Synergistic and Offset Effects of Fungal Species Combinations on Plant Performance

In natural and agricultural ecosystems, survival and growth of plants depend substantially on residing microbes in the endosphere and rhizosphere. Although numerous studies have reported the presence of plant-growth promoting bacteria and fungi in below-ground biomes, it remains a major challenge to...

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Main Authors: Yoshie Hori, Hiroaki Fujita, Kei Hiruma, Kazuhiko Narisawa, Hirokazu Toju
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-09-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2021.713180/full
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spelling doaj-be1138c6a2784bbd83c0090207e8755c2021-09-14T16:47:39ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2021-09-011210.3389/fmicb.2021.713180713180Synergistic and Offset Effects of Fungal Species Combinations on Plant PerformanceYoshie Hori0Hiroaki Fujita1Kei Hiruma2Kazuhiko Narisawa3Hirokazu Toju4Center for Ecological Research, Kyoto University, Kyoto, JapanCenter for Ecological Research, Kyoto University, Kyoto, JapanGraduate School of Arts and Sciences, Multi-Disciplinary Sciences Life Sciences, The University of Tokyo, Tokyo, JapanCollege of Agriculture, Ibaraki University, Mito, JapanCenter for Ecological Research, Kyoto University, Kyoto, JapanIn natural and agricultural ecosystems, survival and growth of plants depend substantially on residing microbes in the endosphere and rhizosphere. Although numerous studies have reported the presence of plant-growth promoting bacteria and fungi in below-ground biomes, it remains a major challenge to understand how sets of microbial species positively or negatively affect plants’ performance. By conducting a series of single- and dual-inoculation experiments of 13 plant-associated fungi targeting a Brassicaceae plant species (Brassica rapa var. perviridis), we here systematically evaluated how microbial effects on plants depend on presence/absence of co-occurring microbes. The comparison of single- and dual-inoculation experiments showed that combinations of the fungal isolates with the highest plant-growth promoting effects in single inoculations did not have highly positive impacts on plant performance traits (e.g., shoot dry weight). In contrast, pairs of fungi with small/moderate contributions to plant growth in single-inoculation contexts showed the greatest effects on plants among the 78 fungal pairs examined. These results on the offset and synergistic effects of pairs of microbes suggest that inoculation experiments of single microbial species/isolates can result in the overestimation or underestimation of microbial functions in multi-species contexts. Because keeping single-microbe systems under outdoor conditions is impractical, designing sets of microbes that can maximize performance of crop plants is an important step for the use of microbial functions in sustainable agriculture.https://www.frontiersin.org/articles/10.3389/fmicb.2021.713180/fullbiodiversityendophytesmicrobial functionsspecies interactionssymbiosisplant-associated microbiomes
collection DOAJ
language English
format Article
sources DOAJ
author Yoshie Hori
Hiroaki Fujita
Kei Hiruma
Kazuhiko Narisawa
Hirokazu Toju
spellingShingle Yoshie Hori
Hiroaki Fujita
Kei Hiruma
Kazuhiko Narisawa
Hirokazu Toju
Synergistic and Offset Effects of Fungal Species Combinations on Plant Performance
Frontiers in Microbiology
biodiversity
endophytes
microbial functions
species interactions
symbiosis
plant-associated microbiomes
author_facet Yoshie Hori
Hiroaki Fujita
Kei Hiruma
Kazuhiko Narisawa
Hirokazu Toju
author_sort Yoshie Hori
title Synergistic and Offset Effects of Fungal Species Combinations on Plant Performance
title_short Synergistic and Offset Effects of Fungal Species Combinations on Plant Performance
title_full Synergistic and Offset Effects of Fungal Species Combinations on Plant Performance
title_fullStr Synergistic and Offset Effects of Fungal Species Combinations on Plant Performance
title_full_unstemmed Synergistic and Offset Effects of Fungal Species Combinations on Plant Performance
title_sort synergistic and offset effects of fungal species combinations on plant performance
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2021-09-01
description In natural and agricultural ecosystems, survival and growth of plants depend substantially on residing microbes in the endosphere and rhizosphere. Although numerous studies have reported the presence of plant-growth promoting bacteria and fungi in below-ground biomes, it remains a major challenge to understand how sets of microbial species positively or negatively affect plants’ performance. By conducting a series of single- and dual-inoculation experiments of 13 plant-associated fungi targeting a Brassicaceae plant species (Brassica rapa var. perviridis), we here systematically evaluated how microbial effects on plants depend on presence/absence of co-occurring microbes. The comparison of single- and dual-inoculation experiments showed that combinations of the fungal isolates with the highest plant-growth promoting effects in single inoculations did not have highly positive impacts on plant performance traits (e.g., shoot dry weight). In contrast, pairs of fungi with small/moderate contributions to plant growth in single-inoculation contexts showed the greatest effects on plants among the 78 fungal pairs examined. These results on the offset and synergistic effects of pairs of microbes suggest that inoculation experiments of single microbial species/isolates can result in the overestimation or underestimation of microbial functions in multi-species contexts. Because keeping single-microbe systems under outdoor conditions is impractical, designing sets of microbes that can maximize performance of crop plants is an important step for the use of microbial functions in sustainable agriculture.
topic biodiversity
endophytes
microbial functions
species interactions
symbiosis
plant-associated microbiomes
url https://www.frontiersin.org/articles/10.3389/fmicb.2021.713180/full
work_keys_str_mv AT yoshiehori synergisticandoffseteffectsoffungalspeciescombinationsonplantperformance
AT hiroakifujita synergisticandoffseteffectsoffungalspeciescombinationsonplantperformance
AT keihiruma synergisticandoffseteffectsoffungalspeciescombinationsonplantperformance
AT kazuhikonarisawa synergisticandoffseteffectsoffungalspeciescombinationsonplantperformance
AT hirokazutoju synergisticandoffseteffectsoffungalspeciescombinationsonplantperformance
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