Ian C. Anderson

Summary: Human colonization since the 19th century has resulted in the global spread of pines beyond their original northern boreal distribution. Although the introduction history of pines is documented through historical records, little is known about the introduction history of their ectomycorrhizal (ECM) fungi, which are critical symbionts for the survival and invasion of pines. Using Suillus luteus as an example, whole genomes of 208 individuals collected across native and introduced ranges were sequenced to reveal the introduction history of pine co‐introduced ECM fungi. Population genomics analyses showed that all introductions originated from Europe. With the exception of North America, introduced populations were genetically differentiated from the European population, with varying magnitudes of population expansion in different introduced regions. Genetic variation within the native European population followed isolation by distance, but not in the introduced range, highlighting the disparity in the spatial‐genetic patterns of native vs exotic habitats. The spread of S. luteus is mediated by human activities accompanying pine introductions, with its demographic history linked to forestry practices. The spatial, temporal, and demographic patterns observed in S. luteus offer insight into the population genetics of a widely introduced ECM fungus and are likely applicable to other pine co‐introduced ECM fungi.

Early management decisions in operational forestry are critical for plantation success because it strongly influences seedling quality at planting. Beyond shaping seedling morphology, nursery inputs can also restructure root-associated fungal communities which has consequences for nutrient acquisition, stress tolerance and disease suppression after planting. In this study, we altered nutrient and fungicide inputs based on mycorrhizal ecological theory and quantified the effects of these treatments on key dimensions of the growth performance of radiata pine seedlings. In parallel, we profiled the root-associated mycobiome, assigning fungal taxa to functional guilds and summarizing their richness, diversity, relative abundance and community structure. Using a composite performance index that integrates the key morphological and health measures into a single response variable, together with conventional statistical models with machine learning approaches, we identified management practises that promote both plant performance and a favourable root fungal community and determined the consistent microbiome changes linked to overall quality of the seedlings. These results suggest that microbial feedback loops occur even in highly managed nursery conditions. More broadly, by combining a composite performance index with predictive modelling, we provide a practical way to test complex management combinations and identify microbiome features associated with high-quality planting stock.

Summary: Ectomycorrhizal fungi (EMF) produce mycelia with variable extension and complexity, which can be classified according to soil ‘exploration types’ (ETs). ETs have received attention as one of the few mycorrhizal trait frameworks, but without an empirical classification of ET functional diversity and environmental preferences, understanding and interpreting EMF biogeographic patterns has been difficult. We conducted a synthesis combining: comparative EMF genomics to describe functional divergence in decomposition and nutrient cycling genes across ETs; and EMF trait distribution modeling across continental Europe, pairing soil and root EMF surveys to establish biogeographic ET niche profiles. We demonstrate a signature of ETs encoded in EMF genomes, which is independent from phylogeny and linked to biomass production strategies. EMF ET relative abundances were separated by soil, root, and dominant tree leaf type habitats and exhibited unique correlations with forest biotic (e.g. plant productivity and plant pathogen densities) and abiotic (e.g. nitrogen deposition and soil pH) conditions. These findings support a theory that EMF niche partitioning can be partially explained by extraradical mycelial traits, with underlying variation in ET biogeography likely arising from distinct decomposition and nutrient cycling potentials. We also identify important limitations to this trait framework and provide a guided outlook for future research.

