observed variation in DNA methylation that causes transmission of the aforementioned altered epigenetic states remains unresolved (Table 1).

Evidence for transgenerational epigenetic inheritance has also been described for non-plant multicellular organisms [37], [38], [39], [40], [41]. For example, studies on agouti viable yellow and axin fused epialleles in mice led to the suggestion that variations in chromatin modifications of retrotransposons that insert upstream of the respective loci, drive heritable changes in gene expression [42], [43]. However, as with plants, the molecular basis for inheritance of such epigenetic traits is still far from being fully understood [44].

A demonstration of transgenerational epigenetic inheritance is consistent with the concept of ‘soft inheritance’, originally coined by Ernst Mayr [45], [46]. Unlike the conventional view of a stably inherited genetic material that is subject to mutagenic changes only by chance, soft inheritance suggests an environmental impact on inherited information, thereby allowing for directed transmission of environmental effects into subsequent generations. An example for soft inheritance that has received some attention, specifically in plants, deals with induction of inherited variability of genome organization. Increased genetic variability within a defined gene pool could represent an evolutionary advantage as it might facilitate selection of well-adapted genotypes under adverse environmental conditions [47]. Accordingly, induction and inheritance of increased genetic variability due to reduced genome stability in response to a variable environment could be considered as an adaptation to such altered conditions. Work by Babara Hohn's group on somatic recombination in Arabidopsis supports this view insofar as it was demonstrated that stressful environments triggered an heritable increase in recombination rates [48]. While additional work provided further evidence for a scenario in which environmental signals cause heritable effects on genome and epigenome stability [49], [50] (Table 2), other researchers reported difficulties in reproducing the results originally obtained by the Hohn group [51]. Whether or not induced transgenerational inheritance of environmentally modulated variations on the epigenome will reshape the current views of adaptive evolution remains a matter of debate.

In recent years a number of excellent reviews addressing this controversial topic have been published [41], [52], [53], [54]. Here we will focus on the interplay between environmental factors and their (heritable) effects on the epigenome in plants. We give a brief introduction of how plants cope with environmental stress and address the molecular switches that contribute to the control of the epigenome and discuss their potential role in transgenerational epigenetic inheritance.

Section snippets

Controlling the epigenetic status in plants

Organisms are required to adjust to environmental fluctuations, and selective forces appear to act on environmentally induced modifications in development, a process suggested to be essential for adaptive speciation [55], [56]. Epigenetic marks such as DNA methylation, histone modifications, and the generation of regulatory small non-coding RNA molecules, represent an efficient means to modulate gene activity in response to internal and external stimuli [57], [58]. The highly dynamic nature of

Strategies of adaptation and acclimatization

Plants regularly encounter unfavorable environmental conditions such as, temperature extremes, drought, radiation, heavy metal and salt stress, as well as exposure to pathogens and herbivores. In general, all these stresses potentially impinge on key physiological functions and could disrupt normal structures. Consequences of metabolic dysfunction, inhibition of photosynthesis, as well as damage of cellular structures, involve severe growth disturbances, reduced fertility or premature

Outlook

To date only few examples of transgenerational epigenetic inheritance have been reported in plants. Although knowledge about the possible mechanisms is steadily emerging, there are still many open questions. However, understanding transgenerational epigenetic inheritance might be the answer to several questions regarding adaptation.

Recent studies on epigenetic variations between populations, individual organisms, and upon different environmental conditions, suggest their importance for

Acknowledgements

Work in the authors' labs is supported by grants from the Austrian Science Fund, EU FP7-ITN and by the GEN-AU program from the Austrian Federal Ministry of Science and Research. We are indebted to Geoffrey Clarke for helpful suggestions on the manuscript. We apologize to authors that some papers worthy of mention may have not been included due to the space limitation in this review.

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