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bioRxiv2018

An information theoretic treatment of sequence-to-expression modeling

Studying a genes regulatory mechanisms is a tedious process that involves identification of candidate regulators by transcription factor (TF) knockout or over-expression experiments, delineation of enhancers by reporter assays, and demonstration of direct TF influence by site mutagenesis, among other approaches. Such experiments are often chosen based on the biologists intuition, from several testable hypotheses. We pursue the goal of making this process systematic by using ideas from information theory to reason about experiments in gene regulation, in the hope of ultimately enabling rigorous experiment design strategies. For this, we make use of a state-of-the-art mathematical model of gene expression, which provides a way to formalize our current knowledge of cis- as well as trans-regulatory mechanisms of a gene. Ambiguities in such knowledge can be expressed as uncertainties in the model, which we capture formally by building an ensemble of plausible models that fit the existing data and defining a probability distribution over the ensemble. We then characterize the impact of a new experiment on our understanding of the genes regulation based on how the ensemble of plausible models and its probability distribution changes when challenged with results from that experiment. This allows us to assess the value of the experiment retroactively as the reduction in entropy of the distribution (information gain) resulting from the experiments results. We fully formalize this novel approach to reasoning about gene regulation experiments and use it to evaluate a variety of perturbation experiments on two developmental genes of D. melanogaster. We also provide objective and biologist-friendly descriptions of the information gained from each such experiment. The rigorously defined information theoretic approaches presented here can be used in the future to formulate systematic strategies for experiment design pertaining to studies of gene regulatory mechanisms.\n\nAuthor summaryIn-depth studies of gene regulatory mechanisms employ a variety of experimental approaches such as identifying a genes enhancer(s) and testing its variants through reporter assays, followed by transcription factor mis-expression or knockouts, site mutagenesis, etc. The biologist is often faced with the challenging problem of selecting the ideal next experiment to perform so that its results provide novel mechanistic insights, and has to rely on their intuition about what is currently known on the topic and which experiments may add to that knowledge. We seek to make this intuition-based process more systematic, by borrowing ideas from the mature statistical field of experiment design. Towards this goal, we use the language of mathematical models to formally describe what is known about a genes regulatory mechanisms, and how an experiments results enhance that knowledge. We use information theoretic ideas to assign a value to an experiment as well as explain objectively what is learned from that experiment. We demonstrate use of this novel approach on two extensively studied developmental genes in fruitfly. We expect our work to lead to systematic strategies for selecting the most informative experiments in a study of gene regulation.

systems biology↗

bioRxiv2018

Selective auxin agonists induce specific AUX/IAA protein degradation to modulate plant development

Auxin phytohormones control most aspects of plant development through a complex and interconnected signaling network. In the presence of auxin, AUXIN/INDOLE-3-ACETIC ACID (AUX/IAA) transcriptional repressors are targeted for degradation by the SKP1-CULLIN1-F-BOX (SCF) ubiquitin-protein ligases containing TRANSPORT INHIBITOR RESISTANT 1/AUXIN SIGNALING F-BOX (TIR1/AFB). CULLIN1-neddylation is required for SCFTIR1/AFB functionality as exemplified by mutants deficient in the NEDD8-activating enzyme subunit AUXIN-RESISTANT 1 (AXR1). Here, we report a chemical biology screen that identifies small molecules requiring AXR1 to modulate plant development. We selected four molecules of interest, RubNeddin1 to 4 (RN1 to 4), among which RN3 and RN4 trigger selective auxin responses at transcriptional, biochemical and morphological levels. This selective activity is explained by their ability to promote the interaction between TIR1 and a specific subset of AUX/IAA proteins, stimulating the degradation of particular AUX/IAA combinations. Finally, via a genetic screen using RN4, we revealed that the chromatin remodeling ATPase BRAHMA is implicated in auxin-mediated apical hook development. These results demonstrate the power of selective auxin agonists to dissect auxin perception for plant developmental functions.

plant biology↗

bioRxiv2016

A computational method for the investigation of multistable systems and its application to genetic switches

