Organ-specific COP1 control of BES1 stability adjusts plant growth patterns under shade or warmth

Rojas, Cecilia Costigliolo; Bianchimano, Luciana; Oh, Jeonghwa; Montepaone, Sofía Romero; Tarkowská, Dana; Minguet, Eugenio G.; Schön, Jonas; Hourquet, Mariano García; Flugel, Timo; Blázquez, Miguel Á.; Choi, Giltsu; Strnad, Miroslav; Mora-Garcı́a, Santiago; Alabadı́, David; Zurbriggen, Matías D.; Casal, Jorge J.

doi:10.1016/j.devcel.2022.07.003

Cited by 25 publications

(15 citation statements)

References 113 publications

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“…PIF4 promotes hypocotyl growth but inhibits cotyledon expansion (Huq and Quail, 2002). The PIF4-mediated inhibition of cotyledon expansion is particularly important under shade (Costigliolo Rojas et al ., 2022). Interestingly, under shade, cotyledon PIF4 protein levels observed in luminometer experiments decreased in the morning and increased in the afternoon in response to PEG compared to the control (Fig.…”

Section: Discussionmentioning

confidence: 99%

Water shortage reducesPHYTOCHROME INTERACTING FACTOR 4, 5and3expression and shade avoidance in Arabidopsis

Semmoloni

Rojas

Yan

et al. 2022

Preprint

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In agricultural crops, forests and grasslands, water deficit often occurs in the presence of cues from neighbouring vegetation. However, most studies have addressed separately the mechanisms of plant growth responses to these two aspects of the environment. Here we show that transferringArabidopsis thalianaseedlings to agar containing polyethylene glycol (PEG) to restrict water availability reduces hypocotyl growth responses to shade without simultaneous affecting cotyledon expansion or its response to shade. Water restriction diminished the activity of thePHYTOCHROME INTERACTING FACTOR 4 (PIF4), PIF5, PIF3andPIF3-LIKE 1gene promoters, particularly in seedlings exposed to simulated shade. The response ofPIF4expression to PEG required the presence of its positive morning regulators CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) and LATE ELONGATED HYPOCOTYL (LHY), which also reduced their expression in response to PEG. Water restriction diminished the nuclear abundance of PIF4 in hypocotyl cells only in the seedlings exposed to shade. In addition to the changes inPIF4levels, post-transcriptional processes also contributed to the response to PEG. Hypocotyl growth showed significant triple interaction among water availability, shade and the presence of PIF4, PIF5 and PIF3. Collectively, these results unveil PIFs as a hub that interlinks shade and drought information to control growth.

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Section: Discussionmentioning

confidence: 99%

Water shortage reducesPHYTOCHROME INTERACTING FACTOR 4, 5and3expression and shade avoidance in Arabidopsis

Semmoloni

Rojas

Yan

et al. 2022

Preprint

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“…In hypocotyl cells, the nuclear levels of COP1 13,21,48 and BES1 (protected from degradation by COP1) 16 are lower under sustained white light than under shade; however, the earliest LFS increased the nuclear levels of both mCherry-COP1 and GFP-BES1 (Fig. 4f-g).…”

Section: Lfs Decrease the Nuclear Abundance Of Pif4mentioning

confidence: 97%

“…Under shade, COP1 increases its nuclear abundance and targets to degradation negative transcriptional regulators of PIFs [13][14][15] . COP1 also protects BRI1-EMS-SUPPRESSOR 1 (BES1) in the hypocotyl, a transcription factor that contributes locally to the promotion of hypocotyl growth 16 .…”

