Evolution Of Host Range Research Articles

Genome resource announcement for emerging pathogen Bipolaris gigantea, isolated from Microstegium vimineum

Bipolaris gigantea is a pathogen of the invasive grass Microstegium vimineum and an emerging pathogen of other hosts such as hemp and barley, causing characteristic eyespot foliar lesions. The fungus is characterized by long pale hyaline conidia measuring about 300 to 350 μm. Previously, this pathogen was classified in the Drechslera genus, and recently reassigned as Bipolaris based on molecular identification. Here, we generated a high-quality draft genome sequence of B. gigantea isolate BGF using long and short read DNA sequencing. The assembled genome, 30.23 Mb in size with a BUSCO completeness score of 98.4%, exhibited synteny with the common grass pathogen B. sorokiniana isolate 10943. Average nucleotide identity (ANI) and single nucleotide polymorphisms (SNP) analyses revealed high sequence identity with B. gigantea isolates from Cannabis sativa fields in Kentucky. This research provides a genomic resource that will contribute to future studies to understand the host range evolution and pathogenicity of this novel pathogen.

Xanthomonas as a Model System for Studying Pathogen Emergence and Evolution.

In this review, we highlight studies in which whole-genome sequencing, comparative genomics, and population genomics have provided unprecedented insights into past and ongoing pathogen evolution. These include new understandings of the adaptive evolution of secretion systems and their effectors. We focus on Xanthomonas pathosystems that have seen intensive study and improved our understanding of pathogen emergence and evolution, particularly in the context of host specialization: citrus canker, bacterial blight of rice, and bacterial spot of tomato and pepper. Across pathosystems, pathogens appear to follow a pattern of bursts of evolution and diversification that impact host adaptation. There remains a need for studies on the mechanisms of host range evolution and genetic exchange among closely related but differentially host-specialized species and to start moving beyond the study of specific strain and host cultivar pairwise interactions to thinking about these pathosystems in a community context.

A chromosome-level genome assembly of the spider mite Tetranychus piercei McGregor

Despite the rapid advances in sequencing technology, limited genomic resources are currently available for phytophagous spider mites, which include many important agricultural pests. One of these pests is Tetranychus piercei (McGregor), a serious banana pest in East Asia exhibiting remarkable tolerance to high temperature. In this study, we assembled a high-quality genome of T. piercei using a combination of PacBio long reads and Illumina short reads sequencing. With the assistance of chromatin conformation capture technology, 99.9% of the contigs were anchored into three pseudochromosomes with a total size of 86.02 Mb. Repetitive elements, accounting for 14.16% of this genome (12.20 Mb), are predominantly composed of long-terminal repeats (30.7%). By combining evidence of ab initio prediction, transcripts, and homologous proteins, we annotated 11,881 protein-coding genes. Both the genome and proteins have high BUSCO completeness scores (>94%). This high-quality genome, along with reliable annotation, provides a valuable resource for investigating the high-temperature tolerance of this species and exploring the genomic basis that underlies the host range evolution of spider mites.

Controlling Recombination to Evolve Bacteriophages.

Recombination among different phages sometimes facilitates their ability to grow on new hosts. Protocols to direct the evolution of phage host range, as might be used in the application of phage therapy, would then benefit from including steps to enable recombination. Applying mathematical and computational models, in addition to experiments using phages T3 and T7, we consider ways that a protocol may influence recombination levels. We first address coinfection, which is the first step to enabling recombination. The multiplicity of infection (MOI, the ratio of phage to cell concentration) is insufficient for predicting (co)infection levels. The force of infection (the rate at which cells are infected) is also critical but is more challenging to measure. Using both a high force of infection and high MOI (>1) for the different phages ensures high levels of coinfection. We also apply a four-genetic-locus model to study protocol effects on recombinant levels. Recombinants accumulate over multiple generations of phage growth, less so if one phage outgrows the other. Supplementing the phage pool with the low-fitness phage recovers some of this 'lost' recombination. Overall, fine tuning of phage recombination rates will not be practical with wild phages, but qualitative enhancement can be attained with some basic procedures.

Molecular modeling and phylogenetic analyses highlight the role of amino acid 347 of the N1 subtype neuraminidase in influenza virus host range and interspecies adaptation.

