Phototropin-mediated perception of light direction in Arabidopsis leaves regulates blade flattening

Abstract

One conserved feature among angiosperms is the development of flat thin leaves. This developmental pattern optimizes light capture and gas exchange for photosynthesis. The blue light receptors phototropins are required for leaf flattening, with the null phot1phot2 mutant showing downwards curled leaves in Arabidopsis. However, key aspects of their function in leaf development remain unknown. Here, we performed a detailed spatiotemporal characterization of phototropin function in Arabidopsis leaves. We found that phototropins perceive light direction in the leaf blade, and similar to their role in hypocotyls they control the spatial pattern of auxin signaling possibly modulating auxin transport, to ultimately regulate cell expansion. Phototropin signaling components in the leaf partially differ from hypocotyls. Moreover, the light response on the upper (adaxial) and lower (abaxial) sides of the leaf blade suggest a partially distinct requirement of phototropin signaling components on each side. In particular, NON PHOTOTROPIC HYPOCOTYL 3 (NPH3) showed an adaxial-specific function. In addition, we show a prominent role of PHYTOCHROME KINASE SUBSTRATE 3 (PKS3) in leaf flattening. Among the auxin transporters tested, PINs and AUX/LAX influence the response most prominently. Overall, our results show that directional blue light perception by the phototropins is a key aspect of leaf development, integrating endogenous and exogenous signals. One sentence summaryPhototropins perceive light direction in the leaf and control the auxin signaling pattern to regulate blade flattening.