Direct photoresponsive inhibition of a p53-like transcription activation domain in PIF3 by Arabidopsis phytochrome B

Yoo, Chan Yul; He, Jiangman; Sang, Qing; Qiu, Yongjian; Long, Ling; Kim, Ruth Jean-Ae; Chong, Emily G.; Hahm, Joseph; Morffy, Nicholas; Zhou, Pei; Strader, Lucia; Nagatani, Akira; Mo, Beixin; Chen, Meng

doi:10.1038/s41467-021-25909-5

Cited by 21 publications

(19 citation statements)

References 75 publications

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“…However, PIF3 is not part of the core circadian clock since its loss-of-function mutant does not result in any circadian defects ( Stephenson et al, 2009 ), and it is genetically separable from the core circadian clock since loss of PRR7 also does not alter PIF3 expression ( Soy et al, 2012 ; Martín et al, 2018 ). PIF3 is regulated by the photoreceptors PHYA and PHYB , which both control stability and inhibit its binding activity ( Soy et al, 2012 ; Yoo et al, 2021 ). Therefore, the PIF3– PHYA “growth” linkage ensures the genetic consistency of how input light information is translated into output of growth, while the sMYB– PRR linkages ensure a balanced timing.…”

Section: Discussionmentioning

confidence: 99%

Core circadian clock and light signaling genes brought into genetic linkage across the green lineage

Michael

2022

Plant Physiology

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The circadian clock is conserved at both the level of transcriptional networks as well as core genes in plants, ensuring that biological processes are phased to the correct time of day. In the model plant Arabidopsis (Arabidopsis thaliana), the core circadian SHAQKYF-type-MYB (sMYB) genes CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) and REVEILLE (RVE4) show genetic linkage with PSEUDO-RESPONSE REGULATOR 9 (PRR9) and PRR7, respectively. Leveraging chromosome-resolved plant genomes and syntenic ortholog analysis enabled tracing this genetic linkage back to Amborella trichopoda, a sister lineage to the angiosperm, and identifying an additional evolutionarily conserved genetic linkage in light signaling genes. The LHY/CCA1–PRR5/9, RVE4/8–PRR3/7, and PIF3–PHYA genetic linkages emerged in the bryophyte lineage and progressively moved within several genes of each other across an array of angiosperm families representing distinct whole-genome duplication and fractionation events. Soybean (Glycine max) maintained all but two genetic linkages, and expression analysis revealed the PIF3–PHYA linkage overlapping with the E4 maturity group locus was the only pair to robustly cycle with an evening phase, in contrast to the sMYB–PRR morning and midday phase. While most monocots maintain the genetic linkages, they have been lost in the economically important grasses (Poaceae), such as maize (Zea mays), where the genes have been fractionated to separate chromosomes and presence/absence variation results in the segregation of PRR7 paralogs across heterotic groups. The environmental robustness model is put forward, suggesting that evolutionarily conserved genetic linkages ensure superior microhabitat pollinator synchrony, while wide-hybrids or unlinking the genes, as seen in the grasses, result in heterosis, adaptation, and colonization of new ecological niches.

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Section: Discussionmentioning

confidence: 99%

Core circadian clock and light signaling genes brought into genetic linkage across the green lineage

Michael

2022

Plant Physiology

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“…Therefore, phys might induce phosphorylation and/or other posttranslational modification of these splicing factors within the PBs, leading to altered target identification and/or protein activity. Alternatively, phys might directly bind to these splicing factors and sequester their activities as has been shown for PIFs ( 39 – 41 ). These possibilities need to be tested in the future to uncover biochemical mechanisms by which phys/splicing factor complexes regulate pre-mRNA splicing and light-regulated developmental processes.…”

Section: Discussionmentioning

confidence: 98%

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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“…Therefore, it is possible that phys might induce phosphorylation and/or other post-translational modification of these splicing factors within the photobodies, leading to altered target identification and/or protein activity. Alternatively, phys might directly bind to these splicing factors and sequester their activities as has been shown for PIFs (37–39). These possibilities need to be tested in the future to uncover molecular and biochemical mechanisms by which phys/splicing factor complexes regulate pre-mRNA splicing and light-regulated developmental processes.…”

Section: Discussionmentioning

confidence: 98%

“…Alternatively, phys might directly bind to these splicing factors and sequester their activities as has been shown for PIFs (37)(38)(39). These possibilities need to be tested in the future to uncover molecular and biochemical mechanisms by which phys/splicing factor complexes regulate pre-mRNA splicing and light-regulated developmental processes.…”

Section: Discussionmentioning

confidence: 99%

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

Kathare¹,

Xin²,

Ganesan³

et al. 2022

Preprint

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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 modulate these aspects by intricately regulating gene expression at multiple levels. Previously, we reported that two splicing factors SFPS (SPLICING FACTOR FOR PHYTOCHROME SIGNALING) and RRC1 (REDUCED RED LIGHT RESPONSES IN CRY1CRY2 BACKGROUND 1), interact with photoactivated phyB to regulate light-mediated pre-mRNA alternative splicing (AS). 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 light-independent early flowering phenotype. SWAP1 physically interacts with both SFPS and RRC1 in a light-independent manner and forms a ternary complex. In addition, SWAP1 also physically interacts with photoactivated phyB and colocalizes with nuclear phyB photobodies. Deep RNA-seq analyses show that SWAP1 regulates the gene expression and pre-mRNA alternative splicing of a large number of genes including those involved in plant responses to light signaling. A comparison with SFPS- and RRC1-regulated events shows that all three splicing factors coordinately regulate the alternative splicing of a subset of genes. Collectively, our study uncovered the function of a new splicing factor, which interacts with photoactivated phyB, in modulating light-regulated development in plants.SIGNIFICANCERegulation of transcription and pre-mRNA alternative splicing is essential for the transcript diversity and modulation of light signaling in plants. Although several transcription factors involved in light signaling have been discovered and characterized in-depth, only a few splicing factors have been shown to be involved in the regulation of light signaling pathways. In this study, we describe the identification and characterization of a new splicing factor SWAP1, which interact with two previously characterized splicing factors, SFPS and RRC1, forming a ternary complex. We show that, like SFPS and RRC1, SWAP1 also interacts with photoactivated phyB, and consistently, swap1 seedlings are hyposensitive to red light. SWAP1 modulates alternative splicing of a large number of genes and a subset of these genes are coordinately regulated by SFPS, RRC1 and SWAP1. These results highlight the importance of not only the transcription factors but also the phyB-interacting splicing factors in light-regulated plant development.

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Direct photoresponsive inhibition of a p53-like transcription activation domain in PIF3 by Arabidopsis phytochrome B

Cited by 21 publications

References 75 publications

Core circadian clock and light signaling genes brought into genetic linkage across the green lineage

Core circadian clock and light signaling genes brought into genetic linkage across the green lineage

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

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