The N1 neuraminidases (NAs) of avian and pandemic human influenza viruses contain tyrosine and asparagine, respectively, at position 347 on the rim of the catalytic site; the biological significance of this difference is not clear. Here, we used molecular dynamics simulation to model the effects of amino acid 347 on N1 NA interactions with sialyllacto-N-tetraoses 6'SLN-LC and 3'SLN-LC, which represent NA substrates in humans and birds, respectively. Our analysis predicted that Y347 plays an important role in the NA preference for the avian-type substrates. The Y347N substitution facilitates hydrolysis of human-type substrates by resolving steric conflicts of the Neu5Ac2-6Gal moiety with the bulky side chain of Y347, decreasing the free energy of substrate binding, and increasing the solvation of the Neu5Ac2-6Gal bond. Y347 was conserved in all N1 NA sequences of avian influenza viruses in the GISAID EpiFlu database with two exceptions. First, the Y347F substitution was present in the NA of a specific H6N1 poultry virus lineage and was associated with the substitutions G228S and/or E190V/L in the receptor-binding site (RBS) of the hemagglutinin (HA). Second, the highly pathogenic avian H5N1 viruses of the Gs/Gd lineage contained sporadic variants with the NA substitutions Y347H/D, which were frequently associated with substitutions in the HA RBS. The Y347N substitution occurred following the introductions of avian precursors into humans and pigs with N/D347 conserved during virus circulation in these hosts. Comparative evolutionary analysis of site 347 revealed episodic positive selection across the entire tree and negative selection within most host-specific groups of viruses, suggesting that substitutions at NA position 347 occurred during host switches and remained under pervasive purifying selection thereafter. Our results elucidate the role of amino acid 347 in NA recognition of sialoglycan substrates and emphasize the significance of substitutions at position 347 as a marker of host range and adaptive evolution of influenza viruses.

Tobacco Mild Green Mosaic Virus (TMGMV) Isolates from Different Plant Families Show No Evidence of Differential Adaptation to Their Host of Origin.

The relevance of tobamoviruses to crop production is increasing due to new emergences, which cannot be understood without knowledge of the tobamovirus host range and host specificity. Recent analyses of tobamovirus occurrence in different plant communities have shown unsuspectedly large host ranges. This was the case of the tobacco mild green mosaic virus (TMGMV), which previously was most associated with solanaceous hosts. We addressed two hypotheses concerning TMGMV host range evolution: (i) ecological fitting, rather than genome evolution, determines TMGMV host range, and (ii) isolates are adapted to the host of origin. We obtained TMGMV isolates from non-solanaceous hosts and we tested the capacity of genetically closely related TMGMV isolates from three host families to infect and multiply in 10 hosts of six families. All isolates systemically infected all hosts, with clear disease symptoms apparent only in solanaceous hosts. TMGMV multiplication depended on the assayed host but not on the isolate's host of origin, with all isolates accumulating to the highest levels in Nicotiana tabacum. Thus, results support that TMGMV isolates are adapted to hosts in the genus Nicotiana, consistent with a well-known old virus-host association. In addition, phenotypic plasticity allows Nicotiana-adapted TMGMV genotypes to infect a large range of hosts, as encountered according to plant community composition and transmission dynamics.

First identification of a novel Aichivirus D in goats with diarrhea

This study identifies a novel Aichivirus D in goats for the first time, and a case-control study suggested that the virus is associated with diarrhea in goats. The goat Aichivirus D shared the highest gnomic sequence homology with ovine Aichivirus D strain, and may origin from ovine Aichivirus D through natural VP1 gene recombination. These findings contribute to a better understanding of the host range and genetic evolution of Aichivirus D.

Tobamoviruses show broad host ranges and little genetic diversity among four habitat types of a heterogeneous ecosystem.

