Differences in the constituents of bacterial microbiota of soils collected from two fields of diverse potato blackleg and soft rot diseases incidences, a case study.
[en] The presence of bacteria from the Dickeya spp. and Pectobacterium spp. in farmlands leads to global crop losses of over $420 million annually. Since 1982, the scientists have started to suspect that the development of disease symptoms in crops might be inhibited by bacteria present in the soil. Here, we characterized in terms of physicochemical properties and the composition of bacterial soil microbiota two fields differing, on the basis of long-term studies, in the occurrence of Dickeya spp.- and Pectobacterium spp.-triggered infections. Majority, i.e. 17 of the investigated physicochemical features of the soils collected from two fields of either low or high potato blackleg and soft rot diseases incidences turned out to be similar, in contrast to the observed 4 deviations in relation to Mg, Mn, organic C and organic substance contents. By performing microbial cultures and molecular diagnostics-based identification, 20 Pectobacterium spp. strains were acquired from the field showing high blackleg and soft rot incidences. In addition, 16S rRNA gene amplicon sequencing followed by bioinformatic analysis revealed differences at various taxonomic levels in the soil bacterial microbiota of the studied fields. We observed that bacteria from the genera Bacillus, Rumeliibacillus, Acidobacterium and Gaiella turned out to be more abundant in the soil samples originating from the field of low comparing to high frequency of pectinolytic bacterial infections. In the herein presented case study, it is shown for the first time that the composition of bacterial soil microbiota varies between two fields differing in the incidences of soft rot and blackleg infections.
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
Babinska-Wensierska, Weronika; Laboratory of Plant Protection and Biotechnology, Intercollegiate Faculty of Biotechnology, University of Gdansk and Medical University of Gdansk, University of Gdansk, 58 Abrahama, 80-307, Gdansk, Poland ; Research and Development Laboratory, Intercollegiate Faculty of Biotechnology, University of Gdansk and Medical University of Gdansk, University of Gdansk, 20 Podwale Przedmiejskie, 80-824, Gdansk, Poland
Motyka-Pomagruk, Agata; Laboratory of Plant Protection and Biotechnology, Intercollegiate Faculty of Biotechnology, University of Gdansk and Medical University of Gdansk, University of Gdansk, 58 Abrahama, 80-307, Gdansk, Poland ; Research and Development Laboratory, Intercollegiate Faculty of Biotechnology, University of Gdansk and Medical University of Gdansk, University of Gdansk, 20 Podwale Przedmiejskie, 80-824, Gdansk, Poland
Fondi, Marco ; Laboratorio di Genetica Microbica, Department of Biology, University of Florence, Via Madonna del Piano 6, Sesto Fiorentino, Florence, Italy
Misztak, Agnieszka ; Université de Liège - ULiège > Département de gestion vétérinaire des Ressources Animales (DRA)
Mengoni, Alessio ; Laboratorio di Genetica Microbica, Department of Biology, University of Florence, Via Madonna del Piano 6, Sesto Fiorentino, Florence, Italy
Lojkowska, Ewa; Laboratory of Plant Protection and Biotechnology, Intercollegiate Faculty of Biotechnology, University of Gdansk and Medical University of Gdansk, University of Gdansk, 58 Abrahama, 80-307, Gdansk, Poland. ewa.lojkowska@biotech.ug.edu.pl ; Research and Development Laboratory, Intercollegiate Faculty of Biotechnology, University of Gdansk and Medical University of Gdansk, University of Gdansk, 20 Podwale Przedmiejskie, 80-824, Gdansk, Poland. ewa.lojkowska@biotech.ug.edu.pl
Language :
English
Title :
Differences in the constituents of bacterial microbiota of soils collected from two fields of diverse potato blackleg and soft rot diseases incidences, a case study.
