Effects of plant tissue permeability on invasion and population bottlenecks of a phytopathogen.

Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
02 Jan 2024
Historique:
received: 28 03 2023
accepted: 05 12 2023
medline: 4 1 2024
pubmed: 4 1 2024
entrez: 3 1 2024
Statut: epublish

Résumé

Pathogen genetic diversity varies in response to environmental changes. However, it remains unclear whether plant barriers to invasion could be considered a genetic bottleneck for phytopathogen populations. Here, we implement a barcoding approach to generate a pool of 90 isogenic and individually barcoded Ralstonia solanacearum strains. We used 90 of these strains to inoculate tomato plants with different degrees of physical permeability to invasion (intact roots, wounded roots and xylem inoculation) and quantify the phytopathogen population dynamics during invasion. Our results reveal that the permeability of plant roots impacts the degree of population bottleneck, genetic diversity, and composition of Ralstonia populations. We also find that selection is the main driver structuring pathogen populations when barriers to infection are less permeable, i.e., intact roots, the removal of root physical and immune barriers results in the predominance of stochasticity in population assembly. Taken together, our study suggests that plant root permeability constitutes a bottleneck for phytopathogen invasion and genetic diversity.

Identifiants

DOI: 10.1038/s41467-023-44234-7 PMID: 38167266
pubmed: 38167266
doi: 10.1038/s41467-023-44234-7
pii: 10.1038/s41467-023-44234-7
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

62

Informations de copyright

© 2024. The Author(s).

