Integration of light and temperature sensing by liquid-liquid phase separation of phytochrome B

Chen, Di; Lyu, Mohan; Kou, Xiaoxia; Li, Jing; Yang, Zhixuan; Gao, Lulu; Li, Yue; Fan, Liu‐Min; Shi, Hui; Zhong, Shangwei

doi:10.1016/j.molcel.2022.05.026

Cited by 115 publications

(98 citation statements)

References 76 publications

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“…Since SFPS, RRC1, and SWAP1 also colocalize within phyB PBs ( Fig. 6 ) ( 30 , 31 ) and phyB PBs have been shown to be liquid-liquid phase separated droplets ( 8 , 9 ), it is possible that these splicing factors are recruited by phyB in these phase-separated environments in a concentrated manner to modulate pre-mRNA AS and gene regulation ( Fig. 7 ).…”

Section: Discussionmentioning

confidence: 99%

“…In dark-grown plants, phys are predominantly localized to the cytosol in the inactive red light absorbing (Pr) form, and upon red light illumination, they are photoconverted to the biologically active far-red light absorbing (Pfr) form and then translocated into the nucleus to form discrete nuclear bodies called photobodies (PBs) ( 3 , 4 ). These PBs are membraneless subnuclear dynamic structures, where phyB undergoes liquid-liquid phase separation and interacts with diverse target proteins to initiate appropriate signaling cascades ( 6 – 9 ). One group of proteins, which were recently identified as interacting with photoactivated phyB and colocalized to PBs, are splicing factors that regulate light-induced pre–messenger RNA (mRNA) alternative splicing (AS) ( 10 ).…”

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confidence: 99%

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SWAP1-SFPS-RRC1 splicing factor complex modulates pre-mRNA splicing to promote photomorphogenesis in Arabidopsis

Kathare

Xin

Ganesan

et al. 2022

Proc. Natl. Acad. Sci. U.S.A.

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Light signals perceived by a group of photoreceptors have profound effects on the physiology, growth, and development of plants. The red/far-red light–absorbing phytochromes (phys) modulate these aspects by intricately regulating gene expression at multiple levels. Here, we report the identification and functional characterization of an RNA-binding splicing factor, SWAP1 (SUPPRESSOR-OF-WHITE-APRICOT/SURP RNA-BINDING DOMAIN-CONTAINING PROTEIN1). Loss-of-function swap1-1 mutant is hyposensitive to red light and exhibits a day length–independent early flowering phenotype. SWAP1 physically interacts with two other splicing factors, (SFPS) SPLICING FACTOR FOR PHYTOCHROME SIGNALING and (RRC1) REDUCED RED LIGHT RESPONSES IN CRY1CRY2 BACKGROUND 1 in a light-independent manner and forms a ternary complex. In addition, SWAP1 physically interacts with photoactivated phyB and colocalizes with nuclear phyB photobodies. Phenotypic analyses show that the swap1sfps , swap1rrc1, and sfpsrrc1 double mutants display hypocotyl lengths similar to that of the respective single mutants under red light, suggesting that they function in the same genetic pathway. The swap1sfps double and swap1sfpsrrc1 triple mutants display pleiotropic phenotypes, including sterility at the adult stage. Deep RNA sequencing (RNA-seq) analyses show that SWAP1 regulates the gene expression and pre–messenger RNA (mRNA) alternative splicing of a large number of genes, including those involved in plant responses to light signaling. A comparative analysis of alternative splicing among single, double, and triple mutants showed that all three splicing factors coordinately regulate the alternative splicing of a subset of genes. Our study uncovered the function of a splicing factor that modulates light-regulated alternative splicing by interacting with photoactivated phyB and other splicing factors.

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Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

SWAP1-SFPS-RRC1 splicing factor complex modulates pre-mRNA splicing to promote photomorphogenesis in Arabidopsis

Kathare

Xin

Ganesan

et al. 2022

Proc. Natl. Acad. Sci. U.S.A.

