Phytobiome and Transcriptional Adaptation of Populus deltoides to Acute Progressive Drought and Cyclic Drought

Plant drought stress causes systematic changes to photosynthesis, metabolism, growth, and potentially the phytobiome. Additionally, drought affects plants in both a species-specific and water-deficit-driven manner, causing the response to drought to be dependent both on how drought is being experien...

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Main Authors: Benjamin J. Garcia, Jessy L. Labbé, Piet Jones, Paul E. Abraham, Ian Hodge, Sharlee Climer, Sara Jawdy, Lee Gunter, Gerald A. Tuskan, Xiaohan Yang, Timothy J. Tschaplinski, Daniel A. Jacobson
Format: Article
Language:English
Published: The American Phytopathological Society 2019-03-01
Series:Phytobiomes Journal
Subjects:
Online Access:https://apsjournals.apsnet.org/doi/full/10.1094/PBIOMES-04-18-0021-R
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spelling doaj-ca6066cf7bc847ee8a6abc03106e770e2020-11-25T01:01:45ZengThe American Phytopathological SocietyPhytobiomes Journal2471-29062019-03-012424926010.1094/PBIOMES-04-18-0021-RPhytobiome and Transcriptional Adaptation of Populus deltoides to Acute Progressive Drought and Cyclic DroughtBenjamin J. Garcia0Jessy L. Labbé1Piet Jones2Paul E. Abraham3Ian Hodge4Sharlee Climer5Sara Jawdy6Lee Gunter7Gerald A. Tuskan8Xiaohan Yang9Timothy J. Tschaplinski10Daniel A. Jacobson11Center for Bioenergy Innovation, Oak Ridge National Laboratory, Oak Ridge, TN 37831Center for Bioenergy Innovation, Oak Ridge National Laboratory, Oak Ridge, TN 37831Center for Bioenergy Innovation, Oak Ridge National Laboratory, Oak Ridge, TN 37831 and The Bredesen Center for Interdisciplinary Research and Graduate Education, University of Tennessee, Knoxville 37996Chemical Sciences Division, Oak Ridge National Laboratory, Oak Ridge, TN 37831Center for Bioenergy Innovation, Oak Ridge National Laboratory, Oak Ridge, TN 37831 and Department of Computer Science, Stanford University, Stanford, CA 94305Department of Mathematics and Computer Science, University of Missouri, St. Louis 63121Center for Bioenergy Innovation, Oak Ridge National Laboratory, Oak Ridge, TN 37831Center for Bioenergy Innovation, Oak Ridge National Laboratory, Oak Ridge, TN 37831Center for Bioenergy Innovation, Oak Ridge National Laboratory, Oak Ridge, TN 37831Center for Bioenergy Innovation, Oak Ridge National Laboratory, Oak Ridge, TN 37831Center for Bioenergy Innovation, Oak Ridge National Laboratory, Oak Ridge, TN 37831Center for Bioenergy Innovation, Oak Ridge National Laboratory, Oak Ridge, TN 37831 and The Bredesen Center for Interdisciplinary Research and Graduate Education, University of Tennessee, Knoxville 37996Plant drought stress causes systematic changes to photosynthesis, metabolism, growth, and potentially the phytobiome. Additionally, drought affects plants in both a species-specific and water-deficit-driven manner, causing the response to drought to be dependent both on how drought is being experienced and on any adaptation to prior drought exposure. Thus, understanding the effect of drought on plants requires assessing drought response in multiple conditions, such as progressive acute drought and recurrent cyclic drought, and at different levels of severity. In this study, we have utilized RNA sequencing to identify changes to the plant transcriptome and the phytobiome during both acute progressive drought and cyclic drought at multiple severities. Co-analysis of the plant and phytobiome, utilizing the same RNAseq data, allows for the identification of novel associations that would not be possible otherwise. We have identified that the drought response ranges from increased transcripts related to photosynthesis and metabolic activity in mild acute drought to decreased transcripts related to photosynthesis and metabolic impairment in severe drought. Moreover, while water deficit is a main driver of transcriptional responses in severe drought, there are increases in reactive oxygen species (ROS) metabolism and photosynthetic transcripts in cyclic severe drought compared with acute severe drought, independent of water deficit. The phytobiome exhibits alternate responses to drought when compared with the transcriptome. Specifically, the phytobiome is affected more by the cyclic or acute nature of the drought rather than the severity of the drought, with the phytobiome having an increase in taxa under cyclic drought that are often reported to have beneficial effects on the plants. Lastly, we have identified associations between taxa in the phytobiome with expression of disease response, ROS metabolism, and photosynthesis transcripts suggesting interplay between the host plant and its phytobiome in response to drought.https://apsjournals.apsnet.org/doi/full/10.1094/PBIOMES-04-18-0021-Rbacteriologymicrobiomemutualismmycologynematologynutrient cyclingrhizosphere and phyllospheresymbiosistranscriptomicsPopulus deltoides
