phot1 Inhibition of ABCB19 Primes Lateral Auxin Fluxes in the Shoot Apex Required For Phototropism

Abstract

It is well accepted that lateral redistribution of the phytohormone auxin underlies the bending of plant organs towards light. In monocots, photoreception occurs at the shoot tip above the region of differential growth. Despite more than a century of research, it is still unresolved how light regulates auxin distribution and where this occurs in dicots. Here, we establish a system in Arabidopsis thaliana to study hypocotyl phototropism in the absence of developmental events associated with seedling photomorphogenesis. We show that auxin redistribution to the epidermal sites of action occurs at and above the hypocotyl apex, not at the elongation zone. Within this region, we identify the auxin efflux transporter ATP-BINDING CASSETTE B19 (ABCB19) as a substrate target for the photoreceptor kinase PHOTOTROPIN 1 (phot1). Heterologous expression and physiological analyses indicate that phosphorylation of ABCB19 by phot1 inhibits its efflux activity, thereby increasing auxin levels in and above the hypocotyl apex to halt vertical growth and prime lateral fluxes that are subsequently channeled to the elongation zone by PIN-FORMED 3 (PIN3). Together, these results provide new insights into the roles of ABCB19 and PIN3 in establishing phototropic curvatures and demonstrate that the proximity of light perception and differential phototropic growth is conserved in angiosperms.

Author Summary

Plants depend on sunlight for photosynthesis and adapt their growth to optimize light capture. Phototropism, the reorientation of growth towards light, is one important adaptive response. Modern studies of phototropism began with experiments in monocotyledonous grasses by Charles Darwin and led ultimately to the discovery of the plant growth hormone auxin, establishing the concept that light perception at the shoot apex triggers differential bending in the tissues below. In the past two decades, molecular-genetic analysis in the model flowering plant Arabidopsis thaliana has identified the principle photoreceptor for phototropism, phot1, as well as the major auxin transporters. Despite extensive efforts, how the photoreceptor regulates auxin transport so as to establish differential growth is still poorly understood, as is whether this process is conserved between monocots and dicots. Here, we introduce a new approach to the study of Arabidopsis phototropism in the absence of developmental events associated with seedling photomorphogenesis. In doing so, we show that the proximity of light perception and differential growth is conserved between monocots and dicots: in both plant types, differential growth is a consequence of lateral auxin movements across the shoot apex. Moreover, we identify two auxin transporters, PIN3 and ABCB19, that contribute to these movements, the latter serving to prime lateral auxin fluxes in the shoot apex. ABCB19 function is regulated by phot1, identifying it as a substrate for this class of photoreceptor kinase.