An invasive plant rapidly increased the similarity of soil fungal pathogen communities

Abstract

Background and Aims Plant invasions can change soil microbial communities and affect subsequent invasions directly or indirectly via foliar herbivory. It has been proposed that invaders promote uniform biotic communities that displace diverse, spatially variable communities (“Biotic Homogenization Hypothesis”), but this has not been experimentally tested for soil microbial communities, so the underlying mechanisms and dynamics are unclear. Here, we compared density-dependent impacts of the invasive plant Alternanthera philoxeroides and its native congener A. sessilis on soil fungal communities, and their feedback effects on plants and a foliar beetle. Methods We conducted a plant-soil feedback (PSF) experiment and a lab bioassay to examine PSFs associated with the native and invasive plants and a beetle feeding on them. We also characterized the soil fungal community using high-throughput sequencing. Key Results We found locally differentiated soil fungal pathogen assemblages associated with high densities of the native plant Alternanthera sessilis but little variation in those associated with the invasive congener A. philoxeroides, regardless of plant density. In contrast, AM fungal assemblages associated with high densities of the invasive plant were more variable. Soil biota decreased plant shoot mass but their effect was weak for the invasive plant growing in native plant conditioned soils. PSFs increased the larval biomass of a beetle reared on leaves of the native plant only. Moreover, PSFs on plant shoot, root and beetle mass were predicted by different pathogen taxa in a plant species-specific manner. Conclusion Our results suggest that plant invasions can rapidly increase the similarity of soil pathogen assemblages even at low plant densities leading to taxonomically and functionally homogeneous soil communities that may limit negative soil effects on invasive plants.

Aboveground herbivory can promote exotic plant invasion through intra‐ and interspecific aboveground–belowground interactions

“…Some invasive plants, such as A. philoxeroides , tend to accumulate soil pathogens and thereby asymmetrically suppress native plants (Eppinga et al ., 2006; Fig. 6a), and such PSF effects could be further enhanced by foliar herbivory (Bezemer et al ., 2013; Wang et al ., 2020). Moreover, similar species‐specific, soil‐induced defenses that are activated upon herbivory or pathogen infection also increase plant performance in other systems (Carrión et al ., 2019; Blundell et al ., 2020).…”

Leguminous cover crops and soya increased soil fungal diversity and suppressed pathotrophs caused by continuous cereal cropping

“…Most Fusarium species are fungal plant pathogens, and can produce mycotoxins in cereal crops and threaten public health through the food chain ( Fones et al, 2020 ). A lower abundance of Powellomyces in the new systems could be an indication of increasing yield stability and sustainability, since the accumulation of Powellomyces can decrease plant shoot mass ( Wang M. et al, 2021 ). By contrast, the enriched saprotrophic Stachybotrys , Staphylotrichum , Penicillium , and the symbiotrophic Podospora in the new systems have been identified as antagonists of soil-borne plant pathogens and the primary decomposers of organic matter in agricultural soils ( Xu et al, 2012 ; Ding et al, 2017 ).…”

Latitudinal variation in the diversity and composition of various organisms associated with an exotic plant: the role of climate and plant invasion

“…Interestingly, A. philoxeroides invasion as well as composition of other plants, rather than climate variables, were the best predictors for the diversity and richness of major functional groups and the composition of putative fungal pathogens, suggesting a stronger role of plant invasion and biotic interactions in shaping some biotic communities along latitudinal gradients. The results, combined with other observational and experimental studies (Bowen et al ., 2017; Wang et al ., 2021), suggest that exotic plant invasion could be a driver, instead of passenger, of biotic homogeneity across latitudes for some groups of organisms, such as putative fungal pathogens.…”

“…This result is consistent with the accumulation of local pathogens hypothesis (Eppinga et al ., 2006). Recently, we found that A. philoxeroides conditioned soils had more abundant and compositionally similar fungal pathogens than soils conditioned by its native congener A. sessilis when grown at high density, and had greater negative feedbacks on the native plant (Lu et al ., 2018; Wang et al ., 2021). Taken together, these findings suggest potential self‐reinforcing impacts of A. philoxeroides invasion via recruiting taxonomically homogeneous soil pathogens in the field.…”

“…philoxeroides rhizosphere bacteria and fungi decreases with latitude, and their compositional similarity decreases with rising latitudinal distance (Lu et al ., 2018). Moreover, recently we have found that the assemblies of fungal pathogens were more similar among A. philoxeroides conditioned soils than among Alternanthera sessilis conditioned soils but only when the plants were grown at high density in a glasshouse experiment (Wang et al ., 2021). These pieces of information suggest a density‐dependent effect of A. philoxeroides on its associated organisms.…”