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1. Genomics of sorghum local adaptation to a parasitic plant

   https://doi.org/10.1073/pnas.1908707117  

   Bellis, Emily S. ; Kelly, Elizabeth A. ; Lorts, Claire M. ; Gao, Huirong ; DeLeo, Victoria L. ; Rouhan, Germinal ; Budden, Andrew ; Bhaskara, Govinal B. ; Hu, Zhenbin ; Muscarella, Robert ; et al ( February 2020 , Proceedings of the National Academy of Sciences)

   Host–parasite coevolution can maintain high levels of genetic diversity in traits involved in species interactions. In many systems, host traits exploited by parasites are constrained by use in other functions, leading to complex selective pressures across space and time. Here, we study genome-wide variation in the staple cropSorghum bicolor(L.) Moench and its association with the parasitic weedStriga hermonthica(Delile) Benth., a major constraint to food security in Africa. We hypothesize that geographic selection mosaics across gradients of parasite occurrence maintain genetic diversity in sorghum landrace resistance. Suggesting a role in local adaptation to parasite pressure, multiple independent loss-of-function alleles at sorghumLOW GERMINATION STIMULANT 1 (LGS1)are broadly distributed among African landraces and geographically associated withS. hermonthicaoccurrence. However, low frequency of these alleles withinS. hermonthica-prone regions and their absence elsewhere implicate potential trade-offs restricting their fixation.LGS1is thought to cause resistance by changing stereochemistry of strigolactones, hormones that control plant architecture and below-ground signaling to mycorrhizae and are required to stimulate parasite germination. Consistent with trade-offs, we find signatures of balancing selection surroundingLGS1and other candidates from analysis of genome-wide associations with parasite distribution. Experiments with CRISPR–Cas9-edited sorghum further indicate that the benefit ofLGS1-mediated resistance strongly depends on parasite genotype and abiotic environment and comes at the cost of reduced photosystem gene expression. Our study demonstrates long-term maintenance of diversity in host resistance genes across smallholder agroecosystems, providing a valuable comparison to both industrial farming systems and natural communities.

    

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2. Genomic evidence for population‐specific responses to co‐evolving parasites in a New Zealand freshwater snail

   https://doi.org/10.1111/mec.14146  

   Bankers, Laura ; Fields, Peter ; McElroy, Kyle E. ; Boore, Jeffrey L. ; Logsdon, Jr., John M. ; Neiman, Maurine ( May 2017 , Molecular Ecology)

   Reciprocal co‐evolving interactions between hosts and parasites are a primary source of strong selection that can promote rapid and often population‐ or genotype‐specific evolutionary change. These host–parasite interactions are also a major source of disease. Despite their importance, very little is known about the genomic basis of co‐evolving host–parasite interactions in natural populations, especially in animals. Here, we use gene expression and sequence evolution approaches to take critical steps towards characterizing the genomic basis of interactions between the freshwater snailPotamopyrgus antipodarumand its co‐evolving sterilizing trematode parasite,Microphallussp., a textbook example of natural coevolution. We found thatMicrophallus‐infectedP. antipodarumexhibit systematic downregulation of genes relative to uninfectedP. antipodarum. The specific genes involved in parasite response differ markedly across lakes, consistent with a scenario where population‐level co‐evolution is leading to population‐specific host–parasite interactions and evolutionary trajectories. We also used anF_ST‐based approach to identify a set of loci that represent promising candidates for targets of parasite‐mediated selection across lakes as well as within each lake population. These results constitute the first genomic evidence for population‐specific responses to co‐evolving infection in theP. antipodarum‐Microphallusinteraction and provide new insights into the genomic basis of co‐evolutionary interactions in nature.

    

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3. Transcriptome assembly and differential gene expression of the invasive avian malaria parasite Plasmodium relictum in Hawaiʻi

   https://doi.org/10.1002/ece3.7401  

   Videvall, Elin ; Paxton, Kristina L. ; Campana, Michael G. ; Cassin‐Sackett, Loren ; Atkinson, Carter T. ; Fleischer, Robert C. ( March 2021 , Ecology and Evolution)

   The malaria parasitePlasmodium relictum(lineage GRW4) was introduced less than a century ago to the native avifauna of Hawaiʻi, where it has since caused major declines of endemic bird populations. One of the native bird species that is frequently infected with GRW4 is the Hawaiʻi ʻamakihi (Chlorodrepanis virens). To achieve a better understanding of the transcriptional activities of this virulent parasite, we performed a controlled challenge experiment of 15 ʻamakihi that were infected with GRW4. Blood samples containing malaria parasites were collected at two time points (intermediate and peak infection stages) from host individuals that were either experimentally infected by mosquitoes or inoculated with infected blood. We then used RNA sequencing to assemble a high‐quality blood transcriptome ofP. relictumGRW4, allowing us to quantify parasite expression levels inside individual birds. We found few significant differences (one to two transcripts) in GRW4 expression levels between host infection stages and between inoculation methods. However, 36 transcripts showed differential expression levels among all host individuals, indicating a potential presence of host‐specific gene regulation across hosts. To reduce the extinction risk of the remaining native bird species in Hawaiʻi, genetic resources of the localPlasmodiumlineage are needed to enable further molecular characterization of this parasite. Our newly built Hawaiian GRW4 transcriptome assembly, together with analyses of the parasite's transcriptional activities inside the blood of Hawaiʻi ʻamakihi, can provide us with important knowledge on how to combat this deadly avian disease in the future.

