Insight into the Bacterial Endophytic Communities of Peach Cultivars Related to Crown Gall Disease Resistance

Li, Qian; Guo, Rongjun; Li, Yujia; Hartman, Wyatt H.; Li, Shifang; Zhang, Zhixiang; Tringe, Susannah G.; Wang, Hongqing; Stabb, Eric V.

doi:10.1128/AEM.02931-18

Insight into the Bacterial Endophytic Communities of Peach Cultivars Related to Crown Gall Disease Resistance

Journal Article · Thu Apr 18 00:00:00 EDT 2019 · Applied and Environmental Microbiology

DOI:https://doi.org/10.1128/AEM.02931-18· OSTI ID:1581341

Li, Qian ^[1]; Guo, Rongjun ^[2]; Li, Yujia ^[2]; Hartman, Wyatt H. ^[3]; Li, Shifang ^[2]; Zhang, Zhixiang ^[2]; Tringe, Susannah G. ^[3]; Wang, Hongqing ^[4]; Stabb, Eric V. ^[5]

China Agriculture Univ., Beijing (China); Chinese Academy of Agricultural Sciences, Beijing (China); USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
Chinese Academy of Agricultural Sciences, Beijing (China)
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
China Agriculture Univ., Beijing (China)
Univ. of Georgia, Athens, GA (United States)

Crown gall disease caused by Agrobacterium tumefaciens severely impacts the production of peach and other fruit trees. Several peach cultivars are partially resistant to A. tumefaciens, but little is known about the roles of endophytic microbiota in disease resistance. In the present study, the endophytic bacterial communities of resistant and susceptible peach cultivars “Honggengansutao” and “Okinawa” were analyzed using universal 16S rRNA gene amplicon sequencing in parallel with the cultivation and characterization of bacterial isolates. A total of 1,357,088 high-quality sequences representing 3,160 distinct operational taxonomic units (OTUs; Proteobacteria, Actinobacteria, Bacteroidetes, and Firmicutes) and 1,200 isolates of 20 genera and 305 distinct ribotypes were collected from peach roots and twigs. It was found that factors including plant developmental stage, cultivar, and A. tumefaciens invasion strongly influenced the peach endophytic communities. The community diversity of endophytic bacteria and the abundance of culturable bacteria were both higher in the roots of the resistant cultivar, particularly after inoculation. Strikingly, the pathogen antagonists Streptomyces and Pseudomonas in roots and Rhizobium in twigs were most frequently detected in resistant plants. Our results suggest that the higher abundance and diversity of endophytic bacteria and increased proportions of antagonistic bacteria might contribute to the natural defense of the resistant cultivar against A. tumefaciens. This work reveals the relationships between endophytic bacteria and disease resistance in peach plants and provides important information for microbiome-based biocontrol of crown gall disease in fruit trees. Agrobacterium tumefaciens as the causal agent of peach crown gall disease can be controlled by planting resistant cultivars. This study profiles the endophytic bacteria in susceptible and resistant peach cultivars, advancing our understanding of the relationships between endophytic bacterial communities and peach crown gall disease, with potential implications for other complex microbiome-plant-pathogen interactions. The resistant cultivar may defend itself by increasing the diversity and abundance of beneficial endophytic bacteria. Finally, the antagonists identified among the genera Streptomyces, Pseudomonas, and Rhizobium may have application potential for biocontrol of crown gall disease in fruit trees.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: China Scholarship Council; USDOE Office of Science (SC)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1581341

Journal Information:: Applied and Environmental Microbiology, Journal Name: Applied and Environmental Microbiology Journal Issue: 9 Vol. 85; ISSN 0099-2240

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

References (80)

