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Transcriptomic responses of a simplified soil microcosm to a plant pathogen and its biocontrol agent reveal a complex reaction to harsh habitat

Michele Perazzolli, Noemí Herrero, Lieven Sterck UGent, Luisa Lenzi, Alberto Pellegrini, Gerardo Puopolo, Yves Van de Peer UGent and Ilaria Pertot (2016) BMC GENOMICS. 17.
abstract
Background: Soil microorganisms are key determinants of soil fertility and plant health. Soil phytopathogenic fungi are one of the most important causes of crop losses worldwide. Microbial biocontrol agents have been extensively studied as alternatives for controlling phytopathogenic soil microorganisms, but molecular interactions between them have mainly been characterised in dual cultures, without taking into account the soil microbial community. We used an RNA sequencing approach to elucidate the molecular interplay of a soil microbial community in response to a plant pathogen and its biocontrol agent, in order to examine the molecular patterns activated by the microorganisms. Results: A simplified soil microcosm containing 11 soil microorganisms was incubated with a plant root pathogen (Armillaria mellea) and its biocontrol agent (Trichoderma atroviride) for 24 h under controlled conditions. More than 46 million paired-end reads were obtained for each replicate and 28,309 differentially expressed genes were identified in total. Pathway analysis revealed complex adaptations of soil microorganisms to the harsh conditions of the soil matrix and to reciprocal microbial competition/cooperation relationships. Both the phytopathogen and its biocontrol agent were specifically recognised by the simplified soil microcosm: defence reaction mechanisms and neutral adaptation processes were activated in response to competitive (T. atroviride) or non-competitive (A. mellea) microorganisms, respectively. Moreover, activation of resistance mechanisms dominated in the simplified soil microcosm in the presence of both A. mellea and T. atroviride. Biocontrol processes of T. atroviride were already activated during incubation in the simplified soil microcosm, possibly to occupy niches in a competitive ecosystem, and they were not further enhanced by the introduction of A. mellea. Conclusions: This work represents an additional step towards understanding molecular interactions between plant pathogens and biocontrol agents within a soil ecosystem. Global transcriptional analysis of the simplified soil microcosm revealed complex metabolic adaptation in the soil environment and specific responses to antagonistic or neutral intruders.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
RHIZOCTONIA-SOLANI, SERRATIA-PLYMUTHICA, GENE ONTOLOGY, Microbial interaction, RNA-Seq, Transcriptomics, Gene expression, QUANTITATIVE PCR DATA, GENOME SEQUENCE, SECONDARY METABOLISM, Plant pathogen, Soil transcriptome, Soil microbial community, Biological control, TRICHODERMA-ATROVIRIDE, ARMILLARIA-MELLEA, PSEUDOMONAS-FLUORESCENS, ASPERGILLUS-NIGER
journal title
BMC GENOMICS
BMC Genomics
volume
17
article number
838
pages
18 pages
Web of Science type
Article
Web of Science id
000386395700001
JCR category
BIOTECHNOLOGY & APPLIED MICROBIOLOGY
JCR impact factor
3.729 (2016)
JCR rank
33/158 (2016)
JCR quartile
1 (2016)
ISSN
1471-2164
DOI
10.1186/s12864-016-3174-4
project
Bioinformatics: from nucleotids to networks (N2N)
language
English
UGent publication?
yes
classification
A1
copyright statement
I have retained and own the full copyright for this publication
id
8157602
handle
http://hdl.handle.net/1854/LU-8157602
date created
2016-11-17 13:03:59
date last changed
2016-12-21 15:41:43
@article{8157602,
  abstract     = {Background: Soil microorganisms are key determinants of soil fertility and plant health. Soil phytopathogenic fungi are one of the most important causes of crop losses worldwide. Microbial biocontrol agents have been extensively studied as alternatives for controlling phytopathogenic soil microorganisms, but molecular interactions between them have mainly been characterised in dual cultures, without taking into account the soil microbial community. We used an RNA sequencing approach to elucidate the molecular interplay of a soil microbial community in response to a plant pathogen and its biocontrol agent, in order to examine the molecular patterns activated by the microorganisms. 
