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. 2022 Apr 7;12(5):107. doi: 10.1007/s13205-022-03163-w

Draft genome sequence of ‘Candidatus Phytoplasma australasia’, strain SS02 associated with sesame phyllody disease

Hemavati Ranebennur 1, Kiran Kirdat 2, Bhavesh Tiwarekar 2, Kirti Rawat 1, V Celia Chalam 3, Amolkumar U Solanke 4, Rashmi Yadav 3, Kuldeep Singh 3, Shivaji Sathe 5, Amit Yadav 2,✉, G P Rao 1,✉
PMCID: PMC8989914  PMID: 35462955

Abstract

‘Candidatus Phytoplasma’ is an uncultivated, intracellular bacterial plant pathogen transmitted by phloem-feeding insect vectors. Among the group of phytoplasmas, the Peanut Witches' Broom or 16SrII group of phytoplasmas associated with various diseases cause severe crop losses every year in India. The ‘Ca. Phytoplasma sp.’ strain SS02 was associated with phyllody disease of sesame plants collected from New Delhi. The genome sequence of strain SS02 was obtained using its genomic DNA enrichment and hybrid assembly of sequences generated on Illumina and Oxford Nanopore Technologies MinION platforms. The hybrid assembly strategy generated a draft genome with 60 contigs totaling 553,228 bp of length with more than 400 × depth coverage and 95.21% of the estimated completeness. The SS02 genome draft sequence contains 465 protein-coding genes, 17 tRNA genes, and 3 rRNA genes. The availability of this draft genome also provided a foundation for genome-scale genotypic analyses.

Introduction

'Ca. Phytoplasma’ is an obligate plant pathogenic phloem-limited bacteria that lack the cell wall, the characteristic feature of the class Mollicutes (Phylum, Mycoplasmatota; formerly, Tenericutes). Many strains of 'Ca. Phytoplasma' were characterized at the genomic level; the prefix 'Candidatus Phytoplasma' is still retained due to the difficulty in growing them on the artificial medium. The phytoplasmas are associated with diseases in many crops like cereals, vegetables, fruits, oilseeds, legumes, plantations, ornamentals, and tree species in India (Rao et al. 2017). The Peanut Witches'Broom (PnWB) (16SrII-C and D) phytoplasma strains are widespread in India; reported in crops like soybean (Glycine max), papaya (Carica papaya), bamboo (Dendrocalamus strictus), rattle pods (Crotalaria juncea), mango (Mangifera indica), tomato (Lycopersicon esculentum), fodder crops like alfalfa (Medicago sativa), Napier Grass (Pennisetum purpureum), sesame (Sesamum indicum), fire cracker flower (Crossandra infundibuliformis), cowpea (Vigna unguiculata), and weeds like wild indigo (Tephrosia purpurea), tick weed (Cleome viscosa), silver cock's comb (Celosia argentea), cattle bush (Trichodesma zeylanicum), croton (Croton bonplandianum), Parthenium hysterophorus and many others with disease incidence ranging from 2 to 10% (Yadav et al. 2015a, b, 2016, 2014; Mahadevakumar et al. 2016; Thorat et al. 2016a, b, 2017a; Madhupriya et al. 2017; Rao et al. 2017; Kirdat et al. 2019, 2020c; Bhat et al. 2021; IRPCM 2004). Among these, sesame phyllody is responsible for a yield loss of up to 100% in severe cases (Rao et al. 2015). There are four phytoplasma groups (the Aster Yellows, 16SrI; PWB, 16SrII; Clover proliferation, 16SrVI and Apple proliferation,16SrIX) belonging to 'Ca. P. asteris', 'Ca. P. aurantifolia', 'Ca. P. sp.', 'Ca. P. trifolii' and 'Ca. P. phoenicium' are associated with sesame phyllody (Asghari Tazehkand et al. 2017; Catal et al. 2013; Dubey et al. 2015; Saheli et al. 2021; Venkataravanappa V et al. 2017). In India, phytoplasma groups, viz. 16SrI-B, 16SrII-C,16SrII-D, and 16SrVI-D were associated with sesame phyllody (Ikten et al. 2011; Rao et al. 2015; Thorat et al. 2017a; Phookan et al. 2019). The 16SrII-D group ('Ca. Phytoplasma sp.') is most abundantly associated with sesame phyllody and other pulse crops (Rao et al. 2017; Thorat et al. 2017b). So far, more than 40 phytoplasma strains have been genome sequenced, including four strains of 'Ca. P. aurantifolia' of PnWB group. Given the widespread occurrence of the 16SrII-D group of phytoplasmas in India, the genome sequence information of strain SS02 was obtained and discussed in the study.

