Light modulates the gravitropic responses through organ-specific PIFs and HY5 regulation of LAZY4 expression in Arabidopsis

Abstract

Light and gravity are two key environmental factors that control plant growth and architecture. However, the molecular basis of the coordination of light and gravity signaling in plants remains obscure. Here, we report that two classes of transcription factors, PHYTOCHROME INTERACTING FACTORS (PIFs) and ELONGATED HYPOCOTYL5 (HY5), can directly bind and activate the expression of LAZY4, a positive regulator of gravitropism in both shoots and roots in Arabidopsis. In hypocotyls, light promotes degradation of PIFs to reduce LAZY4 expression, which inhibits the negative gravitropism of hypocotyls. LAZY4 overexpression can partially rescue the negative gravitropic phenotype of pifq in the dark without affecting amyloplast development. Our identification of the PIFs-LAZY4 regulatory module suggests the presence of another role for PIF proteins in gravitropism, in addition to a previous report demonstrating that PIFs positively regulate amyloplast development to promote negative gravitropism in hypocotyls. In roots, light promotes accumulation of HY5 proteins to activate expression of LAZY4, which promotes positive gravitropism in roots. Together, our data indicate that light exerts opposite regulation of LAZY4 expression in shoots and roots by mediating the protein levels of PIFs and HY5, respectively, to inhibit the negative gravitropism of shoots and promote positive gravitropism of roots in Arabidopsis.

Light-Dark Modulates Root Hydrotropism Associated with Gravitropism by Involving Amyloplast Response in Arabidopsis

“…Our findings show that reduced gravitropism enhances root hydrotropic bending in the dark. Phototropism might also interfere with the hydrotropism, and this interaction may be an important clue for understanding the root sensory mechanism that integrates responses to multiple stimuli in roots (Yang et al, 2020). However, the trade-off between phototropism and hydrotropism remains to be clarified (Cassab et al, 2013).…”

Gravity Signaling in Flowering Plant Roots

“…Our understanding of the mechanisms that modulate root gravitropism in response to other environmental cues has also expanded quite substantially in the last few years. In this review, we discussed the involvement of key light-responsive transcription factors related to PIF and HY5 in the regulation of Arabidopsis hypocotyl and root gravitropism via their impact on LAZY4 expression in the corresponding statocytes, thereby enabling phototropism when needed [ 93 ]. Effects of drought, osmotic/salt shocks, and darkness on starch accumulation in the amyloplasts of statocytes and gravitropic sensitivity were previously reported [ 122 , 123 , 124 ].…”

“…In roots, light was shown to promote expression of HY5 , which binds to enhancers within the LAZY4 gene promoter, leading to increased LAZY4 expression and enhanced positive root gravitropism. In darkness, low HY5 expression resulted in decreased starch accumulation in the statocytes, decreased LAZY4 expression and reduced root gravitropism [ 93 ]. Interestingly light-dependent regulation of expression of another class of transcription factors, the PHYTOCHROME INTERACTING FACTORS (PIFs), was shown to have opposite effects in hypocotyls, with exposure to light resulting in PIF degradation, decreased LAZY4 expression and inhibition of negative hypocotyl gravitropism [ 93 ].…”

“…In darkness, low HY5 expression resulted in decreased starch accumulation in the statocytes, decreased LAZY4 expression and reduced root gravitropism [ 93 ]. Interestingly light-dependent regulation of expression of another class of transcription factors, the PHYTOCHROME INTERACTING FACTORS (PIFs), was shown to have opposite effects in hypocotyls, with exposure to light resulting in PIF degradation, decreased LAZY4 expression and inhibition of negative hypocotyl gravitropism [ 93 ]. Hence, light-dependent regulation of expression of key transcription factor genes allows modulation of the relative roles of gravitropism and phototropism in directing the growth of hypocotyls and roots.…”

PIN‐mediated polar auxin transport regulations in plant tropic responses

“…When auxin gradually accumulates on the lower hypocotyl side, this triggers PIN3 repolarization to the inner side of endodermal cells which (re)establishes a symmetric PIN localization and restoration of the symmetric auxin distribution across the organ, resulting in bending termination. This auxintriggered feedback on PIN repolarization requires the SCF TIR1/AFB auxin signaling (Han et al, 2020), clathrin-mediated endocytosis, GNOM-mediated trafficking, PID-mediated phosphorylation (Rakusová et al, 2016), actin cytoskeleton (Rakusová et al, 2019) and Myosin XI activity (Han et al, 2021). Such an auxin feedback mechanism ensures the fine-tuning of auxin fluxes for termination of asymmetric growth during shoot gravitropic and phototropic responses.…”