Publication date :
2024
Journal title :
Scientific Reports
eISSN :
2045-2322
Publisher :
Nature, England
Volume :
14
Issue :
1
Pages :
18802
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
NCN - Narodowe Centrum Nauki
Funding text :
This work was supported by the Ministry of Science and Higher Education (grant number 531-N107-D801-21) attributed to Ewa Lojkowska\u00A0and National Science Centre in Poland via project Preludium 21 (grant number UMO-2022/45/N/NZ9/01923) attributed to Dr. Weronika Babinska-Wensierska. Dr. Agata Motyka-Pomagruk got support from Ministry of Education and Science in Poland via outstanding young scientists scholarship (SMN/18/0019/2022). We would like to thank Professor George C. DiCenzo from Queen's University for his discussion on the final version of the manuscript. In addition, we are grateful to MSc Christopher Riccardi from University of Florence for advice on the deposition of 16S rRNA raw reads in the Sequence Read Archive repository. Finally, we would like to thank our collaborators for enabling sampling of soil from two selected potato fields and providing all the necessary information on the conducted agrotechnical treatments.This work was supported by the Ministry of Science and Higher Education (grant number 531-N107-D801-21) attributed to Ewa Lojkowska and National Science Centre in Poland via project Preludium 21 (grant number UMO-2022/45/N/NZ9/01923) attributed to Dr. Weronika Babinska-Wensierska. Dr. Agata Motyka-Pomagruk got support from Ministry of Education and Science in Poland via outstanding young scientists scholarship (SMN/18/0019/2022). We would like to thank Professor George C. DiCenzo from Queen's University for his discussion on the final version of the manuscript. In addition, we are grateful to MSc Christopher Riccardi from University of Florence for advice on the deposition of 16S rRNA raw reads in the Sequence Read Archive repository. Finally, we would like to thank our collaborators for enabling sampling of soil from two selected potato fields and providing all the necessary information on the conducted agrotechnical treatments.
Ben Moussa, H., Pédron, J., Bertrand, C., Hecquet, A., Barny, M. A. Pectobacterium quasiaquaticum sp. nov., isolated from waterways. Int. J. Syst. Evol. Microbiol. 71. https://doi.org/10.1099/ijsem.0.005042 (2021).
Toth, I. K. et al. Pectobacterium and Dickeya: Taxonomy and Evolution. In: Van Gijsegem, F., van der Wolf, J.M., Toth, I.K. (eds). Plant Diseases Caused by Dickeya and Pectobacterium Species. Springer, Cham. 13–37. https://doi.org/10.1007/978-3-030-61459-1_2 (2021).
Zhou, J. et al. Isolation and genome analysis of Pectobacterium colocasium sp. nov. and Pectobacterium aroidearum, two new pathogens of taro. Front. Plant Sci. 13, 1141. https://doi.org/10.3389/fpls.2022.852750 (2022).
A. Motyka S. Zoledowska W. Sledz E. Lojkowska Molecular methods as tools to control plant diseases caused by Dickeya and Pectobacterium spp: A minireview N. Biotechnol. 2017 39 181 189 1:CAS:528:DC%2BC2sXhsVGitrjJ 10.1016/J.NBT.2017.08.010 28847714
P.R.J. Birch et al. Crops that feed the world 8: Potato: Are the trends of increased global production sustainable? Food Secur. 2012 4 477 508 10.1007/S12571-012-0220-1
Van der Wolf, J. M. et al. Diseases caused by Pectobacterium and Dickeya Species Around the World. In: Van Gijsegem, F., van der Wolf, J.M., Toth, I.K. (eds). Plant Diseases Caused by Dickeya and Pectobacterium Species. Springer, Cham. 215–261. https://doi.org/10.1007/978-3-030-61459-1_7 (2021).
Dupuis, B., Nkuriyingoma, P., Van Gijsegem, F. Economic Impact of Pectobacterium and Dickeya species on potato crops: A Review and Case study. In: Van Gijsegem, F., van der Wolf, J.M., Toth, I.K. (eds). Plant Diseases Caused by Dickeya and Pectobacterium Species. Springer, Cham. 263–282. https://doi.org/10.1007/978-3-030-61459-1_8 (2021).