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“…As a result, a novel CRY2 function was discovered in regulating m 6 A writer activity through a CR‐dependent and blue‐light mediated LLPS recruitment mechanism that results in controlling 10% of the Arabidopsis mRNA abundance through methylation (X. Wang et al ., 2021 ). A recent report showed that phyB photobodies also form through LLPS (Chen et al ., 2022 ). More specifically, phyB self‐associates into liquid‐like droplets through its C‐terminus in response to R light, whereas the intrinsically disordered N‐terminal extension modulates phyB phase separation in response to temperature changes (Chen et al ., 2022 ).…”

Section: Discussionmentioning

confidence: 99%

“…A recent report showed that phyB photobodies also form through LLPS (Chen et al ., 2022 ). More specifically, phyB self‐associates into liquid‐like droplets through its C‐terminus in response to R light, whereas the intrinsically disordered N‐terminal extension modulates phyB phase separation in response to temperature changes (Chen et al ., 2022 ). However, further evidence is essential to determine if phyB can intrinsically form biomolecular condensates in an in vitro system.…”

Section: Discussionmentioning

confidence: 99%

Light, chromatin, action: nuclear events regulating light signaling in Arabidopsis

et al. 2022

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Summary The plant nucleus provides a major hub for environmental signal integration at the chromatin level. Multiple light signaling pathways operate and exchange information by regulating a large repertoire of gene targets that shape plant responses to a changing environment. In addition to the established role of transcription factors in triggering photoregulated changes in gene expression, there are eminent reports on the significance of chromatin regulators and nuclear scaffold dynamics in promoting light‐induced plant responses. Here, we report and discuss recent advances in chromatin‐regulatory mechanisms modulating plant architecture and development in response to light, including the molecular and physiological roles of key modifications such as DNA, RNA and histone methylation, and/or acetylation. The significance of the formation of biomolecular condensates of key light signaling components is discussed and potential applications to agricultural practices overviewed.

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“…This dual functionality is derived by different mechanisms. Under red light, activated PhyB translocates into the nucleus of plant hypocotyl cells and aggregates to form condensates that aid in signal transduction ( Chen et al., 2022 ). Under high temperatures, PhyB is released from condensates and changes from activated PhyB (Pfr) to its inactive form (Pr).…”

Section: Biomolecular Condensates In Plants and Heat Stress Responsementioning

confidence: 99%

Landscape of biomolecular condensates in heat stress responses

et al. 2022

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High temperature is one of the abiotic stresses that plants face and acts as a major constraint on crop production and food security. Plants have evolved several mechanisms to overcome challenging environments and respond to internal and external stimuli. One significant mechanism is the formation of biomolecular condensates driven by liquid–liquid phase separation. Biomolecular condensates have received much attention in the past decade, especially with regard to how plants perceive temperature fluctuations and their involvement in stress response and tolerance. In this review, we compile and discuss examples of plant biomolecular condensates regarding their composition, localization, and functions triggered by exposure to heat. Bioinformatic tools can be exploited to predict heat-induced biomolecular condensates. As the field of biomolecular condensates has emerged in the study of plants, many intriguing questions have arisen that have yet to be solved. Increased knowledge of biomolecular condensates will help in securing crop production and overcoming limitations caused by heat stress.

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Integration of light and temperature sensing by liquid-liquid phase separation of phytochrome B

Cited by 115 publications

References 76 publications

SWAP1-SFPS-RRC1 splicing factor complex modulates pre-mRNA splicing to promote photomorphogenesis in Arabidopsis

SWAP1-SFPS-RRC1 splicing factor complex modulates pre-mRNA splicing to promote photomorphogenesis in Arabidopsis

Light, chromatin, action: nuclear events regulating light signaling in Arabidopsis

Landscape of biomolecular condensates in heat stress responses

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