New frontiers in belowground ecology for plant protection from root-feeding insects

Abstract

Herbivorous insect pests living in the soil represent a significant challenge to food security given their persistence, the acute damage they cause to plants and the difficulties associated with managing their populations. Ecological research effort into rhizosphere interactions has increased dramatically in the last decade and we are beginning to understand, in particular, the ecology of how plants defend themselves against soil-dwelling pests. In this review, we synthesise information about four key ecological mechanisms occurring in the rhizosphere or surrounding soil that confer plant protection against root herbivores. We focus on root tolerance, root resistance via direct physical and chemical defences, particularly via acquisition of siliconbased plant defences, integration of plant mutualists (microbes and entomopathogenic nematodes, EPNs) and the influence of soil history and feedbacks. Their suitability as management tools, current limitations for their application, and the opportunities for development are evaluated. We identify opportunities for synergy between these aspects of rhizosphere ecology, such as mycorrhizal fungi negatively affecting pests at the root-interface but also increasing plant uptake of silicon, which is also known to reduce herbivory. Finally, we set out research priorities for developing potential novel management strategies. Re: Revision of our review APSOIL-D-16-00199 Dear Prof van Gestel, Many thanks for your email advising us that our paper may be considered for publication pending major revisions. Please find enclosed our revised article New frontiers in belowground ecology for plant protection from root-feeding insects. As you will see this paper has been substantially rewritten and developed. Full details of these changes are in our response to reviewers. We are thankful to both reviewers for constructive comments and suggestions. We are grateful for the extension you provided and very sorry that we were late returning this revision to you. Please don't hesitate to contact me if I can provide further information.

Managing soil functions for a sustainable bioeconomy—Assessment framework and state of the art

“…Pesticide application can also be reduced by promoting antagonists of pests, for example, by adding organic amendments or inoculating soil or seeds with beneficial organisms. The latter is still rare, but researchers see significant advances and potential for this technology (Johnson et al, 2016;Kergunteuil et al, 2016).…”

Pressures on soil functions from soil management in Germany. A foresight review

“…For crop rotations, there are drivers in opposite directions: On the one hand, diversifying crop rotations and/or including non-harvested cover crops and legumes induce improved soil functions in terms of nutrient cycling, soil microbial biomass, and soil biota with relevance for plant Johnson et al 2016), and soil structure with relevance for soil erosion (Bronick and Lal 2005). As such, these measures are useful for counteracting soil degradation threats, including soil biodiversity loss, and mitigating climate change (Table 5).…”

“…Developing plant varieties in terms of their pathogen tolerance and their defense mechanisms below ground is a research topic that may also become more practically relevant in the future once research has advanced (Johnson et al 2016;Rasmann et al 2017) (Table 5). New breeding technologies, such as CRISPR/cas9, can also lead to organisms, including varieties of annual agricultural crops, which can bring risks, such as harming ecosystems (Science for Environment Policy 2016) which could also have an impact on agricultural soils.…”

Crop Traits for Defense against Pests and Disease: Durability, Breakdown and Future Prospects

“…These can include the use of plant mutualists or manipulation of soil conditions, for example by application of chemical constituents such as silicon (Johnson et al, 2016). In terms of plant mutualists, arbuscular mycorrhizal fungi can improve crop productivity, as reported by Robinson-Boyer et al, which may result in better tolerance of pest and disease attack Mitchell et al and also help plants resist attack by root herbivores (Johnson et al, 2016). Moreover, the role of silicon application to the soil and resistance to herbivory is considered in the review by Reynolds et al.…”

“…Plant physical defenses can offer particularly durable resistance to pests and pathogens (Johnson et al, 2016;Moore and Johnson, 2017); ecological studies, for example, have shown plant physical traits to be more effective deterrents to insect herbivory than plant secondary metabolites (Peeters et al, 2007;Cooke and Leishman, 2012). As outlined in the review by Mitchell et al, plant structural traits such as trichomes, spines, and cuticles can provide a physical barrier to arthropod pest attachment, feeding and oviposition, while plant vigor and altered phenology can increase tolerance of pest damage and reduce the incidence of pest attacks.…”