Nitrogen fertilizer rate but not form affects the severity of Fusarium wilt in banana

Nitrogen (N) fertilizers are routinely applied to bananas (Musa spp.) to increase production but may exacerbate plant diseases like Fusarium wilt of banana (FWB), which is the most economically important disease. Here, we characterized the effects of N rate and form on banana plant growth, root prot...

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Main Authors: Ryan Orr, Paul G. Dennis, Yide Wong, Daniel J. Browne, Martha Cooper, Henry W. G. Birt, Hazel R. Lapis-Gaza, Anthony B. Pattison, Paul N. Nelson
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-07-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2022.907819/full
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author Ryan Orr
Paul G. Dennis
Yide Wong
Yide Wong
Yide Wong
Daniel J. Browne
Daniel J. Browne
Martha Cooper
Martha Cooper
Henry W. G. Birt
Henry W. G. Birt
Henry W. G. Birt
Hazel R. Lapis-Gaza
Anthony B. Pattison
Paul N. Nelson
author_facet Ryan Orr
Paul G. Dennis
Yide Wong
Yide Wong
Yide Wong
Daniel J. Browne
Daniel J. Browne
Martha Cooper
Martha Cooper
Henry W. G. Birt
Henry W. G. Birt
Henry W. G. Birt
Hazel R. Lapis-Gaza
Anthony B. Pattison
Paul N. Nelson
author_sort Ryan Orr
collection DOAJ
description Nitrogen (N) fertilizers are routinely applied to bananas (Musa spp.) to increase production but may exacerbate plant diseases like Fusarium wilt of banana (FWB), which is the most economically important disease. Here, we characterized the effects of N rate and form on banana plant growth, root proteome, bacterial and fungal diversity in the rhizosphere, the concentration of Fusarium oxysporum f.sp. cubense (Foc) in the soil, and the FWB severity. Banana plants (Musa subgroup ABB) were grown under greenhouse conditions in soil with ammonium or nitrate supplemented at five N rates, and with or without inoculation with Foc. The growth of non-inoculated plants was positively correlated with the N rate. In bananas inoculated with Foc, disease severity increased with the N rate, resulting in the Foc-inoculated plant growth being greatest at intermediate N rates. The abundance of Foc in the soil was weakly related to the treatment conditions and was a poor predictor of disease severity. Fungal diversity was consistently affected by Foc inoculation, while bacterial diversity was associated with changes in soil pH resulting from N addition, in particular ammonium. N rate altered the expression of host metabolic pathways associated with carbon fixation, energy usage, amino acid metabolism, and importantly stress response signaling, irrespective of inoculation or N form. Furthermore, in diseased plants, Pathogenesis-related protein 1, a key endpoint for biotic stress response and the salicylic acid defense response to biotrophic pathogens, was negatively correlated with the rate of ammonium fertilizer but not nitrate. As expected, inoculation with Foc altered the expression of a wide range of processes in the banana plant including those of defense and growth. In summary, our results indicate that the severity of FWB was negatively associated with host defenses, which was influenced by N application (particularly ammonium), and shifts in microbial communities associated with ammonium-induced acidification.
