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

Abstract

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 ofmore » 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.« less

Authors:
 [1];  [2];  [2];  [3];  [2];  [2];  [3];  [4];  [5]
+ Show Author Affiliations
  1. China Agriculture Univ., Beijing (China); Chinese Academy of Agricultural Sciences, Beijing (China); USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  2. Chinese Academy of Agricultural Sciences, Beijing (China)
  3. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  4. China Agriculture Univ., Beijing (China)
  5. Univ. of Georgia, Athens, GA (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC); China Scholarship Council
OSTI Identifier:
1581341
Grant/Contract Number:  
AC02-05CH11231; 201606350017
Resource Type:
Accepted Manuscript
Journal Name:
Applied and Environmental Microbiology
Additional Journal Information:
Journal Volume: 85; Journal Issue: 9; Journal ID: ISSN 0099-2240
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; agrobacterium tumefaciens; crown gall disease; endophytic bacteria; high-throughput sequencing; peach; resistance

Citation Formats

Li, Qian, Guo, Rongjun, Li, Yujia, Hartman, Wyatt H., Li, Shifang, Zhang, Zhixiang, Tringe, Susannah G., Wang, Hongqing, and Stabb, Eric V. Insight into the Bacterial Endophytic Communities of Peach Cultivars Related to Crown Gall Disease Resistance. United States: N. p., 2019. Web. doi:10.1128/AEM.02931-18.
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Li, Qian, Guo, Rongjun, Li, Yujia, Hartman, Wyatt H., Li, Shifang, Zhang, Zhixiang, Tringe, Susannah G., Wang, Hongqing, & Stabb, Eric V. Insight into the Bacterial Endophytic Communities of Peach Cultivars Related to Crown Gall Disease Resistance. United States. https://doi.org/10.1128/AEM.02931-18
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Li, Qian, Guo, Rongjun, Li, Yujia, Hartman, Wyatt H., Li, Shifang, Zhang, Zhixiang, Tringe, Susannah G., Wang, Hongqing, and Stabb, Eric V. Thu . "Insight into the Bacterial Endophytic Communities of Peach Cultivars Related to Crown Gall Disease Resistance". United States. https://doi.org/10.1128/AEM.02931-18. https://www.osti.gov/servlets/purl/1581341.
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@article{osti_1581341,
title = {Insight into the Bacterial Endophytic Communities of Peach Cultivars Related to Crown Gall Disease Resistance},
author = {Li, Qian and Guo, Rongjun and Li, Yujia and Hartman, Wyatt H. and Li, Shifang and Zhang, Zhixiang and Tringe, Susannah G. and Wang, Hongqing and Stabb, Eric V.},
abstractNote = {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.},
doi = {10.1128/AEM.02931-18},
journal = {Applied and Environmental Microbiology},
number = 9,
volume = 85,
place = {United States},
year = {Thu Apr 18 00:00:00 EDT 2019},
month = {Thu Apr 18 00:00:00 EDT 2019}
}
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https://doi.org/10.1128/AEM.02931-18
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Works referenced in this record:

Culturable endophytic bacterial communities associated with field-grown soybean
journal, February 2016

  • de Almeida Lopes, K. B.; Carpentieri-Pipolo, V.; Oro, T. H.
  • Journal of Applied Microbiology, Vol. 120, Issue 3
  • DOI: 10.1111/jam.13046

Bacillus amyloliquefaciens strain 32a as a source of lipopeptides for biocontrol of Agrobacterium tumefaciens strains
journal, April 2015

  • Ben Abdallah, D.; Frikha-Gargouri, O.; Tounsi, S.
  • Journal of Applied Microbiology, Vol. 119, Issue 1
  • DOI: 10.1111/jam.12797

T-DNA of Agrobacterium tumefaciens encodes an enzyme of cytokinin biosynthesis.
journal, October 1984

