David Jordan

University of Cambridge

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Eric A. Miska

Wellcome/Cancer Research UK Gurdon Institute

Isabela Cunha Navarro

University of Cambridge

Alper Akay

University of East Anglia

Greg J. Stephens

Vrije Universiteit Amsterdam

Chris P. Ponting

MRC Institute of Genetics and Molecular Medicine

Tosif Ahamed

Mount Sinai Hospital

Wilfried Haerty

Earlham Institute

Tomasz Wrzesiński

Earlham Institute

Antonio Carlos Costa

Vrije Universiteit Amsterdam

Fabian Braukmann

University of Cambridge

Cooperative Institutions

University of Cambridge

University of Nebraska–Lincoln

Wellcome/Cancer Research UK Gurdon Institute

Wellcome Trust

University of Queensland

University of Pennsylvania

Medical Research Council

Agriculture and Food

Department of Agriculture, Fisheries and Forestry

Rockefeller University

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Behavioral diversity in microbes and low-dimensional phenotypic spaces

Proceedings of the National Academy of Sciences (2013)

David Jordan Seppe Kuehn Eleni Katifori Stanislas Leibler

Systematic studies of phenotypic diversity—required for understanding evolution—lag behind investigations of genetic diversity. Here we develop a quantitative approach to studying behavioral diversity, which we apply to swimming of the ciliate Tetrahymena. We measure the full-lifetime behavior of hundreds of individual organisms at high temporal resolution, over several generations and in diverse nutrient conditions. To characterize population diversity and temporal variability we introduce a unique statistical framework grounded in the notion of a phenotypic space of behaviors. We show that this space is effectively low dimensional with dimensions that correlate with a two-state “roaming and dwelling” model of swimming behavior. Temporal variability over the lifetime of an individual is correlated with the fraction of time spent roaming whereas diversity between individuals is correlated with the speed of roaming. Quantifying the dynamics of behavioral variation shows that behavior over the lifetime of an individual is strongly nonstationary. Analysis of behavioral dynamics between generations reveals complex patterns of behavioral heritability that point to the importance of considering correlations beyond mothers and daughters. Our description of a low-dimensional behavioral space should enable the systematic study of the evolutionary and ecological bases of phenotypic constraints. Future experimental and theoretical studies of behavioral diversity will have to account for the possibility of nonstationary and environmentally dependent behavioral dynamics that we observe.

Roaming

Dynamics

Variation (astronomy)

Evolutionary Dynamics

10.1073/pnas.1308282110

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Citations (62)

The Orsay Virus as a model for population-wide viral infection dynamics

bioRxiv (Cold Spring Harbor Laboratory) (2021)

Laurence Pirenne Maximilian AH Jakobs David Jordan Kristian Franze Eric A. Miska

Abstract To this day, epidemics pose a considerable threat to mankind. Experimental models that simulate the spread of infectious diseases are thus crucial to the inception of effective control policies. Current models have had great success incorporating virulence and host immune response but do rarely take host genetics, behavior and host environment into account. Here, we present a full-scale imaging setup that utilizes the infection of the nematode C. elegans with a positive-stranded RNA virus (Orsay Virus) to probe key epidemiological parameters and simulate the spread of infection in a whole population. We demonstrate that our system is able to quantify infection levels and host behavior at a high sampling rate and show that different host genetic backgrounds can influence viral spread, while also highlighting the influence of infection on various host behaviors. Future work will allow the isolation of key behavioral and environmental factors that affect viral spread, potentially enabling novel policies to combat the spread of viral infections. Significance Statement In the ongoing COVID-19 pandemic, we struggle to find effective control policies that “stop the spread”. While current animal models of virus spread in populations are highly sophisticated, they rarely explore effects of host behavior and its environment. We developed an experimental animal model system that allows us to visualize virus transmission in whole populations of C. elegans while also measuring behaviors. We were able to demonstrate how C. elegans genetics influences the progression of viral infection in a population and how animals adjust their behavior when infected. In the future, we envision that animal model systems like ours are used to test the effects of viral control policies on viral spread before they are applied in real world scenarios.