Tumour genes in plants: T-DNA encoded cytokinin biosynthesis Buchmann, Ilka; Marner, Franz-Josef; Schröder, Gudrun The EMBO Journal, Vol. 4, Issue 4 https://doi.org/10.1002/j.1460-2075.1985.tb03710.x	journal	April 1985
Lipopeptides from a novel Bacillus methylotrophicus 39b strain suppress Agrobacterium crown gall tumours on tomato plants: Potential of a B. methylotrophicus strain as a biological control agent for crown gall disease Frikha-Gargouri, Olfa; Ben Abdallah, Dorra; Ghorbel, Imen Pest Management Science, Vol. 73, Issue 3 https://doi.org/10.1002/ps.4331	journal	July 2016
Construction of a Tra− deletion mutant of pAgK84 to safeguard the biological control of crown gall Jones, David A.; Ryder, Maarten H.; Clare, Bruce G. Molecular and General Genetics MGG, Vol. 212, Issue 2 https://doi.org/10.1007/BF00334686	journal	May 1988
The host range of crown gall De Cleene, Marcel; De Ley, Jozef The Botanical Review, Vol. 42, Issue 4 https://doi.org/10.1007/BF02860827	journal	October 1976
The Diversity of Archaea and Bacteria in Association with the Roots of Zea mays L. Chelius, M. K.; Triplett, E. W. Microbial Ecology, Vol. 41, Issue 3 https://doi.org/10.1007/s002480000087	journal	February 2001
Biological control of apple crown gall by nonpathogenic Rhizobium vitis strain VAR03-1 Kawaguchi, Akira; Kondo, Ken-ichi; Inoue, Koji Journal of General Plant Pathology, Vol. 78, Issue 4 https://doi.org/10.1007/s10327-012-0388-4	journal	June 2012
Determination of tumorigenic Agrobacterium density in soil by real-time PCR assay and its effect on crown gall disease severity Li, Qian; Guo, Rong-Jun; Li, Shi-Dong European Journal of Plant Pathology, Vol. 142, Issue 1 https://doi.org/10.1007/s10658-014-0586-3	journal	January 2015
The root microbiota—a fingerprint in the soil? Kristin, Aleklett; Miranda, Hart Plant and Soil, Vol. 370, Issue 1-2 https://doi.org/10.1007/s11104-013-1647-7	journal	March 2013
Reviving of the endophytic bacterial community as a putative mechanism of plant resistance Podolich, Olga; Ardanov, Pavlo; Zaets, Iryna Plant and Soil, Vol. 388, Issue 1-2 https://doi.org/10.1007/s11104-014-2235-1	journal	August 2014
Isolation of Endophytic Actinomycetes from Different Cultivars of Tomato and their Activities Against Ralstonia solanacearum in Vitro Tan, H. M.; Cao, L. X.; He, Z. F. World Journal of Microbiology and Biotechnology, Vol. 22, Issue 12 https://doi.org/10.1007/s11274-006-9172-y	journal	April 2006
Identification and characterization of endophytic bacteria isolated from in vitro cultures of peach and pear rootstocks Liaqat, Fakhra; Eltem, Rengin 3 Biotech, Vol. 6, Issue 2 https://doi.org/10.1007/s13205-016-0442-6	journal	June 2016
Biological control of crown gall through bacteriocin production Kerr, A.; Htay, Khin Physiological Plant Pathology, Vol. 4, Issue 1 https://doi.org/10.1016/0048-4059(74)90042-3	journal	January 1974
A study on microbial diversity in different cultivars of Brassica napus in relation to its wilt pathogen, Verticillium longisporum GranÃ©r, Georg; Persson, Paula; Meijer, Johan FEMS Microbiology Letters, Vol. 224, Issue 2 https://doi.org/10.1016/S0378-1097(03)00449-X	journal	July 2003
Agrobacterium tumefaciens as an agent of disease Escobar, Matthew A.; Dandekar, Abhaya M. Trends in Plant Science, Vol. 8, Issue 8 https://doi.org/10.1016/S1360-1385(03)00162-6	journal	August 2003
Efficacy of native antagonistic bacterial isolates in biological control of crown gall disease in Egypt Tolba, I. H.; Soliman, M. A. Annals of Agricultural Sciences, Vol. 58, Issue 1 https://doi.org/10.1016/j.aoas.2013.01.007	journal	June 2013
Relationship between root-endophytic microbial communities and replant disease in specialized apple growing areas in Europe Manici, L. M.; Kelderer, M.; Franke-Whittle, I. H. Applied Soil Ecology, Vol. 72 https://doi.org/10.1016/j.apsoil.2013.07.011	journal	October 2013
