Transition from Seeds to Seedlings: Hormonal and Epigenetic Aspects

Abstract

Transition from seed to seedling is one of the critical developmental steps, dramatically affecting plant growth and viability. Before plants enter the vegetative phase of their ontogenesis, massive rearrangements of signaling pathways and switching of gene expression programs are required. This results in suppression of the genes controlling seed maturation and activation of those involved in regulation of vegetative growth. At the level of hormonal regulation, these events are controlled by the balance of abscisic acid and gibberellins, although ethylene, auxins, brassinosteroids, cytokinins, and jasmonates are also involved. The key players include the members of the LAFL network-the transcription factors LEAFY COTYLEDON1 and 2 (LEC 1 and 2), ABSCISIC ACID INSENSITIVE3 (ABI3), and FUSCA3 (FUS3), as well as DELAY OF GERMINATION1 (DOG1). They are the negative regulators of seed germination and need to be suppressed before seedling development can be initiated. This repressive signal is mediated by chromatin remodeling complexes-POLYCOMB REPRESSIVE COMPLEX 1 and 2 (PRC1 and PRC2), as well as PICKLE (PKL) and PICKLE-RELATED2 (PKR2) proteins. Finally, epigenetic methylation of cytosine residues in DNA, histone post-translational modifications, and post-transcriptional downregulation of seed maturation genes with miRNA are discussed. Here, we summarize recent updates in the study of hormonal and epigenetic switches involved in regulation of the transition from seed germination to the post-germination stage.

Keywords: DNA methylation; desiccation tolerance; epigenetics; germination; histone modification; hormonal regulation; miRNA; post-germination; seeds.

Figure 1

Time course of seed germination. The overall germination times vary from hours to weeks, depending on plant species and environmental conditions. Phase I is characterized by rapid water uptake, accompanied with enhanced hydration of macromolecules, activation of respiration, repair of membranes, mitochondria, and DNA. Phase II is characterized by mobilization of reserves, translation of stored mRNAs, transcription and translation of newly synthesized mRNAs, and activation of protein biosynthesis. The radicle protrusion is considered as the beginning of Phase III. Epigenetic changes (methylation of DNA, as well as trimethylation, ubiquitination, and acetylation of histones), occurring in this phase, result in silencing of the genes related to seed maturation and triggering expression of the genes responsible for vegetative growth of seedlings. “Window of DT (desiccation tolerance)” can be defined as the part of the overall germination period, when seeds can be dried back to their original water contents without a decrease of their viability. Transition from germination to the post-germination stage corresponds to loss of DT.

Figure 2

Epigenetic modifications accompanying the transition from germination to the post-germination stage of plant development. (A) Methylation of cytosines in DNA. CHH methylation (mCHH) is gradually lost during germination. In contrast, CG and CHG methylation (mCG and mCHG) mostly remain stable. (B) Histone post-translational modifications. The genes involved in seed maturation and dormancy are repressed by trimethylation of K27 in histone H3 by PRC2 and ubiquitination at K119 of histone H2A by monoubiquitin ligase PRC1. The repression of the target gene is initiated by recruitment of histone deacetylase 19 (HDA19) by VAL proteins to remove histone acetylation marks and PRC1 to incorporate the H2A ubiquitine marks. Upon its onset, stable repression of the target genes can be constantly maintained by PRC2-mediated trimethylation of K27 in histone H3. (C) Post-transcriptional downregulation of target genes. miRNAs (red wavy line) block the expression of the genes involved in development and dormancy genes by cleavage of their mRNAs with Argonaute1 (AGO1) proteins.