Phytochrome B Output Module Sets Thermosensing Photobody Number and Tunes Arabidopsis Adaptation

Overview

Plants sense and respond to ambient temperature in part through phytochrome B (phyB), a photoreceptor that forms nuclear photobodies (PBs) whose number decreases as temperature increases. While many factors governing photobody size and dynamics have been described, how cells set photobody number per nucleus and whether this is tunable for climate adaptation remains poorly understood. Here, we test the hypothesis that the phyB Output Module (OPM) acts as the primary nucleator that controls photobody number and that natural OPM variation tunes this output in response to climate. Using Arabidopsis seedlings expressing fluorescently tagged phyB constructs, including isolated OPM, OPM point mutants, and natural phyB variants, we quantified photobody formation by 3D confocal fluorescence microscopy. Photobodies were manually scored in three-dimensional z-stacks (>90 nuclei per genotype) under defined growth conditions. Photobody classes were assigned using Oligopaint DNA FISH to label centromeric and pericentromeric chromocenters, enabling positional classification. To link genetic variation with climate, we mined the 1001 Arabidopsis Genomes dataset for OPM-coding variants and assigned accessions to Köppen–Geiger climate classes based on collection coordinates. We find that the OPM alone is sufficient to nucleate the full repertoire of photobody classes formed by full-length phyB, identifying OPM as a universal photobody nucleator. Across all classes, OPM generated photobodies more frequently than full-length phyB, indicating that the Photosensory Module (PSM) modulates OPM nucleation activity, providing a mechanism for environmental regulation. Consistent with this model, four previously identified OPM point mutations significantly reduced photobody number, demonstrating that condensate number is a tunable output of OPM nucleation strength. Importantly, natural OPM variation correlates with climate. Cold-climate accessions predominantly encode OPM variants that form many photobodies (~12 per nucleus), whereas hot-climate variants encode OPM sequences with reduced nucleation activity, forming as few as ~1 photobody per nucleus. Transgenic expression of a hot-climate OPM variant causally recapitulated this reduction in photobody number, directly linking OPM sequence variation to photobody nucleation output. Together, our results establish the phyB Output Module as the molecular “dial” that sets thermosensing photobody number and demonstrate that this dial is tuned by natural genetic variation associated with climate. These findings provide a mechanistic framework for condensate number control, suggest photobody number as a quantitative cellular readout of climate adaptation, and identify OPM as a potential target for engineering temperature-resilient crops. Our work identifies a genetic mechanism that directly links temperature sensing to climate adaptation by showing that natural variation in the phytochrome B output module tunes photobody number in response to local temperature regimes. Photobody number provides a measurable cellular indicator that connects plant genotype to climate origin, allowing scientists to better predict how plant populations may respond as regions warm or transition to new climate zones. This knowledge improves our ability to forecast changes in plant species distributions and community composition under future climate scenarios. The societal impact of this research is particularly significant for agriculture. Developing crop varieties that can maintain growth and yield under rising temperatures is a major global challenge. By identifying OPM as a tunable control point in plant thermosensing, this work offers a concrete molecular target that can be used to guide breeding or genome editing strategies aimed at producing climate resilient crops. Ultimately, this research contributes to efforts to sustain agricultural productivity, protect food security, and support ecosystems in a rapidly changing climate. Beyond plants, this study advances a general principle of how cells control the number of biomolecular condensates through a nucleator mechanism. Subnuclear membraneless organelles are conserved across plants and animals, and related structures such as promyelocytic leukemia bodies play critical roles in human disease, including cancer. Understanding how photobody number is set therefore contributes to broader insight into the regulation and misregulation of subnuclear condensates across biology.

Competition history

• CSEF 2026 Plant Biology (Senior Division) · Entry S-18-01

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