Reduced light access promotes hypocotyl growth via autophagy-mediated recycling

Abstract

Plant growth ultimately depends on fixed carbon, thus the available light for photosynthesis. Due to canopy light absorption properties, vegetative shade combines reduced light and a low red to far-red ratio (LRFR). In shade-avoiding plants, these two conditions independently promote growth adaptations to enhance light access. However, how these conditions, differing in photosynthetically-available light, similarly promote growth remains unknown. Here, we show that Arabidopsis seedlings adjust metabolism according to light conditions to supply resources for hypocotyl growth enhancement. Transcriptome analyses indicate that reduced light induces starvation responses, suggesting a switch to a catabolic state to promote growth. Accordingly, reduced light promotes autophagy. In contrast, LRFR promotes anabolism including biosynthesis of plasma-membrane sterols downstream of PHYTOCHROME-INTERACTING FACTORs (PIFs) acting in hypocotyls. Furthermore, sterol biosynthesis and autophagy are indispensable for shade-induced hypocotyl growth. We conclude that vegetative shade enhances hypocotyl growth by combining autophagy-mediated recycling and promotion of specific anabolic processes. HIGHLIGHTSO_LIReduced light and LRFR induce catabolism and anabolism, respectively C_LIO_LIReduced light promotes autophagy to enhance hypocotyl growth in vegetative shade C_LIO_LILRFR enhances hypocotyl growth by promoting plasma membrane lipid biosynthesis C_LIO_LIIn LRFR, PIFs promote sterol biosynthesis specifically in the hypocotyl C_LI