Whole genome sequences reveal the Xanthomonas perforans population is shaped by the tomato production system.
Journal
The ISME journal
ISSN: 1751-7370
Titre abrégé: ISME J
Pays: England
ID NLM: 101301086
Informations de publication
Date de publication:
02 2022
02 2022
Historique:
received:
23
01
2021
accepted:
23
08
2021
revised:
11
08
2021
pubmed:
8
9
2021
medline:
12
3
2022
entrez:
7
9
2021
Statut:
ppublish
Résumé
Modern agricultural practices increase the potential for plant pathogen spread, while the advent of affordable whole genome sequencing enables in-depth studies of pathogen movement. Population genomic studies may decipher pathogen movement and population structure as a result of complex agricultural production systems. We used whole genome sequences of 281 Xanthomonas perforans strains collected within one tomato production season across Florida and southern Georgia fields to test for population genetic structure associated with tomato production system variables. We identified six clusters of X. perforans from core gene SNPs that corresponded with phylogenetic lineages. Using whole genome SNPs, we found genetic structure among farms, transplant facilities, cultivars, seed producers, grower operations, regions, and counties. Overall, grower operations that produced their own transplants were associated with genetically distinct and less diverse populations of strains compared to grower operations that received transplants from multiple sources. The degree of genetic differentiation among components of Florida's tomato production system varied between clusters, suggesting differential dispersal of the strains, such as through seed or contaminated transplants versus local movement within farms. Overall, we showed that the genetic variation of a bacterial plant pathogen is shaped by the structure of the plant production system.
Identifiants
pubmed: 34489540
doi: 10.1038/s41396-021-01104-8
pii: 10.1038/s41396-021-01104-8
pmc: PMC8776747
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
591-601Informations de copyright
© 2021. The Author(s).
Références
Strange RN, Scott PR. Plant disease: a threat to global food security. Annu Rev Phytopathol. 2005;43:83–116.
doi: 10.1146/annurev.phyto.43.113004.133839
pubmed: 16078878
Savary S, Willocquet L, Pethybridge SJ, Esker P, McRoberts N, Nelson A. The global burden of pathogens and pests on major food crops. Nat Ecol Evol. 2019;3:430–9.
doi: 10.1038/s41559-018-0793-y
pubmed: 30718852
Savary S, Bregaglio S, Willocquet L, Gustafson D, Mason D’Croz D, Sparks A, et al. Crop health and its global impacts on the components of food security. Food Secur. 2017;9:311–27.
doi: 10.1007/s12571-017-0659-1
Garrett KA, Alcalá-Briseño RI, Andersen KF, Buddenhagen CE, Choudhury RA, Fulton JC, et al. Network analysis: a systems framework to address grand challenges in plant pathology. Annu Rev Phytopathol. 2018;56:559–80.
doi: 10.1146/annurev-phyto-080516-035326
pubmed: 29979928
Pautasso M, Xu X, Jeger MJ, Harwood TD, Moslonka-Lefebvre M, Pellis L. Disease spread in small-size directed trade networks: the role of hierarchical categories. J Appl Ecol. 2010;47:1300–9.
doi: 10.1111/j.1365-2664.2010.01884.x
Bryant JM, Grogono DM, Rodriguez-Rincon D, Everall I, Brown KP, Moreno P, et al. Emergence and spread of a human-transmissible multidrug-resistant nontuberculous mycobacterium. Science. 2016;354:751–7.
pubmed: 27846606
pmcid: 5142603
doi: 10.1126/science.aaf8156
Yang C, Zhang X, Fan H, Li Y, Hu Q, Yang R, et al. Genetic diversity, virulence factors and farm-to-table spread pattern of Vibrio parahaemolyticus food-associated isolates. Food Microbiol. 2019;84:103270.
doi: 10.1016/j.fm.2019.103270
pubmed: 31421783
Dallman TJ, Byrne L, Ashton PM, Cowley LA, Perry NT, Adak G, et al. Whole-genome sequencing for national surveillance of Shiga toxin-producing Escherichia coli O157. Clin Infect Dis. 2015;61:305–12.
pubmed: 25888672
pmcid: 4542925
doi: 10.1093/cid/civ318
Kwong JC, Mercoulia K, Tomita T, Easton M, Li HY, Bulach DM, et al. Prospective whole-genome sequencing enhances national surveillance of Listeria monocytogenes. J Clin Microbiol. 2016;54:333–42.