Host ranges of plant viruses are poorly known, as studies have focused on pathogenic viruses in crops and adjacent wild plants. High throughput sequencing (HTS) avoids the bias towards plant-virus interactions that result in disease. Here we study the host ranges of tobamoviruses, important pathogens of crops, by HTS analyses of an extensive sample of plant communities in four habitats of a heterogeneous ecosystem. Sequences of 17 virus operational taxonomic units (OTUs) matched references in the Tobamovirus genus, eight had narrow, and five had wide host ranges. Regardless of host range, each OTU host belonged to taxonomically distant families, suggesting no phylogenetic constraints in host use associated with virus adaptation, and that tobamoviruses may be host generalists. The OTUs identified as TMGMV, TMV, PMMoV and YoMV, had the largest realized host ranges that occurred across habitats, and exhibited host use unrelated to the degree of human intervention. This result is at odds with assumptions that contact transmitted viruses would be more abundant in crops than in wild plant communities, and could be explained by effective seed, contact, or pollinator-mediated transmission, or by survival in the soil. TMGMV and TMV had low genetic diversity that was not structured according to habitat or host plant taxonomy, which indicated that phenotypic plasticity allows virus genotypes to infect new hosts with no need for adaptive evolution. Our results underscore the relevance of ecological factors in host range evolution, in addition to the more often studied genetic factors.

Host Plant Effects on Sexual Selection Dynamics in Phytophagous Insects.

Natural selection is notoriously dynamic in nature, and so, too, is sexual selection. The interactions between phytophagous insects and their host plants have provided valuable insights into the many ways in which ecological factors can influence sexual selection. In this review, we highlight recent discoveries and provide guidance for future work in this area. Importantly, host plants can affect both the agents of sexual selection (e.g., mate choice and male-male competition) and the traits under selection (e.g., ornaments and weapons). Furthermore, in our rapidly changing world, insects now routinely encounter new potential host plants. The process of adaptation to a new host may be hindered or accelerated by sexual selection, and the unexplored evolutionary trajectories that emerge from these dynamics are relevant to pest management and insect conservation strategies. Examining the effects of host plants on sexual selection has the potential to advance our fundamental understanding of sexual conflict, host range evolution, and speciation, with relevance across taxa.

The genome sequence of a spider mite, Tetranychus truncatus, provides insights into interspecific host range variation and the genetic basis of adaptation to a low-quality host plant.

The phytophagous mite Tetranychus truncatus is a serious pest in East Asia but has a relatively narrower host range than the pest mite Tetranychus urticae, which can feed on over 1200 plant species. Here, we generated a high-quality chromosomal level genome of T.truncatus and compared it with that of T.urticae, with an emphasis on the genes related to detoxification and chemoreception, to explore the genomic basis underlying the evolution of host range. We also conducted population genetics analyses (in 86 females from 10 populations) and host transfer experiments (in 4 populations) to investigate transcription changes following transfer to a low-quality host (Solanum melongena, eggplant), and we established possible connections between fitness on eggplant and genes related to detoxification and chemoreception. We found that T.truncatus has fewer genes related to detoxification, transport, and chemoreception than T.urticae, with a particularly strong reduction in gustatory receptor (GR) genes. We also found widespread transcriptional variation among T.truncatus populations, which varied in fitness on eggplant. We characterized selection on detoxification-related genes through ω values and found a negative correlation between expression levels and ω values. Based on the transcription results, as well as the fitness and genetic differences among populations, we identified genes potentially involved in adaptation to eggplant in T.truncatus. Our work provides a genomic resource for this pest mite and new insights into mechanisms underlying the adaptation of herbivorous mites to host plants.

Interspecies killing activity of Pseudomonas syringae tailocins.

Tailocins are ribosomally synthesized bacteriocins, encoded by bacterial genomes, but originally derived from bacteriophage tails. As with both bacteriocins and phage, tailocins are largely thought to be species-specific with killing activity often assumed to be directed against closely related strains. Previous investigations into interactions between tailocin host range and sensitivity across phylogenetically diverse isolates of the phytopathogen Pseudomonas syringae have demonstrated that many strains possess intraspecific tailocin activity and that this activity is highly precise and specific against subsets of strains. However, here we demonstrate that at least one strain of P. syringae, USA011R, defies both expectations and current overarching dogma because tailocins from this strain possess broad killing activity against other agriculturally significant phytopathogens such as Erwinia amylovora and Xanthomonas perforans as well as against the clinical human pathogen Salmonella enterica serovar Choleraesuis. Moreover, we show that the full spectrum of this interspecific killing activity is not conserved across closely related strains with data suggesting that even if tailocins can target different species, they do so with different efficiencies. Our results reported herein highlight the potential for and phenotypic divergence of interspecific killing activity of P. syringae tailocins and establish a platform for further investigations into the evolution of tailocin host range and strain specificity.