Fungal endophyte diversity and community patterns in healthy and yellowing leaves of Citrus limon Douanla-Meli, C.; Langer, E.; Talontsi Mouafo, F. Fungal Ecology, Vol. 6, Issue 3 https://doi.org/10.1016/j.funeco.2013.01.004	journal	June 2013
Impact of metagenomic DNA extraction procedures on the identifiable endophytic bacterial diversity in Sorghum bicolor (L. Moench) Maropola, Mapula Kgomotso Annah; Ramond, Jean-Baptiste; Trindade, Marla Journal of Microbiological Methods, Vol. 112 https://doi.org/10.1016/j.mimet.2015.03.012	journal	May 2015
Adaptation, specialization, and coevolution within phytobiomes Baltrus, David A. Current Opinion in Plant Biology, Vol. 38 https://doi.org/10.1016/j.pbi.2017.04.023	journal	August 2017
Roots from distinct plant developmental stages are capable of rapidly selecting their own microbiome without the influence of environmental and soil edaphic factors Yuan, Jun; Chaparro, Jacqueline M.; Manter, Daniel K. Soil Biology and Biochemistry, Vol. 89 https://doi.org/10.1016/j.soilbio.2015.07.009	journal	October 2015
Random Forests Breiman, Leo Machine Learning, Vol. 45, Issue 1, p. 5-32 https://doi.org/10.1023/A:1010933404324	journal	January 2001
Where less may be more: how the rare biosphere pulls ecosystems strings Jousset, Alexandre; Bienhold, Christina; Chatzinotas, Antonis The ISME Journal, Vol. 11, Issue 4 https://doi.org/10.1038/ismej.2016.174	journal	January 2017
Defining the core Arabidopsis thaliana root microbiome Lundberg, Derek S.; Lebeis, Sarah L.; Paredes, Sur Herrera Nature, Vol. 488, Issue 7409 https://doi.org/10.1038/nature11237	journal	August 2012
Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota Bulgarelli, Davide; Rott, Matthias; Schlaeppi, Klaus Nature, Vol. 488, Issue 7409 https://doi.org/10.1038/nature11336	journal	August 2012
UPARSE: highly accurate OTU sequences from microbial amplicon reads Edgar, Robert C. Nature Methods, Vol. 10, Issue 10 https://doi.org/10.1038/nmeth.2604	journal	August 2013
QIIME allows analysis of high-throughput community sequencing data Caporaso, J. Gregory; Kuczynski, Justin; Stombaugh, Jesse Nature Methods, Vol. 7, Issue 5 https://doi.org/10.1038/nmeth.f.303	journal	April 2010
Involvement of Burkholderiaceae and sulfurous volatiles in disease-suppressive soils Carrión, Víctor J.; Cordovez, Viviane; Tyc, Olaf The ISME Journal, Vol. 12, Issue 9 https://doi.org/10.1038/s41396-018-0186-x	journal	June 2018
Metagenomic insights into communities, functions of endophytes and their associates with infection by root-knot nematode, Meloidogyne incognita, in tomato roots Tian, Bao-Yu; Cao, Yi; Zhang, Ke-Qin Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep17087	journal	November 2015
Purification and characterization of an antibacterial compound produced by Agrobacterium vitis strain E26 with activity against A. tumefaciens Wang, H. M.; Wang, H. X.; Ng, T. B. Plant Pathology, Vol. 52, Issue 2 https://doi.org/10.1046/j.1365-3059.2003.00807.x	journal	April 2003
Microbial diversity determines the invasion of soil by a bacterial pathogen van Elsas, J. D.; Chiurazzi, M.; Mallon, C. A. Proceedings of the National Academy of Sciences, Vol. 109, Issue 4 https://doi.org/10.1073/pnas.1109326109	journal	January 2012
Diversity and heritability of the maize rhizosphere microbiome under field conditions Peiffer, J. A.; Spor, A.; Koren, O. Proceedings of the National Academy of Sciences, Vol. 110, Issue 16 https://doi.org/10.1073/pnas.1302837110	journal	April 2013
Structure, variation, and assembly of the root-associated microbiomes of rice Edwards, Joseph; Johnson, Cameron; Santos-Medellín, Christian Proceedings of the National Academy of Sciences, Vol. 112, Issue 8 https://doi.org/10.1073/pnas.1414592112	journal	January 2015
