Multi-omics Comparison Reveals Landscape of Citrus limon and Citrus sinensis Response to ‘Candidatus Liberibacter asiaticus’

Comparison of the metabolic changes prior to symptom development upon infection with Candidatus Liberibacter asiaticus (CLas), the bacterium associated with citrus greening disease, between citrus hosts with different tolerances is lacking. The objective of this study was to compare the early respon...

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Main Authors: Elizabeth L. Chin, John Ramsey, Surya Saha, Darya Mishchuk, Juan Chavez, Kevin Howe, Xuefei Zhong, Mirella Flores-Gonzalez, Elizabeth Mitrovic, MaryLou Polek, Kris Godfrey, Lukas A. Mueller, James Bruce, Michelle Heck, Carolyn M. Slupsky
Format: Article
Language:English
Published: The American Phytopathological Society 2021-04-01
Series:PhytoFrontiers
Subjects:
Online Access:https://apsjournals.apsnet.org/doi/10.1094/PHYTOFR-09-20-0018-R
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author Elizabeth L. Chin
John Ramsey
Surya Saha
Darya Mishchuk
Juan Chavez
Kevin Howe
Xuefei Zhong
Mirella Flores-Gonzalez
Elizabeth Mitrovic
MaryLou Polek
Kris Godfrey
Lukas A. Mueller
James Bruce
Michelle Heck
Carolyn M. Slupsky
author_facet Elizabeth L. Chin
John Ramsey
Surya Saha
Darya Mishchuk
Juan Chavez
Kevin Howe
Xuefei Zhong
Mirella Flores-Gonzalez
Elizabeth Mitrovic
MaryLou Polek
Kris Godfrey
Lukas A. Mueller
James Bruce
Michelle Heck
Carolyn M. Slupsky
author_sort Elizabeth L. Chin
collection DOAJ
description Comparison of the metabolic changes prior to symptom development upon infection with Candidatus Liberibacter asiaticus (CLas), the bacterium associated with citrus greening disease, between citrus hosts with different tolerances is lacking. The objective of this study was to compare the early response of Lisbon lemon (Citrus limon) and Washington navel orange (Citrus sinensis [L.] Osbeck), two citrus species commercially important to California, to CLas through graft inoculation. Here, we compare the transcriptome, proteome, and metabolome response, using RNA sequencing, liquid chromatography tandem mass spectrometry, and 1H nuclear magnetic resonance, respectively, from our two recently published studies examining the response of the lemon and navel oranges separately, and introduce new micronutrient data from inductively coupled plasma mass spectrometry analysis, focusing on lemons at 10 and 14 weeks postgrafting (wpg), and navels at 8 and 18 wpg, prior to symptom development. Several micronutrients accumulated in presymptomatic infected lemons compared with controls, whereas little change was observed in the navels. Photosynthesis proteins were substantially altered by CLas infection in navels, with fewer changes observed in lemons. The metabolome differed between control and infected navels throughout infection, although differences between control and infected lemons were identified only after symptom expression. Taken together, these findings highlight differences in response to CLas between two varieties with differing tolerances.[Graphic: see text] Copyright © 2021 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.
