Networks Underpinning Symbiosis Revealed Through Cross-Species eQTL Mapping

Guo, Yuelong; Fudali, Sylwia; Gimeno, J.; DiGennaro, Peter; Chang, Stella; Williamson, Valerie M.; Bird, David; Nielsen, Dahlia M.

doi:10.1534/genetics.117.202531

Cited by 16 publications

(13 citation statements)

References 54 publications

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“…Using co-transcriptome GWA, we identified 25 trans-eQTL hotspots dispersed across the genome that modulate either the host or pathogen transcriptomes. This contrasts with previous cross-species eQTL studies, which identified one or only a few cross-species eQTL hotspots (Wu, Cai et al 2015, Guo, Fudali et al 2017. Further, most of the genetic variation detected in our study is distal to the affected transcripts, i.e.…”

Section: Dispersed Interactions Across Host and Pathogen Genomescontrasting

confidence: 99%

“…Previous pathogen-linked eQTL studies typically identified more explicit patterns whereby each host expression profile was explained by only a single major-effect pathogen locus (Guo, Fudali et al 2017) or each pathogen eQTL linked to a specific host network (Wu, Cai et al 2015). In contrast, co-transcriptome eGWA with B. cinerea identified a more complex picture with numerous trans-eQTL hotspots and these linked to multiple transcriptome modules in either the host or the pathogen.…”

Section: Polygenic Modules and Pleiotropy In Cross-species Eqtlmentioning

confidence: 99%

“…Additional studies have begun to invert this scheme by looking at how genetic variation in the pathogen influences the host transcriptome to identify pathogen loci modulating host expression levels, and thus candidate loci for interspecific signals (Wu, Cai et al 2015, Guo, Fudali et al 2017). These studies show that it is possible to identify pathogen loci that influence host gene expression, but they have thus far addressed pathogen populations with limited genetic variation (Wu, Cai et al 2015, Guo, Fudali et al 2017. Expanding these approaches would require conducting a co-transcriptome analysis wherein both the host and pathogen transcriptomes are measured using a natural population of the pathogen.…”

Section: Introductionmentioning

confidence: 99%

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Pathogen genetic control of transcriptome variation in the Arabidopsis thaliana – Botrytis cinerea pathosystem

Soltis¹,

Zhang

Corwin³

et al. 2019

Preprint

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Disease symptoms arise from the interaction of the host and pathogen genomes. However, little is known about how genetic variation in the interaction modulates both organisms' transcriptomes, especially in polygenic interactions like those between generalist pathogens and their plant hosts. To begin mapping how polygenic pathogen variation influences both organisms' transcriptomes, we used the Botrytis cinerea -Arabidopsis thaliana pathosystem.We measured the co-transcriptome across a genotyped and genetically diverse collection of 96 B. cinerea isolates infected on the Arabidopsis wildtype, Col-0. Using the B. cinerea genomic variation, we performed genome-wide association (GWA) for each of 23,947 measurable transcripts in the host, and 9,267 measurable transcripts in the pathogen. Unlike other eGWA studies, there was a relative absence of cis-eQTL that is likely explained by structural variants and allelic heterogeneity within the pathogen's genome. This analysis identified mostly trans-eQTL in the pathogen with eQTL hotspots dispersed across the pathogen genome that altered the pathogen's transcripts, the host's transcripts, or both the pathogen and the host. Gene membership in the trans-eQTL hotspots suggests links to several known and many novel virulence mechanisms in the plant-pathogen interaction. Genes annotated to these hotspots provide potential targets for blocking manipulation of the host response by this ubiquitous generalist pathogen. This shows that genetic control over the co-transcriptome is polygenic, similar to the virulence outcome in the interaction of Botrytis cinerea on Arabidopsis thaliana.