Lignin engineering in field-grown poplar trees affects the endosphere bacterial microbiome Beckers, Bram; Op De Beeck, Michiel; Weyens, Nele Proceedings of the National Academy of Sciences, Vol. 113, Issue 8 https://doi.org/10.1073/pnas.1523264113	journal	January 2016
T-DNA of Agrobacterium tumefaciens encodes an enzyme of cytokinin biosynthesis. Akiyoshi, D. E.; Klee, H.; Amasino, R. M. Proceedings of the National Academy of Sciences, Vol. 81, Issue 19 https://doi.org/10.1073/pnas.81.19.5994	journal	October 1984
Susceptibility of five Prunus rootstocks to Agrobacterium tumefaciens Thomidis, T.; Exadaktylou, E.; Tsipouridis, C. New Zealand Journal of Crop and Horticultural Science, Vol. 33, Issue 4 https://doi.org/10.1080/01140671.2005.9514368	journal	December 2005
Biological Control of Crown Gall in Grapevine and Raspberry by Two Pseudomonas spp. with a Wide Spectrum of Antagonistic Activity Khmel, I. A.; Sorokina, T. A.; Lemanova, N. B. Biocontrol Science and Technology, Vol. 8, Issue 1 https://doi.org/10.1080/09583159830423	journal	March 1998
Search and clustering orders of magnitude faster than BLAST Edgar, Robert C. Bioinformatics, Vol. 26, Issue 19, p. 2460-2461 https://doi.org/10.1093/bioinformatics/btq461	journal	August 2010
FLASH: fast length adjustment of short reads to improve genome assemblies Magoc, T.; Salzberg, S. L. Bioinformatics, Vol. 27, Issue 21 https://doi.org/10.1093/bioinformatics/btr507	journal	September 2011
Streptomyces as a plant's best friend? Viaene, Tom; Langendries, Sarah; Beirinckx, Stien FEMS Microbiology Ecology, Vol. 92, Issue 8 https://doi.org/10.1093/femsec/fiw119	journal	June 2016
SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB Pruesse, E.; Quast, C.; Knittel, K. Nucleic Acids Research, Vol. 35, Issue 21 https://doi.org/10.1093/nar/gkm864	journal	November 2007
The SILVA ribosomal RNA gene database project: improved data processing and web-based tools Quast, Christian; Pruesse, Elmar; Yilmaz, Pelin Nucleic Acids Research, Vol. 41, Issue D1 https://doi.org/10.1093/nar/gks1219	journal	November 2012
Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees Letunic, Ivica; Bork, Peer Nucleic Acids Research, Vol. 44, Issue W1 https://doi.org/10.1093/nar/gkw290	journal	April 2016
Crown Gall of Peaches from Maryland, South Carolina, and Tennessee and Problems with Biological Control Alconero, R. Plant Disease, Vol. 64, Issue 9 https://doi.org/10.1094/PD-64-835	journal	January 1980
Crown gall Kado, C. I. The Plant Health Instructor https://doi.org/10.1094/PHI-I-2002-1118-01	journal	January 2002
Biological Control of Crown Gall with an Agrocin Mutant of Agrobacterium radiobacter Cooksey, D. A. Phytopathology, Vol. 72, Issue 7 https://doi.org/10.1094/Phyto-72-919	journal	January 1982
Dose-Response Relationships in Biological Control of Fusarium Wilt of Radish by Pseudomonas spp. Raaijmakers, Jos M. Phytopathology, Vol. 85, Issue 10 https://doi.org/10.1094/Phyto-85-1075	journal	January 1995
A revision of Rhizobium Frank 1889, with an emended description of the genus, and the inclusion of all species of Agrobacterium Conn 1942 and Allorhizobium undicola de Lajudie et al. 1998 as new combinations: Rhizobium radiobacter, R. rhizogenes, R. rubi, R. undicola and R. vitis. Kuykendall, L. D.; Kerr, A.; Young, J. M. International Journal of Systematic and Evolutionary Microbiology, Vol. 51, Issue 1 https://doi.org/10.1099/00207713-51-1-89	journal	January 2001
Chemotaxis of Rhizobium spp. to Plant Root Exudates Currier, William W.; Strobel, Gary A. Plant Physiology, Vol. 57, Issue 5 https://doi.org/10.1104/pp.57.5.820	journal	May 1976
Biological Control of Crown Gall: Field Measurements and Glasshouse Experiments New, P. B.; Kerr, A. Journal of Applied Bacteriology, Vol. 35, Issue 2 https://doi.org/10.1111/j.1365-2672.1972.tb03699.x	journal	June 1972