Reversion of a resistance-breaking mutation shows reversion costs and high virus diversity at necrotic local lesions.

An instance of host range evolution relevant to plant virus disease control is resistance breaking. Resistance breaking can be hindered by across-host fitness trade-offs generated by negative effects of resistance-breaking mutations on the virus fitness in susceptible hosts. Different mutations in pepper mild mottle virus (PMMoV) coat protein result in the breaking in pepper plants of the resistance determined by the L3 resistance allele. Of these, mutation M138N is widespread in PMMoV populations, despite associated fitness penalties in within-host multiplication and survival. The stability of mutation M138N was analysed by serial passaging in L3 resistant plants. Appearance on passaging of necrotic local lesions (NLL), indicating an effective L3 resistance, showed reversion to nonresistance-breaking phenotypes was common. Most revertant genotypes had the mutation N138K, which affects the properties of the virus particle, introducing a penalty of reversion. Hence, the costs of reversion may determine the evolution of resistance-breaking in addition to resistance-breaking costs. The genetic diversity of the virus population in NLL was much higher than in systemically infected tissues, and included mutations reported to break L3 resistance other than M138N. Infectivity assays on pepper genotypes with different L alleles showed high phenotypic diversity in respect to L alleles in NLL, including phenotypes not reported in nature. Thus, high diversity at NLL may potentiate the appearance of genotypes that enable the colonization of new host genotypes or species. Collectively, the results of this study contribute to better understanding the evolutionary dynamics of resistance breaking and host-range expansions.

A Trait-Based Approach to Predicting Viral Host-Range Evolvability.

Predicting the evolution of virus host range has proven to be extremely difficult, in part because of the sheer diversity of viruses, each with unique biology and ecological interactions. We have not solved this problem, but to make the problem more tractable, we narrowed our focus to three traits intrinsic to all viruses that may play a role in host-range evolvability: mutation rate, recombination rate, and phenotypic heterogeneity. Although each trait should increase evolvability, they cannot do so unbounded because fitness trade-offs limit the ability of all three traits to maximize evolvability. By examining these constraints, we can begin to identify groups of viruses with suites of traits that make them especially concerning, as well as ecological and environmental conditions that might push evolution toward accelerating host-range expansion.

Complete genomic sequences and comparative analysis of two Orf virus isolates from Guizhou Province and Jilin Province, China.

Orf virus (ORFV, species Orf virus) belongs to the typical species of the Parapoxvirus genus of the family Poxviridae, which infects sheep, goats, and humans with worldwide distribution. Although outbreaks of Orf have been reported sequentially in several Chinese provinces, the epidemiology of Orf and genetic diversity of ORFV strains still needs to be further characterized. To further reveal the genomic organization of the ORFV-GZ18 and ORFV-CL18 isolates, the complete genome sequences of two recently obtained ORFV isolates were sequenced using the next-generation sequencing technology and analyzed, which had been deposited in the GenBank database under accession number MN648218 and MN648219, respectively. The complete genomic sequence of ORFV-CL18 was 138,495bp in length, including 131 potential open reading frames (ORFs) flanked by inverted terminal repeats (ITRs) of 3481bp at both ends, which has genomic structure typical Parapoxviruses. The overall genomic organization of the fully sequenced genome of ORFV-GZ18 was consistent with ORFV-CL18 genome, with a complete genome size of 138,446 nucleotides, containing 131 ORFs flanked by ITRs of 3469bp. Additionally, the overall G + C contents of ORFV-GZ18 and ORFV-CL18 genome sequences were about 63.9% and 63.8%, respectively. The phylogenetic analysis showed that both ORFV-GZ18 and ORFV-CL18 were genetically closely related to ORFV-SY17 derived from sheep. In summary, the complete genomic sequences of ORFV-GZ18 and ORFV-CL18 are reported, with the hope it will be useful to investigate the host range, geographic distribution, and genetic evolution of the virus in Southern West and Northern East China.