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spelling doaj.art-6642852f6e724411a7f8960015a5ca322024-02-03T08:55:20ZengThe American Phytopathological SocietyPhytoFrontiers2690-54422021-04-0112768410.1094/PHYTOFR-09-20-0018-RMulti-omics Comparison Reveals Landscape of Citrus limon and Citrus sinensis Response to ‘Candidatus Liberibacter asiaticus’Elizabeth L. Chin0John Ramsey1Surya Saha2Darya Mishchuk3Juan Chavez4Kevin Howe5Xuefei Zhong6Mirella Flores-Gonzalez7Elizabeth Mitrovic8MaryLou Polek9Kris Godfrey10Lukas A. Mueller11James Bruce12Michelle Heck13Carolyn M. Slupsky14Department of Food Science and Technology, University of California, Davis, CAEmerging Pests and Pathogens Research Unit, Robert W. Holley Center for Agriculture and Health, USDA Agricultural Research Service, Ithaca, NYBoyce Thompson Institute for Plant Research, Ithaca, NYDepartment of Food Science and Technology, University of California, Davis, CADepartment of Genome Sciences, University of Washington, Seattle, WAEmerging Pests and Pathogens Research Unit, Robert W. Holley Center for Agriculture and Health, USDA Agricultural Research Service, Ithaca, NYDepartment of Genome Sciences, University of Washington, Seattle, WABoyce Thompson Institute for Plant Research, Ithaca, NYContained Research Facility, University of California, Davis, CANational Clonal Germplasm Repository for Citrus & Dates, Riverside, CAContained Research Facility, University of California, Davis, CAEmerging Pests and Pathogens Research Unit, Robert W. Holley Center for Agriculture and Health, USDA Agricultural Research Service, Ithaca, NYDepartment of Genome Sciences, University of Washington, Seattle, WAEmerging Pests and Pathogens Research Unit, Robert W. Holley Center for Agriculture and Health, USDA Agricultural Research Service, Ithaca, NYDepartment of Food Science and Technology, University of California, Davis, CAComparison of the metabolic changes prior to symptom development upon infection with Candidatus Liberibacter asiaticus (CLas), the bacterium associated with citrus greening disease, between citrus hosts with different tolerances is lacking. The objective of this study was to compare the early response of Lisbon lemon (Citrus limon) and Washington navel orange (Citrus sinensis [L.] Osbeck), two citrus species commercially important to California, to CLas through graft inoculation. Here, we compare the transcriptome, proteome, and metabolome response, using RNA sequencing, liquid chromatography tandem mass spectrometry, and 1H nuclear magnetic resonance, respectively, from our two recently published studies examining the response of the lemon and navel oranges separately, and introduce new micronutrient data from inductively coupled plasma mass spectrometry analysis, focusing on lemons at 10 and 14 weeks postgrafting (wpg), and navels at 8 and 18 wpg, prior to symptom development. Several micronutrients accumulated in presymptomatic infected lemons compared with controls, whereas little change was observed in the navels. Photosynthesis proteins were substantially altered by CLas infection in navels, with fewer changes observed in lemons. The metabolome differed between control and infected navels throughout infection, although differences between control and infected lemons were identified only after symptom expression. Taken together, these findings highlight differences in response to CLas between two varieties with differing tolerances.[Graphic: see text] Copyright © 2021 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.https://apsjournals.apsnet.org/doi/10.1094/PHYTOFR-09-20-0018-R‘Candidatus Liberibacter asiaticus’huanglongbingcitrus greening diseasetranscriptomicsproteomicsmetabolomics
spellingShingle Elizabeth L. Chin
John Ramsey
Surya Saha
Darya Mishchuk
Juan Chavez
Kevin Howe
Xuefei Zhong
Mirella Flores-Gonzalez
Elizabeth Mitrovic
MaryLou Polek
Kris Godfrey
Lukas A. Mueller
James Bruce
Michelle Heck
Carolyn M. Slupsky
Multi-omics Comparison Reveals Landscape of Citrus limon and Citrus sinensis Response to ‘Candidatus Liberibacter asiaticus’
PhytoFrontiers
‘Candidatus Liberibacter asiaticus’
huanglongbing
citrus greening disease
transcriptomics
proteomics
metabolomics
title Multi-omics Comparison Reveals Landscape of Citrus limon and Citrus sinensis Response to ‘Candidatus Liberibacter asiaticus’
title_full Multi-omics Comparison Reveals Landscape of Citrus limon and Citrus sinensis Response to ‘Candidatus Liberibacter asiaticus’
title_fullStr Multi-omics Comparison Reveals Landscape of Citrus limon and Citrus sinensis Response to ‘Candidatus Liberibacter asiaticus’
title_full_unstemmed Multi-omics Comparison Reveals Landscape of Citrus limon and Citrus sinensis Response to ‘Candidatus Liberibacter asiaticus’
title_short Multi-omics Comparison Reveals Landscape of Citrus limon and Citrus sinensis Response to ‘Candidatus Liberibacter asiaticus’
title_sort multi omics comparison reveals landscape of citrus limon and citrus sinensis response to candidatus liberibacter asiaticus
topic ‘Candidatus Liberibacter asiaticus’
huanglongbing
citrus greening disease
transcriptomics
proteomics
metabolomics
url https://apsjournals.apsnet.org/doi/10.1094/PHYTOFR-09-20-0018-R
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