Sarah J Sapsford

Plant-soil feedbacks (PSFs) are essential for understanding plant community dynamics and ecosystem restoration. Glasshouse experiments provide controlled environments to study PSFs, but isolating biotic and abiotic influences remains challenging. Soil sterilization removes biotic components, with biotic effects restored via live inoculum. However, inconsistencies in sterilization methods, inoculum ratios, and storage practices complicate reproducibility. This literature review synthesizes 184 PSF studies from the past 24 years, to document methodological variation and reporting inconsistencies that influence experimental design, interpretation, and cross-study comparability, specifically highlighting variability in sterilization parameters and live inoculum application. Many studies overlooked nutrient flushes and persistent microbial activity post-sterilization. No consensus exists on live inoculum ratios, and storage practices remain poorly reported, limiting cross-study comparability. Reproducibility and realism in PSF estimates may be strengthened through measures including, but not limited to: (1) improved methodological reporting of core parameters, (2) validation of sterilization success, and (3) empirically determined inoculum ratios.

Tuber melanosporum was first harvested in Australia in 1999, and exports began in 2007. Australia is now the world's fourth-largest truffle producer. The main challenges Australian producers face are climate change, obtaining well-mycorrhized seedlings with no contaminants, and preventing entry of the contaminant species T. indicum and T. maculatum to Australia and T. brumale from east to Western Australia. There is also increasing competition from other southern hemisphere countries. Almost all truffle orchards in Australia are in regions with 600–1500 mm annual rainfall and a mean daily mid-summer temperature below 25 °C. As soils in agricultural lands of Australia are frequently acidic, lime is applied to achieve the alkaline pH required by truffles. New truffle orchards should be planned bearing in mind future climatic predictions. The incorporation of more T. borchii and T. aestivum in truffieres, and the possible use of T. magnatum will spread the harvest period, and thus exports. Oaks and hazel are currently used as major hosts, and new host species are being investigated, including Pinus. The cost of establishing a truffiere in Australia is high. However, Australia lacks many pests, diseases, and social problems associated with the European industry, and together with being an environmentally friendly industry, these factors make truffle production an attractive agricultural investment in Australia which will aid regional economies.

1. Biological invasions of plants have profound effects on ecosystem functioning by directly and indirectly altering soil microbiota, especially when invasive plants co-invade with their associated microbiomes. Ecosystem functions may recover slowly following invader removal, with implications for restoration.

2. We investigated the recovery of soil ecosystem function (measured as soil enzymes) following the removal, at different densities and times, of invasive Pinus spp. in New Zealand, and how different enzymatic activities responded to pine legacies.

3. Enzymatic activities were driven by pine legacies via both abiotic (soil nutrients) and biotic (fungi and bacteria) soil properties, with different enzymes showing distinct patterns. The activity of the enzymes cellobiohydrolase (cellulose degrading), β-glucosidase (cellulose degrading), N-acetyl-glucosaminidase (chitin degrading), laccase (lignin oxidising) and acid phosphatase (organic phosphate hydrolysing) were influenced by time since pine removal and by pine density at removal via effects on biotic communities. In comparison, Mn-peroxidase (lignin oxidising) was positively correlated with density of pines at removal and was negatively correlated with time since removal and was only influenced by fungal communities.

4. Synthesis. The recovery of soil enzymatic function following invasive species removal is slow and dependent on pine legacies through the gradual changes in fungal and bacterial communities. The cascading effects of these changes suggest potential implications for the success of future plant establishment and restoration of co-invaded ecosystems.

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.

Plants can strongly influence the performance of subsequent conspecific and heterospecific plants either positively or negatively by conditioning soil abiotic and/or biotic properties via plant litter and root activity. This process is commonly known as ‘plant-soil feedback’, which has been increasingly demonstrated to play a major role in plant community dynamics, ecosystem succession, and the maintenance of biodiversity (e.g., Bever et al. 1997; Ehrenfeld et al. 2005; Kulmatiski et al. 2008; van der Putten et al. 2013). As such, plant-soil feedback effects have major consequences for ecosystem functioning and application potential in areas such as the prediction of vegetation and ecosystem responses to global change, construction/maintenance of sustainable agroecosystems, ecosystem restoration, invasive plant management, and conservation of plant diversity. However, while recent plant-soil feedback studies have emerged aiming to explain underlying mechanisms, our understanding of plant-soil feedback and our ability to determine its relative importance in realistic settings remain limited by inconsistent experimental evidence (e.g., De Long et al. 2019; Gundale and Kardol 2021). Moreover, closely-associated ecological concepts such as priority effects, maternal effects, soil legacy effects, the Janzen–Connell hypothesis, and self-DNA inhibition tend to be considered separately, and recognising overlaps among these concepts can expand our understanding of plant-soil feedback (De Long et al. 2023). Thus, in an attempt to advance our understanding as well as shape novel perspectives to advance this key ecological concept, we gathered 14 articles for this Special Issue, which includes a selection of review, opinion, methods, modelling, and research papers

Many oomycetes are important plant pathogens that cause devastating diseases in agricultural fields, orchards, urban areas, and natural ecosystems. Limitations and difficulties associated with isolating these pathogens have led to a strong uptake of DNA metabarcoding and mass parallel sequencing. At least 21 primer combinations have been designed to amplify oomycetes, or more specifically, Phytophthora species, from environmental samples. We used the Illumina sequencing platform to compare 13 primer combinations on mock communities and environmental samples. The primer combinations tested varied significantly in their ability to amplify Phytophthora species in a mock community and from environmental samples; this was due to either low sensitivity (unable to detect species present in low concentrations) or a lack of specificity (an inability to amplify some species even if they were present in high concentrations). Primers designed for oomycetes underestimated the Phytophthora community compared to Phytophthora-specific primers. We recommend using technical replicates, primer combinations, internal controls, and a phylogenetic approach for assigning a species identity to OTUs or ASVs. Particular care must be taken if sampling substrates where hybrid species could be expected. Overall, the choice of primers should depend upon the hypothesis being tested.

