Uncovering a novel function of the CCR4-NOT complex in phytochrome A-mediated light signalling in plants.
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ABSTRACT:
SUBMITTER: Schwenk P
PROVIDER: S-EPMC8009681 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Plants perceive and transduce information about light quantity, quality, direction and photoperiod via several photoreceptors and use it to adjust their growth and development. A role for photoreceptors has been hypothesized in the injuries that tomato plants develop when exposed to continuous light as the light spectral distribution influences the injury severity. Up to now, however, only indirect clues suggested that phytochromes (PHY), red/far-red photoreceptors, are involved in the continuous-light-induced injuries in tomato. In this study, therefore, we exposed mutant and transgenic tomato plants lacking or over-expressing phytochromes to continuous light, with and without far-red light enrichment. The results show that PHYA over-expression confers complete tolerance to continuous light regardless the light spectrum. Under continuous light with low far-red content, PHYB1 and PHYB2 diminished and enhanced the injury, respectively, yet the effects were small. These results confirm that phytochrome signaling networks are involved in the induction of injury under continuous light.Highlights- PHYA over-expression confers tolerance to continuous light regardless the light spectrum.- In the absence of far-red light, PHYB1 slightly diminishes the continuous light-induced injury.- Continuous light down-regulates photosynthesis genes in sensitive tomato lines.
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Project description:It has been suggested that plant phytochromes are autophosphorylating serine/threonine kinases. However, the biochemical properties and functional roles of putative phytochrome kinase activity in plant light signalling are largely unknown. Here, we describe the biochemical and functional characterization of Avena sativa phytochrome A (AsphyA) as a potential protein kinase. We provide evidence that phytochrome-interacting factors (PIFs) are phosphorylated by phytochromes in vitro. Domain mapping of AsphyA shows that the photosensory core region consisting of PAS-GAF-PHY domains in the N-terminal is required for the observed kinase activity. Moreover, we demonstrate that transgenic plants expressing mutant versions of AsphyA, which display reduced activity in in vitro kinase assays, show hyposensitive responses to far-red light. Further analysis reveals that far-red light-induced phosphorylation and degradation of PIF3 are significantly reduced in these transgenic plants. Collectively, these results suggest a positive relationship between phytochrome kinase activity and photoresponses in plants.
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Project description:The components required for photosynthesis are encoded in two separate genomes, the nuclear and the plastid. To address how synchronization of the two genomes involved can be attained in early light-signalling during chloroplast development we have formulated and experimentally tested a mathematical model simulating light sensing and the following signalling response. The model includes phytochrome B (PhyB), the phytochrome interacting factor 3 (PIF3) and putative regulatory targets of PIF3. Closed expressions of the phyB and PIF3 concentrations after light exposure are derived, which capture the relevant timescales in the response of genes regulated by PIF3. Sequence analysis demonstrated that the promoters of the nuclear genes encoding sigma factors (SIGs) and polymerase-associated proteins (PAPs) required for expression of plastid encoded genes, contain the cis-elements for binding of PIF3. The model suggests a direct link between light inputs via PhyB-PIF3 to the plastid transcription machinery and control over the expression of photosynthesis components both in the nucleus and in the plastids. Using a pluripotent Arabidopsis cell culture in which chloroplasts develop from undifferentiated proplastids following exposure to light, we could experimentally verify that the expression of SIGs and PAPs in response to light follow the calculated expression of a PhyB-PIF3 regulated gene.
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Project description:Phytochromes are red/far-red photochromic photoreceptors central to regulating plant development. Although they are known to enter the nucleus upon light activation and, once there, regulate transcription, this is not the complete picture. Various phytochrome effects are manifested much too rapidly to derive from changes in gene expression, whereas others seem to occur without phytochrome entering the nucleus. Phytochromes also guide directional responses to light, excluding a genetic signaling route and implying instead plasma membrane association and a direct cytoplasmic signal. However, to date, no such association has been demonstrated. Here we report that a phytochrome subpopulation indeed associates physically with another photoreceptor, phototropin, at the plasma membrane. Yeast two-hybrid methods using functional photoreceptor molecules showed that the phytochrome steering growth direction in Physcomitrella protonemata binds several phototropins specifically in the photoactivated Pfr state. Split-YFP studies in planta showed that the interaction occurs exclusively at the plasma membrane. Coimmunoprecipitation experiments provided independent confirmation of in vivo phy-phot binding. Consistent with this interaction being associated with a cellular signal, we found that phytochrome-mediated tropic responses are impaired in Physcomitrella phot(-) mutants. Split-YFP revealed a similar interaction between Arabidopsis phytochrome A and phototropin 1 at the plasma membrane. These associations additionally provide a functional explanation for the evolution of neochrome photoreceptors. Our results imply that the elusive phytochrome cytoplasmic signal arises through binding and coaction with phototropin at the plasma membrane.
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Project description:Plastid-to-nucleus retrograde signals emitted by dysfunctional chloroplasts impact photomorphogenic development, but the molecular link between retrograde- and photosensory-receptor signalling has remained unclear. Here, we show that the phytochrome and retrograde signalling (RS) pathways converge antagonistically to regulate the expression of the nuclear-encoded transcription factor GLK1, a key regulator of a light-induced transcriptional network central to photomorphogenesis. GLK1 gene transcription is directly repressed by PHYTOCHROME-INTERACTING FACTOR (PIF)-class bHLH transcription factors in darkness, but light-activated phytochrome reverses this activity, thereby inducing expression. Conversely, we show that retrograde signals repress this induction by a mechanism independent of PIF mediation. Collectively, our data indicate that light at moderate levels acts through the plant's nuclear-localized sensory-photoreceptor system to induce appropriate photomorphogenic development, but at excessive levels, sensed through the separate plastid-localized RS system, acts to suppress such development, thus providing a mechanism for protection against photo-oxidative damage by minimizing the tissue exposure to deleterious radiation.
