UV-B Perceived by the UVR8 Photoreceptor Inhibits Plant Thermomorphogenesis

Abstract

SummarySmall increases in ambient temperature can elicit striking effects on plant architecture, collectively termed thermomorphogenesis [1]. In Arabidopsis thaliana, these include marked stem elongation and leaf elevation, responses that have been predicted to enhance leaf cooling [2, 3, 4, 5]. Thermomorphogenesis requires increased auxin biosynthesis, mediated by the bHLH transcription factor PHYTOCHROME-INTERACTING FACTOR 4 (PIF4) [6, 7, 8], and enhanced stability of the auxin co-receptor TIR1, involving HEAT SHOCK PROTEIN 90 (HSP90) [9]. High-temperature-mediated hypocotyl elongation additionally involves localized changes in auxin metabolism, mediated by the indole-3-acetic acid (IAA)-amido synthetase Gretchen Hagen 3 (GH3).17 [10]. Here we show that ultraviolet-B light (UV-B) perceived by the photoreceptor UV RESISTANCE LOCUS 8 (UVR8) [11] strongly attenuates thermomorphogenesis via multiple mechanisms inhibiting PIF4 activity. Suppression of thermomorphogenesis involves UVR8 and CONSTITUTIVELY PHOTOMORPHOGENIC 1 (COP1)-mediated repression of PIF4 transcript accumulation, reducing PIF4 abundance. UV-B also stabilizes the bHLH protein LONG HYPOCOTYL IN FAR RED (HFR1), which can bind to and inhibit PIF4 function. Collectively, our results demonstrate complex crosstalk between UV-B and high-temperature signaling. As plants grown in sunlight would most likely experience concomitant elevations in UV-B and ambient temperature, elucidating how these pathways are integrated is of key importance to the understanding of plant development in natural environments.

Molecular mechanisms governing plant responses to high temperatures

“…UV light can abolish thermoresponsive hypocotyl elongation and decrease both the transcript and protein abundance of PIF4. UV light may also inhibit the transcription activity of PIF4 by stabilizing its inhibitory interacting protein LONG HYPOCOTYL IN FAR RED (HFR1), possibly via the inhibition of the HFR1‐degradation‐promoting ubiquitin ligase CONSTITUTIVELY PHOTOMORPHOGENIC 1 (COP1) (Yang et al ; Hayes et al ).…”

Photomorphogenic responses to ultraviolet‐B light

“…1, Kliebenstein et al (); 2, Brown et al (); 3, Brown & Jenkins (); 4, Favory et al (); 5, Brown et al (); 6, Gruber et al (); 7, Feher et al (); 8, Davey et al (); 9, Lang‐Mladek et al (); 10, Morales et al (); 11, Wargent et al (); 12, Demkura & Ballaré (); 13, Cloix et al (); 14, Huang et al (); 15, Heijde et al (); 16, Fasano et al (); 17, Tossi et al (); 18, Huang et al (); 19, Vandenbussche et al (); 20, Hayes et al (); 21, Binkert et al (); 22, Fierro et al (); 23, Mazza & Ballaré ; 24, Xie et al (); 25, Li et al (); 26, Yin et al (); 27, Tilbrook et al (); 28, Velanis et al (); 29, Heilmann et al (). 30, Hayes et al (). 31.…”

Pivotal roles of environmental sensing and signaling mechanisms in plant responses to climate change

“…COP1 by itself constitutes an additional level of combined UV-B and heat stress signaling interference. It is likely that HYH directly competes with PIF4 during combined UV-B and heat stress (Box et al, 2015;de Lucas et al, 2008;Hayes et al, 2017;Lee et al, 2014;Quint et al, 2016). However, in the presence of UV-B, COP1 sequesters UVR8 and becomes unable to stabilize HFR1, which leads to loss of PIF4 activity through lack of HFR1 availability (Hayes et al, 2017;Quint et al, 2016).…”

“…Alternatively, thermomorphogenesis inhibition could prevent excessive elongation of stem by heat and decrease lodging susceptibility(Hayes et al, 2017;Yin, 2017). UV-B-mediated decrease of the distance between soil surface and photosynthetically active tissues might indeed increase heat sensitivity.…”

“…Heat and UV-B signaling systems(Box et al, 2015;Hayes et al, 2017;Quint et al, 2016;Yin et al, 2016) are, respectively, shown in red and purple (online only). Heat and UV-B signaling systems(Box et al, 2015;Hayes et al, 2017;Quint et al, 2016;Yin et al, 2016) are, respectively, shown in red and purple (online only).…”