Toth, I. K. et al. Pectobacterium and Dickeya: Environment to Disease Development. In: Van Gijsegem, F., van der Wolf, J.M., Toth, I.K. (eds). Plant Diseases Caused by Dickeya and Pectobacterium Species. Springer, Cham. 39-84; https://doi.org/10.1007/978-3-030-61459-1_3 (2021).
T. Ge F. Ekbataniamiri S.B. Johnson R.P. Larkin J. Hao Interaction between Dickeya dianthicola and Pectobacterium parmentieri in potato infection under field conditions Microorganisms. 2021 9 1 10 10.3390/MICROORGANISMS9020316
Ficke, W., Naumann K., Skadow, K., Müller, H., Zielke, R. Die Lebensdauer von Pectobacterium carotovorum var. atrosepticum (van Hall) Dowson auf dem Pflanzgut und im Bodem. Arch. Phytopathol. Plant Protect. 9, 281–293 (1973).
J. Van der Wolf R. Czajkowski H. Velvis Effectieve kolonisatie van aardappelplanten door Dickeya soorten (Erwinia chrysanthemi) Gewasbescherming Jaargang. 2009 4 169 171
Czajkowski, R. et al. Detection, identification and differentiation of Pectobacterium and Dickeya species causing potato blackleg and tuber soft rot: A review. Ann. Appl. Biol. 166, 18–38; https://doi.org/10.1111/AAB.12166 (2015).
Peltzer, S., Sivasithamparam, K. Sero-groups of Erwinia carotovora associated with water, soil, tuber, and stems of potato plants in Western Australia. New Zealand J. Agric. 16, 265–270. https://doi.org/10.1080/03015521.1988.10425649 (1988).
A. Motyka-Pomagruk S. Zoledowska W. Sledz E. Lojkowska The occurrence of bacteria from different species of Pectobacteriaceae on seed potato plantations in Poland Eur. J. Plant Pathol. 2021 159 309 325 1:CAS:528:DC%2BB3MXhsFGiurs%3D 10.1007/S10658-020-02163-X/FIGURES/6
Potrykus, M. et al. Biodiversity of Dickeya spp. isolated from potato plants and water sources in temperate climate. Plant Dis.100, 408–417. https://doi.org/10.1094/PDIS-04-15-0439-RE (2016).
Pérombelon, M., & Hyman, L. Survival of soft rot coliforms, Erwinia carotovora subsp. carotovora and E. carotovora subsp. atroseptica in soil in Scotland. J. Appl. Bacteriol. 66, 95–106. https://doi.org/10.1111/j.1365-2672.1989.tb02459.x (1989).
Burr, T. J., & Schroth, M. N. Occurrence of soft rot Erwinia spp. in soil and plant material. Phytopathology. 67, 1382–1387. https://doi.org/10.1094/Phyto-67-1382 (1977).
N.C. Gudmestad G.A. Secor The bionomics of Erwinia carotovora in North Dakota Am. Potato J. 1983 60 759 771 10.1007/BF02856895
N.J. McCarter-Zorner M.D. Harrison G.D. Franc C.E. Quinn I.A. Sells D.C. Graham Soft rot Erwinia bacteria in the rhizosphere of weeds and crop plants in Colorado USA and Scotland UK J. Appl. Bacteriol. 1985 59 357 368 10.1111/j.1365-2672.1985.tb03331.x
De Corato, U. Governance of soil amendment to enhance suppression to soil-borne plant pathogens from a long-term perspective. Appl. Soil Ecol. 182. https://doi.org/10.1016/j.apsoil.2022.104721 (2023).
Schroth, M. N. & Hancock, J. G. Disease-suppressive soil and root-colonizing bacteria. Science. 216. https://doi.org/10.1126/science.216.4553.1376 (1982).