Genetic switches exhibit multistability, form the basis of epigenetic memory, and are found in natural decision making systems, such as cell fate determination in developmental pathways. Synthetic genetic switches can be used for recording the presence of different environmental signals, for changing phenotype using synthetic inputs and as building blocks for higher-level sequential logic circuits. Understanding how multistable switches can be constructed and how they function within larger biological systems is therefore key to synthetic biology. Here we present a new computational tool, called StabilityFinder, that takes advantage of sequential Monte Carlo methods to identify regions of parameter space capable of producing multistable behaviour, while handling uncertainty in biochemical rate constants and initial conditions. The algorithm works by clustering trajectories in phase space, and iteratively minimizing a distance metric. Here we examine a collection of models of genetic switches, ranging from the deterministic Gardner toggle switch to stochastic models containing different positive feedback connections. We uncover the design principles behind making bistable, tristable and quadristable switches, and find that rate of gene expression is a key parameter. We demonstrate the ability of the framework to examine more complex systems and examine the design principles of a three gene switch. Our framework allows us to relax the assumptions that are often used in genetic switch models and we show that more complex abstractions are still capable of multistable behaviour. Our results suggest many ways in which genetic switches can be enhanced and offer designs for the construction of novel switches. Our analysis also highlights subtle changes in correlation of experimentally tunable parameters that can lead to bifurcations in deterministic and stochastic systems. Overall we demonstrate that StabilityFinder will be a valuable tool in the future design and construction of novel gene networks.

synthetic biology↗

bioRxiv2026

Germ granules act as repositories for RNA and protein molecules essential for zebrafish germline development

Germ granules are conserved, phase-separated ribonucleoprotein condensates enriched in germline determinants, yet their precise function remains unclear. Using quantitative live imaging, translational reporters, and targeted disruption of germ granule assembly in zebrafish primordial germ cells, we show that germ granules are dispensable for germ cell fate, migration, and gamete production. Instead, granules act as reservoirs, sequestering transcripts and releasing them gradually for cytoplasmic translation. Under heat stress or translational inhibition, granules further accumulate mRNAs and canonical stress granule factors, indicating a role in buffering RNA and regulatory protein availability rather than serving as sites of localized translation, as previously proposed. Consistent with this reservoir model, cytoplasmic expression of the germline determinants Nanos3 and Dead end is sufficient to direct somatic cells toward a germline fate even in the absence of germ granules. Correspondingly, germ cells lacking granules develop normally but show reduced persistence of germline RNA expression and impaired fertility. Together, these findings establish zebrafish germ granules as protective condensates that safeguard germline determinants and enhance developmental robustness by buffering the timing and rate of RNA translation.

cell biology↗

bioRxiv2016

Potential energy landscapes reveal the information-theoretic nature of the epigenome

Epigenetics is defined as genomic modifications carrying information independent of DNA sequence heritable through cell division. In 1940, Waddington coined the term \"epigenetic landscape\" as a metaphor for pluripotency and differentiation, but epigenetic potential energy landscapes have not yet been rigorously defined. Using well-grounded biological assumptions and principles of statistical physics and information theory, we derive potential energy landscapes from whole genome bisulfite sequencing data that allow us to quantify methylation stochasticity genome-wide and discern epigenetic differences using Shannons entropy and the Jensen-Shannon distance. We discover a \"developmental wheel\" of germ cell lineages and an association between entropy and chromatin structure. Viewing methylation maintenance as a communications system, we introduce methylation channels and show that higher-order chromatin organization can be predicted from their informational properties. Our results provide a fundamental understanding of the information-theoretic nature of the epigenome and a powerful methodology for studying its role in disease and aging.

Genetics↗

bioRxiv2015

Ancient trans-acting siRNAs Confer Robustness and Sensitivity onto the Auxin Response

Novel developmental programs often evolve via cooption of existing genetic networks. To understand this process, we explored cooption of the TAS3 tasiRNA pathway in the moss Physcomitrella patens. We find an ancestral function for this repeatedly redeployed pathway in the spatial regulation of a conserved set of Auxin Response Factors. In moss, this results in stochastic patterning of the filamentous protonemal tissue. Through modeling and experimentation, we demonstrate that tasiRNA regulation confers sensitivity and robustness onto the auxin response. Increased auxin sensitivity parallels increased developmental sensitivity to nitrogen, a key environmental signal. We propose that the properties lent to the auxin response network, along with the ability to stochastically modulate development in response to environmental cues, have contributed to the tasiRNA-ARF modules repeated cooption during evolution. The signaling properties of a genetic network, and not just its developmental output, are thus critical to understanding the evolution of multicellular forms.

