Intraspecific variation in plant–soil feedback depends on plant dominance while interspecific variation is unrelated to plant community structure

Abstract

1 INTRODUCTION

Most plants interact with soil microbes, with interaction outcomes ranging from mutualism to antagonism (Bever et al., 2012). These interactions not only affect the growth of that plant but can also cause shifts in the soil microbiome that persist and affect the recruitment of new individuals into those soils (Bever et al., 2010). These plant–soil feedbacks (PSFs) can thus increase or decrease population growth rates and alter the structure of plant communities (Bennett et al., 2017; Teste et al., 2017). In low-diversity agricultural systems, accumulation of crop diseases can cause negative PSF and significant crop losses (Mariotte et al., 2018). Increasing plant diversity can dilute species-specific pathogens, and thus overall pathogen densities, and increase the diversity and abundance of beneficial microbes (Bennett et al., 2020). Consequently, diversification of agroecosystems should reduce negative PSF and increase positive PSF.

Plant–soil feedback is commonly measured as the effect that plants of a particular species have on conspecific recruitment via changes in the soil; however, in diverse systems, many plant species may condition the soil and respond to these changes (Baxendale et al., 2014; Kulmatiski, 2018). This concept is partially reflected in the measurement of PSF as a pairwise interaction between species (Crawford et al., 2019), yet pairwise PSF is often a poor indicator of plant-community dynamics (Reinhart et al., 2021). This lack of prediction may be because plant neighbourhoods influence microbiome assembly (Mommer et al., 2018) or because root systems are intermingled within soils (Frank et al., 2015) meaning that soils are simultaneously being conditioned by multiple species, even over small spatial scales. Consequently, soil conditioning is likely dependent on the community context. The variability in PSF is further increased by varying responses of plant species to changes in the microbiome (Baxendale et al., 2014), thus limiting our ability to understand the dynamics of diverse plant communities from traditional PSF approaches.

The role of PSF in plant communities may be better considered by integrating the effect and response of multiple species. Averaged across species, the mean effects of soil biota would thus be an estimate of the soil quality and its effect on plant growth. Variability among species may also be important and could have implications for the structure and functioning of ecosystems: An increase in PSF variability could either exacerbate or mitigate fitness inequalities among community members, whereas a reduction in variability suggests that PSF will have limited effects on community dynamics as all plants are affected equally. From a functional perspective, reduced variability coupled with positive or negative community mean PSF could indicate shifts in community productivity, whereas greater variability in PSF should reduce the likelihood that function is affected due to compensatory responses among less affected community members.

Understanding variability in PSF among species can help in designing sustainable cropping systems by mitigating negative and strengthening positive PSFs (Koyama et al., 2022), yet increasing genetic diversity may be more practical in low-diversity agroecosystems as plant genotypes differ greatly in their interactions with soil biota (Gundale & Kardol, 2021; Van Nuland et al., 2016). Whether increasing both species and genetic diversity would have additive benefits depends on whether variability among genotypes and species is correlated and whether genotypes and species respond to different components of the soil microbiome (Schöb et al., 2015). If species are affected by different pathogens or mutualists (i.e. there is a high degree of specificity), we should expect the presence of specific specialized soil biota to increase PSF variability, whereas the presence of shared pathogens or mutualists should reduce variability (Semchenko et al., 2022; Wang et al., 2023). Consequently, regardless of the type of microbiota, microbiome composition could be positively or negatively related to PSF variability. As many crop varieties are bred for resistance to specific pathogens and specialist soil microbes are unlikely to have similar effects on unrelated species (Gilbert & Parker, 2016; Semchenko et al., 2022), we hypothesize that intra- and interspecific variation in PSF responds to different aspects of soil microbiome composition. Microbiome diversity, however, should increase the likelihood that strong pathogens or mutualists are present via selection effects and thus increase intra- and interspecific variability.

Much effort has gone into understanding how PSFs change as a function of ecological conditions, highlighting the roles of climate, soil properties, resource availability and plant community structure in shaping plant–microbe interactions (Beals et al., 2020; De Long et al., 2023; Jiang et al., 2024; Lundell et al., 2022). Many of these studies, however, include relatively limited microbiome data and those that do typically focus on bacteria or fungi (De Long et al., 2023). Few studies have focused on the role of oomycete pathogens in PSF (e.g. Burrill et al., 2023; Domínguez-Begines et al., 2021), despite their importance as plant pathogens (e.g. Phytophthora and Pythium spp. Kamoun et al., 2015). Furthermore, we know that interactions among microbiome components vary among environments and can have strong effects on microbial community assembly and plant–soil feedback (Bahram et al., 2018; Bennett et al., 2017). Nonetheless, interactions among microbiome components are rarely explicitly accounted for when testing the mechanisms of PSF.

To better understand inter- and intraspecific variation in plant responses to soil biota, we focused on how the plant community influences soil microbiomes and PSF in alfalfa (Medicago sativa) agroecosystems. Alfalfa is the most commonly grown forage species globally and is incredibly important to the livestock industry (Annicchiarico et al., 2015). It is a perennial legume that benefits from both rhizobia and mycorrhizal fungi (Püschel et al., 2017), while being susceptible to multiple soil pathogens, which can result in either positive or negative PSF (Awodele & Bennett, 2022). Alfalfa cultivars and other species, however, differ in response to inoculation with soil from alfalfa fields (Awodele & Bennett, 2022). Here, we focus on understanding the drivers of variation in PSF using structural equation models linking the plant community to intra- and interspecific variation in PSF via the soil microbiome (Figure 1). We used this model to test the following hypotheses: (1) Intra- and interspecific variation in PSF will be largely uncorrelated because they are affected by different aspects of the soil microbiome; (2) alfalfa abundance will cause negative intraspecific PSF and increase intraspecific variation in PSF due to increases in species-specific pathogens but will be unrelated to interspecific variation in PSF; and (3) plant species richness will increase positive PSF for both alfalfa and other species mediated by changes in both pathogens and beneficial microbes, resulting in reduced intra- and interspecific variation in PSF.

FIGURE 1

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General structure of the initial structural equation model. We hypothesized that stand age would affect the properties of both soil (pH, texture, carbon, C:N ratio, phosphorus) and the plant stand (species richness, percent alfalfa, alfalfa N and fibre content), which would then alter the structure of soil microbial communities (richness, evenness and composition of bacteria, fungi, oomycetes and AMF). We also hypothesized that changes in the soil microbiome would affect the average and variation in plant–soil feedback among alfalfa cultivars and other plant species.