Q. Wang L. Zhou H. Jin B. Cong H. Yang S. Wang Investigating the responses of microbial communities to banana Fusarium Wilt in suppressive and conducive soils based on soil particle-size differentiation Agronomy. 2022 12 229 1:CAS:528:DC%2BB38XotFSjs78%3D 10.3390/agronomy12020229
Deng, X. et al. Soil microbiome manipulation triggers direct and possible indirect suppression against Ralstonia solanacearum and Fusarium oxysporum. npj Biofilms Microbiomes. 7, 33. https://doi.org/10.1038/s41522-021-00204-9 (2021).
Messiha, N. A. S. et al. Enhancement of soil suppressive potential to bacterial wilt disease caused by Ralstonia solanacearum. Arch. Phytopathol. Pflanzenschutz. 56. 1127–1165, https://doi.org/10.1080/03235408.2023.2267668 (2023).
D.M. Weller J.M. Raaijmakers B.B. McSpadden Gardener L.S. Thomashow Microbial populations responsible for specific soil suppressiveness to plant pathogens Annu. Rev. Phytopathol. 2002 40 309 348 1:CAS:528:DC%2BD38Xos1Cltbs%3D 10.1146/ANNUREV.PHYTO.40.030402.110010 12147763
Ossowicki, A. et al. Microbial and volatile profiling of soils suppressive to Fusarium culmorum of wheat. Proc. R. Soc. B.287. https://doi.org/10.1098/RSPB.2019.2527 (2020).
S. Sraphet B. Javadi Unraveling techniques for plant microbiome structure analysis Divers. 2022 14 206 1:CAS:528:DC%2BB38XhtVSmt7rE 10.3390/D14030206
D.M. Huber Effect of organic amendment on soil-borne plant pathogens Phytopathology. 1970 60 22 10.1094/PHYTO-60-22
Sledz, W., Zoledowska, S., Motyka, A., Kadzinski, L. & Banecki, B. Growth of bacterial phytopathogens in animal manures. Acta Biochim. Pol. 64. https://doi.org/10.18388/abp.2016_1389 (2017).
Dubois, G. E., Schaerer, S. & Dupuis, B. Factors impacting blackleg development caused by Dickeya spp. in the field. Eur. J. Plant. Pathol. 140, 317–327. https://doi.org/10.1007/s10658-014-0465-y (2014).
R. Czajkowski M.C.M. Pérombelon J.A. van Veen J.M. van der Wolf Control of blackleg and tuber soft rot of potato caused by Pectobacterium and Dickeya species: A review Plant Pathol. 2011 60 6 999 1013 10.1111/AAB.12166
Ouattara, H. G. et al. Implication of Bacillus sp. in the production of pectinolytic enzymes during cocoa fermentation. World J. Microbiol. Biotechnol.24, 1753–1760. https://doi.org/10.1007/s11274-008-9683-9 (2008).
R.G. McGuire A. Kelman Calcium in potato tuber cell walls in relation to tissue maceration by Erwinia carotovora pathovar atroseptica Phytopathology. 1986 76 4 401 406 1:CAS:528:DyaL28XktVelu7k%3D 10.1094/Phyto-76-401
Bain, R. A., Millard, P. & Perombelon, M. C. M. The resistance of potato plants to Erwinia carotovora subsp. atroseptica in relation to their calcium and magnesium content. Potato Res. 39(1), 185–193 (1996).
M. Potrykus et al. Simultaneous detection of major blackleg and soft rot bacterial pathogens in potato by multiplex polymerase chain reaction Ann. Appl. Biol. 2014 165 474 487 1:CAS:528:DC%2BC2cXhslyltrbM 10.1111/aab.12156 25506085 4260167
Darrasse, A., Priou, S., Kotoujansky, A., Bertheau, Y. PCR and restriction fragment length polymorphism of a pel gene as a tool to identify Erwinia carotovora in relation to potato diseases. Appl Environ Microbiol.60; https://doi.org/10.1128/aem.60.5.1437-1443 (1994).
