Plant-soil feedback: incorporating untested influential drivers and reconciling terminology

Abstract

Background Plants condition the soil in which they grow, thereby altering the performance of subsequent plants growing in this soil. This phenomenon, known as plant-soil feedback (PSF), has garnered increasing interest. Experiments are moving from single species soil pairings in the glasshouse to community-level field trials. Consequently, our knowledge of the role PSF plays in shaping ecosystem functions has advanced. However, knowledge gaps remain. Scope Here, we explore intrinsic and extrinsic abiotic and biotic drivers of PSF such as maternal effects, plant functional traits, self-DNA, plant-plant competition, herbivory, interactions between soil organisms, temperature, drought, flooding, greenhouse gases, (micro)nutrients, plant-litter-soil feedback and priority effects. These drivers have begun to feature in experiments, thereby increasing our mechanistic understanding of PSF. Nonetheless, many of these topics have received insufficient coverage to determine general principles across larger temporal and spatial scales. Further, conflicting terminology has excluded PSF studies from reviews and meta-analyses. We review terms such as soil sickness, Janzen-Connell hypothesis, soil-related invasive species work, soil legacies, allelopathy and soil-related succession that overlap with PSF but are generally not named as such. Conclusion Holistic experimental designs that consider the continual reciprocal feedback between the extrinsic environment, plants and soil, as well as the unification of terminologies are necessary if we are to realise the full potential of PSF for understanding and steering ecosystem processes. Here, we compile outstanding questions related to PSF research that emphasis the aforementioned topics and suggest ways to incorporate them into future research in order to advance plant-soil ecology.

A trait‐based framework linking the soil metabolome to plant–soil feedbacks

“…Since their discovery, PSF have been formally presented in the context of effects and responses to the 'soil community' (Bever, 1994) and 'specific growth-depressing microorganisms' ( Van der Putten et al, 1993). This microbe-centric perspective is important, and still predominant, but the role of plant and soil chemistry is gaining attention (Mazzoleni et al, 2015;Nettan et al, 2019;Veen et al, 2019;Ehlers et al, 2020;De Long et al, 2023b;Nannipieri et al, 2023;Steinauer et al, 2023). For example, Semchenko et al (2019) experimentally manipulated soil chemical interactions and microbial legacies and found that belowground chemistry and soil biota interacted to promote seedling survival and species coexistence in grassland mesocosms.…”

“…Since their discovery, PSF have been formally presented in the context of effects and responses to the ‘soil community’ (Bever, 1994) and ‘specific growth‐depressing microorganisms’ (Van der Putten et al ., 1993). This microbe‐centric perspective is important, and still predominant, but the role of plant and soil chemistry is gaining attention (Mazzoleni et al ., 2015; Nettan et al ., 2019; Veen et al ., 2019; Ehlers et al ., 2020; Gundale & Kardol, 2021; De Long et al ., 2023b; Nannipieri et al ., 2023; Steinauer et al ., 2023). For example, Semchenko et al .…”

“…greater persistence) than species on the fast side of the gradient. While root conservation traits clearly affect the rate of litter decomposition, the feedback effects of litter on plant growth are less predictable and the underlying mechanisms poorly understood (Zhang et al ., 2016; Gavinet et al ., 2018; Bueno de Mesquita et al ., 2019; Veen et al ., 2019; De Long et al ., 2023a,b).…”

Realistic time-lags and litter dynamics alter predictions of plant–soil feedback across generations

“…Plant performances during the response phase are measured to predict how soil microbes influence plant coexistence (Crawford et al, 2019, Yan et al, 2022. However, despite a vast body of literature showing that soil microbes can exert strong controls over plant species coexistence, connecting the predictions from such two-phase studies to the observed dynamics of plant communities in nature remains challenging (Forero et al, 2019, Beals et al, 2020, Beckman et al, 2022, Png et al, 2023. A promising approach for addressing this challenge is to adopt the classic two-phase design to better reflect the natural conditions under which PSF arises in the field (Gundale & Kardol, 2021).…”

Alteration of the tree–soil microbial system triggers a feedback loop that boosts holm oak decline

“…For instance, microbial metabolism is the great engine of carbon and nutrient cycling contributing to the availability of soil nutrients (Willey et al, 2008). Overall, alterations of these mechanisms at the soil level may exert positive or negative effects on plant growth and fitness (Bezemer et al, 2020) and hence on species composition and ecosystem functioning (Png et al, 2023). Disentangling the individual contribution of the different processes involved in these plant-soil feedback and its responses to natural and anthropogenic disturbances associated with climate change (van der Putten et al, 2016) may further facilitate the implementation of effective climate-adaptive forest management (Refsland et al, 2023).…”