Broad-range antagonistic rhizobacteria Pseudomonas fluorescens and Serratia plymuthica suppress Agrobacterium crown gall tumours on tomato plants: Biocontrol of Agrobacterium by bacterial antagonists Dandurishvili, N.; Toklikishvili, N.; Ovadis, M. Journal of Applied Microbiology, Vol. 110, Issue 1 https://doi.org/10.1111/j.1365-2672.2010.04891.x	journal	November 2010
Inhibitory effect of ACC deaminase-producing bacteria on crown gall formation in tomato plants infected by Agrobacterium tumefaciens or A. vitis: Inhibition of crown gall by ACC deaminase-producing bacteria Toklikishvili, N.; Dandurishvili, N.; Vainstein, A. Plant Pathology, Vol. 59, Issue 6 https://doi.org/10.1111/j.1365-3059.2010.02326.x	journal	July 2010
A new method for non-parametric multivariate analysis of variance: NON-PARAMETRIC MANOVA FOR ECOLOGY Anderson, Marti J. Austral Ecology, Vol. 26, Issue 1 https://doi.org/10.1111/j.1442-9993.2001.01070.pp.x	journal	February 2001
Optimization and biochemical characterization of a bacteriocin from a newly isolated Bacillus subtilis strain 14B for biocontrol of Agrobacterium spp . strains Hammami, I.; Rhouma, A.; Jaouadi, B. Letters in Applied Microbiology, Vol. 48, Issue 2 https://doi.org/10.1111/j.1472-765X.2008.02524.x	journal	February 2009
Characterization of culturable bacterial endophytes of switchgrass ( Panicum virgatum L.) and their capacity to influence plant growth Xia, Ye; Greissworth, Eliana; Mucci, Curtis GCB Bioenergy, Vol. 5, Issue 6 https://doi.org/10.1111/j.1757-1707.2012.01208.x	journal	September 2012
Bacillus amyloliquefaciens strain 32a as a source of lipopeptides for biocontrol of Agrobacterium tumefaciens strains Ben Abdallah, D.; Frikha-Gargouri, O.; Tounsi, S. Journal of Applied Microbiology, Vol. 119, Issue 1 https://doi.org/10.1111/jam.12797	journal	April 2015
Culturable endophytic bacterial communities associated with field-grown soybean de Almeida Lopes, K. B.; Carpentieri-Pipolo, V.; Oro, T. H. Journal of Applied Microbiology, Vol. 120, Issue 3 https://doi.org/10.1111/jam.13046	journal	February 2016
Deciphering the Rhizosphere Microbiome for Disease-Suppressive Bacteria Mendes, R.; Kruijt, M.; de Bruijn, I. Science, Vol. 332, Issue 6033 https://doi.org/10.1126/science.1203980	journal	May 2011
Restructuring of Endophytic Bacterial Communities in Grapevine Yellows-Diseased and Recovered Vitis vinifera L. Plants Bulgari, Daniela; Casati, Paola; Crepaldi, Paola Applied and Environmental Microbiology, Vol. 77, Issue 14 https://doi.org/10.1128/AEM.00051-11	journal	May 2011
Grapevine (Vitis vinifera) Crown Galls Host Distinct Microbiota Faist, Hanna; Keller, Alexander; Hentschel, Ute Applied and Environmental Microbiology, Vol. 82, Issue 18 https://doi.org/10.1128/AEM.01131-16	journal	July 2016
Cocolonization of the Rhizosphere by Pathogenic Agrobacterium Strains and Nonpathogenic Strains K84 and K1026, Used for Crown Gall Biocontrol Penyalver, Ramón; López, María M. Applied and Environmental Microbiology, Vol. 65, Issue 5 https://doi.org/10.1128/AEM.65.5.1936-1940.1999	journal	May 1999
Diversity of Endophytic Bacterial Populations and Their Interaction with Xylella fastidiosa in Citrus Plants Araujo, W. L.; Marcon, J.; Maccheroni, W. Applied and Environmental Microbiology, Vol. 68, Issue 10 https://doi.org/10.1128/AEM.68.10.4906-4914.2002	journal	October 2002
Response of Endophytic Bacterial Communities in Potato Plants to Infection with Erwinia carotovora subsp. atroseptica Reiter, B.; Pfeifer, U.; Schwab, H. Applied and Environmental Microbiology, Vol. 68, Issue 5 https://doi.org/10.1128/AEM.68.5.2261-2268.2002	journal	May 2002
The Hidden World within Plants: Ecological and Evolutionary Considerations for Defining Functioning of Microbial Endophytes Hardoim, Pablo R.; van Overbeek, Leonard S.; Berg, Gabriele Microbiology and Molecular Biology Reviews, Vol. 79, Issue 3 https://doi.org/10.1128/MMBR.00050-14	journal	July 2015
