The epigenetic origin of life history transitions in plants and algae

Abstract

Plants and algae have a complex life history that transitions between distinct life forms called the sporophyte and the gametophyte. This phenomenon-called the alternation of generations-has fascinated botanists and phycologists for over 170 years. Despite the mesmerizing array of life histories described in plants and algae, we are only now beginning to learn about the molecular mechanisms controlling them and how they evolved. Epigenetic silencing plays an essential role in regulating gene expression during multicellular development in eukaryotes, raising questions about its impact on the life history strategy of plants and algae. Here, we trace the origin and function of epigenetic mechanisms across the plant kingdom, from unicellular green algae through to angiosperms, and attempt to reconstruct the evolutionary steps that influenced life history transitions during plant evolution. Central to this evolutionary scenario is the adaption of epigenetic silencing from a mechanism of genome defense to the repression and control of alternating generations. We extend our discussion beyond the green lineage and highlight the peculiar case of the brown algae. Unlike their unicellular diatom relatives, brown algae lack epigenetic silencing pathways common to animals and plants yet display complex life histories, hinting at the emergence of novel life history controls during stramenopile evolution.

Fig. 1

Life cycle schemes in living organisms. Haplo-diplontic life cycles are characterized by mitotic divisions in both the diploid zygote and haploid meiotic spores, which produce distinct and sometimes free-living sporophytes and gametophytes, respectively. The diploid zygote immediately undergoes meiosis in haplontic life cycles, where mitotic divisions of the resulting haploid spores generate a large multicellular individual or more unicellular haploid cells. Conversely, the diploid zygote in organisms with a diplontic life cycle divides mitotically to produce a multicellular individual or more unicellular diploid cells. Once diploid cells of diplontic organisms undergo meiosis, the resulting haploid cells directly differentiate into the gametes

Fig. 2

Co-evolution of life history and epigenetic silencing in plants and algae. Summary of the most predominant life history features and prevalent role played by DNA, H3K9 and H3K27 methylation in the major lineages of plants and algae. A key is provided below to denote what each circle in the diagram represents. Features absent in a particular lineage lack a circle. The summary represents the most salient features garnered in this review and is by no means exhaustive. The phylogenetic tree was constructed using TimeTree (Kumar et al. 2017) with the following representative species: Phaeodactylum tricornutum (Diatoms), Ectocarpus siliculosus (Brown algae), Cyanidioschyzon merolae (Red algae), Chlamydomonas reinhardtii (Green algae), Marchantia polymorpha (Bryophytes), Ceratopteris richardii (Ferns), Picea abies (Gymnosperms) and Arabidopsis thaliana (Angiosperms)

Fig. 3

Loss of DNA-H3K9 methylation patterns the Arabidopsis male gametophyte. Model summarizing how the epigenetic reprogramming of DNA-H3K9 methylation in the VN activates the male gametophytic program. In the sporophyte generation, a subset of pollen-expressed genes remains silenced with constitutive heterochromatin. During pollen development, the VN undergoes extensive reprogramming to disassemble constitutive heterochromatin, which includes the loss of H3K9me2 (yellow dots) and depletion of linker histone H1 (gray ovals). The DNA glycosylase DEMETER (gray pacman) is now able to actively demethylate the high levels of DNA methylation (red dots) known to accumulate in these heterochromatic regions. This exposes cis-regulatory elements (green lines) in the vicinity of pollen-expressed genes normally silenced during sporophytic life, allowing methylation-sensitive TFs to bind and activate their expression. The loss of DNA-H3K9 methylation thus leads to transcriptional reprogramming and facilitates the sporophyte-to-gametophyte transition

Fig. 4

Epigenetic reprogramming in the male gametophyte guides the alternation of generations in Arabidopsis. The haploid epigenome undergoes extensive and differential epigenetic reprogramming during male gametophyte development. In the vegetative cell, the loss of DNA methylation and H3K9me2 relieves transcriptional silencing over pollen-expressed genes normally silenced in the diploid sporophyte to activate genes required for pollen tube growth and sperm delivery. In sperm, the loss of H3K27me3 relieves transcriptional silencing over both sperm-specific genes and master regulators of early embryogenesis. Thus, the loss of DNA-H3K9 methylation facilitates the sporophyte-to-gametophyte transition in the vegetative cell, while the loss of H3K27me3 primes the paternal genome for the gametophyte-to-sporophyte transition after fertilization