Environmental light regulates and optimizes plant growth and development. Genomic profiling of polysome-associated mRNA reveals that light stimulates dramatic changes in translational regulation, which contribute more to light-induced gene expression changes than transcriptional regulation.
Glutathione S-transferases (GSTs) have been well documented to be involved in diverse aspects of biotic and abiotic stresses, especially detoxification processes. Whether they regulate plant development remains unclear. Here, we report on our isolation by reverse transcription-polymerase chain reaction of a plant GST, AtGSTU17, from Arabidopsis (Arabidopsis thaliana) and demonstrate that its expression is regulated by multiple photoreceptors, especially phytochrome A (phyA) under all light conditions. Further physiological studies indicated that AtGSTU17 participates in various aspects of seedling development, including hypocotyl elongation, anthocyanin accumulation, and far-red light-mediated inhibition of greening with a requirement of functional phyA. The loss-of-function mutant of AtGSTU17 (atgstu17) resulted in reduced biomass of seedlings and number of lateral roots in the presence of auxin, as well as insensitivity to abscisic acid (ABA)-mediated inhibition of root elongation, with similarity to different phyA mutant alleles. Moreover, the root phenotype conferred by atgstu17 was reflected by histochemical b-glucuronidase staining of AtGSTU17 promoter activity with the addition of auxin or ABA. Further microarray analysis of wild-type Columbia and atgstu17 seedlings treated with far-red irradiation or ABA revealed that AtGSTU17 might modulate hypocotyl elongation by positively regulating some light-signaling components and negatively regulating a group of auxin-responsive genes and modulate root development by negatively controlling an auxin transport protein in the presence of ABA. Therefore, our data reveal that AtGSTU17 participates in light signaling and might modulate various aspects of Arabidopsis development by affecting glutathione pools via a coordinated regulation with phyA and phytohormones.
SignificanceLight enhances the translation efficiency of thousands of mRNAs during photomorphogenic development in Arabidopsis, but the underlying molecular mechanism remains elusive. Here we show that light activates the auxin-target of rapamycin (TOR)-ribosome protein S6 (RPS6) pathway to enhance translation in deetiolating Arabidopsis. We discovered that CONSTITUTIVE PHOTOMORPHOGENIC 1 (COP1) represses TOR activity in dark-grown seedlings. The perception of far-red and blue light by photoreceptors inactivates COP1, which leads to the derepression of the auxin-TOR-RPS6 pathway and enhanced de novo protein synthesis. Our study revealed a light-triggered signaling pathway for translational regulation. This sophisticated regulation also functions to ensure that young seedlings have strict skotomorphogenic development in the dark and a timely switch to photomorphogenic development.
Far-red (FR) insensitive 219 (FIN219) was previously shown to be involved in phytochrome A-mediated FR light signaling. To further understand its function and regulatory relation with other light-signaling components, a yeast two-hybrid approach was used to isolate FIN219-interacting partners. Here, we demonstrate that FIN219-interacting protein 1 (FIP1) interacts with FIN219 in vitro and in vivo and is composed of 217 amino acids that belong to the tau class of the large glutathione S-transferase gene family. FIP1 was further shown to have glutathione S-transferase activity. The gain of function and partial loss of function of FIP1 resulted in a hyposensitive hypocotyl phenotype under continuous FR (cFR) light and a delayed flowering phenotype under long-day conditions, which suggests that FIP1 may exist in a complex to function in the regulation of Arabidopsis (Arabidopsis thaliana) development. In addition, FIP1 mRNA was down-regulated in the suppressor of phytochrome A-105 1 mutant and differentially expressed in constitutive photomorphogenic 1-4 (cop1-4) and cop1-5 mutants under cFR. Intriguingly, FIP1 expression was up-regulated in the fin219 mutant under all light conditions, except cFR. Furthermore, promoter activity assays revealed that FIP1 expression was light dependent, mainly associated with vascular tissues, and developmentally regulated. Subcellular localization studies revealed that the b-glucuronidase-FIP1 fusion protein was localized in the nucleus and cytoplasm. Taken together, these data indicate that FIP1 may interact with FIN219 to regulate cell elongation and flowering in response to light.Light has a profound effect on plant growth and development. It not only provides an energy source for plant photosynthesis, but also acts as an important signal to regulate gene expression and various aspects of plant development (Kendrick and Kronenberg, 1994). Plants are equipped with different photoreceptors to sense changes in light. At least four different photoreceptor classes are found in Arabidopsis (Arabidopsis thaliana): phytochromes for red (R) and far-red (FR) light, cryptochromes and phototropins for blue (B) and UV-A light, and an unknown photoreceptor for UV-B light. Phytochromes are the most extensively studied among these photoreceptors and exist in phytochrome R-absorbing (Pr) and phytochrome FR-absorbing (Pfr) forms.Research into light signal transduction by molecular genetics, cell biology, and DNA microarray approaches has made great progress (Tepperman et al
Translation initiation is a key step determining protein synthesis. Studies have uncovered a number of alternative translation initiation sites (TISs) in mammalian mRNAs and showed their roles in reshaping the proteome. However, the extent to which alternative TISs affect gene expression across plants remains largely unclear. Here, by profiling initiating ribosome positions, we globally identified in vivo TISs in tomato and Arabidopsis and found thousands of genes with more than one TIS. Of the identified TISs, >19% and >20% were located at unannotated AUG and non-AUG sites, respectively. CUG and ACG were the most frequently observed codons at non-AUG TISs, a phenomenon also found in mammals. In addition, although alternative TISs were usually found in both orthologous genes, the TIS sequences were not conserved, suggesting the conservation of alternative initiation mechanisms but flexibility in using TISs. Unlike upstream AUG TISs, the presence of upstream non-AUG TISs was not correlated with the translational repression of main open reading frames, a pattern observed across plants. Also, the generation of proteins with diverse N-terminal regions through the use of alternative TISs contributes to differential subcellular localization, as mutating alternative TISs resulted in the loss of organelle localization. Our findings uncovered the hidden coding potential of plant genomes and, importantly, the constraint and flexibility of translational initiation mechanisms in the regulation of gene expression across plant species.
The evolution of transcriptional regulatory mechanisms is central to how stress response and tolerance differ between species. However, it remains largely unknown how divergence in cis-regulatory sites and, subsequently, transcription factor (TF) binding specificity contribute to stress-responsive expression divergence, particularly between wild and domesticated species. By profiling wound-responsive gene transcriptomes in wild Solanum pennellii and domesticated S. lycopersicum, we found extensive wound response divergence and identified 493 S. lycopersicum and 278 S. pennellii putative cis-regulatory elements (pCREs) that were predictive of wound-responsive gene expression. Only 24-52% of these wound response pCREs (depending on wound response patterns) were consistently enriched in the putative promoter regions of wound-responsive genes across species. In addition, between these two species, their differences in pCRE site sequences were significantly and positively correlated with differences in wound-responsive gene expression. Furthermore, ∼11-39% of pCREs were specific to only one of the species and likely bound by TFs from different families. These findings indicate substantial regulatory divergence in these two plant species that diverged ∼3-7 million years ago. Our study provides insights into the mechanistic basis of how the transcriptional response to wounding is regulated and, importantly, the contribution of cis-regulatory components to variation in wound-responsive gene expression between a wild and a domesticated plant species.
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