scholarly journals Direct molecular evidence for an ancient, conserved developmental toolkit controlling post-transcriptional gene regulation in land plants

2021 ◽  
Author(s):  
Haiyan Jia ◽  
Kelsey Aadland ◽  
Oralia Kolaczkowski ◽  
Bryan Kolaczkowski

ABSTRACTRNA interference (RNAi) plays important roles in organism development through post-transcriptional regulation of specific target mRNAs. Target specificity is largely controlled by base-pair complementarity between micro-RNA (miRNA) regulatory elements and short regions of the target mRNA. The pattern of miRNA production in a cell interacts with the cell’s mRNA transcriptome to generate a specific network of post-transcriptional regulation that can play critical roles in cellular metabolism, differentiation, tissue/organ development and developmental timing. In plants, miRNA production is orchestrated in the nucleus by a suite of proteins that control transcription of the pri-miRNA gene, post-transcriptional processing and nuclear export of the mature miRNA. In the model plant, Arabidopsis thaliana, post-transcriptional processing of miRNAs is controlled by a pair of physically-interacting proteins, HYL1 and DCL1. However, the evolutionary history of the HYL1-DCL1 interaction is unknown, as is its structural basis. Here we use ancestral sequence reconstruction and functional characterization of ancestral HYL1 in vitro and in vivo to better understand the origin and evolution of the HYL1-DCL1 interaction and its impact on miRNA production and plant development. We found the ancestral plant HYL1 evolved high affinity for both double-stranded RNA (dsRNA) and its DCL1 partner very early in plant evolutionary history, before the divergence of mosses from seed plants (~500 Ma), and these high-affinity interactions remained largely conserved throughout plant evolutionary history. Structural modeling and molecular binding experiments suggest that the second of two double-stranded RNA-binding motifs (DSRMs) in HYL1 may interact tightly with the first of two C-terminal DCL1 DSRMs to mediate the HYL1-DCL1 physical interaction necessary for efficient miRNA production. Transgenic expression of the nearly 200 Ma-old ancestral flowering-plant HYL1 in A. thaliana was sufficient to rescue many key aspects of plant development disrupted by HYL1− knockout and restored near-native miRNA production, suggesting that the functional partnership of HYL1-DCL1 originated very early in and was strongly conserved throughout the evolutionary history of terrestrial plants. Overall, our results are consistent with a model in which miRNA-based gene regulation evolved as part of a conserved plant ‘developmental toolkit’; its role in generating developmental novelty is probably related to the relatively rapid evolution of miRNA genes.

Author(s):  
Xiang Yu ◽  
Bishwas Sharma ◽  
Brian D Gregory

Abstract Ribonucleotides within the various RNA molecules in eukaryotes are marked with more than 160 distinct covalent chemical modifications. These modifications include those that occur internally in messenger RNA (mRNA) molecules such as N6-methyladenosine (m6A) and 5-methylcytosine (m5C), as well as those that occur at the ends of the modified RNAs like the non-canonical 5′ end nicotinamide adenine dinucleotide (NAD+) cap modification of specific mRNAs. Recent findings have revealed that covalent RNA modifications can impact the secondary structure, translatability, functionality, stability and degradation of the RNA molecules in which they are included. Many of these covalent RNA additions have also been found to be dynamically added and removed through writer and eraser complexes, respectively, providing a new layer of epitranscriptome-mediated post-transcriptional regulation that regulates RNA quality and quantity in eukaryotic transcriptomes. Thus, it is not surprising that the regulation of RNA fate mediated by these epitranscriptomic marks has been demonstrated to have widespread effects on plant development and the responses of these organisms to abiotic and biotic stresses. In this review, we highlight recent progress focused on the study of the dynamic nature of these epitranscriptome marks and their roles in post-transcriptional regulation during plant development and response to environmental cues, with an emphasis on the mRNA modifications of non-canonical 5′ end NAD+ capping, m6A and several other internal RNA modifications.


FEBS Journal ◽  
2008 ◽  
Vol 275 (10) ◽  
pp. 2364-2371 ◽  
Author(s):  
Maria C. Palumbo ◽  
Lorenzo Farina ◽  
Alberto De Santis ◽  
Alessandro Giuliani ◽  
Alfredo Colosimo ◽  
...  