Références

Lässig, M., Mustonen, V. & Nourmohammad, A. Steering and controlling evolution—from bioengineering to fighting pathogens. Nat. Rev. Genet. https://doi.org/10.1038/s41576-023-00623-8 (2023).
Didelot, X., Walker, A. S., Peto, T. E., Crook, D. W. & Wilson, D. J. Within-host evolution of bacterial pathogens. Nat. Rev. Microbiol. 14, 150–162 (2016).
pubmed: 26806595 pmcid: 5053366 doi: 10.1038/nrmicro.2015.13
Abel, S., Abel zur Wiesch, P., Davis, B. M. & Waldor, M. K. Analysis of bottlenecks in experimental models of infection. PLoS Pathog. 11, e1004823 (2015).
Planas-Marquès, M. et al. Four bottlenecks restrict colonization and invasion by the pathogen Ralstonia solanacearum in resistant tomato. J. Exp. Bot. 71, 2157–2171 (2020).
pubmed: 32211785 doi: 10.1093/jxb/erz562
da Silva, W. et al. Transmission modes affect the population structure of potato virus Y in potato. PLoS Pathog. 16, e1008608 (2020).
pubmed: 32574227 pmcid: 7347233 doi: 10.1371/journal.ppat.1008608
Wei, Z. et al. Rhizosphere immunity: targeting the underground for sustainable plant health management. Front. Agric. Sci. Eng. 7, 317–328 (2020).
doi: 10.15302/J-FASE-2020346
Genin, S. & Denny, T. P. Pathogenomics of the Ralstonia solanacearum species complex. Annu. Rev. Phytopathol. 50, 67–89 (2012).
pubmed: 22559068 doi: 10.1146/annurev-phyto-081211-173000
Wang, Y., Pruitt, R. N., Nürnberger, T. & Wang, Y. Evasion of plant immunity by microbial pathogens. Nat. Rev. Microbiol. 20, 449–464 (2022).
pubmed: 35296800 doi: 10.1038/s41579-022-00710-3
Kennedy, D. A. & Dwyer, G. Effects of multiple sources of genetic drift on pathogen variation within hosts. PLoS Biol. 16, e2004444 (2018).
pubmed: 29590105 pmcid: 5891033 doi: 10.1371/journal.pbio.2004444
Lässig, M. & Mustonen, V. Eco-evolutionary control of pathogens. Proc. Natl. Acad. Sci. USA 117, 19694–19704 (2020).
pubmed: 32737164 pmcid: 7443876 doi: 10.1073/pnas.1920263117
Dodds, P. N. & Rathjen, J. P. Plant immunity: towards an integrated view of plant-pathogen interactions. Nat. Rev. Genet. 11, 539–548 (2010).
pubmed: 20585331 doi: 10.1038/nrg2812
Lannou, C. Variation and selection of quantitative traits in plant pathogens. Annu. Rev. Phytopathol. 50, 319–338 (2012).
pubmed: 22702351 doi: 10.1146/annurev-phyto-081211-173031
Ebert, D. & Fields, P. D. Host-parasite co-evolution and its genomic signature. Nat. Rev. Genet. 21, 754–768 (2020).
pubmed: 32860017 doi: 10.1038/s41576-020-0269-1
Tan, S. et al. Bacillus amyloliquefaciens T-5 may prevent Ralstonia solanacearum infection through competitive exclusion. Biol. Fertil. Soils 52, 341–351 (2016).
doi: 10.1007/s00374-015-1079-z
Guidot, A. et al. Multihost experimental evolution of the pathogen Ralstonia solanacearum unveils genes involved in adaptation to plants. Mol. Biol. Evol. 31, 2913–2928 (2014).
pubmed: 25086002 doi: 10.1093/molbev/msu229
Zhou, J. & Ning, D. Stochastic community assembly: does it matter in microbial ecology? Microbiol. Mol. Biol. Rev. 81, e00002–e00017 (2017).
pubmed: 29021219 pmcid: 5706748 doi: 10.1128/MMBR.00002-17
Stefansson, T. S., McDonald, B. A. & Willi, Y. The influence of genetic drift and selection on quantitative traits in a plant pathogenic fungus. PLoS One 9, e112523 (2014).
pubmed: 25383967 pmcid: 4226542 doi: 10.1371/journal.pone.0112523
Gibson, A. K. Genetic diversity and disease: the past, present, and future of an old idea. Evolution 76, 20–36 (2022).
pubmed: 34796478 doi: 10.1111/evo.14395
Evans, S., Martiny, J. B. H. & Allison, S. D. Effects of dispersal and selection on stochastic assembly in microbial communities. ISME J. 11, 176–185 (2017).
pubmed: 27494293 doi: 10.1038/ismej.2016.96
Dini-Andreote, F., Stegen, J. C., van Elsas, J. D. & Salles, J. F. Disentangling mechanisms that mediate the balance between stochastic and deterministic processes in microbial succession. Proc. Natl. Acad. Sci. USA 112, E1326–E1332 (2015).
pubmed: 25733885 pmcid: 4371938 doi: 10.1073/pnas.1414261112
López-Villavicencio, M. et al. Competition, cooperation among kin, and virulence in multiple infections. Evolution 65, 1357–1366 (2011).
pubmed: 21121914 doi: 10.1111/j.1558-5646.2010.01207.x
Weaver, S. C., Forrester, N. L., Liu, J. & Vasilakis, N. Population bottlenecks and founder effects: implications for mosquito-borne arboviral emergence. Nat. Rev. Microbiol. 19, 184–195 (2021).
pubmed: 33432235 pmcid: 7798019 doi: 10.1038/s41579-020-00482-8
