Polycomb Repressive Complex 2-mediated histone modification H3K27me3 is associated with embryogenic potential in Norway spruce

Abstract

Epigenetic reprogramming during germ cell formation is essential to gain pluripotency and thus embryogenic potential. The histone modification H3K27me3, which is catalyzed by the Polycomb Repressive Complex 2 (PRC2), regulates important developmental processes in both plants and animals, and defects in PRC2 components cause pleiotropic developmental abnormalities. Nevertheless, the role of H3K27me3 in determining embryogenic potential in gymnosperms is still elusive. To address this, we generated H3K27me3 profiles of Norway spruce embryonic callus (EC) and non-embryogenic callus (NEC) using the CUT&RUN, which is a powerful method for chromatin profiling. Here, we show that H3K27me3 mainly accumulated in genic regions in the Norway spruce genome, similarly to what is observed in other plant species. Interestingly, H3K27me3 levels in EC were much lower than those in the other examined tissues, but markedly increased upon embryo induction. These results show that H3K27me3 levels are associated with the embryogenic potential of a given tissue, and that the early phase of somatic embryogenesis is accompanied by changes in H3K27me3 levels. Thus, our study provides novel insights into the role of this epigenetic mark in spruce embryogenesis and reinforces the importance of PRC2 as a key regulator of cell fate determination across different plant species.

Polycomb Repressive Complex 2 in Eukaryotes—An Evolutionary Perspective

“…Still, our insight into PRC2 evolution in the green lineage is limited (reviewed in the work of [ 250 ]), and most of the current understanding of plant PRC2 composition or function comes from studies in the dicot flowering plant model Arabidopsis thaliana (reviewed in the work of [ 3 , 18 , 45 , 47 , 101 , 251 , 252 , 253 ]) and monocot crop species such as rice ( Oryza sativa ) [ 91 , 254 ], maize ( Zea mays) [ 94 , 255 ], and, more recently, bread wheat ( Triticum aestivum ) [ 97 ]. Information on PRC2 structure and function in the green lineage outside of angiosperms is scarce; however, a recent study in Norway spruce ( Picea abies ) brought first insights into gymnosperm PRC2 function [ 92 ]. Conservation of PRC2 subunits in bryophytes [ 89 ] together with the determination of their developmental roles [ 61 , 62 , 256 ] and recent elucidation of H3K27me3 distribution [ 166 , 257 ] brought first insights into PRC2 function in non-vascular land plants.…”

“…SWN orthologs are only identified in angiosperms (both in monocots and dicots). SWN is already found in the basal angiosperm species Amborella trichopoda , suggesting that SWN could have emerged with the separation of angiosperms and gymnosperms [ 92 , 261 ]. MEA is a shorter paralog of SWN that originated by duplication of SWN during the α whole-genome duplication (αWGD) and neofunctionalization in Brassicaceae [ 89 , 91 , 220 , 221 ].…”

“…Similar genomic distribution of H3K27me3 is also seen in monocots, including maize ( Zea mays ), rice ( Oryza sativa ), or Brachypodium distachyon [ 265 , 267 , 270 , 271 ]. In gymnosperms, H3K27me3 distribution has been studied cytologically [ 272 ] and also genome-wide in P. abies [ 92 ]. H3K27me3 was identified to be consistently located in the mid-arm areas of almost all chromosomes in Pinus sylvestris and Norway spruce, which is comparable to other angiosperms [ 272 ].…”

“…H3K27me3 was identified to be consistently located in the mid-arm areas of almost all chromosomes in Pinus sylvestris and Norway spruce, which is comparable to other angiosperms [ 272 ]. In Norway spruce, H3K27me3 plays a crucial role in embryogenesis, suggesting a conserved role of PRC2 in cell fate determination [ 92 ]. H3K27me3 distribution in the moss P. patens [ 257 ] and in the liverwort Marchantia polymorpha [ 166 ] brought important insights into the targeting of PRC2 in bryophytes.…”

The epigenetic origin of life history transitions in plants and algae

“…Norway spruce (Picea abies) is one such common conifer species that has important ecological and economic value in European forests. Norway spruce harbors diverse histone methylation marks (Fuchs et al 2008), undergoes dynamic changes in H3K27me3 and DNA methylation during embryonic tissue culture (Nakamura et al 2020), exhibits soma clonal methylome variation (Ausin et al 2016;Heer et al 2018) and, like angiosperms, expresses a distinct population of small RNAs in pollen (Nakamura et al 2019). Interestingly, breeders have noted adaptive traits in Norway spruce where epigenetic events early in development (i.e., post-meiotic megagametogenesis and seed maturation) can determine how a tree behaves and grows years later, thus allowing the expression of an altered phenology when grown in a nonnative environment (Yakovlev et al 2012).…”