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• W4313379953 abstract "HomePlant DiseaseVol. 107, No. 3Draft Genome Sequence Resource of CBPPT1, a ‘Candidatus Phytoplasma trifolii’-Related Strain Associated with Potato Purple Top Disease in the Columbia Basin, U.S.A. PreviousNext RESOURCE ANNOUNCEMENT OPENOpen Access licenseDraft Genome Sequence Resource of CBPPT1, a ‘Candidatus Phytoplasma trifolii’-Related Strain Associated with Potato Purple Top Disease in the Columbia Basin, U.S.A.Wei Wei, Jonathan Shao, Kristi D. Bottner-Parker, and Yan ZhaoWei Weihttps://orcid.org/0000-0003-3561-913XMolecular Plant Pathology Laboratory, USDA-ARS, Beltsville, MD 20705Search for more papers by this author, Jonathan ShaoStatistics Group, Northeast Area Bioinformatics, USDA-ARS, Beltsville, MD 20705Search for more papers by this author, Kristi D. Bottner-ParkerMolecular Plant Pathology Laboratory, USDA-ARS, Beltsville, MD 20705Search for more papers by this author, and Yan Zhao†Corresponding author: Y. Zhao; E-mail Address: [email protected]https://orcid.org/0000-0002-0032-7535Molecular Plant Pathology Laboratory, USDA-ARS, Beltsville, MD 20705Search for more papers by this authorAffiliationsAuthors and Affiliations Wei Wei1 Jonathan Shao2 Kristi D. Bottner-Parker1 Yan Zhao1 † 1Molecular Plant Pathology Laboratory, USDA-ARS, Beltsville, MD 20705 2Statistics Group, Northeast Area Bioinformatics, USDA-ARS, Beltsville, MD 20705 Published Online:31 Dec 2022https://doi.org/10.1094/PDIS-08-22-1788-AAboutSectionsPDF ToolsAdd to favoritesDownload CitationsTrack Citations ShareShare onFacebookTwitterLinked InRedditEmailWechat Phytoplasmas are a large group of phloem-inhabiting, insect-transmitted plant pathogenic bacteria lacking a cell wall. They are etiological agents of diseases affecting more than a thousand plant species (Gasparich et al. 2020). Having descended from an ancestral gram-positive, low G + C walled bacterium, phytoplasmas underwent rapid evolution through substantial genome size reduction and recurrent horizontal gene acquisition (Wei et al. 2008; Zhao et al. 2014). Due to loss of many essential genes encoding diverse biosynthetic pathways (Kube et al. 2012; Oshima et al. 2004), phytoplasmas possess limited metabolic capacities and have a strong host dependency. Despite numerous attempts, pure phytoplasma culture has yet to be established in cell-free media. Although extant phytoplasmas have the same habitat specificity and life mode (Zhao et al. 2015) and comprise a monophyletic clade in 16S rRNA gene sequence-based phylogeny, the breadth of their genetic diversity is remarkable (Zhao et al. 2010). As unculturable bacteria, phytoplasmas are currently accommodated in a provisional genus ‘Candidatus Phytoplasma’ (The IRPCM Phytoplasma/Spiroplasma Working Team-Phytoplasma Taxonomy Group 2004). To date, 48 ‘Candidatus Phytoplasma’ species have been formally described (Wei and Zhao 2022). Phytoplasmas are also classified into groups and subgroups based on collective actual enzymatic (Lee et al. 1993, 1998) or computer-simulated (Wei et al. 2007) restriction fragment length polymorphism (RFLP) profiles of their 16S rRNA genes. Thirty-seven such groups have been established in the classification scheme (Jones et al. 2021; Wei and Zhao 2022), with each group containing at least one ‘Candidatus Phytoplasma’ species. Potato purple top (PPT) is a worldwide-occurring potato disease complex attributed to infection by phytoplasmas. Common symptoms of the disease include purple discoloration of terminal shoots and formation of aerial tubers. Affected plants often wilt and die prematurely, causing substantial tuber yield and quality losses (Munyaneza et al. 2005). At least five mutually distinct ‘Candidatus Phytoplasma’ species, including ‘Ca. P. asteris’, ‘Ca. P. aurantifolia’, ‘Ca. P. pruni’, ‘Ca. P. trifolii’, and ‘Ca. P. americanum’, have been linked to PPT disease incidences that have occurred in various geographic areas (Lee et al. 2004, 2006; Santos-Cervantes et al. 2010). The Columbia Basin potato purple top (CBPPT) phytoplasma is the etiological agent responsible for the PPT epidemics that repeatedly occurred in the Pacific Northwest region of the U.S. since 2002 (Munyaneza et al. 2005). The CBPPT phytoplasma is a ‘Ca. P. trifolii’-related strain and is classified in the clover proliferation phytoplasma (CP) group, subgroup A (16SrVI-A). The phytoplasma has a broad