Abel, S. et al. STAMP: Sequence tag-based analysis of microbial population dynamics. Nat. Methods 12, 223–226 (2015).
pubmed: 25599549 pmcid: 4344388 doi: 10.1038/nmeth.3253
Jasinska, W. et al. Chromosomal barcoding of E. coli populations reveals lineage diversity dynamics at high resolution. Nat. Ecol. Evol. 4, 437–452 (2020).
pubmed: 32094541 doi: 10.1038/s41559-020-1103-z
Theodosiou, L., Farr, A. D. & Rainey, P. B. Barcoding populations of Pseudomonas fluorescens SBW25. J. Mol. Evol. 91, 254–262 (2023).
pubmed: 37186220 pmcid: 10275814 doi: 10.1007/s00239-023-10103-6
Vasquez, K. S. et al. Quantifying rapid bacterial evolution and transmission within the mouse intestine. Cell Host Microbe 29, 1454–1468.e4 (2021).
pubmed: 34473943 pmcid: 8445907 doi: 10.1016/j.chom.2021.08.003
Levy, S. F. et al. Quantitative evolutionary dynamics using high-resolution lineage tracking. Nature 519, 181–186 (2015).
pubmed: 25731169 pmcid: 4426284 doi: 10.1038/nature14279
Cira, N. J., Pearce, M. T. & Quake, S. R. Neutral and selective dynamics in a synthetic microbial community. Proc. Natl. Acad. Sci. USA 115, E9842–E9848 (2018).
pubmed: 30266791 pmcid: 6196497 doi: 10.1073/pnas.1808118115
Kashyap, P. L., Rai, P., Kumar, S., Chakdar, H. & Srivastava, A. K. DNA barcoding for diagnosis and monitoring of fungal plant pathogens. In Molecular Markers in Mycology: Diagnostics and Marker Developments (eds. Singh, B. P. & Gupta, V. K.) 87–122 (Springer International Publishing, 2017).
Johnson, P. T. J., de Roode, J. C. & Fenton, A. Why infectious disease research needs community ecology. Science 349, 1259504 (2015).
pubmed: 26339035 pmcid: 4863701 doi: 10.1126/science.1259504
Sharma, P. et al. Meta-analysis of the Ralstonia solanacearum species complex (RSSC) based on comparative evolutionary genomics and reverse ecology. Micro. Genom. 8, 000791 (2022).
Jiang, G. et al. Bacterial wilt in China: history, current status, and future perspectives. Front Plant Sci. 8, 1549 (2017).
pubmed: 28955350 pmcid: 5601990 doi: 10.3389/fpls.2017.01549
Chesneau, T. et al. Sequevar diversity and virulence of Ralstonia solanacearum phylotype I on Mayotte Island (Indian Ocean). Front. Plant Sci. 8, 2209 (2018).
Stukenbrock, E. H. & McDonald, B. A. The origins of plant pathogens in agro-ecosystems. Annu. Rev. Phytopathol. 46, 75–100 (2008).
pubmed: 18680424 doi: 10.1146/annurev.phyto.010708.154114
Chase, J. M., Kraft, N. J. B., Smith, K. G., Vellend, M. & Inouye, B. D. Using null models to disentangle variation in community dissimilarity from variation in α-diversity. Ecosphere 2, art24 (2011).
doi: 10.1890/ES10-00117.1
Fodelianakis, S., Valenzuela-Cuevas, A., Barozzi, A. & Daffonchio, D. Direct quantification of ecological drift at the population level in synthetic bacterial communities. ISME J. 15, 55–66 (2021).
pubmed: 32855435 doi: 10.1038/s41396-020-00754-4
Remigi, P. et al. Transient hypermutagenesis accelerates the evolution of legume endosymbionts following horizontal gene transfer. PLoS Biol. 12, e1001942 (2014).
pubmed: 25181317 pmcid: 4151985 doi: 10.1371/journal.pbio.1001942
Windels, E. M. et al. Population bottlenecks strongly affect the evolutionary dynamics of antibiotic persistence. Mol. Biol. Evol. 38, 3345–3357 (2021).
pubmed: 33871643 pmcid: 8321523 doi: 10.1093/molbev/msab107
Wang, L. et al. Genetic and pathogenic diversity of Ralstonia solanacearum causing potato brown rot in China. Am. J. Potato Res. 94, 403–416 (2017).
doi: 10.1007/s12230-017-9576-2
McDonald, B. A. & Linde, C. Pathogen population genetics, evolutionary potential, and durable resistance. Annu Rev. Phytopathol. 40, 349–379 (2002).
pubmed: 12147764 doi: 10.1146/annurev.phyto.40.120501.101443
Dutta, A., Hartmann, F. E., Francisco, C. S., McDonald, B. A. & Croll, D. Mapping the adaptive landscape of a major agricultural pathogen reveals evolutionary constraints across heterogeneous environments. ISME J. 15, 1402–1419 (2021).
pubmed: 33452474 pmcid: 8115182 doi: 10.1038/s41396-020-00859-w
Gopalan-Nair, R. et al. Convergent rewiring of the virulence regulatory network promotes adaptation of Ralstonia solanacearum on resistant tomato. Mol. Biol. Evol. 38, 1792–1808 (2020).
pmcid: 8097285 doi: 10.1093/molbev/msaa320
Jiang, G. et al. Exploring rhizo-microbiome transplants as a tool for protective plant-microbiome manipulation. ISME Commun. 2, 1–10 (2022).
doi: 10.1038/s43705-022-00094-8