    

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4. Intraspecific antagonism through viral toxin encoded by chronic Sulfolobus spindle-shaped virus

   https://doi.org/10.1098/rstb.2020.0476  

   DeWerff, Samantha J. ; Zhang, Changyi ; Schneider, John ; Whitaker, Rachel J. ( January 2022 , Philosophical Transactions of the Royal Society B: Biological Sciences)

   Virus–host interactions evolve along a symbiosis continuum from antagonism to mutualism. Long-term associations between virus and host, such as those in chronic infection, will select for traits that drive the interaction towards mutualism, especially when susceptible hosts are rare in the population. Virus–host mutualism has been demonstrated in thermophilic archaeal populations where Sulfolobus spindle-shaped viruses (SSVs) provide a competitive advantage to their host Sulfolobus islandicus by producing a toxin that kills uninfected strains. Here, we determine the genetic basis of this killing phenotype by identifying highly transcribed genes in cells that are chronically infected with a diversity of SSVs. We demonstrate that these genes alone confer growth inhibition by being expressed in uninfected cells via a Sulfolobus expression plasmid. Challenge of chronically infected strains with vector-expressed toxins revealed a nested network of cross-toxicity among divergent SSVs, with both broad and specific toxin efficacies. This suggests that competition between viruses and/or their hosts could maintain toxin diversity. We propose that competitive interactions among chronic viruses to promote their host fitness form the basis of virus–host mutualism. This article is part of the theme issue ‘The secret lives of microbial mobile genetic elements’. 

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5. Disruption of the Putative Ribosome-Binding Motif of a Scaffold Protein Impairs Cytochrome c Oxidase Subunit Expression in Leishmania major

   https://doi.org/10.1128/mSphere.00644-18  

   Cardenas, Daviel ; Sylvester, Charity ; Cao, Bo ; Nation, Catherine S. ; Pizarro, Juan C. ; Lu, Hua ; Guidry, Jessie ; Wojcik, Edward J. ; Kelly, Ben L. ( April 2019 , mSphere)

   Moreno, Silvia N. (Ed.)

   ABSTRACT During their parasitic life cycle, through sandflies and vertebrate hosts, Leishmania parasites confront strikingly different environments, including abrupt changes in pH and temperature, to which they must rapidly adapt. These adaptations include alterations in Leishmania gene expression, metabolism, and morphology, allowing them to thrive as promastigotes in the sandfly and as intracellular amastigotes in the vertebrate host. A critical aspect of Leishmania metabolic adaptation to these changes is maintenance of efficient mitochondrial function in the hostile vertebrate environment. Such functions, including generation of ATP, depend upon the expression of many mitochondrial proteins, including subunits of cytochrome c oxidase (COX). Significantly, under mammalian temperature conditions, expression of Leishmania major COX subunit IV (LmCOX4) and virulence are dependent upon two copies of LACK , a gene that encodes the ribosome-associated scaffold protein, LACK ( Leishmania ortholog of RACK1 [receptor for activated C kinase]). Targeted replacement of an endogenous LACK copy with a putative ribosome-binding motif-disrupted variant (LACK R34D35G36 →LACK D34D35E36 ) resulted in thermosensitive parasites that showed diminished LmCOX4 expression, mitochondrial fitness, and replication in macrophages. Surprisingly, despite these phenotypes, LACK D34D35E36 associated with monosomes and polysomes and showed no major impairment of global protein synthesis. Collectively, these data suggest that wild-type (WT) LACK orchestrates robust LmCOX4 expression and mitochondrial fitness to ensure parasite virulence, via optimized functional interactions with the ribosome. IMPORTANCE Leishmania parasites are trypanosomatid protozoans that persist in infected human hosts to cause a spectrum of pathologies, from cutaneous and mucocutaneous manifestations to visceral leishmaniasis caused by Leishmania donovani . The latter is usually fatal if not treated. Persistence of L. major in the mammalian host depends upon maintaining gene-regulatory programs to support essential parasite metabolic functions. These include expression and assembly of mitochondrial L. major cytochrome c oxidase (LmCOX) subunits, important for Leishmania ATP production. Significantly, under mammalian conditions, WT levels of LmCOX subunits require threshold levels of the Leishmania ribosome-associated scaffold protein, LACK. Unexpectedly, we find that although disruption of LACK’s putative ribosome-binding motif does not grossly perturb ribosome association or global protein synthesis, it nonetheless impairs COX subunit expression, mitochondrial function, and virulence. Our data indicate that the quality of LACK’s interaction with Leishmania ribosomes is critical for LmCOX subunit expression and parasite mitochondrial function in the mammalian host. Collectively, these findings validate LACK’s ribosomal interactions as a potential therapeutic target. 

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