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      An effector from the Huanglongbing-associated pathogen targets citrus proteases

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          Abstract

          The citrus industry is facing an unprecedented challenge from Huanglongbing (HLB). All cultivars can be affected by the HLB-associated bacterium ‘Candidatus Liberibacter asiaticus’ ( CLas) and there is no known resistance. Insight into HLB pathogenesis is urgently needed in order to develop effective management strategies. Here, we use Sec-delivered effector 1 (SDE1), which is conserved in all CLas isolates, as a molecular probe to understand CLas virulence. We show that SDE1 directly interacts with citrus papain-like cysteine proteases (PLCPs) and inhibits protease activity. PLCPs are defense-inducible and exhibit increased protein accumulation in CLas-infected trees, suggesting a role in citrus defense responses. We analyzed PLCP activity in field samples, revealing specific members that increase in abundance but remain unchanged in activity during infection. SDE1-expressing transgenic citrus also exhibit reduced PLCP activity. These data demonstrate that SDE1 inhibits citrus PLCPs, which are immune-related proteases that enhance defense responses in plants.

          Abstract

          Greening disease threatens the productivity of citrus crops worldwide yet the pathosystem is poorly understood. Here, Clark et al. show that an effector cloned from the associated bacteria can suppress host plant papain-like cysteine proteases' activity, suggesting its probable role in pathogenesis.

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          Most cited references43

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          The Proteomics Identifications (PRIDE) database and associated tools: status in 2013

          The PRoteomics IDEntifications (PRIDE, http://www.ebi.ac.uk/pride) database at the European Bioinformatics Institute is one of the most prominent data repositories of mass spectrometry (MS)-based proteomics data. Here, we summarize recent developments in the PRIDE database and related tools. First, we provide up-to-date statistics in data content, splitting the figures by groups of organisms and species, including peptide and protein identifications, and post-translational modifications. We then describe the tools that are part of the PRIDE submission pipeline, especially the recently developed PRIDE Converter 2 (new submission tool) and PRIDE Inspector (visualization and analysis tool). We also give an update about the integration of PRIDE with other MS proteomics resources in the context of the ProteomeXchange consortium. Finally, we briefly review the quality control efforts that are ongoing at present and outline our future plans.
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            SMART: recent updates, new developments and status in 2015

            SMART (Simple Modular Architecture Research Tool) is a web resource (http://smart.embl.de/) providing simple identification and extensive annotation of protein domains and the exploration of protein domain architectures. In the current version, SMART contains manually curated models for more than 1200 protein domains, with ∼200 new models since our last update article. The underlying protein databases were synchronized with UniProt, Ensembl and STRING, bringing the total number of annotated domains and other protein features above 100 million. SMART's ‘Genomic’ mode, which annotates proteins from completely sequenced genomes was greatly expanded and now includes 2031 species, compared to 1133 in the previous release. SMART analysis results pages have been completely redesigned and include links to several new information sources. A new, vector-based display engine has been developed for protein schematics in SMART, which can also be exported as high-resolution bitmap images for easy inclusion into other documents. Taxonomic tree displays in SMART have been significantly improved, and can be easily navigated using the integrated search engine.
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              SMART, a simple modular architecture research tool: identification of signaling domains.

              Accurate multiple alignments of 86 domains that occur in signaling proteins have been constructed and used to provide a Web-based tool (SMART: simple modular architecture research tool) that allows rapid identification and annotation of signaling domain sequences. The majority of signaling proteins are multidomain in character with a considerable variety of domain combinations known. Comparison with established databases showed that 25% of our domain set could not be deduced from SwissProt and 41% could not be annotated by Pfam. SMART is able to determine the modular architectures of single sequences or genomes; application to the entire yeast genome revealed that at least 6.7% of its genes contain one or more signaling domains, approximately 350 greater than previously annotated. The process of constructing SMART predicted (i) novel domain homologues in unexpected locations such as band 4.1-homologous domains in focal adhesion kinases; (ii) previously unknown domain families, including a citron-homology domain; (iii) putative functions of domain families after identification of additional family members, for example, a ubiquitin-binding role for ubiquitin-associated domains (UBA); (iv) cellular roles for proteins, such predicted DEATH domains in netrin receptors further implicating these molecules in axonal guidance; (v) signaling domains in known disease genes such as SPRY domains in both marenostrin/pyrin and Midline 1; (vi) domains in unexpected phylogenetic contexts such as diacylglycerol kinase homologues in yeast and bacteria; and (vii) likely protein misclassifications exemplified by a predicted pleckstrin homology domain in a Candida albicans protein, previously described as an integrin.
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                Author and article information

                Contributors
                glcoaker@ucdavis.edu
                wenbo.ma@ucr.edu
                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group UK (London )
                2041-1723
                30 April 2018
                30 April 2018
                2018
                : 9
                : 1718
                Affiliations
                [1 ]ISNI 0000 0001 2222 1582, GRID grid.266097.c, Department of Microbiology and Plant Pathology, , University of California, ; Riverside, 92521 CA USA
                [2 ]ISNI 0000 0004 1936 9684, GRID grid.27860.3b, Department of Plant Pathology, , University of California, ; Davis, 95616 CA USA
                [3 ]ISNI 0000 0001 2222 1582, GRID grid.266097.c, Center for Plant Cell Biology, , University of California, ; Riverside, 92521 CA USA
                [4 ]ISNI 0000 0004 1936 8091, GRID grid.15276.37, Citrus Research and Education Center, , University of Florida, ; Lake Alfred, 33850 FL USA
                [5 ]ISNI 0000 0004 4687 2082, GRID grid.264756.4, Citrus Center, , Texas A&M University, ; Weslaco, 78599 TX USA
                [6 ]ISNI 0000 0001 2222 1582, GRID grid.266097.c, Department of Chemistry, , University of California, ; Riverside, 92521 CA USA
                [7 ]ISNI 0000 0004 1936 8948, GRID grid.4991.5, University of Oxford, ; Oxford, OX1 2JD UK
                [8 ]ISNI 0000 0001 0701 1077, GRID grid.412531.0, Present Address: College of Life and Environmental Sciences, , Shanghai Normal University, ; Shanghai, 200234 China
                Author information
                http://orcid.org/0000-0003-1969-4148
                http://orcid.org/0000-0001-7743-0728
                http://orcid.org/0000-0003-0899-2449
                http://orcid.org/0000-0001-5569-639X
                Article
                4140
                10.1038/s41467-018-04140-9
                5928222
                29712915
                90aa4284-a539-47b6-af9d-43b65108b834
                © The Author(s) 2018

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 8 December 2017
                : 6 April 2018
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