Core microbiomes for sustainable agroecosystems

Toju, Hirokazu; Peay, Kabir G.; Yamamichi, Masato; Narisawa, Kazuhiko; Hiruma, Kiyoshi; Naito, Kunihiko; Fukuda, Shinji; Ushio, Masayuki; Nakaoka, Shinji; Onoda, Yusuke; Yoshida, Kentaro; Schlaeppi, Klaus; Bai, Yang; Sugiura, Ryo; Ichihashi, Yasunori; Minamisawa, Kiwamu; Kiers, E. Toby

doi:10.1038/s41477-018-0139-4

Cited by 704 publications

(545 citation statements)

References 116 publications

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“…Current attempts to enhance the sustainability of modern cropping systems focus on the restoration of natural soil processes (Bender, Wagg, & Heijden, ; Dias, Dukes, & Antunes, ). Specific manipulations of plant–soil interactions have been proposed as one way to improve the sustainability of agriculture and increase yields (Berendsen, Pieterse, & Bakker, ; Ma, Pineda, Wurff, Raaijmakers, & Bezemer, ; Orrell & Bennett, ; Toju et al, ), including through breeding resistance to below‐ground pathogens and the application of beneficial bio products (Bakker, Manter, Sheflin, Weir, & Vivanco, ; Toju et al, ). Manipulating below‐ground communities to influence above‐ground interactions and improve crop performance has received less attention (see Kaplan, Pineda, & Bezemer, ; Pineda, Kaplan, & Bezemer, ).…”

Section: Introductionmentioning

confidence: 99%

Domesticated tomatoes are more vulnerable to negative plant–soil feedbacks than their wild relatives

Carrillo

Ingwell

et al. 2019

Journal of Ecology

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Domesticated plants can differ from their wild counterparts in the strength and outcome of species interactions, both above‐ and belowground. Plant–soil feedbacks influence plant success, and plant‐associated soil microbial communities can influence plant interactions with herbivores and their natural enemies, yet, it remains unclear if domestication has changed these relationships. To determine the effects of domestication on plant–soil interactions, we characterized soil microbial communities associated with various cultivars of domesticated tomato and some of its wild relatives. We measured the strength and direction of plant–soil feedbacks for domesticated and wild tomatoes, and the effects of soil on plant resistance to specialist herbivory by Manduca sexta, and the attraction of a parasitoid wasp, Cotesia congregata. Domesticated tomatoes and their wild relatives had negative plant–soil feedbacks, as conspecifics cultivated soil that negatively impacted performance of subsequent plants (longer germination time, lower biomass) than if they grew in non‐tomato soils. Significant variation existed among domesticated and wild tomato varieties in the strength of these feedbacks, ranging from neutral to strongly negative. For above‐ground plant biomass, tomato wild relatives were unaffected by growing in tomato‐conditioned soil, whereas domesticated tomatoes grew smaller in tomato soil, indicating effects of plant domestication. Overall, increased microbial biomass within the rhizosphere resulted in progressively less‐negative plant–soil feedbacks. Plant cultivars had different levels of resistance to herbivory by M. sexta, but this did not depend on plant domestication or soil type. The parasitoid C. congregata was primarily attracted to herbivore damaged plants, independent of plant domestication status, and for these damaged plants, wasps preferred some cultivars over others, and wild plants grown in tomato soil over wild plants grown in non‐tomato soil. Synthesis. These results indicate that crop tomatoes are more likely to show negative plant–soil feedbacks than wild progenitors, which could partially explain their sensitivity to monocultures in agricultural soils. Furthermore, cultivar‐specific variation in the ability to generate soil microbial biomass, independent of domestication status, appears to buffer the negative consequences of sharing the same soil. Last, soil legacies were relatively absent for herbivores, but not for parasitoid wasps, suggesting trophic level specificity in soil feedbacks on plant–insect interactions.

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Section: Introductionmentioning

confidence: 99%

Domesticated tomatoes are more vulnerable to negative plant–soil feedbacks than their wild relatives

Carrillo

Ingwell

et al. 2019

Journal of Ecology

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“…Given the formidable challenge to achieve agricultural sustainability, while feeding a growing number of people, new approaches have been proposed, and are currently being actively explored. These include microbiome engineering (Mueller & Sachs, ) or core microbiome inoculation (Toju et al ., ), and the use of advanced technological options (drones, robotics) among others (Walter et al ., ).…”

Section: Information Sources For Exploration Of Agricultural Parametementioning

confidence: 99%

Exploring the agricultural parameter space for crop yield and sustainability

Rillig

Lehmann

2019

New Phytologist

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“…The implications of such findings are now driving developments in the fields of healthcare (Hadrich, ). For plants, microbiome research has similarly focused on health and disease in model species, such as Arabidopsis , or agriculturally important crops (Pérez‐Jaramillo et al, ; Toju et al, ); however, attention is now expanding to wild animal and plant microbiomes with the potential to shape conservation practice.…”

Section: Introductionmentioning

confidence: 99%

Conserving the holobiont

et al. 2020

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Organismal biology has undergone a dramatic paradigm shift in the last decade. The realization that host cells and genes are outnumbered by symbiotic microbial cells and their genes has forced us to rethink our focus on ‘individuals’. It is also becoming increasingly clear that the ecology and biology of animals and plants are intimately connected with their microbial partners. In the context of conserving functioning species, such revelatory insights beg the question—what exactly should we be trying to conserve? Here, we review how an understanding of host–microbe interactions can benefit conservation biology. We propose a way forward for conservation biologists, to gather evidence of the potential effects of changes to plant and animal microbiomes, and to incorporate the holobiont concept into applied conservation practice. In humans, microbes influence physiology, health, behaviour and psychology. In animals and plants, microbes similarly influence critically important components of health, communication and (in animals) behaviour. Together, the animal or plant and all of its associated micro‐organisms are termed the holobiont. At the same time, humans are now the strongest evolutionary force on the planet, causing global change at unprecedented scale. We know that microbial diversity in humans has been compromised in urban societies, with a growing list of consequences for health and function. While we still have limited evidence for similar effects in plants and animals, anthropogenic factors that affect diversity are also likely to affect animal and plant microbiomes, with similar associated effects on host function and health. Microbiome research is still in its relative infancy, particularly in its application to plants and animals, yet the tools are becoming more widely available and affordable. Forward‐looking conservation biologists could harness such tools and apply them to the study of plant and animal microbiomes with the goal of understanding which microbiota might be required to ensure future viability of conserved host populations. For now, the precautionary principle applies. We suggest that, to meaningfully and effectively conserve a species, we must also consider how to conserve the bacteria, viruses, fungi and other symbionts intimately associated with that macro‐organism. A free Plain Language Summary can be found within the Supporting Information of this article.

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Core microbiomes for sustainable agroecosystems

Cited by 704 publications

References 116 publications

Domesticated tomatoes are more vulnerable to negative plant–soil feedbacks than their wild relatives

Domesticated tomatoes are more vulnerable to negative plant–soil feedbacks than their wild relatives

Exploring the agricultural parameter space for crop yield and sustainability

Conserving the holobiont

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