Plant Biology↗

bioRxiv2016

A Re-examination of the Role of AUXIN RESPONSE FACTOR 8 in Developmental Abnormalities Caused by the P1/HC-Pro Viral Suppressor of RNA Silencing

Plant viral suppressors of RNA silencing induce developmental defects similar to those caused by mutations in genes involved in the microRNA (miRNA) pathway. These abnormalities were originally thought to reflect a pleiotropic impact of silencing suppressors on miRNA control of plant development. However, subsequent work with the P1/HC-Pro potyviral suppressor of silencing showed that global impairment of the miRNA pathway was not responsible for the phenotypical anomalies. More recently, developmental defects caused by a P1/HC-Pro transgene under control of the 35S promoter were attributed to moderate upregulation of AUXIN RESPONSE FACTOR 8 (ARF8), a target of miR167. The key piece of evidence in that work was that the developmental defects in the 35S-pro:P1/HC-Pro transgenic Arabidopsis were greatly alleviated in the F1 progeny of a cross with plants carrying the arf8-6 mutation. Arf8-6 is a SALK line T-DNA insertion mutant, a class of mutations prone to inducing transcriptional silencing of transgenes expressed from the 35S promoter. Here we report a re-investigation of the role of ARF8 in P1/HC-Pro-mediated developmental defects. We characterized the progeny of a cross between our 35S-pro:P1/HC-Pro transgenic Arabidopsis line and the same arf8-6 T-DNA insertion mutant used in the earlier study. The T-DNA mutation had little effect in the F1 generation, but almost all arf8-6/P1/HC-Pro progeny had lost the P1/HC-Pro phenotype in the F2 generation. However, this loss of phenotype was not correlated with the number of functional copies of the ARF8 gene. Instead, it reflected transcriptional silencing of the 35S-pro:P1/HC-Pro transgene, as evidenced by a pronounced decrease in P1/HC-Pro mRNA2accompanied by the appearance of 35S promoter siRNAs. Furthermore, arf8-8, an independent loss-of-function point mutation, had no detectable effects on P1/HC-Pro phenotype in either the F1 or F2 generations. Together these data argue against the reported role of increased ARF8 expression in mediating developmental defects in P1/HC-Pro transgenic plants.\n\nAuthor SummaryRNA silencing is an important antiviral defense in plants that uses small RNA molecules to target the invading RNA. Plant viruses, however, have countered with proteins that suppress RNA silencing, and one of the best-studied plant viral suppressors of silencing is P1/HC-Pro. When the genetic model plant Arabidopsis thaliana is bioengineered to express P1/HC-Pro, the resulting plants display distinct developmental abnormalities. These abnormalities are thought to arise because P1/HC-Pro also interferes with the arm of RNA silencing that uses small RNAs called microRNAs (miRNAs) to regulate expression of the plant's own genes. Earlier work, however, showed that interference with all miRNAs in general could not be responsible for these developmental defects. More recently, it was reported that enhanced expression of a single miRNA-controlled gene, AUXIN RESPONSE FACTOR 8 (ARF8), underlies the developmental defects caused by P1/HC-Pro. However, using the same ARF8 mutation as that report, as well as a second, independent ARF8 loss-of function mutation, we now show that mis-regulation of ARF8 is not responsible for those defects. One or a few key miRNA-controlled factors might, in fact, underlie the developmental defects caused by P1/HC-Pro; however, our results show that ARF8 is not one of the key factors.

Plant Biology↗

bioRxiv2017

Autogenous Cross-Regulation Of Quaking mRNA Processing And Translation Balances Quaking Functions In Splicing And Translation

Quaking RNA binding protein (RBP) isoforms arise from a single Quaking gene, and bind the same RNA motif to regulate splicing, stability, decay, and localization of a large set of RNAs. However, the mechanisms by which the expression of this single gene is controlled to distribute appropriate amounts of each Quaking isoform to regulate such disparate gene expression processes are unknown. Here we explore the separate mechanisms that regulate expression of two isoforms, Quaking-5 (Qk5) and Quaking-6 (Qk6), in mouse muscle cells. We first demonstrate that Qk5 and Qk6 proteins have distinct functions in splicing and translation respectively, enforced primarily through differential subcellular localization. Using isoform-specific depletion, we find both Qk5 and Qk6 act through cis and trans post-transcriptional regulatory mechanisms on their own and each others transcripts, creating a network of auto- and cross-regulatory controls. Qk5 has a major role in nuclear RNA stability and splicing, whereas Qk6 acts through translational regulation. In different cell types the cross-regulatory influences discovered here generate a spectrum of Qk5/Qk6 ratios subject to additional cell type and developmental controls. These unexpectedly complex feedback loops underscore the importance of the balance of Qk isoforms, especially where they are key regulators of development and cancer.

