Disease-Induced Microbial Shifts in Citrus Indicate Microbiome-Derived Responses to Huanglongbing Across the Disease Severity Spectrum
Plant microbiomes are critical components to plant health and can influence disease outcomes. We provide empirical data describing disease-induced shifts within the citrus microbiome at different levels of huanglongbing (HLB) disease severity. HLB is associated with an invasive phloem-limited bacter...
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The American Phytopathological Society
2020-08-01
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Series: | Phytobiomes Journal |
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doaj-4bcf3d2f933b4d898e531663508312652021-05-14T16:17:52ZengThe American Phytopathological SocietyPhytobiomes Journal2471-29062020-08-014437538710.1094/PBIOMES-04-20-0027-RDisease-Induced Microbial Shifts in Citrus Indicate Microbiome-Derived Responses to Huanglongbing Across the Disease Severity SpectrumNichole A. GinnanTyler DangSohrab BodaghiPaul M. RueggerGreg McCollumGary EnglandGeorgios VidalakisJames BornemanPhilippe E. RolshausenM. Caroline RoperPlant microbiomes are critical components to plant health and can influence disease outcomes. We provide empirical data describing disease-induced shifts within the citrus microbiome at different levels of huanglongbing (HLB) disease severity. HLB is associated with an invasive phloem-limited bacterium, ‘Candidatus Liberibacter asiaticus’, that is introduced into the aerial portions of the tree by an insect vector. Disease manifests as aboveground foliar and fruit symptoms and significant root decline belowground. During the early phase of disease, there were depletions of putative keystone taxa in leaves and roots, followed by enrichments of putative beneficial taxa, suggesting a microbially derived immune response involved in plant protection that is ancillary to immune components encoded in the plant’s genome. In the late phase of disease, we observed enrichments of parasitic and saprophytic microorganisms, particularly in the roots. The community shifts within the root compartment are emblematic of a disease-induced dysbiosis where pathogens other than ‘Ca. L. asiaticus’ begin to dominate the community. Furthermore, we define key taxa enriched in trees with a slower rate of disease development, referred to as survivor trees, that are hallmarks of those found in trees in the early phase of disease that may be drivers of the survivor tree phenotype. We propose a disease ecology model that illustrates the relationship between the pathogen, the microbiome, and the host plant that highlights microorganisms that may serve as disease facilitators or antagonists.https://doi.org/10.1094/PBIOMES-04-20-0027-R |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Nichole A. Ginnan Tyler Dang Sohrab Bodaghi Paul M. Ruegger Greg McCollum Gary England Georgios Vidalakis James Borneman Philippe E. Rolshausen M. Caroline Roper |
spellingShingle |
Nichole A. Ginnan Tyler Dang Sohrab Bodaghi Paul M. Ruegger Greg McCollum Gary England Georgios Vidalakis James Borneman Philippe E. Rolshausen M. Caroline Roper Disease-Induced Microbial Shifts in Citrus Indicate Microbiome-Derived Responses to Huanglongbing Across the Disease Severity Spectrum Phytobiomes Journal |
author_facet |
Nichole A. Ginnan Tyler Dang Sohrab Bodaghi Paul M. Ruegger Greg McCollum Gary England Georgios Vidalakis James Borneman Philippe E. Rolshausen M. Caroline Roper |
author_sort |
Nichole A. Ginnan |
title |
Disease-Induced Microbial Shifts in Citrus Indicate Microbiome-Derived Responses to Huanglongbing Across the Disease Severity Spectrum |
title_short |
Disease-Induced Microbial Shifts in Citrus Indicate Microbiome-Derived Responses to Huanglongbing Across the Disease Severity Spectrum |
title_full |
Disease-Induced Microbial Shifts in Citrus Indicate Microbiome-Derived Responses to Huanglongbing Across the Disease Severity Spectrum |
title_fullStr |
Disease-Induced Microbial Shifts in Citrus Indicate Microbiome-Derived Responses to Huanglongbing Across the Disease Severity Spectrum |
title_full_unstemmed |
Disease-Induced Microbial Shifts in Citrus Indicate Microbiome-Derived Responses to Huanglongbing Across the Disease Severity Spectrum |
title_sort |
disease-induced microbial shifts in citrus indicate microbiome-derived responses to huanglongbing across the disease severity spectrum |
publisher |
The American Phytopathological Society |
series |
Phytobiomes Journal |
issn |
2471-2906 |
publishDate |
2020-08-01 |
description |
Plant microbiomes are critical components to plant health and can influence disease outcomes. We provide empirical data describing disease-induced shifts within the citrus microbiome at different levels of huanglongbing (HLB) disease severity. HLB is associated with an invasive phloem-limited bacterium, ‘Candidatus Liberibacter asiaticus’, that is introduced into the aerial portions of the tree by an insect vector. Disease manifests as aboveground foliar and fruit symptoms and significant root decline belowground. During the early phase of disease, there were depletions of putative keystone taxa in leaves and roots, followed by enrichments of putative beneficial taxa, suggesting a microbially derived immune response involved in plant protection that is ancillary to immune components encoded in the plant’s genome. In the late phase of disease, we observed enrichments of parasitic and saprophytic microorganisms, particularly in the roots. The community shifts within the root compartment are emblematic of a disease-induced dysbiosis where pathogens other than ‘Ca. L. asiaticus’ begin to dominate the community. Furthermore, we define key taxa enriched in trees with a slower rate of disease development, referred to as survivor trees, that are hallmarks of those found in trees in the early phase of disease that may be drivers of the survivor tree phenotype. We propose a disease ecology model that illustrates the relationship between the pathogen, the microbiome, and the host plant that highlights microorganisms that may serve as disease facilitators or antagonists. |
url |
https://doi.org/10.1094/PBIOMES-04-20-0027-R |
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