  • Akiyoshi, D. E.; Klee, H.; Amasino, R. M.
  • Proceedings of the National Academy of Sciences, Vol. 81, Issue 19
  • DOI: 10.1073/pnas.81.19.5994

Impact of metagenomic DNA extraction procedures on the identifiable endophytic bacterial diversity in Sorghum bicolor (L. Moench)
journal, May 2015

  • Maropola, Mapula Kgomotso Annah; Ramond, Jean-Baptiste; Trindade, Marla
  • Journal of Microbiological Methods, Vol. 112
  • DOI: 10.1016/j.mimet.2015.03.012

Involvement of Burkholderiaceae and sulfurous volatiles in disease-suppressive soils
journal, June 2018

The Hidden World within Plants: Ecological and Evolutionary Considerations for Defining Functioning of Microbial Endophytes
journal, July 2015

  • Hardoim, Pablo R.; van Overbeek, Leonard S.; Berg, Gabriele
  • Microbiology and Molecular Biology Reviews, Vol. 79, Issue 3
  • DOI: 10.1128/MMBR.00050-14

Microbial diversity determines the invasion of soil by a bacterial pathogen
journal, January 2012

  • van Elsas, J. D.; Chiurazzi, M.; Mallon, C. A.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 4
  • DOI: 10.1073/pnas.1109326109

Structure, variation, and assembly of the root-associated microbiomes of rice
journal, January 2015

  • Edwards, Joseph; Johnson, Cameron; Santos-Medellín, Christian
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 8
  • DOI: 10.1073/pnas.1414592112

Reviving of the endophytic bacterial community as a putative mechanism of plant resistance
journal, August 2014

Deciphering the Rhizosphere Microbiome for Disease-Suppressive Bacteria
journal, May 2011

Diversity of Endophytic Bacterial Populations and Their Interaction with Xylella fastidiosa in Citrus Plants
journal, October 2002

Streptomyces as a plant's best friend?
journal, June 2016

  • Viaene, Tom; Langendries, Sarah; Beirinckx, Stien
  • FEMS Microbiology Ecology, Vol. 92, Issue 8
  • DOI: 10.1093/femsec/fiw119

Defining the core Arabidopsis thaliana root microbiome
journal, August 2012

  • Lundberg, Derek S.; Lebeis, Sarah L.; Paredes, Sur Herrera
  • Nature, Vol. 488, Issue 7409
  • DOI: 10.1038/nature11237

Relationship between root-endophytic microbial communities and replant disease in specialized apple growing areas in Europe
journal, October 2013

Lignin engineering in field-grown poplar trees affects the endosphere bacterial microbiome
journal, January 2016

  • Beckers, Bram; Op De Beeck, Michiel; Weyens, Nele
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 8
  • DOI: 10.1073/pnas.1523264113

Isolation of Endophytic Actinomycetes from Different Cultivars of Tomato and their Activities Against Ralstonia solanacearum in Vitro
journal, April 2006

  • Tan, H. M.; Cao, L. X.; He, Z. F.
  • World Journal of Microbiology and Biotechnology, Vol. 22, Issue 12
  • DOI: 10.1007/s11274-006-9172-y

FLASH: fast length adjustment of short reads to improve genome assemblies
journal, September 2011

The Diversity of Archaea and Bacteria in Association with the Roots of Zea mays L.
journal, February 2001

The potential for give and take in plant–microbiome relationships
journal, June 2014

Unraveling the plant microbiome: looking back and future perspectives
journal, June 2014

A Community-Based Culture Collection for Targeting Novel Plant Growth-Promoting Bacteria from the Sugarcane Microbiome
journal, January 2018

  • Armanhi, Jaderson Silveira Leite; de Souza, Rafael Soares Correa; Damasceno, Natália de Brito
  • Frontiers in Plant Science, Vol. 8
  • DOI: 10.3389/fpls.2017.02191