The next century will almost certainly see an unprecedented rise in forest pathogen epidemics, requiring a proactive rather than reactive response. Diseases caused by native pathogens with complex aetiologies will become more common, and recognising, characterising and managing these epidemics are difficult because native pathogens are frequently already widespread, and eradication is not feasible. We need to start approaching these issues from a ‘whole ecosystem’ perspective, highlighting the many aspects and entanglements of forest declines and allowing us to respond with management options tailored to each scenario. The approach proposed here provides logical steps based on six questions to untangle the direct and indirect environmental drivers of tree declines.

Removing wilding conifers (invasive non-native trees in the Pinaceae) has become a major focus of conservation and land management in Aotearoa New Zealand. Management of wilding conifers has been supported by applied research on control methods, generally with a short-term focus of removing or containing invasions to prevent further spread. However, a focus on short-term management activities may not achieve desired longer-term outcomes of restoring economic and environmental values. Greater integration of ecological research on wilding conifer impacts and legacies with management can help to ensure long-term goals are achieved. We review how impacts and legacies of wilding conifers develop and persist over time. Several key thresholds or tipping points are identified, where prioritising management may avoid state-changes in ecosystems. We then review the potential of sites to support different land uses after wilding conifers have been controlled, including pasture, plantations and native restoration, and develop a decision support tree to guide successful transition to these land uses. We find that maintaining anthropogenic native tussock grasslands is unlikely to be a sustainable goal on most invaded sites without major sustained management interventions. Native woody cover is likely more sustainable, but often requires additional management of post-removal legacies of wilding conifers, including other invasive plants such as sward-forming non-native grasses. Shade tolerant wilding conifers, such as Douglas-fir, remain a pernicious problem in any effort to prevent reinvasion into woody vegetation. Although there are still questions about the causes and consequences of wilding conifer invasions, ecological research can provide helpful guidance to improve long-term outcomes following wilding conifer control.

Plant invasions can cause biotic homogenisation which can have cascading effects on the diversity of invaded ecosystems. These impacts on diversity are likely to be scale-dependent and thus affect different aspects of diversity (i.e. beta, gamma and alpha). For example, the widespread invasion of non-native pine trees causes a loss of plant gamma diversity; however, the effects of this invasion and co-invasion by ectomycorrhizal fungi on belowground fungal communities remain unknown. We established thirteen 400 m(2) plots across a Pinus nigra density gradient in Canterbury, New Zealand. We sampled twenty-four soil samples from each plot and extracted and sequenced DNA for fungi from each sample independently, allowing determination of within-sample (alpha) and plot-scale (gamma) diversity and turnover (beta-diversity). Pine invasion was associated with a positive unimodal response in soil fungal beta-diversity, reflected by an increase in saprotroph diversity at low pine density following a loss of this group of fungi at high pine densities. Pine invasion was also associated with an overall 47.7% loss of fungal alpha-diversity and a 50% loss of gamma-diversity. Loss of diversity correlated to a shift from a saprotroph-dominated fungal community in low pine density plots to an ectomycorrhizal-dominated community in high pine density plots. However, despite the resulting dominance of ectomycorrhizal fungi, there was no increase in gamma-diversity of ectomycorrhizal fungi as pine density increased. Our results support the concept that low-density invasions increase ecosystem heterogeneity and therefore beta-diversity, but that as aboveground plant communities become more homogenised there is a dramatic loss of fungal diversity across all scales that could inhibit recovery and restoration of invaded ecosystems.

Pathogen accumulation on an invasive plant species can occur over time, through co-invasion, or adaptation of native pathogen species. While accumulated pathogens can reduce the success and spread of an invasive species, they can also spill-over into native plant communities or valuable non-native populations. Transmission of pathogens may be density-dependent, with dense invasive populations creating better opportunities for pathogen spread than scattered individuals. Some pine species (Pinus) and some other Pinaceae (including Pseudotsuga) are extremely invasive trees in New Zealand but trees in the Pinaceae are also used extensively within the forestry industry. Little is known about the foliar pathogens present on invasive populations and whether they pose a risk to industry. We cultured foliar fungi from needles of Pseudotsuga menziesii and Pinus contorta found at both low and high densities of invasion. DNA from fungal cultures was extracted and sequenced using Sanger sequencing. We cultured fungi from a greater proportion of P. menziesii than P. contorta needles and a greater proportion of trees from low versus high densities of invasion. The richness of foliar fungi decreased as a function of density and P. menziesii hosted a greater richness of fungi than P. contorta. We observed no change in the richness of pathogens between P. menziesii and P. contorta or between low and high density invasions. However, we did observe a greater proportion of fungi that were potentially pathogenic at high density than at low density. We identified one major widespread pathogen (Nothophaeocryptopus gaeumannii) and a number of opportunistic potential pathogens (i.e. Sydowia polyspora, Lophodermium pinastri and Alternaria alternata), indicating the possibility of spill-over into commercial plantations.