Breaking new ground in photomorphogenesis: novel regulators in the interplay of light and chloroplast signaling in Arabidopsis thaliana

Abstract

As sessile organisms, plants must consistently adapt to environmental changes, such as variations in temperature, nutrient availability, humidity, light, and many more. Light is of utmost importance as it functions as a source of energy and as information signal. After germination undersoil, seedlings rapidly elongate their hypocotyl to reach the light. Once they emerge, seedlings experience de-etiolation, a complex process that allows a transition to autotrophy by maturing the chloroplast (greening) and promoting seedling photomorphogenic development by arresting the rapid hypocotyl elongation, triggering apical hook opening and opening and expanding of the cotyledons to maximize the photosynthetic area. Light is perceived by photoreceptors such as the phytochromes (PHY) responsible for red/far red light perception. Once plants are exposed to light, the photo-activated phytochromes degrade the Phytochrome Interacting Factors (PIF) transcription factors, which act as photomorphogenesis repressors in the dark, allowing photomorphogenic development. The chloroplast also works as an environmental sensor, and disruptions caused by stresses such as excessive light promote the so-called chloroplast retrograde signaling (RS) that modulates nuclear gene expression and prevents photomorphogenesis development. In the chloroplast, the pentatricopeptide repeat protein GENOMES UNCOUPLED 1 (GUN1) is crucial in generating RS, but its mechanism and nature remain unsolved. In the nucleus, the chloroplast RS represses the GOLDEN2-LIKE1 (GLK1) expression, a chloroplast development and photomorphogenesis promoter. At the beginning of this project, the GUN1/GLK1 module was shown to regulate photomorphogenesis upon chloroplast damage, but further exploration of the pathway was required to fully understand this repression mechanism. We identified BBX16 as a direct GLK1 target that promotes photomorphogenesis in moderate conditions and is repressed by the GUN1/GLK1 module upon chloroplast damage. Although the knowledge about light-induced morphological changes in seedlings is extensive, cotyledon expansion remains vaguely defined. Given the distinct dynamics of growth in the different cell types and the lack of understanding of the genetic regulators involved, this process presents a significant challenge but also an opportunity for organ-expansion research and to gain better understanding of de-etiolation. We first defined the dynamics of cotyledon expansion during de-etiolation by exploring different cell layers and the involvement of the PHY/PIF module in its regulation. Next, to contribute to the cotyledon expansion understanding, we identified UNEXPANDED COTYLEDONS (UCO), a C2H2 zinc finger transcription factor that induces cotyledon expansion when seedlings are exposed to light for the first time and is repressed by RS to prevent expansion in inadequate conditions. Despite our significant contributions to the understanding of the RS pathway, the nature of the GUN1-mediated signal remains unknown, and more regulatory mechanisms are needed to understand this process entirely. To tackle this, we designed a gun1 mutant suppressor screen to identify GUN1 downstream components. We identified NUCLEOLIN-LIKE1 (NUC1), a nucleolar-located protein involved in ribosomal RNA processing and ribosome biogenesis. Our findings indicate that NUC1 is essential for seedling de-etiolation and adaptation to high light stress. Finally, we outlined a coordinated transcriptomic regulation of ribosome biogenesis genes by light in a PIF-dependent manner and by chloroplast damage in a GUN1-dependent manner.

Date of Award	25 Jul 2024
Original language	English
Supervisor	Elena Monte Collado (Director)