Slawiak, M. et al. Biochemical and genetical analysis reveal a new clade of biovar 3 Dickeya spp. strains isolated from potato in Europe. Eur. J. Plant Pathol. 125, 245–261. https://doi.org/10.1007/s10658-009-9479-2 (2009).
M. Waleron K. Waleron A.J. Podhajska E. Lojkowska Genotyping of bacteria belonging to the former Erwinia genus by PCR-RFLP analysis of a recA gene fragment Microbiology. 2002 148 583 595 1:CAS:528:DC%2BD38XhsFSmtbo%3D 10.1099/00221287-148-2-583 11832521
Versalovic, J., Schneider, M., & Bruijn, F. Genomic fingerprinting of bacteria using repetitive sequence-based polymerase chain reaction. Methods Mol. Cell. Biol. (1994).
M. Ansermet S. Schaerer I. Kellenberger M. Tallant B. Dupuis Influence of seed- borne and soil- carried inocula of Dickeya spp. on potato plant transpiration and symptom expression Eur. J. Plant Pathol. 2016 145 459 467 1:CAS:528:DC%2BC28Xht1Klurg%3D 10.1007/s10658-016-0859-0
Hamed, S. M., Kamal, M., Messiha, N. A. S. Potential of algal-based products for the management of potato brown rot disease. Bot Stud.64, 29; https://doi.org/10.1186/s40529-023-00402-y (2023).
Y. Irikiin M. Nishiyama S. Otsuka K. Senoo Rhizobacterial community-level, sole carbon source utilization pattern affects the delay in the bacterial wilt of tomato grown in rhizobacterial community model system Appl. Soil Ecol. 2006 34 27 32 10.1016/j.apsoil.2005.12.003
L. Cangioli et al. Effect of site and phenological status on the potato bacterial rhizomicrobiota Microorganisms. 2022 10 1 1:CAS:528:DC%2BB38XisFGktrfJ 10.3390/microorganisms10091743
R.R. Puri et al. Metagenomic study of endophytic bacterial community of sweet potato (Ipomoea batatas) cultivated in different soil and climatic conditions World J. Microbiol. Biotechnol. 2019 35 1 1:CAS:528:DC%2BC1MXitFOrsL7F 10.1007/S11274-019-2754-2
L. Shivlata T. Satyanarayana Thermophilic and alkaliphilic Actinobacteria: biology and potential applications Front. Microbiol. 2015 1 1014 10.3389/fmicb.2015.01014
H.Y. Li et al. The chemodiversity of paddy soil dissolved organic matter correlates with microbial community at continental scales Microbiome. 2018 187 1 10.1186/s40168-018-0561-x
C. Yang D. Lv S. Jiang H. Lin et al. Soil salinity regulation of soil microbial carbon metabolic function in the Yellow River Delta Sci. Total Environ. 2021 790 1 1:CAS:528:DC%2BB3MXht1yhs77M 10.1016/j.scitotenv.2021.148258
D. Hu Y. Zang Y. Mao Identification of molecular markers that are specific to the class Thermoleophilia Front. Microbiol. 2019 10 1 10.3389/fmicb.2019.01185
S. Kumar S.S. Diksha R. Kumar Biofertilizers: An ecofriendly technology for nutrient recycling and environmental sustainability Curr. Res. Microb. Sci. 2022 3 100094 1:CAS:528:DC%2BB38XosFyjsLg%3D 10.1016/J.CRMICR.2021.100094 35024641
Y. Wang Y. Xu S. Xu J. Yang K. Wang X. Zhan Bacillus subtilis DSM29784 alleviates negative effects on growth performance in broilers by improving the intestinal health under necrotic enteritis challenge Front. Microbiol. 2021 12 1 10.3389/FMICB.2021.723187
Y. Zhao P. Li K. Huang Y. Wang H. Hu Y. Sun Control of postharvest soft rot caused by Erwinia carotovora of vegetables by a strain of Bacillus amyloliquefaciens and its potential modes of action World J. Microbiol. Biotechnol. 2013 29 411 420 1:CAS:528:DC%2BC3sXit1eisLo%3D 10.1007/s11274-012-1193-0 23117674
Li, Z. et al. Biocontrol potential of Myxococcus sp. strain BS against bacterial soft rot of calla lily caused by Pectobacterium carotovorum.Biol. Control. 126, 36–44; https://doi.org/10.1016/J.BIOCONTROL.2018.07.004 (2018).
