Phytohormone and Chromatin Crosstalk: The Missing Link For Developmental Plasticity?

Abstract

Plants grow continuously, forming new meristem-derived organs and tissues throughout their post-embryonic life. As sessile organisms, plants need to constantly integrate and reflect environmental fluctuations in their growth and development, which can translate into high level of developmental plasticity in response to environmental changes (Gaillochet and Lohmann, 2015). Alternatively, variable environments can select for robustness, where organisms function across a wide range of conditions with little change in phenotype. Plant growth is then governed by complex interplay of phytohormone signaling, chromatin structure remodeling and gene expression reprogramming. How these regulatory levels are interconnected remains largely enigmatic, but mechanistic evidence of crosstalk between phytohormone signaling and chromatin organization is emerging. Here we review (1) evidences of molecular mechanisms that mediate the crosstalk between phytohormone signaling, chromatin structure and gene expression (2) how this crosstalk may link to plant developmental plasticity and robustness and finally (3) why meristems may represent central places for this crosstalk allowing plasticity and environmental memory. Phytohormone and epigenetic regulation can interact on multiple levels (Figure 1): (1) phytohormone signaling directly affects expression or activity of key chromatin modifiers, (2) chromatin machinery target genes of the phytohormone metabolic/signaling pathways, (3) both players interact on genes involved in developmental or stress responses. Figure 1. Schematic model of phytohormones and chromatin crosstalk during plant developmental plasticity and robustness. Stem cell niches in SAM, RAM, or cambium are center of morphogenesis giving rise to the aerial and root systems or wood formation in perennials and plasticity in response to various environmental cues. Environmental signals are perceived directly or indirectly by meristems and could affect hormonal balance and/or chromatin structure in a complex crosstalk: (1) hormones can alter chromatin structure and modifiers or (2) chromatin can regulate hormones signaling/biosynthesis. These two mechanisms could then interact separately (3 and 4), jointly or successively (5) affecting genes expression and /or TEs mobilization. Thus, the hormone/chromatin crosstalk can participate in developmental choice (Robustness vs. Plasticity) by controlling cell gene identity in meristems, hormone balance integration, or chromatin stabilization of gene expression. While most of these changes are transient (resetting of hormonal and chromatin modifications) allowing the plant to be respond to new environmental conditions, chromatin states could be maintained through cell division allowing an epigenetic memory and a potential priming of new meristem-derived-organs. Several examples show that components of phytohormone signaling pathways directly control the activity of key chromatin modifiers such as POLYCOMB REPRESSIVE COMPLEX (PRC) 1 and 2 with histone-methyltransferase activity playing a major role in transcriptional regulation during development (Bratzel et al., 2010; Chen et al., 2010, 2016; Ikeuchi et al., 2015; Mozgová et al., 2017). For example, the brassinosteroid (BR) signaling TFs BRASSINAZOLE-RESISTANT 1 (BZR1) recruits the H3K27me3-demethylase EARLY FLOWERING (ELF) 6 to antagonize the H3K27me3-activity of PRC2, a chromatin modifier, at the flowering repressor FLOWERING LOCUS C (FLC), preventing precocious floral transition (Yu et al., 2008; Li et al., 2018). Additionally, chromatin complexes can be post-translationally modified by components of phytohormone signaling pathways that influence their activity. For example, abscisic acid (ABA) signaling induces SnRK-mediated phosphorylation of the chromatin remodeling ATPase BRAHMA (BRM), inhibiting its repressive activity at ABA-responsive genes (Peirats-Llobet et al., 2016). These examples demonstrate that activity of chromatin modifiers can be directed to specific loci or directly modulated by phytohormone signaling cascades. Another possibility is that changes in chromatin structure control phytohormone biosynthesis, signaling and response. Variation in DNA methylation in response to water availability in poplar or among Arabidopsis epigenetic recombinant inbred lines (epiRILs) is associated with changes in jasmonic (JA), salicylic acid (SA) and ethylene responses (Latzel et al., 2012; Lafon-Placette et al., 2018). Similarly, rice plants with reduced H3K27me3 exhibit significant differences in the auxin indole-3-acetic acid (IAA), gibberellin (GA), ABA, JA, and SA content (Liu et al., 2016). Nevertheless, these effects may be pleiotropic and may reflect altered general physiological states. As more direct evidence, PRC2 activity in Arabidopsis seed coat is downregulated by fertilization-dependent auxin, and is required for repressing GA production prior to fertilization, mediating the crosstalk between two phytohormonal pathways (Figueiredo et al., 2015, 2016; Figueiredo and Köhler, 2018). PRC2 also represses auxin biosynthesis and signaling genes in the SAM and leaves of Arabidopsis (Lafos et al., 2011). Conversely, in the RAM, the expression of the auxin efflux carrier-encoding PIN-FORMED (PIN) genes is positively regulated by BRM establishing local auxin maxima and stimulating the expression of the RAM-specifying PLETHORA genes PLT1 and PLT2 (Yang et al., 2015). BRM also binds to GA-related genes to stimulate GA biosynthesis and signaling (Archacki et al., 2013). Apart from biosynthesis and signaling, phytohormone-response genes are under direct control of chromatin modifiers. Initially described as involved in auxin homeostasis (Sorin et al., 2005), the ARGONAUTE protein AGO1, guided by small RNAs and associating with SWI/SNF complexes, was recently described to bind genes activated upon JA, auxin, and SA stimuli in...