Combination of Genomic and Proteomic Approaches to Characterize the Symbiotic Population of the Banana Aphid (Hemiptera: Aphididae)

Clerck, Caroline De; Tsuchida, Tsutomu; Massart, Sébastien; Lepoivre, Philippe; Francis, Frédéric; Jijakli, M. Haïssam

doi:10.1603/en13107

Cited by 19 publications

(23 citation statements)

References 67 publications

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“…The most frequently detected facultative endosymbionts of aphids are Hamiltonella defensa, Regiella insecticola, S. symbiotica, Rickettsia sp., Ricketsiella sp., Spiroplasma sp., the Pea Aphid X-type Symbiont (PAXS) and Wolbachia sp. (Sandström et al, 2001;Oliver et al, 2003;Oliver et al, 2006;Degnan & Moran, 2008b;Guay et al, 2009;Oliver et al, 2010;Tsuchida et al, 2010;Łukasik et al, 2013b;De Clerck et al, 2014). A concise review of endosymbiont occurrence in aphid populations (Zytynska & Weisser, 2016) found that the facultative endosymbionts S. symbiotica and Wolbachia infected the highest proportion of the aphid species assessed (47% and 43%, respectively).…”

Section: Introductionmentioning

confidence: 99%

The price of protection: a defensive endosymbiont impairs nymph growth in the bird cherry‐oat aphid, Rhopalosiphum padi

et al. 2018

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Bacterial endosymbionts have enabled aphids to adapt to a range of stressors, but their effects in many aphid species remain to be established. The bird cherry-oat aphid, Rhopalosiphum padi (Linnaeus), is an important pest of cereals worldwide and has been reported to form symbiotic associations with Serratia symbiotica and Sitobion miscanthi L-type symbiont endobacteria, although the resulting aphid phenotype has not been described. This study presents the first report of R. padi infection with the facultative bacterial endosymbiont Hamiltonella defensa. Individuals of R. padi were sampled from populations in Eastern Scotland, UK, and shown to represent seven R. padi genotypes based on the size of polymorphic microsatellite markers; two of these genotypes harbored H. defensa. In parasitism assays, survival of H. defensa-infected nymphs following attack by the parasitoid wasp Aphidius colemani (Viereck) was 5 fold higher than for uninfected nymphs. Aphid genotype was a major determinant of aphid performance on two Hordeum species, a modern cultivar of barley H. vulgare and a wild relative H. spontaneum, although aphids infected with H. defensa showed 16% lower nymph mass gain on the partially resistant wild relative compared with uninfected individuals. These findings suggest that deploying resistance traits in barley will favor the fittest R. padi genotypes, but symbiont-infected individuals will be favored when parasitoids are abundant, although these aphids will not achieve optimal performance on a poor quality host plant.

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Section: Introductionmentioning

confidence: 99%

The price of protection: a defensive endosymbiont impairs nymph growth in the bird cherry‐oat aphid, Rhopalosiphum padi

et al. 2018

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“…Recent in situ hybridization studies revealed that Wolbachia and Buchnera coexist in host bacteriocytes (G omez-Valero et al, 2004;De Clerck et al, 2014) and they can cooperate to supply essential nutrients to the host (De Clerck et al, 2014). Although it is unclear where Wolbachia resides in T. macrotuberculatus, its detection in almost all of the aphids examined implies that Wolbachia-infected aphids may have advantageous characteristics to dominate in the environment.…”

Section: Discussionmentioning

confidence: 99%

“…In addition to Buchnera, Wolbachia sp. (an a-proteobacterium) has been found in some aphid species (G omez-Valero et al, 2004;Wang et al, 2009;Augustinos et al, 2011;De Clerck et al, 2014). The roles of Wolbachia in hosts range from parasitism to mutualism.…”

Section: Introductionmentioning

confidence: 99%

Seasonal changes in the density of the symbionts Buchnera and Wolbachia of the aphid Tuberculatus macrotuberculatus on Quercus dentata

