Comparison of the Genome Sequences of “Candidatus Portiera aleyrodidarum” Primary Endosymbionts of the Whitefly Bemisia tabaci B and Q Biotypes

Jiang, Zi Feng; Xia, Fangfang; Johnson, Kipp W.; Brown, Christopher D.; Bartom, Elizabeth T.; Tuteja, Jigyasa H.; Grossman, Robert L.; Brumin, Marina; White, Kevin P.; Ghanim, Murad

doi:10.1128/aem.02976-12

Cited by 26 publications

(28 citation statements)

References 15 publications

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“…The error-corrected PacBio reads corresponding to the three symbiont genomes were first extracted by aligning the reads to the reference sequences of related species [88–90]. The extracted PacBio reads for each symbiont were de novo assembled using Sprai (http://zombie.cb.k.u-tokyo.ac.jp/sprai/).…”

Section: Methodsmentioning

confidence: 99%

The draft genome of whitefly Bemisia tabaci MEAM1, a global crop pest, provides novel insights into virus transmission, host adaptation, and insecticide resistance

et al. 2016

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BackgroundThe whitefly Bemisia tabaci (Hemiptera: Aleyrodidae) is among the 100 worst invasive species in the world. As one of the most important crop pests and virus vectors, B. tabaci causes substantial crop losses and poses a serious threat to global food security.ResultsWe report the 615-Mb high-quality genome sequence of B. tabaci Middle East-Asia Minor 1 (MEAM1), the first genome sequence in the Aleyrodidae family, which contains 15,664 protein-coding genes. The B. tabaci genome is highly divergent from other sequenced hemipteran genomes, sharing no detectable synteny. A number of known detoxification gene families, including cytochrome P450s and UDP-glucuronosyltransferases, are significantly expanded in B. tabaci. Other expanded gene families, including cathepsins, large clusters of tandemly duplicated B. tabaci-specific genes, and phosphatidylethanolamine-binding proteins (PEBPs), were found to be associated with virus acquisition and transmission and/or insecticide resistance, likely contributing to the global invasiveness and efficient virus transmission capacity of B. tabaci. The presence of 142 horizontally transferred genes from bacteria or fungi in the B. tabaci genome, including genes encoding hopanoid/sterol synthesis and xenobiotic detoxification enzymes that are not present in other insects, offers novel insights into the unique biological adaptations of this insect such as polyphagy and insecticide resistance. Interestingly, two adjacent bacterial pantothenate biosynthesis genes, panB and panC, have been co-transferred into B. tabaci and fused into a single gene that has acquired introns during its evolution.ConclusionsThe B. tabaci genome contains numerous genetic novelties, including expansions in gene families associated with insecticide resistance, detoxification and virus transmission, as well as numerous horizontally transferred genes from bacteria and fungi. We believe these novelties likely have shaped B. tabaci as a highly invasive polyphagous crop pest and efficient vector of plant viruses. The genome serves as a reference for resolving the B. tabaci cryptic species complex, understanding fundamental biological novelties, and providing valuable genetic information to assist the development of novel strategies for controlling whiteflies and the viruses they transmit.Electronic supplementary materialThe online version of this article (doi:10.1186/s12915-016-0321-y) contains supplementary material, which is available to authorized users.

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Section: Methodsmentioning

confidence: 99%

The draft genome of whitefly Bemisia tabaci MEAM1, a global crop pest, provides novel insights into virus transmission, host adaptation, and insecticide resistance

et al. 2016

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“…For example, independently evolved bacterial symbionts in phloem-feeding whiteflies and mealybugs of the same suborder as the aphids, the Sternorrhyncha, have incomplete genetic capacity for EAA biosynthesis (6,28,29), but the biosynthetic pathways are apparently complete in the bacterial symbionts, e.g., Sulcia, of insects (e.g., cicadas, spittlebugs, and leafhoppers) in the related suborder, the Auchenorryncha (30)(31)(32). Turning to different symbioses, the stimulation of EAA production from Buchnera preparations by the host cell fraction (HF) is reminiscent of enhanced photosynthate release by symbiotic algae isolated from corals or other marine invertebrates and incubated with homogenates of their hosts (33).…”

