In Arabidopsis, low blue light enhances phototropism by releasing cryptochrome 1-mediated inhibition of PIF4 expression

Abstract

Shade-avoiding plants including Arabidopsis thaliana display a number of growth responses elicited by shade cues including elongation of stem-like structures and repositioning of leaves. Shade also promotes phototropism of de-etiolated seedlings through repression of phytochrome B (phyB) presumably to enhance capture of unfiltered sunlight. Light cues indicative of shade include a reduction in the blue and red portions of the solar spectrum and a low red to far-red ratio. Here we show that in Arabidopsis seedlings both low blue and a low red to far-red ratio are required to rapidly enhance phototropism. However, prolonged low blue treatments through reduced cryptochrome 1 (cry1) activation are sufficient to promote phototropism. The enhanced phototropic response of cry1 mutants in the lab and in response to natural canopies depends on PHYTOCHROME INTERACTING FACTORs (PIFs). In favorable light conditions, cry1 limits the expression of PIF4 while in low blue light PIF4 expression increases, which contributes to phototropic enhancement. The analysis of a quantitative DII auxin reporter indicates that low blue light leads to enhanced auxin levels in the hypocotyl and, upon phototropic stimulation, a steeper auxin gradient across the hypocotyl. We conclude that phototropic enhancement by canopy shade results from the combined activities of phytochrome B and cry1 that converge on PIF regulation. ONE SENTENCE SUMMARYThe persistent depletion of blue light in natural canopy shade relieves the inhibitory effect of cryptochrome 1 on PIF4, enhancing phototropism in de-etiolated Arabidopsis seedlings. Financial supportThis work was supported by the University of Lausanne and a grant from the Swiss National Science foundation (n{degrees} 310030B_179558 to C.F.); Human Frontier Science Program organization (HFSP) Grant RPG0054-2013, ANR-12-BSV6-0005 grant (AuxiFlo) to T.V.; The University of Buenos Aires (Grant 20020100100437 to J. J. C.), and Agencia Nacional de Promocion Cientifica y Tecnologica of Argentina (Grant PICT-2018-01695 to J. J. C.). Alessandra Boccaccini and Martina Legris are funded by Marie Curie fellowships H2020-MSCA-IF-2017 grants CRoSh 796283 and Flat-Leaf 796443 respectively.