pubmed: 26607978
pmcid: 4733179
doi: 10.1128/JCM.02344-15
Mather AE, Reid SW, Maskell DJ, Parkhill J, Fookes MC, Harris SR, et al. Distinguishable epidemics of multidrug-resistant Salmonella Typhimurium DT104 in different hosts. Science. 2013;341:1514–7.
pubmed: 24030491
pmcid: 4012302
doi: 10.1126/science.1240578
Richards VP, Velsko IM, Alam T, Zadoks RN, Manning SD, Pavinski Bitar PD, et al. Population gene introgression and high genome plasticity for the zoonotic pathogen Streptococcus agalactiae. Mol Biol Evol. 2019;36:2572–90.
doi: 10.1093/molbev/msz169
pmcid: 6805230
Mellor KC, Petrovska L, Thomson NR, Harris K, Reid SWJ, Mather AE. Antimicrobial resistance diversity suggestive of distinct Salmonella Typhimurium sources or selective pressures in food-production animals. Front Microbiol. 2019;10:708.
pubmed: 31031720
pmcid: 6473194
doi: 10.3389/fmicb.2019.00708
Monteil CL, Yahara K, Studholme DJ, Mageiros L, Méric G, Swingle B, et al. Population-genomic insights into emergence, crop adaptation and dissemination of Pseudomonas syringae pathogens. Micro Genom. 2016;2:e000089.
Perez-Quintero AL, Ortiz-Castro M, Lang JM, Rieux A, Wu G, Liu S, et al. Genomic acquisitions in emerging populations of Xanthomonas vasicola pv. vasculorum infecting corn in the United States and Argentina. Phytopathology. 2020;110:1161–73.
pubmed: 32040377
doi: 10.1094/PHYTO-03-19-0077-R
McCann HC, Li L, Liu Y, Li D, Pan H, Zhong C, et al. Origin and evolution of the kiwifruit canker pandemic. Genome Biol Evol. 2017;9:932–44.
pubmed: 28369338
pmcid: 5388287
doi: 10.1093/gbe/evx055
Quibod IL, Atieza-Grande G, Oreiro EG, Palmos D, Nguyen MH, Coronejo ST, et al. The Green Revolution shaped the population structure of the rice pathogen Xanthomonas oryzae pv. oryzae. ISME J. 2020;14:492–505.
pubmed: 31666657
doi: 10.1038/s41396-019-0545-2
Straub C, Colombi E, McCann H. Population genomics of bacterial plant pathogens. Phytopathology. 2021. https://doi.org/10.1094/PHYTO-09-20-0412-RVW .
Vinatzer BA, Monteil CL, Clarke CR. Harnessing population genomics to understand how bacterial pathogens emerge, adapt to crop hosts, and disseminate. Ann Rev Phytopathol. 2014;52:19–43.
doi: 10.1146/annurev-phyto-102313-045907
Weisberg AJ, Davis EW, Tabima JF, Belcher MS, Miller M, Kuo C, et al. Unexpected conservation and global transmission of agrobacterial virulence plasmids. Science. 2020;368:eaba5256.
pubmed: 32499412
doi: 10.1126/science.aba5256
Jones JB, Lacy GH, Bouzar H, Stall RE, Schaad NW. Reclassification of the xanthomonads associated with bacterial spot disease of tomato and pepper. Syst Appl Microbiol. 2004;27:755–62.
doi: 10.1078/0723202042369884
pubmed: 15612634
Potnis N, Timilsina S, Strayer A, Shantharaj D, Barak JD, Paret ML, et al. Bacterial spot of tomato and pepper: diverse Xanthomonas species with a wide variety of virulence factors posing a worldwide challenge. Mol Plant Pathol. 2015;16:907–20.
pubmed: 25649754
pmcid: 6638463
doi: 10.1111/mpp.12244
VanSickle J, Weldon R. The economic impact of bacterial leaf spot on the tomato industry. Tomato Inst Proc. 2009:30–31 https://plantpath.ifas.ufl.edu/rsol/RalstoniaPublications_PDF/Tomato_Institute_Proceedings_09.pdf .