Macho, A. P., Guidot, A., Barberis, P., Beuzón, C. R. & Genin, S. A competitive index assay identifies several Ralstonia solanacearum type III effector mutant strains with reduced fitness in host plants. Mol. Plant Microbe Interact. 23, 1197–1205 (2010).
pubmed: 20687809 doi: 10.1094/MPMI-23-9-1197
Inoue, K. et al. The behavior of Ralstonia pseudosolanacearum strain OE1-1 and morphological changes of cells in tomato roots. J. Plant Res. 136, 19–31 (2023).
pubmed: 36427093 doi: 10.1007/s10265-022-01427-3
Jiang, G. et al. Modeling and experimental determination of infection bottleneck and within-host dynamics of a soil-borne bacterial plant pathogen. Preprint at https://doi.org/10.1101/061408 (2016).
Langenheder, S. & Székely, A. J. Species sorting and neutral processes are both important during the initial assembly of bacterial communities. ISME J. 5, 1086–1094 (2011).
pubmed: 21270841 pmcid: 3146284 doi: 10.1038/ismej.2010.207
Bergstrom, C. T., McElhany, P. & Real, L. A. Transmission bottlenecks as determinants of virulence in rapidly evolving pathogens. Proc. Natl. Acad. Sci. USA 96, 5095–5100 (1999).
pubmed: 10220424 pmcid: 21822 doi: 10.1073/pnas.96.9.5095
Almario, J. et al. The leaf microbiome of Arabidopsis displays reproducible dynamics and patterns throughout the growing season. mBio 13, e0282521 (2022).
Sloan, W. T., Woodcock, S., Lunn, M., Head, I. M. & Curtis, T. P. Modeling taxa-abundance distributions in microbial communities using environmental sequence data. Micro. Ecol. 53, 443–455 (2007).
doi: 10.1007/s00248-006-9141-x
Fields, B. & Friman, V.-P. Microbial eco-evolutionary dynamics in the plant rhizosphere. Curr. Opin. Microbiol. 68, 102153 (2022).
pubmed: 35504054 doi: 10.1016/j.mib.2022.102153
Zhang, Y. et al. The Tn7-based genomic integration is dependent on an att Tn7 box in the glms gene and is site-specific with monocopy in Ralstonia solanacearum species complex. Mol. Plant Microbe Interact. 34, 720–725 (2021).
pubmed: 33656355 doi: 10.1094/MPMI-11-20-0325-SC
Pagès, H., Aboyoun, P., Gentleman, R. & DebRoy, S. Biostrings: efficient manipulation of biological strings. https://doi.org/10.18129/B9.bioc.Biostrings (2023).
Choi, K.-H. et al. A Tn7-based broad-range bacterial cloning and expression system. Nat. Methods 2, 443–448 (2005).
pubmed: 15908923 doi: 10.1038/nmeth765
Kahm, M., Hasenbrink, G., Lichtenberg-Fraté, H., Ludwig, J. & Kschischo, M. grofit: Fitting biological growth curves with R. J. Stat. Softw. 33, 1–21 (2010).
doi: 10.18637/jss.v033.i07
Jiang, G. et al. The relative importance of soil moisture in predicting bacterial wilt disease occurrence. Soil Ecol. Lett. 3, 356–366 (2021).
doi: 10.1007/s42832-021-0086-2
Edgar, R. C. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10, 996–998 (2013).
pubmed: 23955772 doi: 10.1038/nmeth.2604
Amir, A. et al. Deblur rapidly resolves single-nucleotide community sequence patterns. mSystems 2, e00191-16 (2017).
Edgar, R. C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460–2461 (2010).
pubmed: 20709691 doi: 10.1093/bioinformatics/btq461
R Core Team. The R Stats Package. (2020).
Dixon, P. VEGAN, a package of R functions for community ecology. J. Veg. Sci. 14, 927–930 (2003).
doi: 10.1111/j.1654-1103.2003.tb02228.x
Mendiburu, F. de. agricolae: Statistical procedures for agricultural research (2020).
Paradis, E. & Schliep, K. ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35, 526–528 (2019).
pubmed: 30016406 doi: 10.1093/bioinformatics/bty633
Kassambara, A. ggpubr: ‘ggplot2’ Based Publication Ready Plots (2023).
Muggeo, V. M. R. segmented: Regression models with break-points/change-points (with possibly random effects) estimation (2023).
Stegen, J. C. et al. Quantifying community assembly processes and identifying features that impose them. ISME J. 7, 2069–2079 (2013).
pubmed: 23739053 pmcid: 3806266 doi: 10.1038/ismej.2013.93
Ramoneda, J., Le Roux, J. J., Frossard, E., Frey, B. & Gamper, H. A. Experimental assembly reveals ecological drift as a major driver of root nodule bacterial diversity in a woody legume crop. FEMS Microbiol. Ecol. 96, fiaa083 (2020).
pubmed: 32364226 doi: 10.1093/femsec/fiaa083
Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797 (2004).
pubmed: 15034147 pmcid: 390337 doi: 10.1093/nar/gkh340
Kembel, S. W. et al. Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26, 1463–1464 (2010).
pubmed: 20395285 doi: 10.1093/bioinformatics/btq166
Russel, J. MicEco: various functions for analysis for microbial community data (2021).