The capacity of nutrient-limited forests to enhance carbon (C) sequestration under elevated CO ₂ (eCO ₂ ) remains a critical uncertainty in C cycle modeling. While existing evidence suggests that low phosphorus (P) bioavailability may constrain CO ₂ fertilization effects on plant growth, the extent to which this limitation modulates ecosystem responses to eCO ₂ in forests adapted to P-deficient soils remains poorly understood. Here, using eight P-enabled models, we simulated the magnitudes and mechanisms through which P bioavailability interacts with eCO ₂ , emulating an ecosystem-scale P enrichment experiment at a P-limited Eucalyptus forest undergoing long-term Free-Air CO ₂ Enrichment. While models predicted pronounced P effects on tree growth, P enrichment unexpectedly did not increase the CO ₂ effects on tree growth and ecosystem C sequestration. Models prioritized either CO ₂ -driven or P-driven growth, but rarely both. This tradeoff emerged due to model-specific assumptions on 1) partitioning of the extra P in soil labile versus nonlabile pools; 2) plant photosynthetic acclimation to P deficiency; 3) C and nutrient use strategies regulating plant size and allocation; and 4) microbial-driven soil decomposition processes. By generating divergent yet biologically plausible outcomes, these predictions establish critical testable hypotheses for empirical research and highlight multiple P-related pathways that may influence the future land C sink.

Recent evidence highlights the importance of low‐abundant subordinate plant species in regulating ecosystem functions in grasslands experiencing drought via plant–microbe interactions. We hypothesized that subordinate and dominant species have distinct carbon (C) allocation and nitrogen (N) uptake patterns affecting soil microbes and their functions during a drought event. We collected soil cores with individuals of Paspalum dilatatum (dominant) or Cynodon dactylon (subordinate) from two independent field drought experiments in mesic Australian grasslands. Cores were subjected to a dual‐pulse labelling with ¹³ CO ₂ and ¹⁵ NH ₄ ¹⁵ NO ₃ . Stable isotopes were traced in plant biomass and the microbial community (PLFA‐SIP, DNA/RNA‐SIP and NanoSIM), and soil nutrient cycling was measured via enzymatic activities. The subordinate species invested more C below‐ground and had higher N uptake in response to drought compared to the dominant, and the active soil microbial community displayed small but consistent differences. The subordinate species showed higher arbuscular mycorrhizae colonization rates but with similar C exchange to the dominant species in response to drought. Synthesis . Our results suggest that the subordinate species achieves higher drought resistance in biomass and soil functions via increased below‐ground functioning. The data presented here provide a basis to explain the underlying mechanisms behind the response of grassland communities and their C cycling to drought.

Summary: Human colonization since the 19 ^th century has resulted in the global spread of pines across the Southern Hemisphere, well beyond their original northern boreal distribution. Such introductions moved not only the pines but also expanded the distribution of their symbiotic partners. Although the introduction of pines is documented through historical records, little is known about the introduction history of their ectomycorrhizal fungi, which are critical symbionts for the survival and invasion of pines. Using Suillus luteus as an example, population genomic analyses of 208 individuals across both native and introduced ranges showed that all introductions originated from Europe, likely mediated by human activities along with pine introductions. With the exception of North America, introduced populations were genetically differentiated from the Europe population, with varying magnitudes of population expansion in different introduced regions, often linked to forestry practices. Genetic variation within the native European population followed isolation by distance, but not in the introduced range, highlighting the disparity in the spatial genetic patterns of native versus exotic habitats. This study provides insight into the population genetics of a globally introduced ectomycorrhizal fungus whose introduction process is likely applicable to other pine-co-introduced ectomycorrhizal fungi.

Summary: Pine‐fungal co‐invasions into native ecosystems are increasingly prevalent across the southern hemisphere. In Australia, invasive pines slowly spread into native eucalypt forests, creating novel mixed forests. We sought to understand how pine‐fungal co‐invasions impact interconnected above‐ and belowground ecosystem characteristics. We sampled beneath mature Pinus radiata and Eucalyptus racemosa in a pine‐invaded eucalypt forest in New South Wales, Australia. We measured microbial community composition via amplicon sequencing of 16S, ITS2, and 18S rDNA regions, microbial metabolic activity via Biolog plate substrate utilization, and soil, leaf litter, and understory plant characteristics. Pines were associated with decreased topsoil moisture, increased pine litter, and decreased eucalypt litter total phosphorus content. Soils and roots beneath pines had distinct microbial community composition and activity relative to eucalypts, including decreased bacterial diversity, decreased microbial utilization of several C‐ and N‐rich substrates, and enrichment of pine‐associated ectomycorrhizae. Introduced suilloid fungi were abundant across both pine and eucalypt soils and roots. Many ecosystem impacts increased with pine size. Invasive pines and their ectomycorrhizae have significant impacts on eucalypt forest properties as they grow. Interconnected impacts at the scale of individual trees should be considered when managing invaded forests and predicting effects of pine invasions.

