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

Abstract

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.

Complex patterns in tolerance and resistance to pests and diseases underpin the domestication of tomato

“…The lack of genetic correlation between resistance traits in our experimental set‐up goes in line with previous findings in wild tomatoes (e.g. Thaler & Karban, ; Koricheva et al , ), but also extends the observed pattern to later stages of the domestication of tomato (see also Carrillo et al , ).…”

“…The lack of genetic correlation between resistance traits in our experimental set-up goes in line with previous findings in wild tomatoes (e.g. Thaler & Karban, 1997;Koricheva et al, 2004), but also extends the observed pattern to later stages of the domestication of tomato (see also Carrillo et al, 2019). Resistance to insect herbivory mediated by glandular trichomes is well represented in the genus Solanum, where four types of glandular trichomes (I, IV, VI, VII) and four nonglandular (II, III, V, VIII) have been described (Glas et al, 2012).…”

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

“…Wild sunflower accessions are slightly more readily colonized by mycorrhizae (Turrini et al, 2016) and also less resistant to pathogens than domesticated lines (Leff et al, 2016). With regard to the crops studied here, previous studies have indicated that cultivated lettuce and maize plants assemble different microbiomes than their wild relatives (Cardinale et al, 2015;Szoboszlay et al, 2015), and that cultivated tomato plants respond differently to soil conditioning compared to their wild counterparts (Carrillo et al, 2019). It is also important to note that these studies found substantial cultivar-level variation in the microbiomes of these crop species, which emphasizes the need to not only characterize the responses of different plant species to microbiomes, but also a diverse range of genotypes within species.…”

Crops and their wild progenitors recruit beneficial and detrimental soil biota in opposing ways

“…Nevertheless, whether these shifts in rhizosphere microbial communities can affect the outcome of plant soil feedbacks is less studied, with a few exceptions. For instance, Carrillo et al (2019) found that soils trained by domesticated tomatoes promote more negative feedbacks than its wild progenitors, and that was associated with shifts in the microbial biomass. Similarly, Miller & Menalled (2015) found negative feedbacks in plants growing in soils previously trained by crops, in comparison with plants growing in soils trained by wild species.…”

“…Previous evidence showed that soils trained by domesticated tomatoes promoted more negative PSF than their relatives through shifts in microbial community composition (Carrillo et al, 2019). Although few case studies have provided useful insights, a broader analysis about the functional consequences of domestication on PSF in crops is missing.…”