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      Protein interaction networks at the host–microbe interface in Diaphorina citri, the insect vector of the citrus greening pathogen

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          The Asian citrus psyllid ( Diaphorina citri) is the insect vector responsible for the worldwide spread of ‘ Candidatus Liberibacter asiaticus’ (CLas), the bacterial pathogen associated with citrus greening disease. Developmental changes in the insect vector impact pathogen transmission, such that D. citri transmission of CLas is more efficient when bacteria are acquired by nymphs when compared with adults. We hypothesize that expression changes in the D. citri immune system and commensal microbiota occur during development and regulate vector competency. In support of this hypothesis, more proteins, with greater fold changes, were differentially expressed in response to CLas in adults when compared with nymphs, including insect proteins involved in bacterial adhesion and immunity. Compared with nymphs, adult insects had a higher titre of CLas and the bacterial endosymbionts Wolbachia, Profftella and Carsonella. All Wolbachia and Profftella proteins differentially expressed between nymphs and adults are upregulated in adults, while most differentially expressed Carsonella proteins are upregulated in nymphs. Discovery of protein interaction networks has broad applicability to the study of host–microbe relationships. Using protein interaction reporter technology, a D. citri haemocyanin protein highly upregulated in response to CLas was found to physically interact with the CLas coenzyme A (CoA) biosynthesis enzyme phosphopantothenoylcysteine synthetase/decarboxylase. CLas pantothenate kinase, which catalyses the rate-limiting step of CoA biosynthesis, was found to interact with a D. citri myosin protein. Two Carsonella enzymes involved in histidine and tryptophan biosynthesis were found to physically interact with D. citri proteins. These co-evolved protein interaction networks at the host–microbe interface are highly specific targets for controlling the insect vector responsible for the spread of citrus greening.

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          Most cited references 60

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          The Phyre2 web portal for protein modeling, prediction and analysis.

          Phyre2 is a suite of tools available on the web to predict and analyze protein structure, function and mutations. The focus of Phyre2 is to provide biologists with a simple and intuitive interface to state-of-the-art protein bioinformatics tools. Phyre2 replaces Phyre, the original version of the server for which we previously published a paper in Nature Protocols. In this updated protocol, we describe Phyre2, which uses advanced remote homology detection methods to build 3D models, predict ligand binding sites and analyze the effect of amino acid variants (e.g., nonsynonymous SNPs (nsSNPs)) for a user's protein sequence. Users are guided through results by a simple interface at a level of detail they determine. This protocol will guide users from submitting a protein sequence to interpreting the secondary and tertiary structure of their models, their domain composition and model quality. A range of additional available tools is described to find a protein structure in a genome, to submit large number of sequences at once and to automatically run weekly searches for proteins that are difficult to model. The server is available at A typical structure prediction will be returned between 30 min and 2 h after submission.
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            ProteomeXchange provides globally co-ordinated proteomics data submission and dissemination