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Project description:Stomata are pores found on the surfaces of leaves, and they regulate gas exchange between the plant and the environment [1]. Stomatal development is highly plastic and is influenced by environmental signals [2]. Light stimulates stomatal development, and this response is mediated by plant photoreceptors [3-5], with the red-light photoreceptor phytochrome B (phyB) having a dominant role in white light [3]. Light also regulates stomatal development systemically, with the irradiance perceived by mature leaves modulating stomatal development in young leaves [6, 7]. Here, we show that phyB is required for this systemic response. Using a combination of tissue-specific expression and an inducible expression system in the loss-of-function phyB-9 mutant [8], we show that phyB expression in the stomatal lineage, mesophyll, and phloem is sufficient to restore wild-type stomatal development. Induction of PHYB in mature leaves also rescues stomatal development in young untreated leaves, whereas phyB mutants are defective in the systemic regulation of stomatal development. Our data show that phyB acts systemically to regulate cell fate decisions in the leaf epidermis.
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Project description:The identification of genetic variants that predispose individuals to cardiovascular disease and a better understanding of their targets would be highly advantageous. Genome-wide association studies have identified variants that associate with QT-interval length (a measure of myocardial repolarization). Three of the strongest associating variants (single-nucleotide polymorphisms) are located in the putative promotor region of CNOT1, a gene encoding the central CNOT1 subunit of CCR4-NOT: a multifunctional, conserved complex regulating gene expression and mRNA stability and turnover. We isolated the minimum fragment of the CNOT1 promoter containing all three variants from individuals homozygous for the QT risk alleles and demonstrated that the haplotype associating with longer QT interval caused reduced reporter expression in a cardiac cell line, suggesting that reduced CNOT1 expression might contribute to abnormal QT intervals. Systematic siRNA-mediated knockdown of CCR4-NOT components in human induced pluripotent stem cell-derived cardiomyocytes (hiPSC-CMs) revealed that silencing CNOT1 and other CCR4-NOT genes reduced their proliferative capacity. Silencing CNOT7 also shortened action potential duration. Furthermore, the cardiac-specific knockdown of Drosophila orthologs of CCR4-NOT genes in vivo (CNOT1/Not1 and CNOT7/8/Pop2) was either lethal or resulted in dilated cardiomyopathy, reduced contractility or a propensity for arrhythmia. Silencing CNOT2/Not2, CNOT4/Not4 and CNOT6/6L/twin also affected cardiac chamber size and contractility. Developmental studies suggested that CNOT1/Not1 and CNOT7/8/Pop2 are required during cardiac remodeling from larval to adult stages. To summarize, we have demonstrated how disease-associated genes identified by GWAS can be investigated by combining human cardiomyocyte cell-based and whole-organism in vivo heart models. Our results also suggest a potential link of CNOT1 and CNOT7/8 to QT alterations and further establish a crucial role of the CCR4-NOT complex in heart development and function.This article has an associated First Person interview with the first author of the paper.
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Project description:Seeds maintain a dormant state to withstand adverse conditions and germinate when conditions become favourable to give rise to a new generation of flowering plants. Seed dormancy and germination are tightly controlled by internal and external signals. Although phytochrome photoreceptors are proposed to regulate primary seed dormancy, the underlying molecular mechanism remains elusive. Here we show that the REVEILLE1 (RVE1) and RVE2 transcription factors promote primary seed dormancy and repress red/far-red-light-reversible germination downstream of phytochrome B (phyB) in Arabidopsis thaliana. RVE1 and RVE2 expression is downregulated after imbibition and by phyB. RVE1 directly binds to the promoter of GIBBERELLIN 3-OXIDASE 2, inhibits its transcription and thus suppresses the biosynthesis of bioactive gibberellins. In addition, DELAY OF GERMINATION 1 also acts downstream of phyB. This study identifies a signalling pathway that integrates environmental light input with internal factors to control both seed dormancy and germination.
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Project description:The serine/threonine kinase HIPK2 functions as a regulator of developmental processes and as a signal integrator of a wide variety of stress signals, such as DNA damage, hypoxia, and reactive oxygen intermediates. Because the kinase is generated in a constitutively active form, its expression levels are restricted by a variety of different mechanisms. Here we identify the CCR4-NOT complex as a new regulator of HIPK2 abundance. Down-regulation or knockout of the CCR4-NOT complex member CNOT2 leads to reduced HIPK2 protein levels without affecting the expression level of HIPK1 or HIPK3. A fraction of all HIPK family members associates with the CCR4-NOT components CNOT2 and CNOT3. HIPKs also phosphorylate the CCR4-NOT complex, a feature that is shared with their yeast progenitor kinase, YAK1. Functional assays reveal that HIPK2 and HIPK1 restrict CNOT2-dependent mRNA decay. HIPKs are well known regulators of transcription, but the mutual regulation between CCR4-NOT and HIPKs extends the regulatory potential of these kinases by enabling posttranscriptional gene regulation.
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