Variability in DNA methylation and generational plasticity in the Lombardy poplar, a single genotype worldwide distributed since the eighteenth century

In the absence of genetic diversity, plants rely on the capacity of phenotypic plasticity to cope with shifts in environmental conditions. Understanding the mechanisms behind phenotypic plasticity and how local phenotypic adjustments are transferred to clonal offspring, will provide insight into its ecological and evolutionary significance. Epigenetic changes have recently been proposed to play a crucial role in rapid environmental adaptation. While the contribution of epigenetic changes to phenotypic plasticity has been extensively studied in sexual reproducing model organisms, little work has been done on vegetative generations of asexual reproducing plant species.
We studied epigenetic variation and bud set phenology of the Lombardy poplar (Populus nigra cv. Italica Duroi), a cultivated tree representing a single genotype worldwide distributed since the 18th century. Bud set observations and epigenetic variation were studied on vegetative offspring resulting from cuttings grown for one season in a common glasshouse environment. The cuttings were collected from 60 adult Lombardy poplars growing in different environments. The physiological condition of the cuttings was determined by measuring weight and nutrient condition. Methylation sensitive amplified polymorphisms were used to obtain global patterns of DNA methylation. Using logistic regression models, we investigated correlations among epigenotype, bud phenology and the climate at the home site of the donor trees, while accounting for physiological effects.
We found significant epigenetic variation as well as significant variation in bud phenology, in the absence of genetic variation. Remarkably, phenology of bud set observed at the end of the growing season in the common environment was significantly correlated with climate variables at the home site of the mother trees, specifically the average temperature of January and monthly potential evapotranspiration.
Although we could not directly detect significant effects of epigenetic variation on phenology, our results suggest that, in the Lombardy poplar, epigenetic marks contribute to the variation of phenotypic response that can be transferred onto asexually reproduced offspring resulting in locally adapted ecotypes. This contributes to the growing evidence that epigenetic-based transgenerational inheritance might be relevant for adaptation and evolution in contrasting or rapidly changing environments.

在缺乏遗传多样性的情况下，植物依赖表型可塑性（phenotypic plasticity）的能力以应对环境条件的变化。解析表型可塑性背后的调控机制，以及局部表型调整如何传递给无性系后代，将有助于我们理解其生态与进化意义。近年来，表观遗传（epigenetic）变化被认为在快速环境适应中发挥关键作用。尽管表观遗传变化对表型可塑性的贡献已在有性繁殖的模式生物中得到广泛研究，但针对无性繁殖植物物种的营养世代的相关研究仍较为匮乏。本研究以意大利杨（Populus nigra cv. Italica Duroi）为研究对象——这一栽培树种自18世纪起便以单一基因型在全球范围内分布。我们对在统一温室环境中生长一季的插条产生的营养后代的表观遗传变异与芽物候（bud set phenology）进行了观测与分析。插条采集自生长于不同生境的60株成年意大利杨。通过测定插条的重量与营养状况，我们确定了其生理状态。本研究采用甲基化敏感扩增多态性（methylation sensitive amplified polymorphisms）技术获取全基因组DNA甲基化（DNA methylation）模式，并借助逻辑回归模型，在控制生理效应的前提下，探究了表观基因型、芽物候与供体树木原生境气候之间的相关性。本研究在无遗传变异的背景下，观测到了显著的表观遗传变异与芽物候变异。值得注意的是，在统一环境中生长季末期观测到的芽物候，与母树原生境的气候变量显著相关，尤其是1月平均气温与月潜在蒸散量。尽管本研究未能直接检测到表观遗传变异对物候的显著影响，但研究结果表明，在意大利杨中，表观遗传标记参与了可传递给无性繁殖后代的表型响应变异，进而形成了本地适应的生态型。这一发现为越来越多的证据提供了支持，即基于表观遗传的跨代遗传（transgenerational inheritance）可能在异质或快速变化的环境中，对物种的适应与进化具有重要意义。