            To the Editor There is a growing trend towards public dissemination of proteomics data, which is facilitating the assessment, reuse, comparative analyses and extraction of new findings from published data 1, 2 . This process has been mainly driven by journal publication guidelines and funding agencies. However, there is a need for better integration of public repositories and coordinated sharing of all the pieces of information needed to represent a full mass spectrometry (MS)–based proteomics experiment. Your July 2009 editorial “Credit where credit is overdue” 3 exposed the situation in the proteomics field, where full data disclosure is still not common practise. Olsen and Mann 4 identified different levels of information in the typical experiment, starting from raw data and going through peptide identification and quantification, protein identifications and ratios and the resulting biological conclusions. All of these levels should be captured and properly annotated in public databases, using the existing MS proteomics repositories for the MS data (raw data, identification and quantification results) and metadata, whereas the resulting biological information should be integrated in protein knowledgebases, such as UniProt 5 . A recent editorial in Nature Methods 6 again highlighted the need for a stable repository for raw MS proteomics data. In this Correspondence, we report on the first implementation of the ProteomeXchange consortium, an integrated framework for submission and dissemination of MS-based proteomics data. Among the existing MS proteomics repositories with a broad target audience, the PRIDE (PRoteomics IDEntifications) database 7 (European Bioinformatics Institute, EBI, Cambridge, UK; and PeptideAtlas 8 (Institute for Systems Biology, ISB, Seattle, USA; are two of the most prominent. Both are mainly focused on tandem MS (MS/MS) data storage. Whereas PRIDE represents the information as originally analysed by the researcher (thus constituting a primary resource), data in PeptideAtlas are reprocessed through a common pipeline (the Trans-Proteomic Pipeline) to provide a uniformly analyzed view on the data with a focus on low protein false discovery rates (constituting a secondary resource). In addition, ISB has set up the first repository for SRM data, PASSEL 9 (PeptideAtlas SRM Experiment Library, There are other resources dedicated to storing MS proteomics data, each of them with different focuses and functionalities, for instance GPMDB (where data are reprocessed using the search engine X!Tandem) 10 . At a higher abstraction level, resources like UniProt and neXtProt are integrating proteomics results into a wider context of functional annotation from many different sources, including antibody-based methods. Although most of the proteomics resources mentioned have existed for a long time, they have acted independently with limited coordination of their activities. As a result, data providers were unclear to which repository they should submit their dataset, and in what form, with choices ranging from full raw data to highly processed identifications and quantifications. In addition, no repository could store both raw data and results. Similar issues arose for data consumers, who could not always find the data supporting a protein modification in UniProt, or know whether a particular dataset from PRIDE had been integrated into PeptideAtlas. The ProteomeXchange (PX) consortium ( was formed in 2006 (ref. 11) to overcome these challenges, developing from a loose collaboration into an international consortium of major stakeholders in the domain, comprising, among others, primary (PRIDE, PASSEL) and secondary resources (PeptideAtlas, UniProt), proteomics bioinformaticians, investigators (including some involved in the HUPO Human Proteome Project), and representatives from journals regularly publishing proteomics data (Supplementary Notes, section 7). The aim of the ProteomeXchange consortium is to provide a common framework and infrastructure for the cooperation of proteomics resources by defining and implementing consistent, harmonised, user-friendly data deposition and exchange procedures among the major public proteomics repositories. ProteomeXchange provides unified data submission for multiple MS data types and delivers different ‘views’ of the deposited data, such as the raw data suitable for reprocessing, the author-generated identifications and highly filtered composite results in resources like UniProt, all linked by a universal shared identifier. Authors are able to cite the resulting ProteomeXchange accession number for datasets reported in their publications. As such, a dataset (with appropriate metadata) is becoming publishable per se and can be tracked if used by various consumers in different publications. Individual resources can join ProteomeXchange by implementing the ProteomeXchange data submission and dissemination guidelines, and metadata requirements. In the current version (, the mandatory information comprises: (i) mass spectrometer output files (raw data, either in a binary format, or in a standard open format such as mzML); (ii) processed identification results (two submission modes are available, see below); and (iii) sufficient metadata to provide a suitable biological and technological background, including method information such as transition lists in the case of SRM data. Other types of information, such as peak list files (processed versions of mass spectra most often used in the identification process) and quantification results can also be provided. Two main MS proteomics workflows are now fully supported: tandem MS and SRM data (Fig. 1 and Supplementary Fig. 1). PRIDE acts as the initial submission point for MS/MS data, whereas PASSEL is the initial submission point for SRM data. It is expected that in most cases, one ProteomeXchange dataset will correspond to data from one publication, and it will be clearly linked to it. However, this concept is flexible and a mechanism for grouping different ProteomeXchange datasets is also available, for example for large-scale collaborative studies. At present, two different submission modes are available for MS/MS data: - ‘Complete submission’: this requires peptide and protein identification results to be fully supported and integrated in the receiving repository (PRIDE at present). The search engine output files (plus the associated spectra) must therefore first be converted to PRIDE XML or mzIdentML format (a process supported by several popular and user-friendly tools, Supplementary Notes, section 5). Complete submissions make the data fully available for querying, and thus maximise the potential for data re-use in MS. This in turn increases the visibility of the associated publication. A DOI (Digital Object Identifier) is assigned to each dataset, allowing formalized credit to be given to submitters and their principal investigators, through a citation index, as proposed in your editorial 3 . - ‘Partial submission’: For these submissions, peptide or protein identification results cannot be integrated in PRIDE because data converters and exporters to the supported formats are not yet available. In this case, search engine output files can be directly provided in their original format. Although partial submissions are searchable by their metadata, they are not fully searchable by results such as protein identifiers, and will not receive a DOI. However, partial submissions are important as they allow data from novel experimental approaches to be deposited into the ProteomeXchange resources, rather than having to reject these until the workflows have been mapped into a representation in PRIDE or another ProteomeXchange partner. For the submission of MS/MS datasets, a stand-alone, open-source Java tool has been made available, the ‘ProteomeXchange submission tool’ ( (Supplementary Notes section 5, Supplementary Figs. 2–10). The tool allows interactive submission of small datasets as well as large- scale batch submissions. For SRM datasets, a web form ( can be used for submission to PASSEL. Similar to the guidelines stated above for MS/MS datasets, PASSEL submissions require mass spectrometer output files, study metadata, peptide reagents, analysis result files and the actual SRM transition lists, the information that drives the instrument data acquisition. Once datasets are submitted, they are checked by a curator and then loaded into the main PASSEL database, which facilitates interactive exploration of the data and results. The submitted information and files can selectively be made available to journal editors and reviewers during manuscript peer review. Once the manuscript is accepted for publication or the submitter informs the receiving repository directly, the data will be publicly released (Fig. 1). At this point, the availability of the dataset, as well as basic metadata, will be disseminated through a public RSS feed ( The RSS feed includes a link to an XML message (ProteomeXchange XML), which is created by the receiving repository (Supplementary Notes, section 3), and made available from ProteomeCentral, the portal for all public ProteomeXchange datasets ( (Supplementary Notes, section 2). Repositories such as PeptideAtlas or GPMDB as well as any interested end users can subscribe to this RSS feed and trigger actions, including incorporation of the data into local resources, re-processing or biological analysis. This reprocessing is already occurring in practice. For example, two ProteomeXchange datasets (PXD000134 and PXD000157) have been used in the latest build of the human proteome in PeptideAtlas, and PXD000013 (ref. 12) was reprocessed and nominated as technical dataset of the year 2012 by GPMDB ( - 201210071). ProteomeXchange started to accept regular submissions in June 2012. By the beginning of August 2013, 373 ProteomeXchange datasets have been submitted (consisting of 341 tandem MS and 32 SRM datasets, Fig. 2), a total of ~25 TB of data. The largest submission so far (currently still private) comprised 5 TB of data. For a current list of the publicly available datasets, see In summary, ProteomeXchange provides an infrastructure for efficient and reliable public dissemination of proteomics data, supporting crucial validation, analysis and reuse. By providing and linking different interpretations of the data we aim to maximise dataset visibility as well as their potential benefit to different communities. Citability and traceability are addressed through the assignment of DOIs and a common identifier space. The consortium is open to the participation of additional resources (Supplementary Notes, Section 9). Although all repositories depend on continuous funding for continuous operation, the ProteomeXchange core repositories PRIDE and PeptideAtlas are well established, with first publications in 2005 (ref. 7,8), and have strong institutional backing (Supplementary Notes, section 8), ensuring that the data will remain reliably available for the foreseeable future. We are confident that the ProteomeXchange infrastructure will support the growing trend towards public availability of proteomics data, maximising its benefit to the scientific community through increased ease of access, greater ability to re-assess interpretations and extract further biological insight, and greater citation rates for the submitters. Supplementary Material 1
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              Genomics and evolution of heritable bacterial symbionts.

