Soil pathogen-aphid interactions under differences in soil organic matter and mineral fertilizer

Stijn van Gils*, Giovanni Tamburini, Lorenzo Marini, Arjen Biere, Maaike van Agtmaal, Olaf Tyc, Martine Kos, David Kleijn, Wim H. van der Putten

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

1 Citation (Scopus)

Abstract

There is increasing evidence showing that microbes can influence plant-insect interactions. In addition, various studies have shown that aboveground pathogens can alter the interactions between plants and insects. However, little is known about the role of soil-borne pathogens in plant-insect interactions. It is also not known how environmental conditions, that steer the performance of soil-borne pathogens, might influence these microbe-plant-insect interactions. Here, we studied effects of the soil-borne pathogen Rhizoctonia solani on aphids (Sitobion avenae) using wheat (Triticum aestivum) as a host. In a greenhouse experiment, we tested how different levels of soil organic matter (SOM) and fertilizer addition influence the interactions between plants and aphids. To examine the influence of the existing soil microbiome on the pathogen effects, we used both unsterilized field soil and sterilized field soil. In unsterilized soil with low SOM content, R. solani addition had a negative effect on aphid biomass, whereas it enhanced aphid biomass in soil with high SOM content. In sterilized soil, however, aphid biomass was enhanced by R. solani addition and by high SOM content. Plant biomass was enhanced by fertilizer addition, but only when SOM content was low, or in the absence of R. solani. We conclude that belowground pathogens influence aphid performance and that the effect of soil pathogens on aphids can be more positive in the absence of a soil microbiome. This implies that experiments studying the effect of pathogens under sterile conditions might not represent realistic interactions. Moreover, pathogen-plant-aphid interactions can be more positive for aphids under high SOM conditions. We recommend that soil conditions should be taken into account in the study of microbe-plant-insect interactions.

Original languageEnglish
Article numbere0179695
Number of pages14
JournalPLoS ONE
Volume12
Issue number8
DOIs
Publication statusPublished - 1 Aug 2017

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Organic minerals
Aphids
Fertilizers
Pathogens
mineral fertilizers
Biological materials
Minerals
Aphidoidea
soil organic matter
Soil
Soils
pathogens
plant-insect relations
soil
Thanatephorus cucumeris
Insects
Biomass
microorganisms
plant pathogens
biomass

Cite this

van Gils, Stijn ; Tamburini, Giovanni ; Marini, Lorenzo ; Biere, Arjen ; van Agtmaal, Maaike ; Tyc, Olaf ; Kos, Martine ; Kleijn, David ; van der Putten, Wim H. / Soil pathogen-aphid interactions under differences in soil organic matter and mineral fertilizer. In: PLoS ONE. 2017 ; Vol. 12, No. 8.
@article{65d292ce5be64e28a775256d06768517,
title = "Soil pathogen-aphid interactions under differences in soil organic matter and mineral fertilizer",
abstract = "There is increasing evidence showing that microbes can influence plant-insect interactions. In addition, various studies have shown that aboveground pathogens can alter the interactions between plants and insects. However, little is known about the role of soil-borne pathogens in plant-insect interactions. It is also not known how environmental conditions, that steer the performance of soil-borne pathogens, might influence these microbe-plant-insect interactions. Here, we studied effects of the soil-borne pathogen Rhizoctonia solani on aphids (Sitobion avenae) using wheat (Triticum aestivum) as a host. In a greenhouse experiment, we tested how different levels of soil organic matter (SOM) and fertilizer addition influence the interactions between plants and aphids. To examine the influence of the existing soil microbiome on the pathogen effects, we used both unsterilized field soil and sterilized field soil. In unsterilized soil with low SOM content, R. solani addition had a negative effect on aphid biomass, whereas it enhanced aphid biomass in soil with high SOM content. In sterilized soil, however, aphid biomass was enhanced by R. solani addition and by high SOM content. Plant biomass was enhanced by fertilizer addition, but only when SOM content was low, or in the absence of R. solani. We conclude that belowground pathogens influence aphid performance and that the effect of soil pathogens on aphids can be more positive in the absence of a soil microbiome. This implies that experiments studying the effect of pathogens under sterile conditions might not represent realistic interactions. Moreover, pathogen-plant-aphid interactions can be more positive for aphids under high SOM conditions. We recommend that soil conditions should be taken into account in the study of microbe-plant-insect interactions.",
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Soil pathogen-aphid interactions under differences in soil organic matter and mineral fertilizer. / van Gils, Stijn; Tamburini, Giovanni; Marini, Lorenzo; Biere, Arjen; van Agtmaal, Maaike; Tyc, Olaf; Kos, Martine; Kleijn, David; van der Putten, Wim H.

In: PLoS ONE, Vol. 12, No. 8, e0179695, 01.08.2017.

Research output: Contribution to journalArticleAcademicpeer-review

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AU - Tamburini, Giovanni

AU - Marini, Lorenzo

AU - Biere, Arjen

AU - van Agtmaal, Maaike

AU - Tyc, Olaf

AU - Kos, Martine

AU - Kleijn, David

AU - van der Putten, Wim H.

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AB - There is increasing evidence showing that microbes can influence plant-insect interactions. In addition, various studies have shown that aboveground pathogens can alter the interactions between plants and insects. However, little is known about the role of soil-borne pathogens in plant-insect interactions. It is also not known how environmental conditions, that steer the performance of soil-borne pathogens, might influence these microbe-plant-insect interactions. Here, we studied effects of the soil-borne pathogen Rhizoctonia solani on aphids (Sitobion avenae) using wheat (Triticum aestivum) as a host. In a greenhouse experiment, we tested how different levels of soil organic matter (SOM) and fertilizer addition influence the interactions between plants and aphids. To examine the influence of the existing soil microbiome on the pathogen effects, we used both unsterilized field soil and sterilized field soil. In unsterilized soil with low SOM content, R. solani addition had a negative effect on aphid biomass, whereas it enhanced aphid biomass in soil with high SOM content. In sterilized soil, however, aphid biomass was enhanced by R. solani addition and by high SOM content. Plant biomass was enhanced by fertilizer addition, but only when SOM content was low, or in the absence of R. solani. We conclude that belowground pathogens influence aphid performance and that the effect of soil pathogens on aphids can be more positive in the absence of a soil microbiome. This implies that experiments studying the effect of pathogens under sterile conditions might not represent realistic interactions. Moreover, pathogen-plant-aphid interactions can be more positive for aphids under high SOM conditions. We recommend that soil conditions should be taken into account in the study of microbe-plant-insect interactions.

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DO - 10.1371/journal.pone.0179695

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JO - PLoS ONE

JF - PLoS ONE

SN - 1932-6203

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van Gils S, Tamburini G, Marini L, Biere A, van Agtmaal M, Tyc O et al. Soil pathogen-aphid interactions under differences in soil organic matter and mineral fertilizer. PLoS ONE. 2017 Aug 1;12(8). e0179695. https://doi.org/10.1371/journal.pone.0179695