Plant roots live in constant contact with diverse microbes in the soil. Plant fitness, therefore, relies on signaling pathways that mount an effective immune response against pathogens while fostering mutualistic symbioses. Plant pathways, and specifically immune genes that may act as “switches,” discriminating between pathogenic or mutualistic fungi, remain largely unknown. Using Eucalyptus grandis as a model system, we investigate alterations to the root transcriptomic landscape during pre‐symbiosis with either the pathogen Armillaria luteobubalina or the mutualistic fungus Pisolithus microcarpus. Comparative analyses identified three strongly counter‐regulated genes that may act as immune switches to accommodate or to repress fungal colonization. We characterized two of these, a MYB‐like and RAN‐like zinc finger protein, using a transgenic approach and demonstrated that they have bifunctional roles in the regulation of cell death and a hypersensitive‐like response, depending on the lifestyle of the associated fungus. Using co‐expression network analysis, we identified hypothetical pathways correlated to these genes. We functionally validated these predictions using plants with transgenic roots with increased or decreased transcription of these genes, thereby showing the power of co‐expression networks as an a priori approach to identify key immune response pathways in plants. Overall, our results demonstrate that prior to physical contact with microbes, MYB‐like and RAN‐like zinc finger proteins are key regulators of plant immune signaling that respond to fungal signals and enable or repress symbiotic establishment.

The importance of phosphorus (P) in regulating ecosystem responses to climate change has fostered P-cycle implementation in land surface models, but their CO ₂ effects predictions have not been evaluated against measurements. Here, we perform a data-driven model evaluation where simulations of eight widely used P-enabled models were confronted with observations from a long-term free-air CO ₂ enrichment experiment in a mature, P-limited Eucalyptus forest. We show that most models predicted the correct sign and magnitude of the CO ₂ effect on ecosystem carbon (C) sequestration, but they generally overestimated the effects on plant C uptake and growth. We identify leaf-to-canopy scaling of photosynthesis, plant tissue stoichiometry, plant belowground C allocation, and the subsequent consequences for plant-microbial interaction as key areas in which models of ecosystem C-P interaction can be improved. Together, this data-model intercomparison reveals data-driven insights into the performance and functionality of P-enabled models and adds to the existing evidence that the global CO ₂ -driven carbon sink is overestimated by models.

The capacity for terrestrial ecosystems to sequester additional carbon (C) with rising CO₂ concentrations depends on soil nutrient availability^1,2. Previous evidence suggested that mature forests growing on phosphorus (P)-deprived soils had limited capacity to sequester extra biomass under elevated CO₂ (refs. ^3–6), but uncertainty about ecosystem P cycling and its CO₂ response represents a crucial bottleneck for mechanistic prediction of the land C sink under climate change⁷. Here, by compiling the first comprehensive P budget for a P-limited mature forest exposed to elevated CO₂, we show a high likelihood that P captured by soil microorganisms constrains ecosystem P recycling and availability for plant uptake. Trees used P efficiently, but microbial pre-emption of mineralized soil P seemed to limit the capacity of trees for increased P uptake and assimilation under elevated CO₂ and, therefore, their capacity to sequester extra C. Plant strategies to stimulate microbial P cycling and plant P uptake, such as increasing rhizosphere C release to soil, will probably be necessary for P-limited forests to increase C capture into new biomass. Our results identify the key mechanisms by which P availability limits CO₂ fertilization of tree growth and will guide the development of Earth system models to predict future long-term C storage.