Organic management promotes natural pest control through altered plant resistance to insects

Abstract

rganic farming is characterized by management practices that promote soil biodiversity and beneficial ecological interactions to offset the need for synthetic inputs such as inorganic fertilizers and biocides. Pest and nutrient management in organic agriculture is largely accomplished through various diversification methods, including cover crops, crop rotations, trap crops and promotion of active soil microbial communities [1][2][3][4][5] . Although organic agriculture is often thought to be less productive in terms of yield as compared to conventional farming, it offers great potential to enhance ecosystem services and agricultural sustainability [5][6][7] .Accumulating evidence suggests that organic management practices also reduce pest populations and increase resilience to pest damage 8,9 . Decreased insect pests on long-term organic farms have largely been attributed to practices that limit pest build-up, increase predator biodiversity, and increase the numbers of beneficial insects [9][10][11][12][13] . The nitrogen contents of plants grown on organic farms are often lower than those of conventional systems 11,12 . Plants that are nitrogen-limited are often less attractive to herbivores, which could also explain the lower pest pressure observed in organic systems 12,14,15 . However, very little is known about the impact of organic management for plant defence capacity.Organic management strategies can increase microbial activity and biomass in soils 1,2,16 , alter microbial communities 17 and in some cases enhance plant associations with beneficial microbes in the rhizosphere 3,4 . Microorganisms that associate with plant roots play a critical role in resistance to abiotic and biotic stress [18][19][20] . Mycorrhizal fungi have been shown to induce plant systemic resistance 21,22 and can reduce susceptibility to pathogens 23 and herbivores 24 . Plant growth-promoting rhizobacteria commonly found in soil microbial pools, as well as commercial inoculants, induce defences and other physiological changes in the host plant that influence above-ground herbivores 19,[25][26][27][28] . Despite the known interactions between organic management, plant-microbe associations and changes in crop resistance, the potential of these interactions to reduce pest damage in agricultural systems remains largely untapped.In this study, we report that organic management influences pest populations through changes in plant resistance. We explore linkages between insect settling and performance, rhizosphere communities and phytohormones related to plant defence with tomato (Solanum lycopersicum) and the beet leafhopper (Circulifer tenellus), an important pest of California's processing tomato industry 29 . We demonstrate that tomatoes grown using conventional management are preferentially settled by leafhopper pests and have lower salicylic acid (SA) levels compared to tomatoes grown using organic management. Our results indicate that differences in insect preference were due at least partially to changes in SA accumulation and rhi...

Soil Microbiomes From Fallow Fields Have Species-Specific Effects on Crop Growth and Pest Resistance

“…This finding is in line with our previous work, which has suggested that successional shifts in soil microbiomes are an important factor driving increases in the herbivore resistance of a wild plant ( Howard et al., 2020 ), yet the underlying mechanisms for this microbe-mediated resistance are still unresolved. However, it is becoming clearer that various early successional forbs and grasses ( Pineda et al., 2020 ), as well as organic management practices ( Blundell et al., 2020 ), can condition soil to promote herbivore resistance. Thus, in addition to providing related ecosystem services as habitat for natural enemies of pests ( Denys and Tscharntke, 2002 ), fallow land may be worth investigating as sources of beneficial soil microbiomes that are adapted to local edaphic conditions, not only potentially improving their establishment and efficacy ( Hawkes and Connor, 2017 ), but also reducing the non-target risks of introducing non-native microbes ( Hart et al., 2018 ).…”

“…that induced systemic pathogen susceptibility increased tomato plants' resistance to T. ni, further indicating that the salicylic acid-jasmonic acid trade-off may play an important role in mediating rhizosphere microbial influence on insect herbivory (Haney et al, 2018). Another recent study (Blundell et al, 2020) implicated salicylic acid as an important mediator of soil microbe-influenced resistance to a hemipteran herbivore (which generally tend to be more strongly affected by salicylic acid-versus jasmonic acid-mediated defenses), further emphasizing the potential importance of rhizosphere microbes affecting plant-insect interactions through altering phytohormonal signaling. Thus, changes in the functional composition of soil microbial communities, including the abundance of pathogens-which are expected to shift over fallow succession (Hannula et al, 2017)-could affect herbivore resistance through altering plant defense responses.…”

“…This condition is typically avoided by reducing the abundance of suitable plant hosts through crop rotation or polyculture (Bennett et al, 2012). With regard to insect pests, one recent study suggests that the lower insect resistance of plants in conventionally versus organically managed fields is at least partially due to differences in soil microbial communities (Blundell et al, 2020). Recent work has also shown that soil microbiomes conditioned by non-crop plants, such as grassland species, can reduce the susceptibility of chrysanthemums to both pathogens and insect herbivores (Ma et al, 2017;Ma et al, 2019;Pineda et al, 2020), suggesting that soil microbiomes from natural systems could be used to improve crop performance.…”

Western Corn Rootworm, Plant and Microbe Interactions: A Review and Prospects for New Management Tools

“…Plant-insect-microbe interactions occurring in the rhizosphere can have dramatic effects across trophic levels, above and below ground, and can shape plant, herbivore, and microbial communities [152]. Beneficial microbial communities can provide plants with increased pest resistance [153]. Plants release a suite of chemicals from roots upon insect damage to which specific microbes respond.…”

“…In the case of maize, benzoxazinoids have been shown to alter the rhizosphere microbiome, providing potential benefits to maize in the form of pest suppression in following generations [155]. Organic practices that promote soil health can also alter plant resistance to aboveground pest pressure [153]. However, there has been little work to investigate how these rhizosphere interactions affect western corn rootworm.…”