Section: Introductionmentioning

confidence: 99%

Sensory perception of fluctuating light in Arabidopsis

Belmonte,

Tissot,

Rabinovich

et al. 2024

Preprint

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When exposed to shade from neighbours, competitive plants modify their growth patterns to improve access to light. In dense plant stands, ranging from forests to humid grasslands and crops, shade is interrupted by sunflecks penetrating the canopy. Relatively infrequent, minute-scale interruptions can significantly contribute to the daily light input. However, given the short duration and the time gap between these low frequency sunflecks (LFS), whether plants can sense them was unknown. Here we show that phytochrome B (phyB), cryptochrome 1 (cry1), cry2, and UV RESISTANCE LOCUS 8 (UVR8) cooperatively perceive LFS to reduce hypocotyl growth inArabidopsis thaliana. LFS also enhanced the expression of photosynthetic and photo-protective genes and initiated pre-emptive acclimation to water restriction. Repeated LFS increased the nuclear abundance of cry1 and UVR8. This positive feedback enhanced the sensitivity to subsequent LFS and even to the shade between LFS. LFS reduced the nuclear abundance of the growth regulator PHYTOCHROME INTERACTING FACTOR 4 (PIF4), which only slowly recovered upon return to shade, further amplifying the signal. The dynamics of the photo-sensory system under fluctuating light helps adjust plants to the prevailing conditions.

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“…Notably, warm temperatures also enhance COP1 nuclear localization to destabilize HY5 proteins, thus promoting hypocotyl elongation (Park et al., 2017; Toledo‐Ortiz et al., 2014). In addition, in response to warm temperatures or shade, COP1 not only enhances ubiquitination and degradation of DELLA proteins (Blanco‐Touriñán et al., 2020) (Figure 2), but also promotes BES1 degradation in the cotyledons through the ubiquitin/26S proteasomal pathway (Costigliolo Rojas et al., 2022). However, COP1 stabilizes BES1 protein in the hypocotyls, thus playing opposite roles in regulating BES stability in the cotyledons and hypocotyls (Costigliolo Rojas et al., 2022).…”

Section: Plant Response Strategies To Both Shade and Abiotic Stressmentioning

confidence: 99%

“…In addition, in response to warm temperatures or shade, COP1 not only enhances ubiquitination and degradation of DELLA proteins (Blanco‐Touriñán et al., 2020) (Figure 2), but also promotes BES1 degradation in the cotyledons through the ubiquitin/26S proteasomal pathway (Costigliolo Rojas et al., 2022). However, COP1 stabilizes BES1 protein in the hypocotyls, thus playing opposite roles in regulating BES stability in the cotyledons and hypocotyls (Costigliolo Rojas et al., 2022). Interestingly, PIF4 and HY5 were recently shown to act as the key transcription factors mediating warm temperature‐induced elongation of hypocotyls and roots, respectively (Lee et al., 2021), but it remains to be investigated whether they similarly mediate tissue‐specific responses to shade.…”

Section: Plant Response Strategies To Both Shade and Abiotic Stressmentioning

confidence: 99%

Molecular mechanisms underlying coordinated responses of plants to shade and environmental stresses

Han,

Ma,

Terzaghi

et al. 2024

The Plant Journal

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SUMMARYShade avoidance syndrome (SAS) is triggered by a low ratio of red (R) to far‐red (FR) light (R/FR ratio), which is caused by neighbor detection and/or canopy shade. In order to compete for the limited light, plants elongate hypocotyls and petioles by deactivating phytochrome B (phyB), a major R light photoreceptor, thus releasing its inhibition of the growth‐promoting transcription factors PHYTOCHROME‐INTERACTING FACTORs. Under natural conditions, plants must cope with abiotic stresses such as drought, soil salinity, and extreme temperatures, and biotic stresses such as pathogens and pests. Plants have evolved sophisticated mechanisms to simultaneously deal with multiple environmental stresses. In this review, we will summarize recent major advances in our understanding of how plants coordinately respond to shade and environmental stresses, and will also discuss the important questions for future research. A deep understanding of how plants synergistically respond to shade together with abiotic and biotic stresses will facilitate the design and breeding of new crop varieties with enhanced tolerance to high‐density planting and environmental stresses.

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Organ-specific COP1 control of BES1 stability adjusts plant growth patterns under shade or warmth

Cited by 25 publications

References 113 publications

Water shortage reducesPHYTOCHROME INTERACTING FACTOR 4, 5and3expression and shade avoidance in Arabidopsis

Water shortage reducesPHYTOCHROME INTERACTING FACTOR 4, 5and3expression and shade avoidance in Arabidopsis

Sensory perception of fluctuating light in Arabidopsis

Molecular mechanisms underlying coordinated responses of plants to shade and environmental stresses

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