N. Weinert et al. Bacterial diversity on the surface of potato tubers in soil and the influence of the plant genotype FEMS Microbiol. Ecol. 2010 74 114 123 1:CAS:528:DC%2BC3cXht1CmtrnM 10.1111/J.1574-6941.2010.00936.X 20698886
Radhakrishnan, R., Hashem, A., Abd Allah, E.F. Bacillus: A biological tool for crop improvement through bio-molecular changes in adverse environments. Front. Physiol.8, 667; https://doi.org/10.3389/FPHYS.2017.00667/BIBTEX (2017).
A.K. Saxena M. Kumar H. Chakdar N. Anuroopa D.J. Bagyaraj Bacillus species in soil as a natural resource for plant health and nutrition J. Appl. Microbiol. 2020 128 1583 1594 1:STN:280:DC%2BB3MjntVertg%3D%3D 10.1111/JAM.14506 31705597
F. Zhao et al. Vermicompost can suppress Fusarium oxysporum f. sp. lycopersici via generation of beneficial bacteria in a long-term tomato monoculture soil Plant Soil. 2019 440 491 505 1:CAS:528:DC%2BC1MXptlOhtLY%3D 10.1007/s11104-019-04104-y
S. Chungopast N. Phankamolsil W. Thaymuang A. Phommuangkhuk S. Karuna T. Inboonchuay Correlation of soil physiochemical properties, microorganism numbers, and bacterial communities following unburned and burned sugarcane harvest Appl. Environ. Soil Sci. 2023 1 1687 7667 1:CAS:528:DC%2BB3sXit1Oisb7I 10.1155/2023/9618349
W. Xiong et al. Distinct roles for soil fungal and bacterial communities associated with the suppression of vanilla Fusarium wilt disease Soil Biol. Biochem. 2017 107 198 207 1:CAS:528:DC%2BC2sXhsVelurw%3D 10.1016/J.SOILBIO.2017.01.010
Lacey, J. Ecology of Actinomycetes in fodders and related substrates. Zentralblatt fur Bakteriol. Parasitenkunde, Infekt. und Hyg (1978).
S. Kalam A. Basu A.R. Podile Functional and molecular characterization of plant growth promoting Bacillus isolates from tomato rhizosphere Heliyon. 2020 6 1 10.1016/J.HELIYON.2020.E04734
A. Beneduzi A. Ambrosini L.M. Passaglia Plant growth-promoting rhizobacteria (PGPR): Their potential as antagonists and biocontrol agents Genet. Mol. Biol. 2012 35 1044 1051 1:CAS:528:DC%2BC3sXhvV2gtL8%3D 10.1590/s1415-47572012000600020 23411488 3571425
Matilla, M. A. & Krell, T. Plant growth promotion and biocontrol mediated by plant-associated bacteria. In: Plant microbiome: Stress response. Springer. 5, 45–80. https://doi.org/10.1007/978-981-10-5514-0_3 (2018).