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spelling doaj.art-e9696ffa4cc14f93a5ebaa81a33413e22022-12-22T02:14:06ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2022-07-011310.3389/fpls.2022.907819907819Nitrogen fertilizer rate but not form affects the severity of Fusarium wilt in bananaRyan Orr0Paul G. Dennis1Yide Wong2Yide Wong3Yide Wong4Daniel J. Browne5Daniel J. Browne6Martha Cooper7Martha Cooper8Henry W. G. Birt9Henry W. G. Birt10Henry W. G. Birt11Hazel R. Lapis-Gaza12Anthony B. Pattison13Paul N. Nelson14College of Science and Engineering, James Cook University, Cairns, QLD, AustraliaSchool of Earth and Environmental Sciences, The University of Queensland, Brisbane, QLD, AustraliaAustralian Institute of Tropical Health and Medicine (AITHM), James Cook University, Cairns, QLD, AustraliaCentre for Tropical Bioinformatics and Molecular Biology, James Cook University, Cairns, QLD, AustraliaCentre for Molecular Therapeutics, James Cook University, Cairns, QLD, AustraliaAustralian Institute of Tropical Health and Medicine (AITHM), James Cook University, Cairns, QLD, AustraliaCentre for Molecular Therapeutics, James Cook University, Cairns, QLD, AustraliaAustralian Institute of Tropical Health and Medicine (AITHM), James Cook University, Cairns, QLD, AustraliaCentre for Tropical Bioinformatics and Molecular Biology, James Cook University, Cairns, QLD, AustraliaSchool of Earth and Environmental Sciences, The University of Queensland, Brisbane, QLD, AustraliaDepartment of Plant Science, The Pennsylvania State University, University Park, PA, United StatesHuck Institutes of the Life Sciences, The Pennsylvania State University, University Park, PA, United StatesDepartment of Agriculture and Fisheries, South Johnstone, QLD, AustraliaDepartment of Agriculture and Fisheries, South Johnstone, QLD, AustraliaCollege of Science and Engineering, James Cook University, Cairns, QLD, AustraliaNitrogen (N) fertilizers are routinely applied to bananas (Musa spp.) to increase production but may exacerbate plant diseases like Fusarium wilt of banana (FWB), which is the most economically important disease. Here, we characterized the effects of N rate and form on banana plant growth, root proteome, bacterial and fungal diversity in the rhizosphere, the concentration of Fusarium oxysporum f.sp. cubense (Foc) in the soil, and the FWB severity. Banana plants (Musa subgroup ABB) were grown under greenhouse conditions in soil with ammonium or nitrate supplemented at five N rates, and with or without inoculation with Foc. The growth of non-inoculated plants was positively correlated with the N rate. In bananas inoculated with Foc, disease severity increased with the N rate, resulting in the Foc-inoculated plant growth being greatest at intermediate N rates. The abundance of Foc in the soil was weakly related to the treatment conditions and was a poor predictor of disease severity. Fungal diversity was consistently affected by Foc inoculation, while bacterial diversity was associated with changes in soil pH resulting from N addition, in particular ammonium. N rate altered the expression of host metabolic pathways associated with carbon fixation, energy usage, amino acid metabolism, and importantly stress response signaling, irrespective of inoculation or N form. Furthermore, in diseased plants, Pathogenesis-related protein 1, a key endpoint for biotic stress response and the salicylic acid defense response to biotrophic pathogens, was negatively correlated with the rate of ammonium fertilizer but not nitrate. As expected, inoculation with Foc altered the expression of a wide range of processes in the banana plant including those of defense and growth. In summary, our results indicate that the severity of FWB was negatively associated with host defenses, which was influenced by N application (particularly ammonium), and shifts in microbial communities associated with ammonium-induced acidification.https://www.frontiersin.org/articles/10.3389/fpls.2022.907819/fulldisease triangleproteomicsammoniumnitrateqPCRbanana
spellingShingle Ryan Orr
Paul G. Dennis
Yide Wong
Yide Wong
Yide Wong
Daniel J. Browne
Daniel J. Browne
Martha Cooper
Martha Cooper
Henry W. G. Birt
Henry W. G. Birt
Henry W. G. Birt
Hazel R. Lapis-Gaza
Anthony B. Pattison
Paul N. Nelson
Nitrogen fertilizer rate but not form affects the severity of Fusarium wilt in banana
Frontiers in Plant Science
disease triangle
proteomics
ammonium
nitrate
qPCR
banana
title Nitrogen fertilizer rate but not form affects the severity of Fusarium wilt in banana
title_full Nitrogen fertilizer rate but not form affects the severity of Fusarium wilt in banana
title_fullStr Nitrogen fertilizer rate but not form affects the severity of Fusarium wilt in banana
title_full_unstemmed Nitrogen fertilizer rate but not form affects the severity of Fusarium wilt in banana
title_short Nitrogen fertilizer rate but not form affects the severity of Fusarium wilt in banana
title_sort nitrogen fertilizer rate but not form affects the severity of fusarium wilt in banana
topic disease triangle
proteomics
ammonium
nitrate
qPCR
banana
url https://www.frontiersin.org/articles/10.3389/fpls.2022.907819/full
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