molecular biology↗

bioRxiv2015

Dis-integrating the fly: A mutational perspective on phenotypic integration and covariation

The structure of environmentally induced phenotypic covariation can influence the effective strength and magnitude of natural selection. Yet our understanding of the factors that contribute to and influence the evolutionary lability of such covariation is poor. Most studies have either examined environmental variation without accounting for covariation, or examined phenotypic and genetic covariation without distinguishing the environmental component. In this study we examined the effect of mutational perturbations on different properties of environmental covariation, as well as mean shape. We use strains of Drosophila melanogaster bearing well-characterized mutations known to influence wing shape, as well as naturally-derived strains, all reared under carefully-controlled conditions and with the same genetic background. We find that mean shape changes more freely than the covariance structure, and that different properties of the covariance matrix change independently from each other. The perturbations affect matrix orientation more than they affect matrix eccentricity or total variance. Yet, mutational effects on matrix orientation do not cluster according to the developmental pathway that they target. These results suggest that it might be useful to consider a more general concept of decanalization, involving all aspects of variation and covariation.

Evolutionary Biology↗

bioRxiv2017

Large-scale determination and characterization of cell type-specific regulatory elements in the human genome

Histone modifications have been widely elucidated to play vital roles in gene regulation and cell identity. The Roadmap Epigenomics Consortium generated a reference catalogue of several key histone modifications across >100s of human cell types and tissues. Decoding these epigenomes into functional regulatory elements is a challenging task in computational biology. To this end, we adopted a differential chromatin modification analysis framework to comprehensively determine and characterize cell type-specific regulatory elements (CSREs) and their histone modification codes in the human epigenomes of five histone modifications across 127 tissues or cell types. The CSREs show significant relevance with cell type-specific biological functions and diseases and cell identity. Clustering of CSREs with their specificity signals reveals diverse histone codes, demonstrating the diversity of functional roles of CSREs within the same cell or tissue. Last but not least, dynamics of CSREs from close cell types or tissues can give a detailed view of developmental processes such as normal tissue development and cancer occurrence.

bioinformatics↗

bioRxiv2018

Beating Swords into Ploughshares: Domestication of a Phage Lysin for Housekeeping Function

Temperate phages constitute a potentially beneficial genetic reservoir for bacterial innovation despite being selfish entities encoding an infection cycle inherently at odds with bacterial fitness. These phages integrate their genomes into the bacterial host during infection, donating new, but deleterious, genetic material: the phage genome encodes toxic genes, such as lysins, that kill the bacterium during the phage infection cycle. Remarkably, some bacteria have exploited the destructive properties of phage genes for their own benefit by co-opting them as toxins for functions related to bacterial warfare, virulence, and secretion. However, do toxic phage genes ever become raw material for functional innovation? Here we report on a toxic phage gene whose product has lost its toxicity and has become a domain of a core cellular factor, SpmX, throughout the bacterial order Caulobacterales. Using a combination of phylogenetics, bioinformatics, structural biology, cell biology, and biochemistry, we have investigated the origin and function of SpmX and determined that its occurrence is the result of the detoxification of a phage peptidoglycan hydrolase gene. We show that the retained, attenuated activity of the phage-derived domain plays an important role in proper cell morphology and developmental regulation in representatives of this large bacterial clade. To our knowledge, this is the first observation of phage gene domestication in which a toxic phage gene has been co-opted for a housekeeping function.

microbiology↗

bioRxiv2018

Nucleo-cytoplasmic trafficking regulates nuclear surface area during nuclear organogenesis

