Plants have benefited from interactions with symbionts for coping with challenging environments since the colonisation of land. The mechanisms of symbiont-mediated beneficial effects and similarities and differences to pathogen strategies are mostly unknown. Here, we use 106 (effector-) proteins, secreted by the symbiont Serendipita indica (Si) to modulate host physiology, to map interactions with Arabidopsis thaliana host proteins. Using integrative network analysis, we show significant convergence on target-proteins shared with pathogens and exclusive targeting of Arabidopsis proteins in the phytohormone signalling network. Functional in planta screening and phenotyping of Si effectors and interacting proteins reveals previously unknown hormone functions of Arabidopsis proteins and direct beneficial activities mediated by effectors in Arabidopsis. Thus, symbionts and pathogens target a shared molecular microbe-host interface. At the same time Si effectors specifically target the plant hormone network and constitute a powerful resource for elucidating the signalling network function and boosting plant productivity.

Summary: Subject to an ever‐changing world, plants must respond to harmful conditions and environmental fluctuations. Their evolutionary success can be attributed to their plasticity in both perceiving and integrating these variations to facilitate adaptation. The epigenetic control of gene expression through histone modification affords plants this flexibility by fine‐tuning gene expression and imprinting a transcriptional memory of specific conditions. Histone H3 lysine 27 trimethylation (H3K27me3) is a repressive modification held in balance across the genome by its writer, the Polycomb Repressive Complex 2, and its erasers, Jumonji‐class histone lysine demethylases. While extensively studied as a mark controlling cell‐fate identity and developmental transitions, recent efforts have shown that stress‐responsive loci are also regulated by H3K27me3. In this review, I explore the emerging roles of these H3K27me3 writers and erasers as central hubs in stress adaptation, highlighting their context‐dependent regulation and interplay with other chromatin marks. By examining H3K27me3 dynamics, I provide an updated perspective on its versatile functions beyond development, emphasising its relevance in enhancing plant adaptation and resilience to changing environments.

Plants must respond to short-term stresses, but a regulated and proportionate response is essential for long-term survival. A tightrope walker crossing a high wire must balance every step with precision—overreacting to a gust of wind would be as dangerous as not reacting at all. One example of this negative feedback is the expression of the master transcriptional regulators C-REPEAT BINDING FACTOR1/2 (CBF1/2) during the cold response. Upon low temperature perception, CBF1/2 are massively induced during the first hour but rapidly return to steady state after only 6 h.

The polycomb protein VERNALIZATION2 (VRN2) is a plant-specific subunit of the polycomb repressive complex 2 (PRC2), a conserved eukaryotic holoenzyme that represses gene expression by depositing the histone H3K27me3 mark in chromatin. Previous work established VRN2 as an oxygen-regulated target of the N-degron pathway that may function as a sensor subunit connecting PRC2 activity to the perception of positional and environmental cues. Here we show that VRN2 is enriched in hypoxic meristematic regions and emerging leaves of Arabidopsis under non-stressed conditions, and that vrn 2 mutants are larger than wild type, indicating that VRN2-PRC2 negatively regulates growth and development. This growth phenotype is caused by ectopic expression of genes that promote cell expansion, including many SAUR genes and other direct PIF transcription factor targets. Analysis of SAUR19 promoter activity and expression dynamics revealed that VRN2 is required to specifically repress these genes in the light. Moreover, we show that VRN2 is epistatic to PIF4, and directly binds and methylates histones of key loci in the PIF4 transcriptional network to provide robust light-responsive control of gene expression and growth. We propose that hypoxia-stabilised VRN2-PRC2 sets a conditionally repressed chromatin state at PIF-regulated hub genes early in leaf ontogeny coinciding with the cell division phase, and that this is required for enhancing their subsequent repression via a light-responsive signalling cascade as cells enter the expansion phase. Thus, we have identified VRN2-PRC2 as core component of a spatially regulated and developmentally encoded epigenetic mechanism that co-ordinates environment-responsive growth by facilitating light-triggered suppression of PIF signalling.