Horvath DM, Stall RE, Jones JB, Pauly MH, Vallad GE, Dahlbeck D, et al. Transgenic resistance confers effective field level control of bacterial spot disease in tomato. PLOS One. 2012;7:e42036.
pubmed: 22870280
pmcid: 3411616
doi: 10.1371/journal.pone.0042036
Kunwar S, Iriarte F, Fan Q, Evaristo da Silva E, Ritchie L, Nguyen NS, et al. Transgenic expression of EFR and Bs2 genes for field management of bacterial wilt and bacterial spot of tomato. Phytopathology. 2018;108:1402–11.
pubmed: 29923802
doi: 10.1094/PHYTO-12-17-0424-R
Jones JB, Bouzar H, Somodi GC, Stall RE, Pernezny K, El-Morsy G, et al. Evidence for the preemptive nature of tomato race 3 of Xanthomonas campestris pv. vesicatoria in Florida. Phytopathology. 1998;88:33–38.
pubmed: 18944996
doi: 10.1094/PHYTO.1998.88.1.33
Timilsina S, Jibrin MO, Potnis N, Minsavage GV, Kebede M, Schwartz A, et al. Multilocus sequence analysis of xanthomonads causing bacterial spot of tomato and pepper plants reveals strains generated by recombination among species and recent global spread of Xanthomonas gardneri. Appl Environ Microbiol. 2015;81:1520–9.
pubmed: 25527544
pmcid: 4309686
doi: 10.1128/AEM.03000-14
United States Department of Agriculture. National Agricultural Statistics Service. Washington, DC: United States Department of Agriculture; 2019.
Klein-Gordon JM, Xing Y, Garrett KA, Abrahamian P, Paret ML, Minsavage GV, et al. Assessing changes and associations in the Xanthomonas perforans population across Florida commercial tomato fields via a state-wide survey. Phytopathology. 2021;111:1029–1041.
Vallad GE, Timilsina S, Adkison H, Potnis N, Minsavage G, Jones J, et al. A recent survey of xanthomonads causing bacterial spot of tomato in Florida provides insights into management strategies. Tomato Inst Proc. 2013:25–27 https://swfrec.ifas.ufl.edu/docs/pdf/veghort/tomato-institute/proceedings/ti13_proceedings.pdf .
Timilsina S, Pereira-Martin JA, Minsavage GV, Iruegas-Bocardo F, Abrahamian P, Potnis N, et al. Multiple recombination events drive the current genetic structure of Xanthomonas perforans in Florida. Front Microbiol. 2019;10:448.
pubmed: 30930868
pmcid: 6425879
doi: 10.3389/fmicb.2019.00448
Burlakoti R, Hsu C, Chen J, Wang J. Population dynamics of Xanthomonads associated with bacterial spot of tomato and pepper during twenty-seven years across Taiwan. Plant Dis. 2018;102:1348–56.
doi: 10.1094/PDIS-04-17-0465-RE
pubmed: 30673574
Araújo ER, Costa JR, Ferreira MASV, Quezada-Duval AM. Widespread distribution of Xanthomonas perforans and limited presence of X. gardneri in Brazil. Plant Pathol. 2017;66:159–68.
doi: 10.1111/ppa.12543
Jones JB, Pohronezny KL, Stall RE, Jones JP. Survival of Xanthomonas campestris pv. vesicatoria in Florida on tomato crop residue, weeds, seeds, and volunteer tomato plants. Phytopathology. 1986;76:430–4.
doi: 10.1094/Phyto-76-430
Sijam K, Chang CJ, Gitaitis RD. An agar medium for the isolation and identification of Xanthomonas campestris pv. vesicatoria from seed. Phytopathology. 1991;81:831–4.
doi: 10.1094/Phyto-81-831
Abrahamian P, Timilsina S, Minsavage GV, Potnis N, Jones JB, Goss EM, et al. Molecular epidemiology of Xanthomonas perforans outbreaks in tomato plants from transplant to field as determined by single-nucleotide polymorphism analysis. Appl Environ Microbiol. 2019;85:e01220–01219.
pubmed: 31253682
pmcid: 6715834
doi: 10.1128/AEM.01220-19
Abrahamian P, Sharma A, Jones J, Vallad GE. Dynamics and spread of bacterial spot epidemics in tomato transplants grown for field production. Plant Dis. 2021 in press.