Results: A simplified soil microcosm containing 11 soil microorganisms was incubated with a plant root pathogen (Armillaria mellea) and its biocontrol agent (Trichoderma atroviride) for 24 h under controlled conditions. More than 46 million paired-end reads were obtained for each replicate and 28,309 differentially expressed genes were identified in total. Pathway analysis revealed complex adaptations of soil microorganisms to the harsh conditions of the soil matrix and to reciprocal microbial competition/cooperation relationships. Both the phytopathogen and its biocontrol agent were specifically recognised by the simplified soil microcosm: defence reaction mechanisms and neutral adaptation processes were activated in response to competitive (T. atroviride) or non-competitive (A. mellea) microorganisms, respectively. Moreover, activation of resistance mechanisms dominated in the simplified soil microcosm in the presence of both A. mellea and T. atroviride. Biocontrol processes of T. atroviride were already activated during incubation in the simplified soil microcosm, possibly to occupy niches in a competitive ecosystem, and they were not further enhanced by the introduction of A. mellea. 
Conclusions: This work represents an additional step towards understanding molecular interactions between plant pathogens and biocontrol agents within a soil ecosystem. Global transcriptional analysis of the simplified soil microcosm revealed complex metabolic adaptation in the soil environment and specific responses to antagonistic or neutral intruders.},
  articleno    = {838},
  author       = {Perazzolli, Michele and Herrero, Noem{\'i} and Sterck, Lieven and Lenzi, Luisa and Pellegrini, Alberto and Puopolo, Gerardo and Van de Peer, Yves and Pertot, Ilaria},
  issn         = {1471-2164},
  journal      = {BMC GENOMICS},
  keyword      = {RHIZOCTONIA-SOLANI,SERRATIA-PLYMUTHICA,GENE ONTOLOGY,Microbial interaction,RNA-Seq,Transcriptomics,Gene expression,QUANTITATIVE PCR DATA,GENOME SEQUENCE,SECONDARY METABOLISM,Plant pathogen,Soil transcriptome,Soil microbial community,Biological control,TRICHODERMA-ATROVIRIDE,ARMILLARIA-MELLEA,PSEUDOMONAS-FLUORESCENS,ASPERGILLUS-NIGER},
  language     = {eng},
  pages        = {18},
  title        = {Transcriptomic responses of a simplified soil microcosm to a plant pathogen and its biocontrol agent reveal a complex reaction to harsh habitat},
  url          = {http://dx.doi.org/10.1186/s12864-016-3174-4},
  volume       = {17},
  year         = {2016},
}

Chicago
Perazzolli, Michele, Noemí Herrero, Lieven Sterck, Luisa Lenzi, Alberto Pellegrini, Gerardo Puopolo, Yves Van de Peer, and Ilaria Pertot. 2016. “Transcriptomic Responses of a Simplified Soil Microcosm to a Plant Pathogen and Its Biocontrol Agent Reveal a Complex Reaction to Harsh Habitat.” Bmc Genomics 17.
APA
Perazzolli, M., Herrero, N., Sterck, L., Lenzi, L., Pellegrini, A., Puopolo, G., Van de Peer, Y., et al. (2016). Transcriptomic responses of a simplified soil microcosm to a plant pathogen and its biocontrol agent reveal a complex reaction to harsh habitat. BMC GENOMICS, 17.
Vancouver
1.
Perazzolli M, Herrero N, Sterck L, Lenzi L, Pellegrini A, Puopolo G, et al. Transcriptomic responses of a simplified soil microcosm to a plant pathogen and its biocontrol agent reveal a complex reaction to harsh habitat. BMC GENOMICS. 2016;17.
MLA
Perazzolli, Michele, Noemí Herrero, Lieven Sterck, et al. “Transcriptomic Responses of a Simplified Soil Microcosm to a Plant Pathogen and Its Biocontrol Agent Reveal a Complex Reaction to Harsh Habitat.” BMC GENOMICS 17 (2016): n. pag. Print.