              Insect heritable symbionts have proven to be ubiquitous, based on molecular screening of various insect lineages. Recently, molecular and experimental approaches have yielded an immensely richer understanding of their diverse biological roles, resulting in a burgeoning research literature. Increasingly, commonalities and intermediates are being discovered between categories of symbionts once considered distinct: obligate mutualists that provision nutrients, facultative mutualists that provide protection against enemies or stress, and symbionts such as Wolbachia that manipulate reproductive systems. Among the most far-reaching impacts of widespread heritable symbiosis is that it may promote speciation by increasing reproductive and ecological isolation of host populations, and it effectively provides a means for transfer of genetic information among host lineages. In addition, insect symbionts provide some of the extremes of cellular genomes, including the smallest and the fastest evolving, raising new questions about the limits of evolution of life.

                Author and article information

                R Soc Open Sci
                R Soc Open Sci
                Royal Society Open Science
                The Royal Society Publishing
                February 2017
                8 February 2017
                8 February 2017
                : 4
                : 2
                [1 ]Robert W. Holley Center for Agriculture and Health, Emerging Pests and Pathogens Research Unit, USDA Agricultural Research Service , Ithaca, NY, USA
                [2 ]Boyce Thompson Institute for Plant Research , Ithaca, NY, USA
                [3 ]Department of Genome Sciences, University of Washington , Seattle, WA, USA
                [4 ]Plant Pathology Department, Faculty of Agriculture, Tarbiat Modares University , Tehran, Iran
                [5 ]US Horticultural Research Laboratory, Subtropical Insects and Horticulture Research Unit, USDA Agricultural Research Service , Ft. Pierce, FL, USA
                [6 ]Plant Pathology and Plant-Microbe Biology Section, School of Integrative Plant Science, Cornell University , Ithaca, NY, USA
                Author notes
                Author for correspondence: J. S. Ramsey e-mail: jsr47@

                Electronic supplementary material is available online at

                © 2017 The Authors.

                Published by the Royal Society under the terms of the Creative Commons Attribution License, which permits unrestricted use, provided the original author and source are credited.

                Funded by: Citrus Research Board,;
                Award ID: 5300-155
                Award ID: 5300-163
                Funded by: USDA ARS;
                Award ID: 6034-22320-001-00
                Award ID: 8062-22000-021-00
                Cellular and Molecular Biology
                Research Article
                Custom metadata
                February, 2017


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