Skip to main content
SpringerLink
Log in

Comparative genomic analysis of subspecies of Pantoea stewartii reveals distinct variations

  • Original Article
  • Published:
Journal of Plant Pathology Aims and scope Submit manuscript

Abstract

Pantoea stewartii subsp. stewartii (Pnss) and P. stewartii subsp. indologenes (Pnsi) are closely related plant pathogens that differ in their host specificities. Pnss is the causal agent of Stewart’s wilt of corn, whereas Pnsi causes disease on millets but not corn. Comparative genomics is a valuable method for characterizing the differences between genomes, but there are few studies on this important quarantine pathogen. Here, we compared publicly available genomes of seven strains of Pnss and three strains of Pnsi. Pan- and core-genome analyses showed that strains isolated from close geographical regions are more similar in their genome structures. Gene content and collinearity analyses further revealed numerous strain-specific genes. In particular, the Pnss type strain DC283 contained over 1200 additional genes compared with other strains. Importantly, we also identified eleven genes that are only present in Pnsi genomes and thus may be useful to distinguish between Pnss and Pnsi strains. Overall, this study characterized the common and distinct genomic features of Pnss and Pnsi, which lay the foundation for future development of molecular methods to detect the Stewart’s wilt pathogen in maize for quarantine regulations and distinguish its two subspecies.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Addy HS, Askora A, Kawasaki T, Fujie M, Yamada T (2012a) The filamentous phage φRSS1 enhances virulence of Phytopathogenic Ralstonia solanacearum on tomato. Phytopathology 102:244–251

    Article  Google Scholar 

  • Addy HS, Askora A, Kawasaki T, Fujie M, Yamada T (2012b) Loss of virulence of the Phytopathogen Ralstonia solanacearum through infection by φRSM filamentous phages. Phytopathology 102:469–477

    Article  CAS  Google Scholar 

  • Braun EJ (1982) Ultrastructural investigation of resistant and susceptible maize inbreds infected with Erwinia stewartii. Phytopathology 72:159–166

    Article  Google Scholar 

  • Chen F, Mackey AJ, Stoeckert CJ Jr, Roos DS (2006) OrthoMCL-DB: querying a comprehensive multi-species collection of ortholog groups. Nucleic Acids Res 34:D363–D368

    Article  CAS  Google Scholar 

  • Comandatore F, Sassera D, Montagna M, Kumar S, Koutsovoulos G, Thomas G, Repton C, Babayan SA, Gray N, Cordaux R, Darby A, Makepeace B, Blaxter M (2013) Phylogenomics and analysis of shared genes suggest a single transition to mutualism in Wolbachia of nematodes. Genome Biol Evol 5:1668–1674

    Article  Google Scholar 

  • Coplin DL, Majerczak DR, Zhang YX, Kim WS, Jock S, Geider K (2002) Identification of Pantoea stewartii subsp. stewartii by PCR and strain differentiation by PFGE. Plant Dis 86:304–311

    Article  CAS  Google Scholar 

  • Coutinho TA, Venter SN (2009) Pantoea ananatis: an unconventional plant pathogen. Mol Plant Pathol 10:325–335

    Article  CAS  Google Scholar 

  • Darling ACE, Mau B, Blattner FR, Perna NT (2004) Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res 14:1394–1403

    Article  CAS  Google Scholar 

  • Daubin V, Moran NA, Ochman H (2003) Phylogenetics and the cohesion of bacterial genomes. Science 301:829–832

    Article  CAS  Google Scholar 

  • Fegan M, Prior P (2005) How complex is the Ralstonia solanacearum species complex. In: Allen C, Prior P, Hayward A (eds) Bacterial wilt disease and the Ralstonia solanacearum species complex. American Phytopathological Society, Madison, pp 449–461

    Google Scholar 

  • Gehring I, Geider K (2012) Identification of Erwinia species isolated from apples and pears by differential PCR. J Microbiol Methods 89:57–62