Throughout development, nuclei must be assembled following every cell division to establish a functional organelle from compact, mitotic chromatin. During nuclear organogenesis, chromatin expands to establish a nucleus of a given size seperate from the cytoplasm. Determining how nuclear organogenesis is regulated is particularly significant in the context of certain cancers in which scaling relationships between cell and nuclear sizes are not maintained. Controlling cell size in vitro using a microfluidics approach, we determined that neither nuclear volume nor surface area scale directly with cell size. Looking to explain differential nuclear scaling relationships, we developed a simple mechano-chemical mathematical model. In simulating biological perturbations in silico, our model predicted crucial roles for nucleo-cytoplasmic trafficking in regulating nuclear expansion and in restricting the recruitment of a potential nuclear surface area factor. In mammalian tissue culture, inhibiting nuclear export increased nuclear expansion rates and reduced the amount of nuclear lamin, a candidate surface area factor, being recruited to assembling nuclei, supporting our models predictions. Targeting the principal nuclear export component in the Drosophila syncytial embryo, Embargoed, we show that nuclear expansion rates are also increased in this developmental context, consistent with our model. Using the MS2-reporter system in fly embryos, we demonstrate a role for nuclear export in regulating transcription activation timing and dynamics, suggesting that regulating nuclear assembly is crucial for downstream nuclear function. Taken together, we propose a simple model through which nuclear organogenesis is achieved and demonstrate a role for nuclear export in regulating nuclear assembly.

cell biology↗

bioRxiv2015

Feedback Control in Planarian Stem Cell Systems

Background In planarian flatworms, the mechanisms underlying the activity of collectively pluripotent adult stem cells (neoblasts) and their descendants can now be studied from the level of the individual gene to the entire animal. Flatworms maintain startling developmental plasticity and regenerative capacity in response to variable nutrient conditions or injury. We develop a model for cell dynamics in such animals, using methods of nonlinear dynamics, assuming that fully differentiated cells exert feedback control on neoblast activity. Results Our model predicts a number of whole organism level and general cell biological and behaviours, some of which have been empirically observed or inferred in planarians and others that have not. As previously observed empirically we find: 1) a curvilinear relationship between external food and planarian steady state size; 2) the fraction of neoblasts in the steady state is constant regardless of planarian size; 3) a burst of controlled apoptosis during regeneration after amputation as the number of differentiated cells are adjusted towards their correct homeostatic/steady state level. In addition our model describes the following properties that can inform and be tested by future experiments: 4) the strength of feedback control from differentiated cells to neoblasts (i.e. the activity of the signalling system) and from neoblasts on themselves in relation to absolute number depends upon the level of food in the environment; 5) planarians adjust size when food level reduces initially through increased apoptosis and then through a reduction in neoblast self-renewal activity; 6) following wounding or excision of differentiated cells, different time scales characterize both recovery of size and the two feedback functions; 7) the temporal pattern of feedback controls differs noticeably during recovery from a removal or neoblasts or a removal of differentiated cells; and 8) the signaling strength for apoptosis of differentiated cells depends upon both the absolute and relative deviations of the number of differentiated cells from their homeostatic level.\n\nConclusions We offer the first analytical framework for organizing experiments on planarian flatworm stem cell dynamics in a form that allows models to be compared with quantitative cell data based on underlying molecular mechanisms and thus facilitates the interplay between empirical studies and modeling. This framework is the foundation for studying cell migration during wound repair, the determination of homeostatic levels of differentiated cells by natural selection, and stochastic effects.

Systems Biology↗

bioRxiv2013

DCL1, a Protein that Produces Plant MicroRNA, Coordinates Meristem Activity

Abstract Abstract Introduction Results Discussion Materials and Methods Authors' contributions Funding References The ubiquity and importance of short duplex RNAs, termed microRNA (miRNA), for normal development in higher eukaryotes are becoming increasingly clear. We had previously shown that reduction-of-function mutations in Arabidopsis thaliana DCL1 (DICER-LIKE1) gene, affecting the nucleus-localized protein that produces 19-25 nucleotides long miRNA species from longer double stranded RNA precursors, cause a delay in flowering by prolonging the period of juvenile organ development. Here we show that DCL1 transcription is increased at the critical phase of juvenile to reproductive developmental transition, and that DCL1 protein is localized in meri ...