S. Jafra J. Przysowa A. Gwizdek-Wisniewska J.M. van der Wolf Potential of bulb-associated bacteria for biocontrol of hyacinth soft rot caused by Dickeya zeae J. Appl. Microbiol. 2009 106 268 277 1:CAS:528:DC%2BD1MXisVemtbc%3D 10.1111/j.1365-2672.2008.04000.x 19054227
A. Ossowicki S. Jafra P. Garbeva The antimicrobial volatile power of the rhizospheric isolate Pseudomonas donghuensis P482 PLoS ONE. 2017 12 1 1:CAS:528:DC%2BC2sXht1WjurnO 10.1371/journal.pone.0174362
N. Gerayeli S. Baghaee-Ravari S. Tarighi Evaluation of the antagonistic potential of Bacillus strains against Pectobacterium carotovorum subsp. carotovorum and their role in the induction of resistance to potato soft rot infection Eur. J. Plant Pathol. 2018 150 1049 1063 10.1007/s10658-017-1344-0
Y.R. Des Essarts et al. Biocontrol of the potato blackleg and soft rot diseases caused by Dickeya dianthicola Appl. Environ. Microbiol. 2016 82 268 278 2016ApEnM.82.268R 1:CAS:528:DC%2BC28XhsVKmsb%2FL 10.1128/AEM.02525-15
Sansinenea, E. Bacillus spp.: As Plant Growth-Promoting Bacteria. In: Singh, H., Keswani, C., Reddy, M., Sansinenea, E., García-Estrada, C. (eds) Secondary Metabolites of Plant Growth Promoting Rhizomicroorganisms. Springer. 225–237; https://doi.org/10.1007/978-981-13-5862-3_11 (2019).
S.G. Reynolds The gravimetric method of soil moisture determination Part I A study of equipment, and methodological problems J. Hydrol. 1970 11 3 10.1016/0022-1694(70)90066-1
J.C. Meneley Isolation of Soft-Rot Erwinia spp. from agricultural soils using an enrichment technique Phytopathology. 1976 66 367 10.1094/PHYTO-66-367
V. Hélias P. Hamon E. Huchet J.V.D. Wolf D. Andrivon Two new effective semiselective crystal violet pectate media for isolation of Pectobacterium and Dickeya Plant Pathol. 2012 61 339 345 10.1111/J.1365-3059.2011.02508.X
Laurila, J. et al. Symptoms and yield reduction caused by Dickeya spp. strains isolated from potato and river water in Finland. Eur. J. Plant Pathol. 126, 249–262. https://doi.org/10.1007/s10658-009-9537-9 (2010).
Frechon, D. et al. Evaluation of a PCR kit for the detection of Erwinia carotovora subsp. atroseptica on potato tubers. Potato Res.41, 163–173. https://doi.org/10.1007/BF02358439 (1998).
Kang, H. W., Kwon, S. W. & Go, S. J. PCR-based specific and sensitive detection of Pectobacterium carotovorum ssp. carotovorum by primers generated from a URP-PCR fingerprinting-derived polymorphic band. Plant Pathol. 52, 127–133. https://doi.org/10.1046/j.1365-3059.2003.00822.x (2003).
R. Sasada M. Weinstein A. Prem M. Jin J. Bhasin FIGARO: An efficient and objective tool for optimizing microbiome rRNA gene trimming parameters J. Biomol. Tech. 2020 31 1
Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet. J. 17, 10–12. https://doi.org/10.14806/EJ.17.1.200 (2011).
Andrews, S. FastQC: A Quality Control Tool for High Throughput Sequence Data http://www.bioinformatics.babraham.ac.uk/projects/fastqc/ (2010).
E. Bolyen et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2 Nat. Biotechnol. 2019 37 852 857 1:CAS:528:DC%2BC1MXhsVeksr%2FO 10.1038/S41587-019-0209-9 31341288 7015180
B.J. Callahan P.J. McMurdie M.J. Rosen A.W. Han A.J.A. Johnson S.P. Holmes DADA2: High-resolution sample inference from Illumina amplicon data Nat. Methods. 2016 13 581 583 1:CAS:528:DC%2BC28XosVWitb4%3D 10.1038/NMETH.3869 27214047 4927377
C. Quast et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools Nucleic Acids Res. 2013 41 1 10.1093/NAR/GKS1219
P.J. McMurdie S. Holmes phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data PLoS One. 2013 8 1 10.1371/JOURNAL.PONE.0061217
M.I. Love W. Huber S. Anders Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 Genome Biol. 2014 15 1 21 1:CAS:528:DC%2BC2MXjtVCrsL8%3D 10.1186/s13059-014-0550-8