DNA Preparation for Genome Sequencing Sesame (Sesamum indicum L.) plant samples exhibiting typical phyllody and witches' broom symptoms were collected from New Delhi, India. The genomic DNA was extracted from 100 mg of symptomatic leaf tissues by a CTAB method (Doyle 1990). The presence of phytoplasma was confirmed by amplifying the 16S rRNA gene using primers P1 (Deng and Hiruki 1991) and P7 (Schneider 1995) followed by a nested PCR with primers R16F2n and R16R2 (Gundersen and Lee 1996). The 16S rRNA gene sequences were obtained directly by sequencing using bacterial universal primers 343R, 704F, 907R, 1028F and 1492R (Baker et al. 2003) on ABI® 3730xl DNA Analyser. The assembled sequences were analyzed using the EzBioCloud database (Yoon et al. 2017) to search phylogenetically closest relative. Further, the strain SS02 was genome sequenced by the procedure described earlier (Kirdat et al. 2020a, b). Briefly, total nucleic acids were extracted from the strain SS02 plant sample and enriched for prokaryotic DNA selection using the NEBNext microbiome enrichment kit (Cat. No. E2612, New England BioLabs, USA). The enriched DNA of strain SS02 was amplified using illustra Ready-To-Go GenomiPhi V3 DNA amplification kits (Cat. No. 25–6601, GE Healthcare, USA). Following the manufacturer's instructions, it was sequenced on the Illumina NovaSeq 6000 platform. Simultaneously, the enriched and amplified DNA of SS02 strain was sequenced on the Oxford Nanopore Technology (ONT) MinION platform by following the manufacturer's instructions.

All Illumina reads were quality checked with FastQC v0.11.8 (Brown et al. 2017). The ONT sequencing data were base-called with quality filtering (> Q7) using GUPPY v3.5.4. All QC-passed Illumina reads (> Q30) were subjected to metagenomic assembly using MEGAHIT v1.1.3 (Li et al. 2016). This assembly was subjected to binning, using MetaBAT2 v2.12.1 (Kang et al. 2015). Raw reads were mapped on bins corresponding to phytoplasma. Additionally, Illumina reads were mapped on PnWB phytoplasma NTU2011 (AMWZ00000000) (Chung et al. 2013), 'Ca. P. aurantifolia' WBDL (MWKN00000000) and 'Ca. P. aurantifolia' NCHU2014 (CP040925) (Chang et al. 2015) genome sequences, using Bowtie2 v2.2.6 (Langmead and Salzberg 2012). Finally, all mapped reads and QC-passed ONT reads were used to generate the hybrid assembly in Unicycler v0.5.0 (Wick et al. 2017), followed by polishing using Pilon (Walker et al. 2014). Bin quality check, genome completeness, and taxonomic assignments were performed using CheckM v1.0.14 (Parks et al. 2015). Assembly quality was checked using QUAST v5.0.2 (Gurevich et al. 2013). The genome coverage was calculated using BBMap (Bushnell 2014). All scaffolds were used as the queries to run a BLASTX search against the GenBank non-redundant protein database to identify contaminating scaffolds. The genome was annotated using the NCBI Prokaryotic Genome Annotation Pipeline (PGAP) (Zhao et al. 2012). All contigs and raw sequencing data were deposited in the DDBJ/ENA/GenBank database with accession number JAHBAJ020000000 under the BioSample ID SAMN19066185 BioProject ID PRJNA727971. Further, the comparison of orthologous gene clusters among SS02, WBDL, NTU2011 and NCHU2014 genomes using OrthoVenn2 (Xu et al. 2019). The eggNOG-mapper v2 was used for functional annotation (Clusters of Orthologous Groups, COG) of the PGAP annotated proteins of SS02 and closely related strains viz. WBDL, NTU2011 and NCHU2014 genomes (Huerta-Cepas et al. 2019; Cantalapiedra et al. 2021).