Somewhere I belong: phylogeny and morphological evolution in a species-rich lineage of ectoparasitic flatworms infecting cichlid fishes.

A substantial portion of biodiversity has evolved through adaptive radiation. However, the effects of explosive speciation on species interactions remain poorly understood. Metazoan parasites infecting radiating host lineages could improve our knowledge because of their intimate host relationships. Yet limited molecular, phenotypic and ecological data discourage multivariate analyses of evolutionary patterns and encourage the use of discrete characters. Here, we assemble new molecular, morphological and host range data widely inferred from a species-rich lineage of parasites (Cichlidogyrus, Platyhelminthes: Monogenea) infecting cichlid fishes to address data scarcity. We infer a multimarker (28S/18S rDNA, ITS1, COI mtDNA) phylogeny of 58 of 137 species and characterize major lineages through synapomorphies inferred from mapping morphological characters. We predict the phylogenetic position of species without DNA data through shared character states, a morphological phylogenetic analysis, and a classification analysis with support vector machines. Based on these predictions and a cluster analysis, we assess the systematic informativeness of continuous characters, search for continuous equivalents for discrete characters, and suggest new characters for morphological traits not analysed to date. We also model the attachment/reproductive organ and host range evolution using the data for 136 of 137 described species and multivariate phylogenetic comparative methods (PCMs). We show that discrete characters not only can mask phylogenetic signals, but also are key for characterizing species groups. Regarding the attachment organ morphology, a divergent evolutionary regime for at least one lineage was detected and a limited morphological variation indicates host and environmental parameters affecting its evolution. However, moderate success in predicting phylogenetic positions, and a low systematic informativeness and high multicollinearity of morphological characters call for a revaluation of characters included in species characterizations.

Use of an exotic host plant shifts immunity, chemical defense, and viral burden in wild populations of a specialist insect herbivore.

Defense against natural enemies constitutes an important driver of herbivore host range evolution in the wild. Populations of the Baltimore checkerspot butterfly, Euphydryas phaeton (Nymphalidae), have recently incorporated an exotic plant, Plantago lanceolata (Plantaginaceae), into their dietary range. To understand the tritrophic consequences of utilizing this exotic host plant, we examined immune performance, chemical defense, and interactions with a natural entomopathogen (Junonia coenia densovirus, Parvoviridae) across wild populations of this specialist herbivore. We measured three immune parameters, sequestration of defensive iridoid glycosides (IGs), and viral infection load in field‐collected caterpillars using either P. lanceolata or a native plant, Chelone glabra (Plantaginaceae). We found that larvae using the exotic plant exhibited reduced immunocompetence, compositional differences in IG sequestration, and higher in situ viral burdens compared to those using the native plant. On both host plants, high IG sequestration was associated with reduced hemocyte concentration in the larval hemolymph, providing the first evidence of incompatibility between sequestered chemical defenses and the immune response (i.e., the “vulnerable host” hypothesis) from a field‐based study. However, despite this negative relationship between IG sequestration and cellular immunity, caterpillars with greater sequestration harbored lower viral loads. While survival of virus‐infected individuals decreased with increasing viral burden, it ultimately did not differ between the exotic and native plants. These results provide evidence that: (1) phytochemical sequestration may contribute to defense against pathogens even when immunity is compromised and (2) herbivore persistence on exotic plant species may be facilitated by sequestration and its role in defense against natural enemies.

Viral protein instability enhances host-range evolvability.

Viruses are highly evolvable, but what traits endow this property? The high mutation rates of viruses certainly play a role, but factors that act above the genetic code, like protein thermostability, are also expected to contribute. We studied how the thermostability of a model virus, bacteriophage λ, affects its ability to evolve to use a new receptor, a key evolutionary transition that can cause host-range evolution. Using directed evolution and synthetic biology techniques we generated a library of host-recognition protein variants with altered stabilities and then tested their capacity to evolve to use a new receptor. Variants fell within three stability classes: stable, unstable, and catastrophically unstable. The most evolvable were the two unstable variants, whereas seven of eight stable variants were significantly less evolvable, and the two catastrophically unstable variants could not grow. The slowly evolving stable variants were delayed because they required an additional destabilizing mutation. These results are particularly noteworthy because they contradict a widely supported contention that thermostabilizing mutations enhance evolvability of proteins by increasing mutational robustness. Our work suggests that the relationship between thermostability and evolvability is more complex than previously thought, provides evidence for a new molecular model of host-range expansion evolution, and identifies instability as a potential predictor of viral host-range evolution.