    Article  CAS  Google Scholar 

  • Gehring I, Wensing A, Gernold M, Wiedemann W, Coplin DL, Geider K (2014) Molecular differentiation of Pantoea stewartii subsp indologenes from subspecies stewartii and identification of new isolates from maize seeds. J Appl Microbiol 116:1553–1562

    Article  CAS  Google Scholar 

  • Genin S (2010) Molecular traits controlling host range and adaptation to plants in Ralstonia solanacearum. New Phytol 187:920–928

    Article  Google Scholar 

  • Kurtz S, Phillippy A, Delcher AL, Smoot M, Shumway M, Antonescu C, Salzberg SL (2004) Versatile and open software for comparing large genomes. Genome Biol 5:R12–R12

    Article  Google Scholar 

  • Lamka GL, Hill JH, Mcgee DC, Braun EJ (1991) Development of an immunosorbent assay for seed-borne Erwinia stewartii in corn seed. Phytopathology 81:839–846

    Article  Google Scholar 

  • Lefebure T, Stanhope MJ (2007) Evolution of the core and pan-genome of Streptococcus: positive selection, recombination, and genome composition. Genome Biol 8:R71–R71

    Article  Google Scholar 

  • Lerat E, Daubin V, Ochman H, Moran NA (2005) Evolutionary origins of genomic repertoires in bacteria. PLoS Biol 3:e130–e130

    Article  Google Scholar 

  • Li P, Wang DC, Yan JL, Zhou JN, Yue DY, Jiang ZD, Cao BH, He ZF, Zhang L-H (2016) Genomic analysis of phylotype I strain EP1 reveals substantial divergence from other strains in the Ralstonia solanacearum species complex. Front Microbiol 7:01719

    Google Scholar 

  • Mergaert J, Verdonck L, Kersters K (1993) Transfer of Erwinia ananas (synonym, Erwinia uredovora) and Erwinia stewartii to the genus Pantoea emend as Pantoea ananas (serrano 1928) comb. nov. and Pantoea stewartii (smith 1898) comb. nov., respectively, and description of Pantoea stewartii subsp indologenes subsp. nov. Int J Syst Bacteriol 43:162–173

    Article  Google Scholar 

  • Pataky J, Ikin R (2003a) Pest risk analysis : the risk of introducing Erwinia stewartii in maize seed. The Innternational Seed Federation, Nyon

    Google Scholar 

  • Pataky J, Ikin R (2003b) Pest risk analysis: the risk of introducing Erwinia stewartii in maize seed. The International Seed Federation, Nyon

    Google Scholar 

  • Peeters N, Guidot A, Vailleau F, Valls M (2013) Ralstonia solanacearum, a widespread bacterial plant pathogen in the post-genomic era. Mol Plant Pathol 14:651–662

    Article  CAS  Google Scholar 

  • Powell S, Szklarczyk D, Trachana K, Roth A, Kuhn M, Muller J, Arnold R, Rattei T, Letunic I, Doerks T, Jensen LJ, von Mering C, Bork P (2012) eggNOG v3.0: orthologous groups covering 1133 organisms at 41 different taxonomic ranges. Nucleic Acids Res 40:D284–D289

    Article  CAS  Google Scholar 

  • Prior P, Ailloud F, Dalsing BL, Remenant B, Sanchez B, Allen C (2016) Genomic and proteomic evidence supporting the division of the plant pathogen Ralstonia solanacearum into three species. BMC Genomics 17:90

    Article  Google Scholar 

  • Roper MC (2011) Pantoea stewartii subsp. stewartii: lessons learned from a xylem-dwelling pathogen of sweet corn. Mol Plant Pathol 12:628–637

    Article  CAS  Google Scholar 

  • Stumpf S, Kvitko B, Gitaitis R, Dutta B (2018) Isolation and characterization of novel Pantoea stewartii subsp. indologenes strains exhibiting center rot in onion. Plant Dis 102:727–733