The obtained 16S rRNA gene sequences of SS02 showed 98.76% similarity with the reference sequence of 'Ca. P. aurantifolia' strain WBDL (U15442) when analyzed on EzBioCloud database (Yoon et al. 2017). The genome sequencing of the strain SS02 resulted in 42,296,107 reads (150 × 2 chemistry) using the Illumina NovaSeq 6000 platform, while the ONT MinION sequencing data generated 33,607 reads. The final SS02 genome assembly contained 60 scaffolds corresponding to 553,228 bp in length. The estimated coverage for Illumina was 407x, while that for ONT was 4.3x. The completeness of assembly was 95.21% of the estimated genome size, and the GC content was 23.55%. The SS02 genome was predicted to have 465 protein-coding genes, 17 transfer RNA (tRNA), and one rRNA operon (Table 1). The COG functional category distribution of genes in the strain SS02 revealed approximately 106 (22.79%) genes for translation, ribosomal structure, and biogenesis, 51 (10.96%) genes for replication, recombination, and repair, and 31 (6.6%) genes were assigned for putative functions as the abundant assigned categories. Approximately 83 (17.84%) genes were categorized with transport mechanisms. The distribution of gene components between SS02 and its closely related strain genomes describe the similar composition of COG functional categories as shown in Fig. 1. Further, the Orthovenn analysis assigned 465 proteins into 412 clusters shared by the strain SS02 and closely related strains (WBDL, NTU2011and NCHU2014) and 53 singletons. Figure 2 shows overlapping cluster numbers shared between SS02 and closely related species.

Table 1.

Genome statistics of 'Ca. Phytoplasma sp.' strain SS02 (JAHBAJ020000000)

Genome statistics SS02 Tools used
Assembly Unicycler
Genome size in contigs (bp) 553,228 Quast
GC content (%) 23.55 Quast
Number of contigs 60 Quast
Contig N50 length (bp) 30,531 Quast
L50 7 Quast
Genome Coverage 407.962x BBMap
Annotation Tools used
Protein-coding genes 465 PGAP
Genome completeness (%) 95.21 CheckM
No. of tRNA genes 17 tRNAscan-SE
No. of rRNA genes 3 PGAP
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Fig. 1.

Fig. 1

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The COG functional category distribution of genes in SS02 and closely related strains, viz. WBDL, NTU201, and NCHU2014 using the eggNOG-mapper v2

Fig. 2.

Fig. 2

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Comparison of orthologous gene clusters among SS02, WBDL, NTU2011, and NCHU2014 genomes using OrthoVenn2

Acknowledgements

The authors are thankful to the Director, ICAR-Indian Agricultural Research Institute (IARI) and Director, ICAR-National Bureau of Plant Genetic Resources (NBPGR), New Delhi, for providing facilities.

Author contributions

HR and KR collected the samples and did the primitive identification of phytoplasma in sesame samples. KK prepared the DNA samples for Illumina sequencing and performed ONT sequencing. BT assembled and analyzed the SS02 genome. HR, GR, BT, and KK wrote the first manuscript draft. AY and AS edited the manuscript; CC, KS, GR, and AY provided the funding. AY supervised the sequencing bioinformatics analysis and finalized the manuscript draft. All authors read the final draft and approved it.

Funding

The authors acknowledge the funding support by the Department of Biotechnology (DBT), Govt. of India, New Delhi, under the project BT/Ag/Network/Sesame/2019-20.

Data availability

The Whole Genome Shotgun sequence for strain SS02 have been deposited in the DDBJ/ENA/GenBank database under accession numbers JAHBAJ000000000. The version described in this paper is JAHBAJ020000000 under the BioSample ID SAMN19066185 and BioProject ID PRJNA727971.

Declarations

Conflict of interest

The authors declare no conflict of interest.

Footnotes

The first three authors Hemavati Ranebennur, Kiran Kirdat and Bhavesh Tiwarekar have contributed equally.

Contributor Information

Amit Yadav, Email: amityadav@nccs.res.in.

G. P. Rao, Email: gprao_gor@rediffmail.com

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

The Whole Genome Shotgun sequence for strain SS02 have been deposited in the DDBJ/ENA/GenBank database under accession numbers JAHBAJ000000000. The version described in this paper is JAHBAJ020000000 under the BioSample ID SAMN19066185 and BioProject ID PRJNA727971.

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