Tomato Domestication Attenuated Responsiveness to a Beneficial Soil Microbe for Plant Growth Promotion and Induction of Systemic Resistance to Foliar Pathogens

Crop domestication events followed by targeted breeding practices have been pivotal for improvement of desirable traits and to adapt cultivars to local environments. Domestication also resulted in a strong reduction in genetic diversity among modern cultivars compared to their wild relatives, though...

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Main Authors: Amit K. Jaiswal, Tesfaye D. Mengiste, James R. Myers, Daniel S. Egel, Lori A. Hoagland
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-12-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2020.604566/full
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author Amit K. Jaiswal
Tesfaye D. Mengiste
James R. Myers
Daniel S. Egel
Lori A. Hoagland
author_facet Amit K. Jaiswal
Tesfaye D. Mengiste
James R. Myers
Daniel S. Egel
Lori A. Hoagland
author_sort Amit K. Jaiswal
collection DOAJ
description Crop domestication events followed by targeted breeding practices have been pivotal for improvement of desirable traits and to adapt cultivars to local environments. Domestication also resulted in a strong reduction in genetic diversity among modern cultivars compared to their wild relatives, though the effect this could have on tripartite relationships between plants, belowground beneficial microbes and aboveground pathogens remains undetermined. We quantified plant growth performance, basal resistance and induced systemic resistance (ISR) by Trichoderma harzianum, a beneficial soil microbe against Botrytis cinerea, a necrotrophic fungus and Phytophthora infestans, a hemi-biotrophic oomycete, in 25 diverse tomato genotypes. Wild tomato related species, tomato landraces and modern commercial cultivars that were conventionally or organically bred, together, representing a domestication gradient were evaluated. Relationships between basal and ISR, plant physiological status and phenolic compounds were quantified to identify potential mechanisms. Trichoderma enhanced shoot and root biomass and ISR to both pathogens in a genotype specific manner. Moreover, improvements in plant performance in response to Trichoderma gradually decreased along the domestication gradient. Wild relatives and landraces were more responsive to Trichoderma, resulting in greater suppression of foliar pathogens than modern cultivars. Photosynthetic rate and stomatal conductance of some tomato genotypes were improved by Trichoderma treatment whereas leaf nitrogen status of the majority of tomato genotypes were not altered. There was a negative relationship between basal resistance and induced resistance for both diseases, and a positive correlation between Trichoderma-ISR to B. cinerea and enhanced total flavonoid contents. These findings suggest that domestication and breeding practices have altered plant responsiveness to beneficial soil microbes. Further studies are needed to decipher the molecular mechanisms underlying the differential promotion of plant growth and resistance among genotypes, and identify molecular markers to integrate selection for responsiveness into future breeding programs.
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spelling doaj.art-84ef1632531c43c2a76707a2d35a63a12022-12-21T19:46:53ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2020-12-011110.3389/fmicb.2020.604566604566Tomato Domestication Attenuated Responsiveness to a Beneficial Soil Microbe for Plant Growth Promotion and Induction of Systemic Resistance to Foliar PathogensAmit K. Jaiswal0Tesfaye D. Mengiste1James R. Myers2Daniel S. Egel3Lori A. Hoagland4Department of Horticulture and Landscape Architecture, Purdue University, West Lafayette, IN, United StatesDepartment of Botany and Plant Pathology, Purdue University, West Lafayette, IN, United StatesDepartment of Horticulture, Oregon State University, Corvallis, OR, United StatesDepartment of Botany and Plant Pathology, Purdue University, West Lafayette, IN, United StatesDepartment of Horticulture and Landscape Architecture, Purdue University, West Lafayette, IN, United StatesCrop domestication events followed by targeted breeding practices have been pivotal for improvement of desirable traits and to adapt cultivars to local environments. Domestication also resulted in a strong reduction in genetic diversity among modern cultivars compared to their wild relatives, though the effect this could have on tripartite relationships between plants, belowground beneficial microbes and aboveground pathogens remains undetermined. We quantified plant growth performance, basal resistance and induced systemic resistance (ISR) by Trichoderma harzianum, a beneficial soil microbe against Botrytis cinerea, a necrotrophic fungus and Phytophthora infestans, a hemi-biotrophic oomycete, in 25 diverse tomato genotypes. Wild tomato related species, tomato landraces and modern commercial cultivars that were conventionally or organically bred, together, representing a domestication gradient were evaluated. Relationships between basal and ISR, plant physiological status and phenolic compounds were quantified to identify potential mechanisms. Trichoderma enhanced shoot and root biomass and ISR to both pathogens in a genotype specific manner. Moreover, improvements in plant performance in response to Trichoderma gradually decreased along the domestication gradient. Wild relatives and landraces were more responsive to Trichoderma, resulting in greater suppression of foliar pathogens than modern cultivars. Photosynthetic rate and stomatal conductance of some tomato genotypes were improved by Trichoderma treatment whereas leaf nitrogen status of the majority of tomato genotypes were not altered. There was a negative relationship between basal resistance and induced resistance for both diseases, and a positive correlation between Trichoderma-ISR to B. cinerea and enhanced total flavonoid contents. These findings suggest that domestication and breeding practices have altered plant responsiveness to beneficial soil microbes. Further studies are needed to decipher the molecular mechanisms underlying the differential promotion of plant growth and resistance among genotypes, and identify molecular markers to integrate selection for responsiveness into future breeding programs.https://www.frontiersin.org/articles/10.3389/fmicb.2020.604566/fullinduce systemic resistanceplant growthtomato domesticationbeneficial microbescontrol efficacygray mold
spellingShingle Amit K. Jaiswal
Tesfaye D. Mengiste
James R. Myers
Daniel S. Egel
Lori A. Hoagland
Tomato Domestication Attenuated Responsiveness to a Beneficial Soil Microbe for Plant Growth Promotion and Induction of Systemic Resistance to Foliar Pathogens
Frontiers in Microbiology
induce systemic resistance
plant growth
tomato domestication
beneficial microbes
control efficacy
gray mold
title Tomato Domestication Attenuated Responsiveness to a Beneficial Soil Microbe for Plant Growth Promotion and Induction of Systemic Resistance to Foliar Pathogens
title_full Tomato Domestication Attenuated Responsiveness to a Beneficial Soil Microbe for Plant Growth Promotion and Induction of Systemic Resistance to Foliar Pathogens
title_fullStr Tomato Domestication Attenuated Responsiveness to a Beneficial Soil Microbe for Plant Growth Promotion and Induction of Systemic Resistance to Foliar Pathogens
title_full_unstemmed Tomato Domestication Attenuated Responsiveness to a Beneficial Soil Microbe for Plant Growth Promotion and Induction of Systemic Resistance to Foliar Pathogens
title_short Tomato Domestication Attenuated Responsiveness to a Beneficial Soil Microbe for Plant Growth Promotion and Induction of Systemic Resistance to Foliar Pathogens
title_sort tomato domestication attenuated responsiveness to a beneficial soil microbe for plant growth promotion and induction of systemic resistance to foliar pathogens
topic induce systemic resistance
plant growth
tomato domestication
beneficial microbes
control efficacy
gray mold
url https://www.frontiersin.org/articles/10.3389/fmicb.2020.604566/full
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