From generalist to specialists: Variation in the host range and performance of anther-smut pathogens on Dianthus.

Determining the processes that drive the evolution of pathogen host range can inform our understanding of disease dynamics and the potential for host shifts. In natural populations, patterns of host range could be driven by genetically based differences in pathogen infectivity or ecological differences in host availability. In northwestern Italy, four reproductively isolated lineages of the fungal plant-pathogen Microbotryum have been shown to co-occur on several species in the genus Dianthus. We carried out cross-inoculation experiments to determine whether patterns of realized host range in these four lineages were driven by differences in infectivity and to test whether there was evidence of a trade-off between host range and within-host reproduction. We found strong concordance between field patterns of host range and pathogen infectivity on different Dianthus species using experimental inoculation, indicating that infection ability is a major driving force of host range. However, we found no evidence of a trade-off between the ability to infect a wider range of host species and spore production on a shared host.

Pectobacterium brasiliense: Genomics, Host Range and Disease Management.

Pectobacterium brasiliense (Pbr) is considered as one of the most virulent species among the Pectobacteriaceae. This species has a broad host range within horticulture crops and is well distributed elsewhere. It has been found to be pathogenic not only in the field causing blackleg and soft rot of potato, but it is also transmitted via storage causing soft rot of other vegetables. Genomic analysis and other cost-effective molecular detection methods such as a quantitative polymerase chain reaction (qPCR) are essential to investigate the ecology and pathogenesis of the Pbr. The lack of fast, field deployable point-of-care testing (POCT) methods, specific control strategies and current limited genomic knowledge make management of this species difficult. Thus far, no comprehensive review exists about Pbr, however there is an intense need to research the biology, detection, pathogenicity and management of Pbr, not only because of its fast distribution across Europe and other countries but also due to its increased survival to various climatic conditions. This review outlines the information available in peer-reviewed literature regarding host range, detection methods, genomics, geographical distribution, nomenclature and taxonomical evolution along with some of the possible management and control strategies. In summary, the conclusions and a further directions highlight the management of this species.

Innate preference hierarchies coupled with adult experience, rather than larval imprinting or transgenerational acclimation, determine host plant use in Pieris rapae.

The evolution of host range drives diversification in phytophagous insects, and understanding the female oviposition choices is pivotal for understanding host specialization. One controversial mechanism for female host choice is Hopkins’ host selection principle, where females are predicted to increase their preference for the host species they were feeding upon as larvae. A recent hypothesis posits that such larval imprinting is especially adaptive in combination with anticipatory transgenerational acclimation, so that females both allocate and adapt their offspring to their future host. We study the butterfly Pieris rapae, for which previous evidence suggests that females prefer to oviposit on host individuals of similar nitrogen content as the plant they were feeding upon as larvae, and where the offspring show higher performance on the mother's host type. We test the hypothesis that larval experience and anticipatory transgenerational effects influence female host plant acceptance (no‐choice) and preference (choice) of two host plant species (Barbarea vulgaris and Berteroa incana) of varying nitrogen content. We then test the offspring performance on these hosts. We found no evidence of larval imprinting affecting female decision‐making during oviposition, but that an adult female experience of egg laying in no‐choice trials on the less‐preferred host Be. incana slightly increased the P. rapae propensity to oviposit on Be. incana in subsequent choice trials. We found no transgenerational effects on female host acceptance or preference, but negative transgenerational effects on larval performance, because the offspring of P. rapae females that had developed on Be. incana as larvae grew slower on both hosts, and especially on Be. incana. Our results suggest that among host species, preferences are guided by hard‐wired preference hierarchies linked to species‐specific host traits and less affected by larval experience or transgenerational effects, which may be more important for females evaluating different host individuals of the same species.