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Section: Dispersed Interactions Across Host and Pathogen Genomescontrasting

confidence: 99%

Section: Polygenic Modules and Pleiotropy In Cross-species Eqtlmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Pathogen genetic control of transcriptome variation in the Arabidopsis thaliana – Botrytis cinerea pathosystem

Soltis¹,

Zhang

Corwin³

et al. 2019

Preprint

View full text Add to dashboard Cite

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“…For example, by comparing metagenomes to metatranscriptomes in the human gut, it was discovered that only a few specialized bacteria express unique biosynthesis pathways that may reflect the microbiome response to changing diets or other environmental perturbations in hosts 67,68 . Experimental approaches that compare how microbial genetic variation alters host gene expression (interspecies eQTLs 69 ), and vice versa, provide a promising way forward to understand the links between host-microbiome response to selection at the whole system scale.…”

Section: Eqmentioning

confidence: 99%

Can the microbiome influence host evolutionary trajectories?

Henry

Bruijning

Forsberg

et al. 2019

Preprint

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The microbiome shapes many traits in hosts, but we still do not understand how it influences host evolution. To impact host evolution, the microbiome must be heritable and have phenotypic effects on the host. However, the complex inheritance and context-dependence of the microbiome challenges traditional models of organismal evolution. Here, we take a multifaceted approach to identify conditions in which the microbiome influences host evolutionary trajectories. We explore quantitative genetic models to highlight how microbial inheritance and phenotypic effects can modulate host evolutionary responses to selection. We synthesize the literature across diverse taxa to find common scenarios of microbiome driven host evolution. First, hosts may leverage locally adapted microbes, increasing survivorship in stressful environments. Second, microbial variation may increase host phenotypic variation, enabling exploration of novel fitness landscapes. We further illustrate these effects by performing a meta-analysis of artificial selection in Drosophila, finding that bacterial diversity also frequently responds to host selection. We conclude by outlining key avenues of research and experimental procedures to improve our understanding of the complex interplay between hosts and microbiomes. By synthesizing perspectives through multiple conceptual and analytical approaches, we show how microbiomes can influence the evolutionary trajectories of hosts.

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“…Proteomic profiling identified candidate grasshopper host proteins with roles in neurogenesis that were impacted by infection with the nematomorph Spinochordodes tellinii (Biron et al ., ), and induced hydrophilic behaviour to enable completion of the parasite life‐cycle, which resulted in host death through drowning (Thomas et al ., ). High throughput transcriptomics has similarly uncovered genes underlying complex altered host phenotypes in response to parasite infections (de Bekker et al ., ; Geffre et al ., ; Guo et al ., ).…”

Section: Introductionmentioning

confidence: 99%

Infection by the castrating parasitic nematode Sphaerularia bombi changes gene expression in Bombus terrestris bumblebee queens

Colgan

Carolan

Sumner

et al. 2019

Insect Molecular Biology

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Parasitism can result in dramatic changes in host phenotype, which are themselves underpinned by genes and their expression. Understanding how hosts respond at the molecular level to parasites can therefore reveal the molecular architecture of an altered host phenotype. The entomoparasitic nematode Sphaerularia bombi is a parasite of bumblebee (Bombus) hosts where it induces complex behavioural changes and host castration. To examine this interaction at the molecular level, we performed genome‐wide transcriptional profiling using RNA‐Sequencing (RNA‐Seq) of S. bombi‐infected Bombus terrestris queens at two critical time‐points: during and just after overwintering diapause. We found that infection by S. bombi affects the transcription of genes underlying host biological processes associated with energy usage, translation, and circadian rhythm. We also found that the parasite affects the expression of immune genes, including members of the Toll signalling pathway providing evidence for a novel interaction between the parasite and the host immune response. Taken together, our results identify host biological processes and genes affected by an entomoparasitic nematode providing the first steps towards a molecular understanding of this ecologically important host–parasite interaction.

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Networks Underpinning Symbiosis Revealed Through Cross-Species eQTL Mapping

Abstract: Interactions between species are pervasive among plants, animals, and microbes, and identifying the molecular signals involved is an active area of research..

Cited by 16 publications

References 54 publications

Pathogen genetic control of transcriptome variation in the Arabidopsis thaliana – Botrytis cinerea pathosystem

Pathogen genetic control of transcriptome variation in the Arabidopsis thaliana – Botrytis cinerea pathosystem

Can the microbiome influence host evolutionary trajectories?

Infection by the castrating parasitic nematode Sphaerularia bombi changes gene expression in Bombus terrestris bumblebee queens

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