    Article  CAS  Google Scholar 

  • Vernikos G, Medini D, Riley DR, Tettelin H (2015) Ten years of pan-genome analyses. Curr Opin Microbiol 23:148–154

    Article  CAS  Google Scholar 

  • Wensing A, Zimmermann S, Geider K (2010) Identification of the corn pathogen Pantoea stewartii by mass spectrometry of whole-cell extracts and its detection with novel PCR primers. Appl Environ Microbiol 76:6248–6256

    Article  CAS  Google Scholar 

  • Wu Q, Jiang Z, Liao J, Chen Z, Li H, Mei M, Zhang L-H (2007) Identification of genetic markers to distinguish the virulent and avirulent subspecies of Pantoea stewartii by comparative proteomics and genetic analysis. Appl Microbiol Biotechnol 74:186–193

    Article  CAS  Google Scholar 

  • Xu R, Chen Q, Robleh Djama Z, Tambong JT (2010) Miniprimer PCR assay targeting multiple genes: a new rapid and reliable tool for genotyping Pantoea stewartii subsp. stewartii. Lett Appl Microbiol 50:216–222

    Article  CAS  Google Scholar 

  • Zakham F, Aouane O, Ussery D, Benjouad A, Ennaji MM (2012) Computational genomics-proteomics and phylogeny analysis of twenty one mycobacterial genomes (tuberculosis & non tuberculosis strains). Microb Info Exp 2:7

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the State Key Laboratory for Conservation and Utilization of Subtropical Agro–bioresources (No. SKLCUSA–b201715). National Key Project for Basic Research of China (973 Program, No. 2015CB150600).

Author information

Authors and Affiliations

  1. Ministry of Education Key Laboratory for Ecology of Tropical Islands, Hainan Provincial Key Laboratory for Tropical Plant and Animal Ecology, College of Life Sciences, Hainan Normal University, Haikou, 571158, China

    Peng Li, Ying Zhang & Yuqingqing Sun

  2. Southwest Forestry University, Kunming, 650224, China

    Xingxing Wu

  3. Yunnan Forestry Technological College, Kunming, 670224, China

    Xingxing Wu

  4. Dehong Teachers’ College, Mangshi, 678400, China

    Zhiyuan Wang

  5. Integrative Microbiology Research Centre, Guangdong Province Key Laboratory of Microbial Signals and Disease Control, College of Agriculture, South China Agricultural University, Guangzhou, 510642, China

    Jianuan Zhou & Xiaofan Zhou

Authors
  1. Peng Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ying Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yuqingqing Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xingxing Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zhiyuan Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jianuan Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Xiaofan Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

PL and XZ designed the experiments, PL, YZ, YS, XY, ZY, and XZ analyzed the data and wrote the paper, XW, ZW, JZ and XZ revised the manuscript.

Corresponding authors

Correspondence to Peng Li or Xiaofan Zhou.

Ethics declarations

The authors declare no potential conflicts of interest, and the research involving no human participants and/or animals.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 16 kb)

SI Fig. 1

Nucleic acid co-linearity of strain DC283 vs strain M073a (A), RSA13 (B), A206 (C), and LMG2632 (D), respectively. The sequence of DC283 is ordered as the reference bacterium based on MUMmer 3.22, then the figure is generated by the Mauve rearrangement viewer. The upper and following axes of co-linear graph are constructed, and pairwised nucleic acid sequence of two alignments is marked in the coordinate diagram according to its position information. The locally collinear blocks (LSB) below a genome’s center line are in the reverse complement orientation relative to the reference genome. Lines between genomes trace each orthologous LCB through every genome. Large gray regions within an LCB signify the presence of lineage-specific sequence at that site. (PDF 669 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, P., Zhang, Y., Sun, Y. et al. Comparative genomic analysis of subspecies of Pantoea stewartii reveals distinct variations. J Plant Pathol 101, 997–1004 (2019). https://doi.org/10.1007/s42161-019-00328-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42161-019-00328-0

Keywords

Search

Navigation