The Use of Beneficial Microbial Endophytes for Plant Biomass and Stress Tolerance Improvement
journal, January 2010

Search and clustering orders of magnitude faster than BLAST
journal, August 2010

Biological control of crown gall through bacteriocin production
journal, January 1974

phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data
journal, April 2013

Biological control of apple crown gall by nonpathogenic Rhizobium vitis strain VAR03-1
journal, June 2012

  • Kawaguchi, Akira; Kondo, Ken-ichi; Inoue, Koji
  • Journal of General Plant Pathology, Vol. 78, Issue 4
  • DOI: 10.1007/s10327-012-0388-4

UPARSE: highly accurate OTU sequences from microbial amplicon reads
journal, August 2013

Biological Control of Crown Gall: Field Measurements and Glasshouse Experiments
journal, June 1972

Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees
journal, April 2016

  • Letunic, Ivica; Bork, Peer
  • Nucleic Acids Research, Vol. 44, Issue W1
  • DOI: 10.1093/nar/gkw290

Tumour genes in plants: T-DNA encoded cytokinin biosynthesis
journal, April 1985

Fungal endophyte diversity and community patterns in healthy and yellowing leaves of Citrus limon
journal, June 2013

Adaptation, specialization, and coevolution within phytobiomes
journal, August 2017

The SILVA ribosomal RNA gene database project: improved data processing and web-based tools
journal, November 2012

  • Quast, Christian; Pruesse, Elmar; Yilmaz, Pelin
  • Nucleic Acids Research, Vol. 41, Issue D1
  • DOI: 10.1093/nar/gks1219

The host range of crown gall
journal, October 1976

  • De Cleene, Marcel; De Ley, Jozef
  • The Botanical Review, Vol. 42, Issue 4
  • DOI: 10.1007/BF02860827

Agrobacterium tumefaciens as an agent of disease
journal, August 2003

Dose-Response Relationships in Biological Control of Fusarium Wilt of Radish by Pseudomonas spp.
journal, January 1995

Where less may be more: how the rare biosphere pulls ecosystems strings
journal, January 2017

  • Jousset, Alexandre; Bienhold, Christina; Chatzinotas, Antonis
  • The ISME Journal, Vol. 11, Issue 4
  • DOI: 10.1038/ismej.2016.174

Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators.
journal, January 1994

SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB
journal, November 2007

  • Pruesse, E.; Quast, C.; Knittel, K.
  • Nucleic Acids Research, Vol. 35, Issue 21
  • DOI: 10.1093/nar/gkm864

The root microbiota—a fingerprint in the soil?
journal, March 2013

Chemotaxis of Rhizobium spp. to Plant Root Exudates
journal, May 1976

  • Currier, William W.; Strobel, Gary A.
  • Plant Physiology, Vol. 57, Issue 5
  • DOI: 10.1104/pp.57.5.820

Cross-Kingdom Similarities in Microbiome Ecology and Biocontrol of Pathogens
journal, November 2015

Bacterial Endophyte Colonization and Distribution within Plants
journal, November 2017

Efficacy of native antagonistic bacterial isolates in biological control of crown gall disease in Egypt
journal, June 2013

Crown gall
journal, January 2002

Grapevine (Vitis vinifera) Crown Galls Host Distinct Microbiota
journal, July 2016

  • Faist, Hanna; Keller, Alexander; Hentschel, Ute
  • Applied and Environmental Microbiology, Vol. 82, Issue 18
  • DOI: 10.1128/AEM.01131-16

QIIME allows analysis of high-throughput community sequencing data
journal, April 2010

  • Caporaso, J. Gregory; Kuczynski, Justin; Stombaugh, Jesse
  • Nature Methods, Vol. 7, Issue 5
  • DOI: 10.1038/nmeth.f.303

Determination of tumorigenic Agrobacterium density in soil by real-time PCR assay and its effect on crown gall disease severity
journal, January 2015