Auteurs

Gaofei Jiang (G)

College of Resources and Environment, College of Plant Protection, Interdisciplinary Research Center for Agriculture Green Development in Yangtze River Basin, Southwest University, Chongqing, China.
Key Laboratory of Plant Immunity, Jiangsu Provincial Key Laboratory for Organic Solid Waste Utilization, Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, National Engineering Research Center for Organic-based Fertilizers, Nanjing Agricultural University, Nanjing, China.
ORCID: 0000-0002-5331-739X

Yuling Zhang (Y)

Key Laboratory of Plant Immunity, Jiangsu Provincial Key Laboratory for Organic Solid Waste Utilization, Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, National Engineering Research Center for Organic-based Fertilizers, Nanjing Agricultural University, Nanjing, China.

Min Chen (M)

College of Environmental Science and Engineering, Shaanxi University of Science & Technology, Xi'an, China.

Josep Ramoneda (J)

Institute for Research in Environmental Sciences, University of Colorado, Boulder, CO, USA.
ORCID: 0000-0002-1806-2889

Liangliang Han (L)

Department of Biomedical Science, City University of Hong Kong, Kowloon Tong, Hong Kong SAR, China.

Yu Shi (Y)

State Key Laboratory of Crop Stress Adaptation and Improvement, School of Life Sciences, Henan University, Kaifeng, Henan, China.

Rémi Peyraud (R)

iMEAN, Ramonville Saint Agne, Occitanie, FR, France.
ORCID: 0000-0002-7580-042X

Yikui Wang (Y)

Vegetable Research Institute, Guangxi Academy of Agricultural Science, Nanning, China.
ORCID: 0000-0003-0697-5696

Xiaojun Shi (X)

College of Resources and Environment, College of Plant Protection, Interdisciplinary Research Center for Agriculture Green Development in Yangtze River Basin, Southwest University, Chongqing, China.
ORCID: 0000-0001-5740-4098

Xinping Chen (X)

College of Resources and Environment, College of Plant Protection, Interdisciplinary Research Center for Agriculture Green Development in Yangtze River Basin, Southwest University, Chongqing, China.
ORCID: 0000-0002-6245-0133

Wei Ding (W)

College of Resources and Environment, College of Plant Protection, Interdisciplinary Research Center for Agriculture Green Development in Yangtze River Basin, Southwest University, Chongqing, China.

Alexandre Jousset (A)

Key Laboratory of Plant Immunity, Jiangsu Provincial Key Laboratory for Organic Solid Waste Utilization, Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, National Engineering Research Center for Organic-based Fertilizers, Nanjing Agricultural University, Nanjing, China.
ORCID: 0000-0002-6805-2486

Yasufumi Hikichi (Y)

Faculty of Agriculture and Marine Science, Kochi University, Nankoku, Japan.

Kouhei Ohnishi (K)

Faculty of Agriculture and Marine Science, Kochi University, Nankoku, Japan.

Fang-Jie Zhao (FJ)

Key Laboratory of Plant Immunity, Jiangsu Provincial Key Laboratory for Organic Solid Waste Utilization, Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, National Engineering Research Center for Organic-based Fertilizers, Nanjing Agricultural University, Nanjing, China.
ORCID: 0000-0002-0164-169X

Yangchun Xu (Y)

Key Laboratory of Plant Immunity, Jiangsu Provincial Key Laboratory for Organic Solid Waste Utilization, Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, National Engineering Research Center for Organic-based Fertilizers, Nanjing Agricultural University, Nanjing, China.
ORCID: 0000-0003-2740-5561

Qirong Shen (Q)

Key Laboratory of Plant Immunity, Jiangsu Provincial Key Laboratory for Organic Solid Waste Utilization, Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, National Engineering Research Center for Organic-based Fertilizers, Nanjing Agricultural University, Nanjing, China.
ORCID: 0000-0002-5662-9620

Francisco Dini-Andreote (F)

Department of Plant Science & Huck Institutes of the Life Sciences, The Pennsylvania State University, University Park, PA, USA.
The One Health Microbiome Center, Huck Institutes of the Life Sciences, The Pennsylvania State University, University Park, PA, USA.
ORCID: 0000-0002-6654-0769

Yong Zhang (Y)

College of Resources and Environment, College of Plant Protection, Interdisciplinary Research Center for Agriculture Green Development in Yangtze River Basin, Southwest University, Chongqing, China. bioyongzhang@swu.edu.cn.
College of Environmental Science and Engineering, Shaanxi University of Science & Technology, Xi'an, China. bioyongzhang@swu.edu.cn.

Zhong Wei (Z)

Key Laboratory of Plant Immunity, Jiangsu Provincial Key Laboratory for Organic Solid Waste Utilization, Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, National Engineering Research Center for Organic-based Fertilizers, Nanjing Agricultural University, Nanjing, China. weizhong@njau.edu.cn.
ORCID: 0000-0002-7967-4897

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