Plant Biology↗

bioRxiv2015

Latent developmental and evolutionary shapes embedded within the grapevine leaf

O_LIAcross plants, leaves exhibit profound diversity in shape. As a single leaf expands, its shape is in constant flux. Plants may also produce leaves with different shapes at successive nodes. Additionally, leaf shape varies among individuals, populations, and species due to evolutionary processes and environmental influences.\nC_LIO_LIBecause leaf shape can vary in many different ways, theoretically the effects of distinct developmental and evolutionary processes are separable, even within the shape of a single leaf. Here, we measure the shapes of >3,200 leaves representing >270 vines from wild relatives of domesticated grape (Vitis spp.) to determine if leaf shapes attributable to genetics and development are separable from each other.\nC_LIO_LIWe isolate latent shapes (multivariate signatures that vary independently from each other) embedded within the overall shape of leaves. These latent shapes can predict developmental stages independent from species identity and vice versa. Shapes predictive of development are then used to stage leaves from 1,200 varieties of domesticated grape (Vitis vinifera), revealing that changes in timing underlie leaf shape diversity.\nC_LIO_LIOur results indicate distinct latent shapes combine to produce a composite morphology in leaves, and that developmental and evolutionary contributions to shape vary independently from each other.\nC_LI

Plant Biology↗

bioRxiv2018

Continuous visualization of differences between biological conditions in single-cell data

In high-dimensional single cell data, comparing changes in functional markers between conditions is typically done across manual or algorithm-derived partitions based on population-defining markers. Visualizations of these partitions is commonly done on low-dimensional embeddings (eg. t-SNE), colored by per-partition changes. Here, we provide an analysis and visualization tool that performs these comparisons across overlapping k-nearest neighbor (KNN) groupings. This allows one to color low-dimensional embeddings by marker changes without hard boundaries imposed by partitioning. We devised an objective optimization of k based on minimizing functional marker KNN imputation error. Proof-of-concept work visualized the exact location of an IL-7 responsive subset in a B cell developmental trajectory on a t-SNE map independent of clustering. Per-condition cell frequency analysis revealed that KNN is sensitive to detecting artifacts due to marker shift, and therefore can also be valuable in a quality control pipeline. Overall, we found that KNN groupings lead to useful multiple condition visualizations and efficiently extract a large amount of information from mass cytometry data. Our software is publicly available through the Bioconductor package Sconify.

systems biology↗

bioRxiv2017

Base composition, speciation, and why the mitochondrial barcode precisely classifies

While its mechanism and biological significance are unknown, the utility of a short mitochondrial DNA sequence as a \"barcode\" providing accurate species identification has revolutionized the classification of organisms. Since highest accuracy was achieved with recently diverged species, hopes were raised that barcodes would throw light on the speciation process. Indeed, a failure of a maternally-donated, rapidly mutating, mitochondrial genome to coadapt its gene products with those of a paternally-donated nuclear genome could result in developmental failure, thus creating a post-zygotic barrier leading to reproductive isolation and sympatric branching into independent species. However, the barcode itself encodes a highly conserved, species-invariant, protein, and the discriminatory power resides in the non-amino acid specific bases of synonymous codons. It is here shown how the latter could register changes in the oligonucleotide frequencies of nuclear DNA that, when they fail to match in pairing meiotic chromosomes, could reproductively isolate the parents (whose hybrid is sterile) so launching a primary divergence into two species. It is proposed that, while not itself contributing to speciation, the barcode sequence provides an index of the nuclear DNA oligonucleotide frequencies that drive speciation.

evolutionary biology↗

bioRxiv2017

Plant miRNA Regulation Is Environmentally And Developmentally-Sensitive

Development and fitness of any organism rely on properly controlled gene expression. This is especially true for plants, as their development is determined by both internal and external cues. MicroRNAs (miRNAs) are embedded in the genetic cascades that integrate and translate those cues into developmental programs. miRNAs negatively regulate their target genes mainly post-transcriptionally through two co-existing mechanisms; mRNA cleavage and translational inhibition. It is unclear whether the efficiency of miRNA-guided regulation is generally influenced by factors like ambient temperature or developmental stage. Here we show that plant miRNA accumulation, as well as miRNAs mode of action can be temperature- and development-sensitive. Higher temperatures tend to induce a more pronounced accumulation of mature miRNAs. Both parameters have also an impact on the expression patterns of the core players involved in miRNA performance. We show that efficiency of miRNA-mediated gene silencing declines with age during vegetative development in a temperature-dependent manner. Co-existence of cleavage and translational inhibition was also found to be dependent on temperature and developmental stage. Therefore, each miRNA family specifically regulates their respective targets, while temperature and growth influence the performance of miRNA-dependent regulation in a more general way.

plant biology↗