2019 ◽  
Author(s):  
Martin Silvert ◽  
Lluis Quintana-Murci ◽  
Maxime Rotival

AbstractArchaic admixture is increasingly recognized as an important source of diversity in modern humans, with Neanderthal haplotypes covering 1-3% of the genome of present-day Eurasians. Recent work has shown that archaic introgression has contributed to human phenotypic diversity, mostly through the regulation of gene expression. Yet, the mechanisms through which archaic variants alter gene expression, and the forces driving the introgression landscape at regulatory regions remain elusive. Here, we explored the impact of archaic introgression on transcriptional and post-transcriptional regulation, focusing on promoters and enhancers across 127 different tissues as well as microRNA-mediated regulation. Although miRNAs themselves harbor few archaic variants, we found that some of these variants may have a strong impact on miRNA-mediated gene regulation. Enhancers were by far the regulatory elements most affected by archaic introgression, with one third of the tissues tested presenting significant enrichments. Specifically, we found strong enrichments of archaic variants in adipose-related tissues and primary T cells, even after accounting for various genomic and evolutionary confounders such as recombination rate and background selection. Interestingly, we identified signatures of adaptive introgression at enhancers of some key regulators of adipogenesis, raising the interesting hypothesis of a possible adaptation of early Eurasians to colder climates. Collectively, this study sheds new light onto the mechanisms through which archaic admixture have impacted gene regulation in Eurasians and, more generally, increases our understanding of the contribution of Neanderthals to the regulation of acquired immunity and adipose homeostasis in modern humans.


2020 ◽  
Author(s):  
Anieli Cristina Maraschi ◽  
Samuel Coelho Faria ◽  
John Campbell McNamara

ABSTRACTPalaemonid shrimps include species from distinct osmotic niches that hyper-regulate hemolymph osmolality and ionic concentrations in dilute media but hypo-regulate in saline media. Their gill epithelia express ion transporters like the Na+-K+-2Cl- symporter (NKCC) thought to play a role in salt secretion. Using a palaemonid series from niches including marine tide pools through estuaries (Palaemon) to coastal and continental fresh waters (Macrobrachium), we established their critical upper salinity limits (UL50) and examined their short-(24 h) and long-term (120 h) hypo-regulatory abilities at salinities corresponding to 80% of the UL50’s (80%UL50). We tested for phylogenetic correlations between gill NKCC gene and protein expression and hemolymph Cl- hypo-regulatory capability, and evaluated whether niche salinity might have driven gill NKCC expression. The Palaemon species from saline habitats showed the highest UL50’s and greatest hypo-regulatory capabilities compared to the Macrobrachium species among which UL50’s were higher in the diadromous than in the hololimnetic species. While basal gill NKCC mRNA transcription rates differed among species, expressions were unaffected by exposure time or salinity, suggesting post-transcriptional regulation of protein synthesis. Unexpectedly, hemolymph Cl-hyper-regulatory capability correlated with gill NKCC gene expression, while gill NKCC protein synthesis was associated with hyper-regulation of hemolymph osmolality at the 80%UL50’s of almost all Macrobrachium species, suggesting a role for the gill NKCC symporter in salt uptake. The evolutionary history of osmoregulation in these palaemonid shrimps suggests that, while some molecular and systemic mechanisms have accompanied cladogenetic events during radiation into different osmotic niches, others may be driven by salinity.


2016 ◽  
Vol 91 (1-2) ◽  
pp. 131-147 ◽  
Author(s):  
Marion Clavel ◽  
Thierry Pélissier ◽  
Thomas Montavon ◽  
Marie-Aude Tschopp ◽  
Marie-Noëlle Pouch-Pélissier ◽  
...  

2021 ◽  
Author(s):  
Zi-Yue Wang ◽  
Dong-ling Li ◽  
Xiaorui Tian ◽  
Chun-yang Zhang

MicroRNAs (miRNAs) play key roles in the post-transcriptional regulation of genes, and their aberrant expression may disturb the normal gene regulation network to induce various diseases, and thus accurate detection...


2020 ◽  
Vol 70 (1) ◽  
pp. 162-180
Author(s):  
Jeffrey P Rose ◽  
Cassio A P Toledo ◽  
Emily Moriarty Lemmon ◽  
Alan R Lemmon ◽  
Kenneth J Sytsma

Abstract Phylogenomic data from a rapidly increasing number of studies provide new evidence for resolving relationships in recently radiated clades, but they also pose new challenges for inferring evolutionary histories. Most existing methods for reconstructing phylogenetic hypotheses rely solely on algorithms that only consider incomplete lineage sorting (ILS) as a cause of intra- or intergenomic discordance. Here, we utilize a variety of methods, including those to infer phylogenetic networks, to account for both ILS and introgression as a cause for nuclear and cytoplasmic-nuclear discordance using phylogenomic data from the recently radiated flowering plant genus Polemonium (Polemoniaceae), an ecologically diverse genus in Western North America with known and suspected gene flow between species. We find evidence for widespread discordance among nuclear loci that can be explained by both ILS and reticulate evolution in the evolutionary history of Polemonium. Furthermore, the histories of organellar genomes show strong discordance with the inferred species tree from the nuclear genome. Discordance between the nuclear and plastid genome is not completely explained by ILS, and only one case of discordance is explained by detected introgression events. Our results suggest that multiple processes have been involved in the evolutionary history of Polemonium and that the plastid genome does not accurately reflect species relationships. We discuss several potential causes for this cytoplasmic-nuclear discordance, which emerging evidence suggests is more widespread across the Tree of Life than previously thought. [Cyto-nuclear discordance, genomic discordance, phylogenetic networks, plastid capture, Polemoniaceae, Polemonium, reticulations.]


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