Host range conferred by the virulence-specifying plasmid of Agrobacterium tumefaciens Loper, J. E.; Kado, C. I. Journal of Bacteriology, Vol. 139, Issue 2 https://doi.org/10.1128/jb.139.2.591-596.1979	journal	August 1979
Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. Fuqua, W. C.; Winans, S. C.; Greenberg, E. P. Journal of Bacteriology, Vol. 176, Issue 2 https://doi.org/10.1128/jb.176.2.269-275.1994	journal	January 1994
Structure and Functions of the Bacterial Microbiota of Plants Bulgarelli, Davide; Schlaeppi, Klaus; Spaepen, Stijn Annual Review of Plant Biology, Vol. 64, Issue 1 https://doi.org/10.1146/annurev-arplant-050312-120106	journal	April 2013
Bacterial Communities Associated with the Leaves and the Roots of Arabidopsis thaliana Bodenhausen, Natacha; Horton, Matthew W.; Bergelson, Joy PLoS ONE, Vol. 8, Issue 2 https://doi.org/10.1371/journal.pone.0056329	journal	February 2013
phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data McMurdie, Paul J.; Holmes, Susan PLoS ONE, Vol. 8, Issue 4 https://doi.org/10.1371/journal.pone.0061217	journal	April 2013
Non-random species loss in bacterial communities reduces antifungal volatile production Hol, W. H. Gera; Garbeva, Paolina; Hordijk, Cornelis Ecology, Vol. 96, Issue 8 https://doi.org/10.1890/14-2359.1	journal	August 2015
Systemic Acquired Resistance Induced by Agrobacterium tumefaciens in Peach and Differential Expression of PR1 Genes Hao, Fengge; Wang, Lirong; Cao, Ke HortScience, Vol. 50, Issue 5 https://doi.org/10.21273/HORTSCI.50.5.666	journal	May 2015
The Use of Beneficial Microbial Endophytes for Plant Biomass and Stress Tolerance Improvement Mei, Chuansheng; Flinn, Barry Recent Patents on Biotechnology, Vol. 4, Issue 1 https://doi.org/10.2174/187220810790069523	journal	January 2010
Biological Control of Crown Gall on Peach and Cherry Rootstock Colt by Native Agrobacterium radiobacter Isolates~!2009-05-11~!2009-08-25~!2010-02-11~! Gupta, A. K.; Khosla, Kishore; Bhardwaj, S. S. The Open Horticulture Journal, Vol. 3, Issue 1 https://doi.org/10.2174/1874840601003010001	journal	March 2010
Unraveling the plant microbiome: looking back and future perspectives Berg, Gabriele; Grube, Martin; Schloter, Michael Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00148	journal	June 2014
Root-associated bacterial endophytes from Ralstonia solanacearum resistant and susceptible tomato cultivars and their pathogen antagonistic effects Upreti, Reshmi; Thomas, Pious Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00255	journal	April 2015
Cross-Kingdom Similarities in Microbiome Ecology and Biocontrol of Pathogens Berg, Gabriele; Krause, Robert; Mendes, Rodrigo Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.01311	journal	November 2015
The potential for give and take in plantâ€“microbiome relationships Lebeis, Sarah L. Frontiers in Plant Science, Vol. 5 https://doi.org/10.3389/fpls.2014.00287	journal	June 2014
A Community-Based Culture Collection for Targeting Novel Plant Growth-Promoting Bacteria from the Sugarcane Microbiome Armanhi, Jaderson Silveira Leite; de Souza, Rafael Soares Correa; Damasceno, Natália de Brito Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.02191	journal	January 2018
Bacterial Endophyte Colonization and Distribution within Plants Kandel, Shyam; Joubert, Pierre; Doty, Sharon Microorganisms, Vol. 5, Issue 4 https://doi.org/10.3390/microorganisms5040077	journal	November 2017
Inside the root microbiome: Bacterial root endophytes and plant growth promotion Gaiero, Jonathan R.; McCall, Crystal A.; Thompson, Karen A. American Journal of Botany, Vol. 100, Issue 9 https://doi.org/10.3732/ajb.1200572	journal	September 2013
Endophytic Fungi from Wild Banana (Musa acuminata Colla) Works Against Anthracnose Disease Caused by Colletotrichum musae ., W. Nuangmek; ., E. H. C. McKenzie; ., S. Lumyong Research Journal of Microbiology, Vol. 3, Issue 5 https://doi.org/10.3923/jm.2008.368.374	journal	May 2008

