Phytochrome-interacting factor PIF3 integrates phytochrome B and UV-B signaling pathways to regulate gibberellin- and auxin-dependent growth in cucumber hypocotyls

Abstract

In Arabidopsis, the photoreceptors phytochrome B- (PhyB) and UVB resistance 8- (UVR8) mediated light responses play a major role in regulating photomorphogenic hypocotyl growth, but how they crosstalk to coordinate this process is not well understood. Here we report map-based cloning and functional characterization of a UVB-insensitive, long-hypocotyl mutant, lh1, and a wild-type-like lh2 mutant in cucumber, Cucumis sativus, which encodes a defective CsPhyB and a key gibberellic acid (GA) biosynthesis enzyme CsGA20ox-2, respectively. The lh2 mutation was epistatic to lh1 and partly suppressed long-hypocotyl phenotype in the lhl1lh2 double mutant. We identified phytochrome interacting factor (PIF) CsPIF3 that played a critical role in integrating the red/far-red and UVB light responses for hypocotyl growth. We show that two modules, CsPhyB-CsPIF3-CsGA20ox-2 (GA oxidase2)-DELLA and CsPIF3-CsARF18 (auxin response factor 18) mediate CsPhyB-regulated hypocotyl elongation through GA and auxin pathways, respectively, in which CsPIF3 binds to the G-/E-box motifs in the promoters of CsGA20ox-2 and CsARF18 to regulate their expression. We also identified a new physical interaction between CsPIF3 and CsUVR8 mediating CsPhyB-dependent, UVB-induced hypocotyl growth inhibition. Our work suggests that hypocotyl growth in cucumber involves a complex interplay of multiple photoreceptor- and phytohormone-mediated signaling pathways that show both conservation with and divergence from those in Arabidopsis.

Genome-Wide Identification of Phytochrome-Interacting Factor (PIF) Gene Family in Potatoes and Functional Characterization of StPIF3 in Regulating Shade-Avoidance Syndrome

“…Phytochrome-interacting factors have been discovered as regulatory hubs that integrate environmental cues into transcriptional scenarios, and functional characterizations have shown that PIF proteins are widely involved in plant growth, development, and stress response biological processes [30,31]. Several PIF genes have been identified in many species; for example, eight candidate PIF genes have been reported in Arabidopsis [9], tomatoes [12], maize [11,32], apples [13,33], and Brachypodium distachyon [15]; six have been reported in rice [10] and Physcomitrella patens [17]; and only one has been reported in Marchantia polymorpha [16].…”

“…Specifically, the interaction between CsPhyB and CsPIF3, followed by downstream engagement with CsGA20ox-2-DELLA and CsPIF3-CsARF18, modulates hypocotyl elongation via gibberellin and auxin routes. CsPIF3's transcriptional control is affected through its binding to G/E-box motifs within the CsGA20ox-2 and CsARF18 promoter regions [30]. Considering the central role of PIFs in light signal transduction, this study explored the effect of light intensity on StPIF expression levels.…”

The Role of Light Quality in Regulating Early Seedling Development

“…Current evidence suggests that PHYs exist in Pfr (active form) and Pr (inactive form) forms, which are interconvertible. When a PHY molecule absorbs Red light, it is converted from Pr to Pfr; when it absorbs Far−Red light, it is converted back to Pr [ 7 , 41 ]. This reversible conversion between Pr and Pfr serves as major molecular switches in the PHY signaling pathway, and their pathway and downstream components have been extensively studied.…”

“…The assimilative function of light provides the energy necessary for photosynthesis, suggesting light is the ultimate energy source for green plant metabolism, and the photosynthetic efficiency depends on the spectral wavelength (light quality) [ 2 , 3 , 4 ]. On the other hand, the signaling function of light activates and regulates many key signaling pathways related to plant photomorphogenesis [ 5 , 6 , 7 , 8 , 9 , 10 , 11 ]. In developmental biology, the response of plant growth patterns to light spectra is known as photomorphogenesis, which occurs during seed germination, seedling development, and the transition from vegetative to anthesis (photoperiodic phenomenon) [ 12 , 13 , 14 ].…”

The Role of Light Quality in Regulating Early Seedling Development

“…The assimilative function of light provides the energy necessary for photosynthesis, suggesting light is the ultimate energy source for green plant metabolism, and the photosynthetic efficiency depends on the spectral wavelength (light quality) [2][3][4]. On the other hand, the signaling function of light activates and regulates many key signaling pathways related to plant photomorphogenesis [5][6][7][8][9][10][11]. In developmental biology, the response of plant growth patterns to light spectra is known as photomorphogenesis, which occurs during seed germination, seedling development, and the transition from vegetative to anthesis (photoperiodic phenomenon) [12][13][14].…”