Yakovlev I.   Fossdal C.   Skrøppa T.   Kvaalen H.   Olsen J.   Johnsen Ø.  

An adaptive epigenetic memory regulation in Norway spruce

Reporter: Yakovlev I.

In forest trees, environmental conditions during the reproduction can greatly influence progeny performance. We found that the temperature during post meiotic megagametogenesis (zygotic embryogenesis) and seed maturation somehow shifted the developmental program of the embryos in the seeds, resulting in significant and long lasting phenotypic changes in the progeny. Traits that are affected include the timing of dehardening and bud burst in the spring; leader shoot growth cessation in the summer, and bud set and cold acclimation in the autumn. All processes are advanced or delayed in correspondence with the temperature during female reproduction. Colder reproductive environment advance bud set and cold acclimation during autumn and dehardening and bud burst during spring in their progenies. Temperature dependent difference in timing of terminal bud formation in identical clones was equivalent to a 4–6° latitudinal ecotypic difference. The progeny actually “remember” the temperatures and photoperiod prevailing during zygotic embryogenesis and seed maturation and this memory, affecting the climatic adaptation in this species, is an epigenetic phenomenon.
This phenomenon is not only of evolutionary significance but has clear practical implications. This memory can help the conifer to cope with the anticipated rapid change in temperature. It will have importance for the deployment of seedlings produced in seed orchards containing clones that are translocated to warmer sites, and it may be used to produce seedlings that have specific adaptive properties. So, it is possible to produce distinct phenotypes (epitypes) in Norway spruce, not well documented in other tree species so far.
The molecular mechanism behind this striking epigenetic memory phenomenon is not yet clear but transcriptional changes have been implicated. In epigenetically different progenies, transcriptional analysis revealed that seedlings from full-sib families produced at different embryogenesis temperature under long and short day conditions differed. Suppressive subtracted cDNA libraries revealed considerable differences in their transcriptomes. Using qRT-PCR, microRNA pathways genes PaDCL1 and 2 and PaSGS3 as well as transposons related genes are differential expression in the epigenetically different progenies with phenotypic differences in bud burst and bud set.
MicroRNAs (miRNAs) are endogenous small RNAs, exerting epigenetic gene regulatory impacts. The possible role of these in epigenetic phenomena has been studied. Norway spruce contains a set of conserved miRNAs as well as a large proportion of novel non-conserved miRNAs. From concatemerized small RNA libraries from seedlings from the same parent trees, originated from seeds developed in a cold and warm environment from one family with distinct epigenetic effects and one with little response miRNAs potentially involved in this molecular memory was found. Most of the miRNAs were targeted to unknown genes or genes with no known function. The expression of seven conserved and nine novel miRNAs showed significant differences in transcript levels in progenies showing distinct epigenetic difference in bud set, but not in the progenies from a non-responding family, making them excellent candidate miRNAs. The differentially expression of specific miRNAs indicate their putative participation in the epigenetic regulation.

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