UV-B detected by the UVR8 photoreceptor antagonizes auxin signaling and plant shade avoidance

Abstract

Plants detect different facets of their radiation environment via specific photoreceptors to modulate growth and development. UV-B is perceived by the photoreceptor UV RESISTANCE LOCUS 8 (UVR8). The molecular mechanisms linking UVR8 activation to plant growth are not fully understood, however. When grown in close proximity to neighboring vegetation, shade-intolerant plants initiate dramatic stem elongation to overtop competitors. Here we show that UV-B, detected by UVR8, provides an unambiguous sunlight signal that inhibits shade avoidance responses in Arabidopsis thaliana by antagonizing the phytohormones auxin and gibberellin. UV-B triggers degradation of the transcription factors PHYTOCHROME INTERACTING FACTOR 4 and PHYTOCHROME INTERACTING FACTOR 5 and stabilizes growth-repressing DELLA proteins, inhibiting auxin biosynthesis via a dual mechanism. Our findings show that UVR8 signaling is closely integrated with other photoreceptor pathways to regulate auxin signaling and plant growth in sunlight.

Fig. 1.

UV-B inhibits Arabidopsis shade avoidance in a UVR8-dependent manner. (A) WT (Ler) and uvr8-1 rosettes grown in WL in 16-h light/8-h dark cycles for 10 d before transfer to WL, +FR, +UVB, and +UV-B+FR for a further 9 d. (B) Dissected fourth leaf of plants grown as in A. (C and D) Petiole angle from the horizontal (C) and petiole length (D) of leaf 4 in plants grown as in A, at 19 d and 18 d, respectively. n ≥ 22 ± SE. Different letters indicate statistically significant (P < 0.05) differences between means.

Fig. 2.

UV-B–mediated inhibition of seedling shade avoidance requires UVR8, but only partially involves HY5/HYH and UVR8-COP1 interaction. (A) WT (Ler) and uvr8-1 seedlings grown for 3 d in continuous WL before transfer to WL, +FR, +UV-B, and +FR+UV-B for a further 4 d. (B) Hypocotyl lengths of seedlings grown as in A. (C) Ler and uvr8-1 seedlings grown for 3 d in continuous WL before transfer to WL, low blue (low B), +UV-B, and low B+UV-B for a further 4 d. (D) Hypocotyl lengths of seedlings grown as in B. (E and F) HY5 (E) and HYH (F) transcript abundance of 7-d-old seedlings transferred to experimental conditions for 1 h. n = 3 ± SE. *Significant difference (P < 0.05) compared with WL. (G) Hypocotyl lengths of WT (Ws), hy5KS50, hyh, and hy5KS50/hyh double mutants grown as in A. (H) Hypocotyl lengths of Ler, uvr8-1, and GFP-ΔC27-UVR8 seedlings grown as in A. For hypocotyl assays, data represent mean length ± SE. n = 40. Different letters indicate statistically significant differences (P < 0.05) between means.

Fig. 3.

UV-B inhibits auxin biosynthesis in a UVR8-dependent and HY5/HYH-independent manner. (A) pDR5:GUS seedlings grown for 3 d in continuous WL before transfer to WL, +FR, +UV-B, and +FR+UV-B for a further 4 d, stained for 24 h. (B–D) Relative transcript abundance of YUCCA8, YUCCA9, and IAA29 in 7-d-old WT (Ler) and uvr8-1 seedlings transferred to experimental conditions for 4 h. (E–G) Relative transcript abundance of YUCCA8, YUCCA9, and IAA29 in 7-d-old WT (Ws) and hy5ks50/hyh seedlings transferred to experimental conditions for 4 h. n = 3 ± SE. *Significant difference (P < 0.05) in transcript abundance compared with WL. **Significant difference (P < 0.05) in transcript abundance compared with +FR.

Fig. 4.

DELLA proteins are stabilized by UV-B and contribute to shade avoidance inhibition. (A and B) Relative transcript abundance of GA2ox1 in 7-d-old Ler and uvr8-1 (A) and Ws and hy5ks50/hyh (B) seedlings transferred to experimental conditions for 4 h. n = 3 ± SE. *Significant increase in transcript abundance by +UV-B treatment. (C) Western blot showing RGA-GFP abundance in pRGA:GFP-RGA seedlings grown for 10 d in WL in 16-h light/8-h dark cycles. Protein extracts from tissue samples harvested predawn and after 6 h of WL, +FR, +UVB, and +UV-B +FR. A Ponceau stain of rbcL is shown below as a loading control. (D) Hypocotyl lengths of Ler and DELLA global null seedlings grown as in A. n = 40 ± SE. Different letters indicate statistically significant differences (P < 0.05) between means.

Fig. 5.

UV-B decreases PIF4 and PIF5 protein abundance. Western blots showing PIF4-HA (A) and PIF5-HA (B) abundance in 35S:PIF-HA seedlings grown for 10 d in WL in 16-h light/8-h dark cycles. Proteins were extracted from tissue samples harvested predawn and after 2 h of WL, +FR, +UVB, and +UV-B+FR. A Ponceau stain of rbcL is shown below each blot as a loading control.

Fig. 6.

Hypothesized role of UV-B in shade avoidance. UV-B perceived by the photoreceptor UVR8 interacts with COP1 and up-regulates transcription of HY5 and HYH. GA2ox1 levels increase, reducing GA, and increasing DELLA stability, which inhibits PIF function. In a separate pathway, UV-B signaling blocks low R:FR-mediated up-regulation of auxin biosynthesis, in part through enhanced degradation of PIF4 and PIF5. Together, UV-B inhibits auxin biosynthesis and elongation growth, inhibiting shade avoidance.