RNA virus

10.1101/2021.03.02.433572

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Citations (1)

Canalisation and plasticity on the developmental manifold of Caenorhabditis elegans

Molecular Systems Biology (2023)

David Jordan Eric A. Miska

Abstract How do the same mechanisms that faithfully regenerate complex developmental programmes in spite of environmental and genetic perturbations also allow responsiveness to environmental signals, adaptation and genetic evolution? Using the nematode Caenorhabditis elegans as a model, we explore the phenotypic space of growth and development in various genetic and environmental contexts. Our data are growth curves and developmental parameters obtained by automated microscopy. Using these, we show that among the traits that make up the developmental space, correlations within a particular context are predictive of correlations among different contexts. Furthermore, we find that the developmental variability of this animal can be captured on a relatively low‐dimensional phenotypic manifold and that on this manifold, genetic and environmental contributions to plasticity can be deconvolved independently. Our perspective offers a new way of understanding the relationship between robustness and flexibility in complex systems, suggesting that projection and concentration of dimension can naturally align these forces as complementary rather than competing.

Robustness

Developmental plasticity

Evolutionary developmental biology

Caenorhabditis

10.15252/msb.202311835

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Citations (4)

Translational adaptation to heat stress is mediated by 5-methylcytosine RNA modification inCaenorhabditis elegans

bioRxiv (Cold Spring Harbor Laboratory) (2020)

Isabela Cunha Navarro Francesca Tuorto David Jordan Carine Legrand Jonathan Price

ABSTRACT Methylation of carbon-5 of cytosines (m 5 C) is a post-transcriptional nucleotide modification of RNA found in all kingdoms of life. While individual m 5 C-methyltransferases have been studied, the impact of the global cytosine-5 methylome on development, homeostasis and stress remains unknown. Here, using Caenorhabditis elegans , we generated the first organism devoid of m 5 C in RNA, demonstrating that this modification is non-essential. We determined the localisation and enzymatic specificity of m 5 C sites in RNA in vivo and showed that animals devoid of m 5 C are sensitive to temperature stress. At the molecular level, we showed that loss of m 5 C specifically impacts decoding of leucine and proline thus reducing the translation efficiency of transcripts enriched in these amino acids. Finally, we found translation of leucine UUG codons to be the most strongly affected upon heat shock, suggesting a role of m 5 C tRNA wobble methylation in the adaptation to heat stress.

5-Methylcytosine

Cytosine

Wobble base pair

10.1101/2020.03.21.001735

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Genetic diversity of C4 photosynthesis pathway genes in Sorghum bicolor (L.)

Research Square (Research Square) (2019)

Yongfu Tao Barbara George‐Jaeggli Marie Bouteillé-Pallas Shuaishuai Tai Alan Cruickshank

Abstract Background C4 photosynthesis has evolved in over 60 different plant taxa and is an excellent example of convergent evolution. Plants using the C4 photosynthetic pathway have an efficiency advantage, particularly in hot and dry environments. They account for 23% of global primary production and include some of our most productive cereals. While previous genetic studies comparing phylogenetically related C3 and C4 species have elucidated the genetic diversity underpinning the C4 photosynthetic pathway, no previous studies have described the genetic diversity of the genes involved in this pathway within a C4 crop species. Enhanced understanding of the allelic diversity and selection signatures of genes in this pathway may present opportunities to improve photosynthetic efficiency, and ultimately yield, by exploiting natural variation. Results Here, we present the first genetic diversity survey of 8 known C4 gene families in an important C4 crop, Sorghum bicolor (L.) Moench using sequence data of 48 genotypes covering wild and domesticated sorghum accessions. Average nucleotide diversity of C4 gene families varied more than 20-fold from the NADP-MDH gene family (θπ =0.2×10-3) to the PPDK gene family (θπ = 5.21×10-3). Genetic diversity of C4 genes was reduced by 22.43% in cultivated sorghum compared to wild and weedy sorghum, indicating that the group of wild and weedy sorghum may constitute an untapped reservoir for alleles related to the C4 photosynthetic pathway. A SNP-level analysis identified purifying selection signals on C4 PPDK and CA genes, and balancing selection signals on C4 PPDK-RP and PEPC genes. Allelic distribution of these C4 genes was consistent with selection signals detected.Conclusions Domestication of sorghum has reshaped diversity of C4 pathway. A better understanding of the genetic diversity of this pathway in sorghum paves the way for mining the natural allelic variation for the improvement of photosynthesis.