Cited By (1)

Changes of Root Endophytic Bacterial Community Along a Chronosequence of Intensively Managed Lei Bamboo (Phyllostachys praecox) Forests in Subtropical China Zhang, Xiaoping; Zhong, Zheke; Gai, Xu Microorganisms, Vol. 7, Issue 12 https://doi.org/10.3390/microorganisms7120616	journal	November 2019

Similar Records

Crown gall transformation of tobacco callus cells by cocultivation with Agrobacterium tumefaciens

Journal Article · Mon Sep 17 00:00:00 EDT 1984 · Biochem. Biophys. Res. Commun.; (United States) · OSTI ID:5956551

Relatively rare root endophytic bacteria drive plant resource allocation patterns and tissue nutrient concentration in unpredictable ways

Journal Article · Sun Oct 27 20:00:00 EDT 2019 · American Journal of Botany · OSTI ID:1606051

Distinct Microbial Communities within the Endosphere and Rhizosphere of Populus deltoides Roots across Contrasting Soil Types.

Journal Article · Fri Dec 31 23:00:00 EST 2010 · Applied and Environmental Microbiology · OSTI ID:1024268

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
agrobacterium tumefaciens
crown gall disease
endophytic bacteria
high-throughput sequencing
peach
resistance

Insight into the Bacterial Endophytic Communities of Peach Cultivars Related to Crown Gall Disease Resistance

Citation Formats

References (80)

Cited By (1)

Similar Records

Related Subjects