  • Li, Qian; Guo, Rong-Jun; Li, Shi-Dong
  • European Journal of Plant Pathology, Vol. 142, Issue 1
  • DOI: 10.1007/s10658-014-0586-3

Endophytic Fungi from Wild Banana (Musa acuminata Colla) Works Against Anthracnose Disease Caused by Colletotrichum musae
journal, May 2008

  • ., W. Nuangmek; ., E. H. C. McKenzie; ., S. Lumyong
  • Research Journal of Microbiology, Vol. 3, Issue 5
  • DOI: 10.3923/jm.2008.368.374

Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota
journal, August 2012

  • Bulgarelli, Davide; Rott, Matthias; Schlaeppi, Klaus
  • Nature, Vol. 488, Issue 7409
  • DOI: 10.1038/nature11336

Bacterial Communities Associated with the Leaves and the Roots of Arabidopsis thaliana
journal, February 2013

Response of Endophytic Bacterial Communities in Potato Plants to Infection with Erwinia carotovora subsp. atroseptica
journal, May 2002

Construction of a Tra− deletion mutant of pAgK84 to safeguard the biological control of crown gall
journal, May 1988

  • Jones, David A.; Ryder, Maarten H.; Clare, Bruce G.
  • Molecular and General Genetics MGG, Vol. 212, Issue 2
  • DOI: 10.1007/BF00334686

Biological Control of Crown Gall in Grapevine and Raspberry by Two Pseudomonas spp. with a Wide Spectrum of Antagonistic Activity
journal, March 1998

  • Khmel, I. A.; Sorokina, T. A.; Lemanova, N. B.
  • Biocontrol Science and Technology, Vol. 8, Issue 1
  • DOI: 10.1080/09583159830423

Diversity and heritability of the maize rhizosphere microbiome under field conditions
journal, April 2013

  • Peiffer, J. A.; Spor, A.; Koren, O.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 16
  • DOI: 10.1073/pnas.1302837110

Inside the root microbiome: Bacterial root endophytes and plant growth promotion
journal, September 2013

  • Gaiero, Jonathan R.; McCall, Crystal A.; Thompson, Karen A.
  • American Journal of Botany, Vol. 100, Issue 9
  • DOI: 10.3732/ajb.1200572

Biological Control of Crown Gall with an Agrocin Mutant of Agrobacterium radiobacter
journal, January 1982

A study on microbial diversity in different cultivars of Brassica napus in relation to its wilt pathogen, Verticillium longisporum
journal, July 2003

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~!
journal, March 2010

Random Forests
journal, January 2001

Susceptibility of five Prunus rootstocks to Agrobacterium tumefaciens
journal, December 2005

  • Thomidis, T.; Exadaktylou, E.; Tsipouridis, C.
  • New Zealand Journal of Crop and Horticultural Science, Vol. 33, Issue 4
  • DOI: 10.1080/01140671.2005.9514368

Non-random species loss in bacterial communities reduces antifungal volatile production
journal, August 2015

  • Hol, W. H. Gera; Garbeva, Paolina; Hordijk, Cornelis
  • Ecology, Vol. 96, Issue 8
  • DOI: 10.1890/14-2359.1

Structure and Functions of the Bacterial Microbiota of Plants
journal, April 2013

Restructuring of Endophytic Bacterial Communities in Grapevine Yellows-Diseased and Recovered Vitis vinifera L. Plants
journal, May 2011

  • Bulgari, Daniela; Casati, Paola; Crepaldi, Paola
  • Applied and Environmental Microbiology, Vol. 77, Issue 14
  • DOI: 10.1128/AEM.00051-11

Cocolonization of the Rhizosphere by Pathogenic Agrobacterium Strains and Nonpathogenic Strains K84 and K1026, Used for Crown Gall Biocontrol
journal, May 1999

Host range conferred by the virulence-specifying plasmid of Agrobacterium tumefaciens
journal, August 1979

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