Nucleotide diversity

10.21203/rs.2.15980/v1

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Canalisation and plasticity on the developmental manifold ofCaenorhabditis elegans

bioRxiv (Cold Spring Harbor Laboratory) (2023)

David Jordan Eric A. Miska

How do the same mechanisms that faithfully regenerate complex developmental programs in spite of environmental and genetic perturbations also permit responsiveness to environmental signals, adaptation, and genetic evolution? Using the nematode Caenorhabditis elegans as a model, we explore the phenotypic space of growth and development in various genetic and environmental contexts. Our data are growth curves and developmental parameters obtained by automated microscopy. Using these, we show that among the traits that make up the developmental space, correlations within a particular context are predictive of correlations among different contexts. Further we find that the developmental variability of this animal can be captured on a relatively low dimensional phenoptypic manifold and that on this manifold, genetic and environmental contributions to plasticity can be deconvolved independently. Our perspective offers a new way of understanding the relationship between robustness and flexibility in complex systems, suggesting that projection and concentration of dimension can naturally align these forces as complementary rather than competing.

Robustness

Developmental plasticity

10.1101/2023.04.14.536891

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Citations (2)

SID-2 negatively regulates development likely independent of nutritional dsRNA uptake

RNA Biology (2020)

Fabian Braukmann David Jordan Benjamin H. Jenkins Albert Koulman Eric A. Miska

RNA interference (RNAi) is a gene regulatory mechanism based on RNA-RNA interaction conserved through eukaryotes. Surprisingly, many animals can take-up human-made double stranded RNA (dsRNA) from the environment to initiate RNAi suggesting a mechanism for dsRNA-based information exchange between organisms and their environment. However, no naturally occurring example has been identified since the discovery of the phenomenon 22 years ago. Therefore it remains enigmatic why animals are able to take up dsRNA. Here, we explore other possible functions by performing phenotypic studies of dsRNA uptake deficient sid-2 mutants in Caenorhabditis elegans. We find that SID-2 does not have a nutritional role in feeding experiments using genetic sensitized mutants. Furthermore, we use robot assisted imaging to show that sid-2 mutants accelerate growth rate and, by maternal contribution, body length at hatching. Finally, we perform transcriptome and lipidome analysis showing that sid-2 has no effect on energy storage lipids, but affects signalling lipids and the embryo transcriptome. Overall, these results suggest that sid-2 has mild effects on development and is unlikely functioning in the nutritional uptake of dsRNA. These findings broaden our understanding of the biological role of SID-2 and motivate studies identifying the role of environmental dsRNA uptake.

RNA Silencing

Lipidome

10.1080/15476286.2020.1827619

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Citations (4)

Comparison between ergot resistant and susceptible lines for environmental sensitivity

D. J. Herde M. J. Ryley David Jordan R. G. Henzell V. J. Galea

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Additional file 3: of Identification of functional long non-coding RNAs in C. elegans

Figshare (2019)

Alper Akay David Jordan Isabela Cunha Navarro Tomasz Wrzesiński Chris P. Ponting

a Annotation of the lncRNAs in C. elegans, including genomic position, multi-exonic or mono-exonic nature, distance to CAGE peak, distance to closest locus, overlap with previously annotated lncRNA, overlap with epigenomic marks and miRNA binding sites, GC proportion, nucleotide conservation, number of libraries in which the locus is expressed, median and mean expression (FPKM), stage of highest expression, closest upstream and downstream protein-coding genes, correlation of expression and associated P value, reported phenotype for the protein. b Reported phenotypes for upstream and downstream protein-coding genes of knockout and knock-down lncRNAs (XLSX 810 kb)

Identification

10.6084/m9.figshare.7734371

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Additional file 13: of Identification of functional long non-coding RNAs in C. elegans

Figshare (2019)

Alper Akay David Jordan Isabela Cunha Navarro Tomasz Wrzesiński Chris P. Ponting

Raw data of length measurements (CSV 4 kb)

Identification

10.6084/m9.figshare.7734350

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