Energy use efficiency is characterized by an epigenetic component that can be directed through artificial selection to increase yield

Abstract

Quantitative traits, such as size and weight in animals and seed yield in plants, are distributed normally, even within a population of genetically identical individuals. For example, in plants, various factors, such as local soil quality, microclimate, and sowing depth, affect growth differences among individual plants of isogenic populations. Besides these physical factors, also epigenetic components contribute to differences in growth and yield. The network that regulates crop yield is still not well understood. Although this network is expected to have epigenetic elements, it is completely unclear whether it would be possible to shape the epigenome to increase crop yield. Here we show that energy use efficiency is an important factor in determining seed yield in canola (Brassica napus) and that it can be selected artificially through an epigenetic feature. From an isogenic canola population of which the individual plants and their self-fertilized progenies were recursively selected for respiration intensity, populations with distinct physiological and agronomical characteristics could be generated. These populations were found to be genetically identical, but epigenetically different. Furthermore, both the DNA methylation patterns as well as the agronomical and physiological characteristics of the selected lines were heritable. Hybrids derived from parent lines selected for high energy use efficiencies had a 5% yield increase on top of heterosis. Our results demonstrate that artificial selection allows the increase of the yield potential by selecting populations with particular epigenomic states. Brassica napus ͉ epigenome

Epigenetic Variation, Inheritance, and Selection in Plant Populations

“…In stressed Nicotiana tabacum and Arabidopsis plants, as well as in their unstressed progeny, homologous recombination occurs at a higher frequency than in control plants (Molinier et al 2006;Boyko et al 2007Boyko et al , 2010Kathiria et al 2010). Furthermore, environmentally induced changes in DNA methylation patterns and gene expression are transmitted to unstressed offspring (Hauben et al 2009;Verhoeven et al 2010;Bilichak et al 2012). In several cases, plant responses to biotic stress, such as enhanced defense reactions to herbivore and plant pathogen attacks, persist in the next generation, indicating inherited resistance (Kathiria et al 2010;Luna et al 2012;Rasmann et al 2012;Slaughter et al 2012).…”

“…Such epialleles contribute to the phenotypic diversity of a population and, hence, may have a role in adaptation and evolution. Moreover, the formation of certain epialleles may be triggered by the environment, as suggested in several recent plant studies (Molinier et al 2006;Hauben et al 2009;Boyko et al 2010;Kathiria et al 2010;Lang-Mladek et al 2010;Verhoeven and van Gurp 2012). If such effects last for several generations, the modern evolutionary synthesis will have to be expanded.…”

Assessing elements of an extended evolutionary synthesis for plant domestication and agricultural origin research

“…In any case, TEI as strictly defined does appear to be empirically demonstrated with examples from plants, albeit, at this point, infrequently (99,100). Prominent examples notably include maize (101) and canola (Brassica napus L.) (97). Moreover, methylation and histone epigenetic effects have been clearly demonstrated to modulate phenotypic variability for agronomically important traits, such as seed yield in canola (in addition to heritability, epigenetic factors also were shown to be amenable to manipulation through artificial selection), fruit ripening (with tomato as the model plant), plant height, and flowering time (high heritability was shown in the latter), and also, interestingly to cause an unusual frequency of dramatic phenotypic changes in hybrids as a result of novel regulatory interactions (e.g., refs.…”

“…However, more stability than once thought possible is being documented (e.g., ref. 97). Many examples of epigenetic processes are found in plants (as discussed below) and are little disputed.…”

Chromatin and epigenetics in all their states: Meeting report of the first conference on Epigenetic and Chromatin Regulation of Plant Traits - January 14 – 15, 2016 - Strasbourg, France

“…Energy efficiency and energy homeostasis have an epigenetic component that can be directed and stabilized by using artificial selection, resulting in superior agronomic traits in crops. 53,54 For example, Brassica napus isogenic lines artificially selected for their enhanced drought stress tolerance displayed upregulated transcriptomic stress response related with particular epigenetic variations, including differential H3K4me3 at several drought-responsive genes. 32 Martin Schmidt, from Mieke Van Lijsebettens's group (VIB, PSB, Ghent University, Ghent, Belgium), presented work on a selected Oryza sativa line with improved energy use efficiency and seed yield.…”