plant host range and is capable of infecting potato, tomato, broccoli, carrot, radish, and many other vegetable crops (Lee et al. 2004, 2006; Santos-Cervantes et al. 2010). Since the CBPPT phytoplasma induces virescence symptoms in several hosts and is transmitted from plant to plant by beet leafhopper (Circulifer tenellus, Munyaneza et al. 2010), it has a trivial name, beet leafhopper-transmitted virescence agent or BLTVA.The CBPPT phytoplasma and its alternative host, tomato, have been used as a model system to study phytoplasma–host interactions. Studies revealed that (i) a single infection of the CBPPT phytoplasma was able to induce multiple mutually distinct symptoms in tomato sequentially and (ii) the symptom type on a given branch varied depending on the developmental stage of the apex when it became affected by the phytoplasma (Wei et al. 2013, 2019). Such findings led to a hypothesis that phytoplasma infection can derail the genetically preprogrammed fate of a developing meristem, thereby changing the growth pattern and morphology of the host (Wei et al. 2013). Conceivably, phytoplasma pathogenesis is a multifaceted process that involves complex interactions between the pathogen and its plant host. Previous studies in our laboratory suggested that, in CBPPT phytoplasma-infected tomato plants, the homeostasis of auxin, cytokinin, and gibberellin was disrupted, as the biosynthesis, signaling, and distribution of these phytohormones were altered. Studies also revealed that CBPPT phytoplasma infection in tomato significantly changed the expression profiles of numerous genes including defense-related genes, key meristem switching genes, bioactive gibberellin synthesis genes, marker genes involved in premature leaf senescence, and axillary bud release (Ding et al. 2013; Wei et al. 2013; Wei and Zhao 2022). However, it remains unknown what pathogenicity factor(s) the CBPPT phytoplasma possesses and how these factors trigger the above- observed host responses. As the first step toward answering these questions, the genome of a representative strain of the CBPPT phytoplasma, CBPPT1, was sequenced.The phytoplasma strain CBPPT1 was originally identified in diseased potato plants growing in Washington State (Lee et al. 2004) and was transmitted to Madagascar periwinkle (Catharanthus roseus) via dodder (Cuscuta campestris), a parasitic vine. Once established in periwinkle, the strain was maintained in a greenhouse via serial shoot graft transmission. Over the years, the phytoplasma has consistently induced the same set of characteristic symptoms in the experimental host, indicating its pathogenicity remains essentially unchanged. Infected periwinkle shoots exhibiting phyllody symptom were used for genomic DNA extraction using a modified DNA extraction protocol as described by Lee et al. (1991). The DNA was sent to BGI-Americas for library construction and sequencing on the Illumina HiSeq 4000 platform. A total of 468,647,184 clean reads, with an average length of 150 bp (Q20 = 96.19%), were obtained. Genome assembly and analysis were performed at the USDA-ARS’ in-house bioinformatics facility. The phytoplasma reads were separated from the plant host reads by mapping the reads to available phytoplasma genomes using the bowtie2 program (v2.4.5, Langmead and Salzberg 2012). All completed and draft phytoplasma genomes in the National Center for Biotechnology Information (NCBI) BioProject database (https://www.ncbi.nlm.nih.gov/bioproject/) were used in the mapping. The assembly was performed using the Velvet assembler (v1.2.10, Zerbino and Birney 2008) and the SPAdes assembler (v3.14.0, Prjibelski et al. 2020). The phytoplasma contigs were further verified based on their nucleotide sequence identity scores with previously sequenced phytoplasma genomes using the BLASTN program.The assembled draft genome of CBPPT1 consists of 71 contigs totaling 512,902 bp with an average coverage of 1,434 and an N50 value of 78,175. Approximately 90% of the assembled sequences are in the 10 largest contigs. The G + C content of the CBPPT1 draft genome is 22.62%. One RNA operon and 26 tRNA genes were identified using software Barrnap (v0.8) and tRNAscan (v1.4), respectively (Fichant and Burks 1991; Seemann 2013). The rRNA gene sequence of CBPPT1 shares 99.61% sequence identity with that of CP (AY390261), the reference strain of ‘Ca. P. trifolii’ and the representative strain of group 