Yao

2018

Entomologia Exp Applicata

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Seasonal changes in leaf traits and tannins, including hydrolysable tannins (HTs) and condensed tannins (CTs), affect aphid body size and demographic patterns. The aphid Tuberculatus macrotuberculatus Essig & Kuwana (Hemiptera: Aphididae) feeds on the leaves of the daimyo oak, Quercus dentata Thunberg (Fagaceae), does not alternate hosts, and is attended continuously by ants. Buchnera aphidicola Munson et al. (a γ‐proteobacterium, hereafter Buchnera) is the primary symbiont of most aphid species. It provides essential amino acids to host aphids. Wolbachia sp. (an α‐proteobacterium) is present in some aphid species. This study investigated the effects of seasonal tannin and leaf trait fluctuations in Q. dentata on aphid performance and Buchnera and Wolbachia densities in T. macrotuberculatus. As the season progressed, the water content and HT concentration in Q. dentata leaves decreased, CT concentration in Q. dentata leaves increased, and T. macrotuberculatus performance decreased. Buchnera density varied in accordance with host aphid performance, whereas Wolbachia density did not vary throughout the season, suggesting that although Buchnera depends on the host plant and host aphid performance for growth, Wolbachia may have a high tolerance for oligotrophic environments and may exist independent of the nutritional metabolism of the host aphid. Although the role of Wolbachia in T. macrotuberculatus remains unclear, it may be associated with resistance to parasitoid wasps and plant secondary metabolites.

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“…In particular, P. nigronervosa is the primary vector of the Banana bunchy top virus (BBTV), the most severe viral disease of banana worldwide (Dale 1987). P. nigronervosa carries at least two bacterial symbionts: Buchnera aphidicola and Wolbachia (de Clerck et al 2014). Buchnera aphidicola is an obligate (primary) symbiont present in almost all aphid species and provides essential amino acids to the aphids (Baumann 1995;Douglas 1998;Hansen and Moran 2011;Shigenobu and Wilson 2011).…”

Section: Introductionmentioning

confidence: 99%

“…In contrast, Wolbachia is considered a facultative (secondary) symbiont and is found in a few aphid species at low abundance (Augustinos et al 2011;Jones et al 2011). Interestingly, Wolbachia is found systematically across the P. nigronervosa range (de Clerck et al 2014) and is also present in the closely related species P. caladii van der Goot (Jones et al 2011), which rarely colonizes banana, and prefers other plant species of the order Zingiberales (Foottit et al 2010).…”

Section: Introductionmentioning

confidence: 99%

Genome sequence of the banana aphid, Pentalonia nigronervosa Coquerel (Hemiptera: Aphididae) and its symbionts

Mathers

Mugford

Hogenhout

et al. 2020

Preprint

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The banana aphid, Pentalonia nigronervosa Coquerel (Hemiptera: Aphididae), is a major pest of cultivated bananas (Musa spp., order Zingiberales), primarily due to its role as a vector of Banana bunchy top virus (BBTV), the most severe viral disease of banana worldwide. Here, we generated a highly complete genome assembly of P. nigronervosa using a single PCR-free Illumina sequencing library. Using the same sequence data, we also generated complete genome assemblies of the P. nigronervosa symbiotic bacteria Buchnera aphidicola and Wolbachia. To improve our initial assembly of P. nigronervosa we developed a k-mer based deduplication pipeline to remove genomic scaffolds derived from the assembly of haplotigs (allelic variants assembled as separate scaffolds). To demonstrate the usefulness of this pipeline, we applied it to the recently generated assembly of the aphid Myzus cerasi, reducing the duplication of conserved BUSCO genes by 25%. Phylogenomic analysis of P. nigronervosa, our improved M. cerasi assembly, and seven previously published aphid genomes, spanning three aphid tribes and two subfamilies, reveals that P. nigronervosa falls within the tribe Macrosiphini, but is an outgroup to other Macrosiphini sequenced so far. As such, the genomic resources reported here will be useful for understanding both the evolution of Macrosphini and for the study of P. nigronervosa. Furthermore, our approach using low cost, high-quality, Illumina short-reads to generate complete genome assemblies of understudied aphid species will help to fill in genomic black spots in the diverse aphid tree of life.

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Combination of Genomic and Proteomic Approaches to Characterize the Symbiotic Population of the Banana Aphid (Hemiptera: Aphididae)

Cited by 19 publications

References 67 publications

The price of protection: a defensive endosymbiont impairs nymph growth in the bird cherry‐oat aphid, Rhopalosiphum padi

The price of protection: a defensive endosymbiont impairs nymph growth in the bird cherry‐oat aphid, Rhopalosiphum padi

Seasonal changes in the density of the symbionts Buchnera and Wolbachia of the aphid Tuberculatus macrotuberculatus on Quercus dentata

Genome sequence of the banana aphid, Pentalonia nigronervosa Coquerel (Hemiptera: Aphididae) and its symbionts

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