Baym M, Kryazhimskiy S, Lieberman TD, Chung H, Desai MM, Kishony R. Inexpensive multiplexed library preparation for megabase-sized genomes. PLOS One. 2015;10:e0128036.
pubmed: 26000737
pmcid: 4441430
doi: 10.1371/journal.pone.0128036
Tudor-Nelson SM, Minsavage GV, Stall RE, Jones JB. Bacteriocin-like substances from tomato race 3 strains of Xanthomonas campestris pv. vesicatoria. Bacteriology. 2003;93:1415–21.
Schwartz A, Potnis N, Timilsina S, Wilson M, Patane J, Martins J, et al. Phylogenomics of Xanthomonas field strains infecting pepper and tomato reveals diversity in effector repertoires and identifies determinants of host specificity. Front Microbiol. 2015;6:535.
pubmed: 26089818
pmcid: 4452888
doi: 10.3389/fmicb.2015.00535
Nurk S, Bankevich A, Antipov D, Gurevich AA, Korobeynikov A, Lapidus A, et al. Assembling single-cell genomes and mini-metagenomes from chimeric MDA products. J Comput Biol. 2013;20:714–37.
pubmed: 24093227
pmcid: 3791033
doi: 10.1089/cmb.2013.0084
Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9:357–9.
pubmed: 22388286
pmcid: 3322381
doi: 10.1038/nmeth.1923
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The sequence alignment/map format and SAMtools. Bioinform. 2009;25:2078–9.
doi: 10.1093/bioinformatics/btp352
Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A, Sakthikumar S, et al. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLOS One. 2014;9:e112963.
pubmed: 25409509
pmcid: 4237348
doi: 10.1371/journal.pone.0112963
Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 2015;25:1043–55.
pubmed: 25977477
pmcid: 4484387
doi: 10.1101/gr.186072.114
Chen IA, Chu K, Palaniappan K, Pillay M, Ratner A, Huang J, et al. IMG/M v.5.0: an integrated data management and comparative analysis system for microbial genomes and microbiomes. Nucleic Acids Res. 2019;47:D666–d677. D1
pubmed: 30289528
doi: 10.1093/nar/gky901
Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics. 2014;30:2068–9.
pubmed: 24642063
doi: 10.1093/bioinformatics/btu153
Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30:772–80.
pubmed: 23329690
pmcid: 3603318
doi: 10.1093/molbev/mst010
Rice P, Longden I, Bleasby A. EMBOSS: the European molecular biology open software suite. Trends Genet. 2000;16:276–7.
pubmed: 10827456
doi: 10.1016/S0168-9525(00)02024-2
Darriba D, Posada D, Kozlov AM, Stamatakis A, Morel B, Flouri T. ModelTest-NG: a new and scalable tool for the selection of DNA and protein evolutionary models. Mol Biol Evol. 2019;37:291–4.
pmcid: 6984357
doi: 10.1093/molbev/msz189
Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30:1312–3.
pubmed: 24451623
pmcid: 3998144
doi: 10.1093/bioinformatics/btu033
Stamatakis A, Hoover P, Rougemont J. A rapid bootstrap algorithm for the RAxML web servers. Syst Biol. 2008;57:758–71.
pubmed: 18853362
doi: 10.1080/10635150802429642
Didelot X, Wilson DJ. ClonalFrameML: efficient inference of recombination in whole bacterial genomes. PLOS Comput Biol. 2015;11:e1004041.
pubmed: 25675341
pmcid: 4326465
doi: 10.1371/journal.pcbi.1004041
Tonkin-Hill G, Lees JA, Bentley SD, Frost SDW, Corander J. RhierBAPS: an R implementation of the population clustering algorithm hierBAPS. Wellcome Open Res. 2018;3:93.
pubmed: 30345380
pmcid: 6178908
doi: 10.12688/wellcomeopenres.14694.1
Cheng L, Connor TR, Sirén J, Aanensen DM, Corander J. Hierarchical and spatially explicit clustering of DNA sequences with BAPS software. Mol Biol Evol. 2013;30:1224–8.
pubmed: 23408797
pmcid: 3670731
doi: 10.1093/molbev/mst028
Letunic I, Bork P. Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics. 2007;23:127–8.
pubmed: 17050570
doi: 10.1093/bioinformatics/btl529
Csardi G, Nepusz T. The igraph software package for complex network research. 2006; InterJ., Complex Systems:1695.
R Core Team. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2020.
Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009;25:1754–60.
pubmed: 19451168
pmcid: 2705234
doi: 10.1093/bioinformatics/btp324
Canteros BI, Minsavage GV, Jones JB, Stall RE. Diversity of plasmids in Xanthomonas campestris pv. vesicatoria. Phytopathology. 1995;85:1482–6.
doi: 10.1094/Phyto-85-1482
Li H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv. 2013. https://arxiv.org/abs/1303.3997 .
Broad Institute: Picard. http://broadinstitute.github.io/picard/ 2019.
Garrison E, Marth G. Haplotype-based variant detection from short-read sequencing. arXiv. 2012. https://arxiv.org/abs/1207.3907 .
Garrison, E, Kronenberg, ZN, Dawson, ET, Pedersen, BS, Prins, P. Vcflib and tools for processing the VCF variant call format. BioRxiv. 2021.
Li H. Tabix: fast retrieval of sequence features from generic TAB-delimited files. Bioinformatics. 2011;27:718–9.
pubmed: 21208982
pmcid: 3042176
doi: 10.1093/bioinformatics/btq671
Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA, et al. The variant call format and VCFtools. Bioinformatics. 2011;27:2156–8.
pubmed: 21653522
pmcid: 3137218
doi: 10.1093/bioinformatics/btr330
Cingolani P, Platts A, Wang LL, Coon M, Nguyen T, Wang L, et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff. Fly. 2012;6:80–92.
pubmed: 22728672
pmcid: 3679285
doi: 10.4161/fly.19695
R Core Team. A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2019.
RStudio Team. RStudio: Integrated Development for R. Boston, MA: RStudio Inc.; 2016.
Knaus B, Grünwald NJ. vcfR: a package to manipulate and visualize variant call format data in R. Mol Ecol Res. 2017;17:44–53.
doi: 10.1111/1755-0998.12549
Jombart T. adegenet: a R package for the multivariate analysis of genetic markers. Bioinform. 2008;24:1403–5.
doi: 10.1093/bioinformatics/btn129
Kamvar ZN, Tabima JF, Grünwald NJ. Poppr: an R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ. 2014;2:e281.
pubmed: 24688859
pmcid: 3961149
doi: 10.7717/peerj.281
Grünwald NJ, Kamvar ZN, Everhart SE. Population genetics and genomics in R: Discriminant analysis of principal components (DAPC). 2020. https://grunwaldlab.github.io/Population_Genetics_in_R/DAPC.html .
Wickham H. ggplot2: elegant graphics for data analysis. New York: Springer-Verlag; 2016.
Tabima JF, Knaus B, Grünwald NJ. Population genetics and genomics in R: GBS analysis. 2020. https://grunwaldlab.github.io/Population_Genetics_in_R/gbs_analysis.html .
Dray S, Dufour A. The ade4 package: implementing the duality diagram for ecologists. J Stat Softw. 2007;22:1–20.
doi: 10.18637/jss.v022.i04
Kamvar ZN, Everhart SE, Grünwald NJ. Population genetics and genomics in R: AMOVA. 2020. https://grunwaldlab.github.io/Population_Genetics_in_R/AMOVA.html .
Rozas J, Ferrer-Mata A, Sanchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE, et al. DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol Biol Evol. 2017;34:3299–302.
doi: 10.1093/molbev/msx248
pubmed: 29029172
Lischer HE, Excoffier L. PGDSpider: an automated data conversion tool for connecting population genetics and genomics programs. Bioinformatics. 2012;28:298–9.
doi: 10.1093/bioinformatics/btr642
pubmed: 22110245
Excoffier L, Lischer HEL. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour. 2010;10:564–7.
doi: 10.1111/j.1755-0998.2010.02847.x
pubmed: 21565059
Newberry EA, Bhandari R, Minsavage GV, Timilsina S, Jibrin MO, Kemble J, et al. Independent evolution with the gene flux originating from multiple Xanthomonas species explains genomic heterogeneity in Xanthomonas perforans. Appl Environ Microbiol. 2019;85:e00885–19.
Jibrin MO, Potnis N, Timilsina S, Minsavage GV, Vallad GE, Roberts PD, et al. Genomic inference of recombination-mediated evolution in Xanthomonas euvesicatoria and X. perforans. Appl Environ Microbiol. 2018; 84:e00136–18.