collection DOAJ
language English
format Article
sources DOAJ
author Benjamin J. Garcia
Jessy L. Labbé
Piet Jones
Paul E. Abraham
Ian Hodge
Sharlee Climer
Sara Jawdy
Lee Gunter
Gerald A. Tuskan
Xiaohan Yang
Timothy J. Tschaplinski
Daniel A. Jacobson
spellingShingle Benjamin J. Garcia
Jessy L. Labbé
Piet Jones
Paul E. Abraham
Ian Hodge
Sharlee Climer
Sara Jawdy
Lee Gunter
Gerald A. Tuskan
Xiaohan Yang
Timothy J. Tschaplinski
Daniel A. Jacobson
Phytobiome and Transcriptional Adaptation of Populus deltoides to Acute Progressive Drought and Cyclic Drought
Phytobiomes Journal
bacteriology
microbiome
mutualism
mycology
nematology
nutrient cycling
rhizosphere and phyllosphere
symbiosis
transcriptomics
Populus deltoides
author_facet Benjamin J. Garcia
Jessy L. Labbé
Piet Jones
Paul E. Abraham
Ian Hodge
Sharlee Climer
Sara Jawdy
Lee Gunter
Gerald A. Tuskan
Xiaohan Yang
Timothy J. Tschaplinski
Daniel A. Jacobson
author_sort Benjamin J. Garcia
title Phytobiome and Transcriptional Adaptation of Populus deltoides to Acute Progressive Drought and Cyclic Drought
title_short Phytobiome and Transcriptional Adaptation of Populus deltoides to Acute Progressive Drought and Cyclic Drought
title_full Phytobiome and Transcriptional Adaptation of Populus deltoides to Acute Progressive Drought and Cyclic Drought
title_fullStr Phytobiome and Transcriptional Adaptation of Populus deltoides to Acute Progressive Drought and Cyclic Drought
title_full_unstemmed Phytobiome and Transcriptional Adaptation of Populus deltoides to Acute Progressive Drought and Cyclic Drought
title_sort phytobiome and transcriptional adaptation of populus deltoides to acute progressive drought and cyclic drought
publisher The American Phytopathological Society
series Phytobiomes Journal
issn 2471-2906
publishDate 2019-03-01
description Plant drought stress causes systematic changes to photosynthesis, metabolism, growth, and potentially the phytobiome. Additionally, drought affects plants in both a species-specific and water-deficit-driven manner, causing the response to drought to be dependent both on how drought is being experienced and on any adaptation to prior drought exposure. Thus, understanding the effect of drought on plants requires assessing drought response in multiple conditions, such as progressive acute drought and recurrent cyclic drought, and at different levels of severity. In this study, we have utilized RNA sequencing to identify changes to the plant transcriptome and the phytobiome during both acute progressive drought and cyclic drought at multiple severities. Co-analysis of the plant and phytobiome, utilizing the same RNAseq data, allows for the identification of novel associations that would not be possible otherwise. We have identified that the drought response ranges from increased transcripts related to photosynthesis and metabolic activity in mild acute drought to decreased transcripts related to photosynthesis and metabolic impairment in severe drought. Moreover, while water deficit is a main driver of transcriptional responses in severe drought, there are increases in reactive oxygen species (ROS) metabolism and photosynthetic transcripts in cyclic severe drought compared with acute severe drought, independent of water deficit. The phytobiome exhibits alternate responses to drought when compared with the transcriptome. Specifically, the phytobiome is affected more by the cyclic or acute nature of the drought rather than the severity of the drought, with the phytobiome having an increase in taxa under cyclic drought that are often reported to have beneficial effects on the plants. Lastly, we have identified associations between taxa in the phytobiome with expression of disease response, ROS metabolism, and photosynthesis transcripts suggesting interplay between the host plant and its phytobiome in response to drought.
topic bacteriology
microbiome
mutualism
mycology
nematology
nutrient cycling
rhizosphere and phyllosphere
symbiosis
transcriptomics
Populus deltoides
url https://apsjournals.apsnet.org/doi/full/10.1094/PBIOMES-04-18-0021-R
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