16SrVI, confirming CBPPT1 is a ‘Ca. P. trifolii’-related strain. The CBPPT1 is the first ‘Ca. P. trifolii’-related strain and the first 16SrVI phytoplasma whose genome is sequenced.The completeness of the CBPPT1 draft genome assembly was assessed by examining the presence of benchmarking universal single-copy orthologs using software BUSCO v5 (Manni et al. 2021). The obtained BUSCO score, 62.1%, was then compared with those of complete phytoplasma genomes. Currently, there are 12 complete phytoplasma genomes available for comparative analysis, and the BUSCO scores of these genomes range from 58.9 to 63.9%, with an average of 61.2%. It is reasonable to conclude that the CBPPT1 draft genome is near completion as its BUSCO score is above the average score of the 12 complete phytoplasma genomes.Protein coding genes (CDS) were predicted using Genemark (v3.36) and the gene annotation was performed using the BLASTP program against the nr database at the NCBI and the Blast2GO module of the OmicsBox (v2.0.36, BioBam Bioinformatics 2019). A total of 554 CDS were predicted. Among them, 442 were assigned to at least one gene ontology (GO) term, and 402 were assigned to InterPro functional categories.The genome size of different phytoplasmas varies, ranging from 530 to 1,350 kbp (Marcone et al. 1999). Apparently, the genome size of CBPPT1 is at the low end of the spectrum. Consistent with its small size, it has only one rRNA operon and possesses much less repetitive genes when compared with other phytoplasmas such as ‘Ca. P. asteris’-related strain OYM (Oshima et al. 2004) and ‘Ca. P. australiense’-related strain SLY (Andersen et al. 2013). Nevertheless, the CBPPT1 genome contains multiple putative pathogenicity genes (Table 1) including those encoding homologs of SAP54 and SAP05, which are known phytoplasma virulence factors (effectors) responsible for phyllody and witches’-broom symptoms, respectively (Huang et al. 2021; MacLean et al. 2014). Among other putative CBPPT1 pathogenicity genes are those encoding more than a dozen secretory proteins, most of which belong to the SVM family (Table 1). In genomes of other phytoplasmas, SVM protein genes often reside in prophage-derived pathogenicity islands (Wei et al. 2008).Table 1. Putative effectors and other secretory proteins encoded by the CBPPT1 genomeLocus tagContig no.Length (aa)AnnotationM8044_0001532152Immunodominant membrane proteinM8044_0003626256Hypothetical proteinM8044_0003876200Hypothetical protein (SAP09-like)M8044_000392690SVM family protein (SAP44-like)M8044_0004661043Hypothetical proteinM8044_00048313125Phytoplasma effector causing phyllody symptoms (SAP54-like)M8044_00048413774ATP-dependent Zn proteaseM8044_0004931568SVM family proteinM8044_00049415111SVM family proteinM8044_00050817125SVM family proteinM8044_00050917259SVM family proteinM8044_00051822158Putative secreted protein (SAP42-like)M8044_00051922188SVM family proteinM8044_00053029188SVM family protein (SAP19-like)M8044_0005353687Hypothetical protein (SAP53-like)M8044_00053639125Hypothetical protein (SAP05-like)Table 1. Putative effectors and other secretory proteins encoded by the CBPPT1 genomeView as image HTML Since CBPPT phytoplasma is capable of inducing multiple mutually distinct and developmental stage-dependent symptoms in the host, the phytoplasma may possess multiple pathogenicity factors and each could interact with host component(s) in a stage-specific manner, leading to distinct symptoms as previously postulated (Wei et al. 2019). We hope the draft CBPPT1 genome sequence can serve as a resource for the search for and eventual identification of such pathogenicity factors.Data AvailabilityThe draft genome sequence data of the ‘Candidatus Phytoplasma trifolii’-related strain CBPPT1 have been uploaded to the NCBI’s BioProject database under accession number PRJNA839414. The annotated sequence has been deposited in the GenBank under accession number JANHJP000000000.The author(s) declare no conflict of interest.Literature CitedAndersen, M. T., Liefting, L. W., Havukkala, I., and Beever, R. 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The American Phytopathological Society, 2022.FundingU.S. Department of Agriculture, Agricultural Research ServiceKeywordsBLTVAclover proliferation groupgenomephytoplasmapotato purple topThe author(s) declare no conflict of interest.PDF download" @default.
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