The epigenetic memory of temperature during embryogenesis modifies the expression of bud burst-related genes in Norway spruce epitypes

Abstract

Main conclusion Epigenetic memory affects the timing of bud burst phenology and the expression of bud burst-related genes in genetically identical Norway spruce epitypes in a manner usually associated with ecotypes. In Norway spruce, a temperature-dependent epigenetic memory established during embryogenesis affects the timing of bud burst and bud set in a reproducible and predictable manner. We hypothesize that the clinal variation in these phenological traits, which is associated with adaptation to growth under frost-free conditions, has an epigenetic component. In Norway spruce, dehydrins (DHNs) have been associated with extreme frost tolerance. DHN transcript levels decrease gradually prior to flushing, a time when trees are highly sensitive to frost. Furthermore, EARLY BUD BREAK 1 genes (EBB1) and the FT-TFL1-LIKE 2-gene (PaFTL2) were previously suggested to be implied in control of bud phenology. Here we report an analysis of transcript levels of 12 DHNs, 3 EBB1 genes and FTL2 in epitypes of the same genotype generated at different epitype-inducing temperatures, before and during spring bud burst. Earlier flushing of epitypes originating from embryos developed at 18 °C as compared to 28 °C, was associated with differential expression of these genes between epitypes and between buds and last year’s needles. The majority of these genes showed significantly different expressions between epitypes in at least one time point. The general trend in DHN expression pattern in buds showed the expected reduction in transcript levels when approaching flushing, whereas, surprisingly, transcript levels peaked later in needles, mainly at the moment of bud burst. Collectively, our results demonstrate that the epigenetic memory of temperature during embryogenesis affects bud burst phenology and expression of the bud burst-related DHN, EBB1 and FTL2 genes in genetically identical Norway spruce epitypes.Electronic supplementary materialThe online version of this article (doi:10.1007/s00425-017-2713-9) contains supplementary material, which is available to authorized users.

Phenology and growth of Fagus sylvatica and Quercus robur seedlings in response to temperature variation in the parental versus offspring generation

“…; Carneros et al . ), further studies are needed to confirm this. An increase in minimum and mean temperatures during the reproductive period seems to have more influence than increasing maximum temperature during the reproductive period in oak seedlings.…”

“…For example, in Norway spruce, Carneros et al . () found that an epigenetic memory mechanism affects both the timing of bud burst phenology and the expression of bud burst‐related genes in genetically identical Norway spruce epitypes (clones only differing in an epigenetic alteration in a gene), allowing them to adapt rapidly to a changing environment. The temperature sum experienced by the developing embryo and photoperiod conditions during embryogenesis epigenetically shift the growth cycle of the embryos, giving rise to different epitypes from the same genotype (Yakovlev et al .…”

“…Temperature in early development (from fertilisation to juvenile development) of the parents and during embryogenesis of the parental generation has been reported to influence the phenology of the next generation (Burton & Metcalfe ; Carneros et al . ; Dewan et al . ; Donelson et al .…”

A Method for Experimental Warming of Developing Tree Seeds With A Common Garden Demonstration of Seedling Responses

“…> 2 years for many pine species) present more opportunities for suboptimal temperatures to reduce seed quality [4]. Heat experienced by parental plants and directly by seeds can reduce seed viability and seedling vigor [3,9], and maladaptively affect progeny bud burst phenology and cold hardiness [17]. And while effects of elevated temperature during tree seed development have been studied with clones in temperature-controlled greenhouses [18], and by inferring temperature differences during seed development based on provenance climates [19], there is a dearth of knowledge of the consequences of warming during seed development in ecologically-realistic settings.…”

Improved propagation efficiency in a laboratory–nursery interface for somatic embryogenesis in Norway spruce

“…Majada et al (2001) suggested that in vitro development and germination are controlled by genes, although they are highly affected by environmental conditions, which can be manipulated (von Aderkas et al 2008(von Aderkas et al , 2015. Additionally, the temperature during multiplication and embryo maturation has been observed to have a delayed effect (epigenetic memory) on, e.g., survival, height growth and bud set in Norway spruce (Kvaalen and Johnsen 2008;Carneros et al 2017).…”