New Constitutively Active Phytochromes Exhibit Light-Independent Signaling Activity

Jeong, A Young; Lee, Si-Seok; Han, Yun‐Jeong; Shin, Ah-Young; Baek, Ayoung; Ahn, Taeho; Kim, Min-Gon; Kim, Young Soon; Lee, Keun Woo; Nagatani, Akira; Kim, Jeong-Il

doi:10.1104/pp.16.00342

Cited by 18 publications

(19 citation statements)

References 62 publications

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“…The residue triplet would facilitate the refolding process during the photoconversion and reduce the prospects of a misfolded PHY tongue. Indeed, mutating the PhyA and PhyB tyrosines that correspond to residues Tyr 176 and Phe 203 in DrBphP renders them constitutively active (33,34).…”

Section: Redundant Routes For Coupling the Phy Tongue To The Chromophorementioning

confidence: 99%

On the (un)coupling of the chromophore, tongue interactions, and overall conformation in a bacterial phytochrome

Takala

Lehtivuori

Berntsson

et al. 2018

Journal of Biological Chemistry

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Phytochromes are photoreceptors in plants, fungi, and various microorganisms and cycle between metastable red light-absorbing (Pr) and far-red light-absorbing (Pfr) states. Their light responses are thought to follow a conserved structural mechanism that is triggered by isomerization of the chromophore. Downstream structural changes involve refolding of the so-called tongue extension of the phytochrome-specific GAF-related (PHY) domain of the photoreceptor. The tongue is connected to the chromophore by conserved DIP and PRSF motifs and a conserved tyrosine, but the role of these residues in signal transduction is not clear. Here, we examine the tongue interactions and their interplay with the chromophore by substituting the conserved tyrosine (Tyr) in the phytochrome from the extremophile bacterium with phenylalanine. Using optical and FTIR spectroscopy, X-ray solution scattering, and crystallography of chromophore-binding domain (CBD) and CBD-PHY fragments, we show that the absence of the Tyr hydroxyl destabilizes the β-sheet conformation of the tongue. This allowed the phytochrome to adopt an α-helical tongue conformation regardless of the chromophore state, hence distorting the activity state of the protein. Our crystal structures further revealed that water interactions are missing in the Y263F mutant, correlating with a decrease of the photoconversion yield and underpinning the functional role of Tyr in phytochrome conformational changes. We propose a model in which isomerization of the chromophore, refolding of the tongue, and globular conformational changes are represented as weakly coupled equilibria. The results also suggest that the phytochromes have several redundant signaling routes.

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Section: Redundant Routes For Coupling the Phy Tongue To The Chromophorementioning

confidence: 99%

On the (un)coupling of the chromophore, tongue interactions, and overall conformation in a bacterial phytochrome

Takala

Lehtivuori

Berntsson

et al. 2018

Journal of Biological Chemistry

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“…Besides the mRNA levels, PHY protein activity can also be manipulated. In Arabidopsis thaliana and Avena sativa, specific amino acid changes in the photosensor module domains result in a light-independent constitutive biological activity (Jeong et al, 2016;Su and Lagarias, 2007). This is the case of the mutation Tyr 276 -to-His in the conserved GAF domain of Arabidopsis PHYB that renders constitutive PHY-dependent photomorphogenic responses, even in the darkness (Hu et al, 2009;Oka et al, 2011;Su and Lagarias, 2007).…”

Section: Introductionmentioning

confidence: 99%

Beyond the limits of photoperception: constitutively active PHYTOCHROME B2 overexpression as a means of improving fruit nutritional quality in tomato

Alves

Lira

Pikart

et al. 2020

Plant Biotechnology Journal

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Summary Photoreceptor engineering has recently emerged as a means for improving agronomically beneficial traits in crop species. Despite the central role played by the red/far‐red photoreceptor phytochromes (PHYs) in controlling fruit physiology, the applicability of PHY engineering for increasing fleshy fruit nutritional content remains poorly exploited. In this study, we demonstrated that the fruit‐specific overexpression of a constitutively active GAF domain Tyr252‐to‐His PHYB2 mutant version (PHYB2Y252H) significantly enhances the accumulation of multiple health‐promoting antioxidants in tomato fruits, without negative collateral consequences on vegetative development. Compared with the native PHYB2 overexpression, PHYB2Y252H‐overexpressing lines exhibited more extensive increments in transcript abundance of genes associated with fruit plastid development, chlorophyll biosynthesis and metabolic pathways responsible for the accumulation of antioxidant compounds. Accordingly, PHYB2Y252H‐overexpressing fruits developed more chloroplasts containing voluminous grana at the green stage and overaccumulated carotenoids, tocopherols, flavonoids and ascorbate in ripe fruits compared with both wild‐type and PHYB2‐overexpressing lines. The impacts of PHYB2 or PHYB2Y252H overexpression on fruit primary metabolism were limited to a slight promotion in lipid biosynthesis and reduction in sugar accumulation. Altogether, these findings indicate that mutation‐based adjustments in PHY properties represent a valuable photobiotechnological tool for tomato biofortification, highlighting the potential of photoreceptor engineering for improving quality traits in fleshy fruits.

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“…All Arabidopsis thaliana lines used in this work were in the Colombia (Col‐0) background except for the L er phyb‐5 mutant. The phyb‐9 , phyb‐5 , aba1‐6 , per1‐2 and abi5 ‐ 3 mutants have been described previously (Barrero et al ., ; Lee et al ., , 2016b; Jeong et al ., ).…”

Section: Methodsmentioning

confidence: 97%

Shoot phytochrome B modulates reactive oxygen species homeostasis in roots via abscisic acid signaling in Arabidopsis

Kim

et al. 2018

The Plant Journal

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Underground roots normally reside in darkness. However, they are often exposed to ambient light that penetrates through cracks in the soil layers which can occur due to wind, heavy rain or temperature extremes. In response to light exposure, roots produce reactive oxygen species (ROS) which promote root growth. It is known that ROS-induced growth promotion facilitates rapid escape of the roots from non-natural light. Meanwhile, long-term exposure of the roots to light elicits a ROS burst, which causes oxidative damage to cellular components, necessitating that cellular levels of ROS should be tightly regulated in the roots. Here we demonstrate that the red/far-red light photoreceptor phytochrome B (phyB) stimulates the biosynthesis of abscisic acid (ABA) in the shoots, and notably the shoot-derived ABA signals induce a peroxidase-mediated ROS detoxification reaction in the roots. Accordingly, while ROS accumulate in the roots of the phyb mutant that exhibits reduced primary root growth in the light, such an accumulation of ROS did not occur in the dark-grown phyb roots that exhibited normal growth. These observations indicate that mobile shoot-to-root ABA signaling links shoot phyB-mediated light perception with root ROS homeostasis to help roots adapt to unfavorable light exposure. We propose that ABA-mediated shoot-to-root phyB signaling contributes to the synchronization of shoot and root growth for optimal propagation and performance in plants.

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New Constitutively Active Phytochromes Exhibit Light-Independent Signaling Activity

Cited by 18 publications

References 62 publications

On the (un)coupling of the chromophore, tongue interactions, and overall conformation in a bacterial phytochrome

On the (un)coupling of the chromophore, tongue interactions, and overall conformation in a bacterial phytochrome

Beyond the limits of photoperception: constitutively active PHYTOCHROME B2 overexpression as a means of improving fruit nutritional quality in tomato

Shoot phytochrome B modulates reactive oxygen species homeostasis in roots via abscisic acid signaling in Arabidopsis

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