Section: Discussionmentioning

confidence: 99%

Shared Metabolic Pathways in a Coevolved Insect-Bacterial Symbiosis

Russell

Bouvaine

Newell

et al. 2013

Appl Environ Microbiol

104

112

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The symbiotic bacterium Buchnera aphidicola lacks key genes in the biosynthesis of five essential amino acids (EAAs), and yet its animal hosts (aphids) depend on the symbiosis for the synthesis of these EAAs (isoleucine, leucine, methionine, phenylalanine, and valine). We tested the hypothesis, derived from genome annotation, that the missing Buchnera reactions are mediated by host enzymes, with the exchange of metabolic intermediates between the partners. The specialized host cells bearing Buchnera were separated into a Buchnera fraction and a Buchnera-free host cell fraction (HF). Addition of HF to isolated Buchnera preparations significantly increased the production of leucine and phenylalanine, and recombinant enzymes mediating the final reactions in branched-chain amino acid and phenylalanine synthesis rescued the production of these EAAs by Buchnera preparations without HF. The likely precursors for the missing proximal reactions in isoleucine and methionine synthesis were identified, and they differed from predictions based on genome annotations: synthesis of 2-oxobutanoate, the aphid-derived precursor of isoleucine synthesis, was stimulated by homoserine and not threonine via threonine dehydratase, and production of the homocysteine precursor of methionine was driven by cystathionine, not cysteine, via reversal of the transsulfuration pathway. The evolution of shared metabolic pathways in this symbiosis can be attributed to host compensation for genomic deterioration in the symbiont, involving changes in host gene expression networks to recruit specific enzymes to the host cell.

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“…Here, we take advantage of the availability of additional Portiera genomes that were independently sequenced from different populations and biotypes in the B . tabaci species complex (Santos-Garcia et al 2012; Jiang et al 2013). We also report the complete Portiera genome from the distantly related host species Trialeurodes vaporarium .…”

Section: Introductionmentioning

confidence: 99%

The Evolution of Genomic Instability in the Obligate Endosymbionts of Whiteflies

Sloan

Moran

2013

Genome Biology and Evolution

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Many insects depend on ancient associations with intracellular bacteria to perform essential metabolic functions. These endosymbionts exhibit striking examples of convergence in genome architecture, including a high degree of structural stability that is not typical of their free-living counterparts. However, the recently sequenced genome of the obligate whitefly endosymbiont Portiera revealed features that distinguish it from other ancient insect associates, such as a low gene density and the presence of perfectly duplicated sequences. Here, we report the comparative analysis of Portiera genome sequences both within and between host species. In one whitefly lineage (Bemisia tabaci), we identify large-scale structural polymorphisms in the Portiera genome that exist even within individual insects. This variation is likely mediated by recombination across identical repeats that are maintained by gene conversion. The complete Portiera genome sequence from a distantly related whitefly host (Trialeurodes vaporarium) confirms a history of extensive genome rearrangement in this ancient endosymbiont. Using gene-order-based phylogenetic analysis, we show that the majority of rearrangements have occurred in the B. tabaci lineage, coinciding with an increase in the rate of nucleotide substitutions, a proliferation of short tandem repeats (microsatellites) in intergenic regions, and the loss of many widely conserved genes involved in DNA replication, recombination, and repair. These results indicate that the loss of recombinational machinery is unlikely to be the cause of the extreme structural conservation that is generally observed in obligate endosymbiont genomes and that large, repetitive intergenic regions are an important substrate for genomic rearrangements.

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Comparison of the Genome Sequences of “Candidatus Portiera aleyrodidarum” Primary Endosymbionts of the Whitefly Bemisia tabaci B and Q Biotypes

Cited by 26 publications

References 15 publications

The draft genome of whitefly Bemisia tabaci MEAM1, a global crop pest, provides novel insights into virus transmission, host adaptation, and insecticide resistance

The draft genome of whitefly Bemisia tabaci MEAM1, a global crop pest, provides novel insights into virus transmission, host adaptation, and insecticide resistance

Shared Metabolic Pathways in a Coevolved Insect-Bacterial Symbiosis

The Evolution of Genomic Instability in the Obligate Endosymbionts of Whiteflies

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