Mycorrhizal research now: from the micro‐ to the macro‐scale

Abstract

Mycorrhizal symbioses are complex relationships between plants and fungi that significantly affect ecosystem dynamics and functions across terrestrial environments. These symbiotic interactions, which involve a diverse range of fungal lineages, including Mucoromycotina, Glomeromycotina, Ascomycota, and Basidiomycota, as well as various plant hosts, are critical for nutrient cycling, carbon sequestration, plant growth, and resilience of both partners to environmental stressors. Recent advances in molecular biology, genetics, and ecosystem sciences have enhanced our understanding of mycorrhizal symbioses and illuminated the mechanisms that govern these intricate interactions and their ecological implications. In this New Phytologist Special Issue on ‘Mycorrhizal research now: from the micro- to the macro-scale’, we bring together a collection of studies, which examine various types of mycorrhizal symbioses, such as arbuscular mycorrhizal, orchid mycorrhizal, ericoid mycorrhizal, and ectomycorrhizal associations. These studies explored the molecular, physiological, and ecological dimensions of mycorrhizal interactions, uncovering the complex conversations between plants and fungi and illuminating their broader ecological implications. By integrating molecular, physiological, and ecological perspectives, this collection endeavors to untangle the multifaceted interactions between plants and fungi and their cascading effects on terrestrial ecosystems. Through distilling the key insights from these diverse studies, our goal is to identify emerging themes and future directions for mycorrhizal research. Martin & van der Heijden (2024, in this issue pp. 1486–1506) review genomic studies that revealed genes involved in nutrient uptake and symbiosis development, and discuss adaptations that are fundamental to the evolution of mycorrhizal lifestyles. Their work integrated genomics with ecological theory, thereby enhancing our understanding of the evolutionary dynamics and functional significance of mycorrhizal symbioses, including how mycorrhizal symbioses hold promise for sustainable agriculture and forestry by enhancing nutrient acquisition and stress tolerance. The elucidation of small RNA-mediated transcriptional regulation by Ledford et al. (2024, in this issue pp. 1534–1544) offers novel insights into the molecular mechanisms governing arbuscular mycorrhizal symbiosis. The intricate regulatory networks of secreted effector proteins and small RNAs orchestrate symbiotic interactions, thereby providing potential targets for manipulating symbiotic efficiency and enhancing plant productivity in the agricultural and restoration contexts. Research conducted by Giovannetti et al. (2024a) sheds light on the intricate communication networks that exist between plants and arbuscular mycorrhizal fungi during their symbiotic interactions. These findings provide new insights into the molecular communication underlying both symbiotic and pathogenic signaling pathways, offering new perspectives on the evolution of mutualistic relationships and the coevolutionary struggle between plants and their microbial partners (Giovannetti et al., 2024b, in this issue pp. 1404–1407). One of the central themes of mycorrhizal research is nutrient cycling; mycorrhizas play a significant role in mineralizing nutrients and transporting carbon across the soil profile (Mahmood et al., 2024, in this issue pp. 1545–1560). The use of molecular, isotopic, and ecological approaches has continued to advance our understanding. Resource exchange between plants and fungal symbionts is crucial for nutrient cycling (Zhao et al., 2024, in this issue pp. 1507–1522). Market theories of resource exchange have recently dominated the understanding of mycorrhizal interactions (Dickie et al., 2015). However, Bogar (2024, in this issue pp. 1523–1528) suggests that market exchange theories should be re-examined, particularly in predicting short-term outcomes. This is supported by the study by Corrêa et al. (2024, in this issue pp. 1561–1575), who did not find support for market theories in regulating arbuscular mycorrhizal interactions with rice plants, suggesting that nutrient exchange is driven by a surplus of resources. Lekberg et al. (2024, in this issue pp. 1576–1588) found that mycorrhizal nutrient supply to plants is higher at high P sites than at low P sites, contrary to expectations under market theory. Plett et al. (2024, in this issue pp. 1589–1602) also found that nitrogen transfer from ectomycorrhizal fungi to plants is correlated with free amino acids in fungal hyphae, which may be consistent with a surplus of resources driving exchange, while direct C for N exchange was not supported. Understanding the exchange of resources between plants and fungi in mycorrhizas is a complex challenge that requires examination of community characteristics. Lekberg et al. (2024) argue that the use of a whole-community soil inoculum can explain differences in their observations compared with previous, more controlled, single-fungus experiments. Additionally, the nutrient acquisition traits of fungi may be habitat-specific, as suggested by the higher nutrient concentrations in endemic ectomycorrhizal fungi than in cosmopolitan species (McPolin et al., 2024, in this issue pp. 1603–1613). Plant communities, particularly in terms of mycorrhizal strategies, also play key roles in nutrient cycling. Bönisch et al. (2024, in this issue pp. 1614–1629) show that having multiple mycorrhizal strategies is a key driver of plant diversity effects. Further, Gille et al. (2024, in this issue pp. 1630–1644) shed light on the intricate interplay between symbiotic and nonsymbiotic plants in terrestrial ecosystems. Nonmycorrhizal plant species, such as Cyperaceae, are cosmopolitan and found in various ecosystems, calling for a deeper understanding of their role. Zhang et al. (2024, in this issue pp. 1645–1660) conducted a study to examine the molecular mechanisms associated with mycorrhiza-assisted iron processing in plants and discovered that there are trade-offs between symbiosis and plant growth. This research provides insights into strategies for enhancing plant nutrition and stress tolerance in agricultural and natural ecosystems. Perotto & Balestrini (2024, in this issue pp. 1408–1416) examined the mechanisms of nutrient transfer in arbuscular mycorrhizal and orchid mycorrhizal associations, which led to the identification of conserved traits that underlie symbiotic interactions. Through their elucidation of the structural and functional similarities between various mycorrhizal types, these researchers have made significant contributions to the development of a unified framework that aids in understanding the evolutionary trajectories and ecological significance of mycorrhizal symbioses. The fate of mycorrhizal carbon in the food web was explored by Kakouridis et al. (2024, in this issue pp. 1661–1675). They utilized nanoSIMS imaging and isotope ratio mass spectrometry (IRMS) to track labeled C and found that fractionation of C on soil aggregates and specific groups of bacteria were enriched with AM fungi-originating C. Along the same lines, L. Wang et al. (2024, in this issue pp. 1529–1533) summarized how the mycorrhizal core microbiome matters for mycorrhizal nutrient cycling and operation of the mycorrhizal holobiont. Auer et al.'s (2024, in this issue pp. 1676–1690) study elucidated the role of fungal guilds in soil functioning, carbon stabilization, and overall ecosystem resilience, highlighting the delicate balance within soil microbial communities and their implications for ecosystem functioning and stability. Groundbreaking meta-transcriptomic work emphasizes the significance of less-studied groups of soil fungi, such as Mucoromycota and specifically Mortierella, and demonstrates the value of using minimal amplification of fungal transcriptomes to gain a deeper understanding of the interactions between mycorrhizal and saprotrophic fungi in ecosystems. Along the same lines, Wu et al. (2024, in this issue pp. 1417–1425) proposed a conceptual framework that elucidates four pathways through which arbuscular mycorrhizal fungi influence soil organic matter dynamics. This framework integrates microbial community ecology with biogeochemical cycling to enhance our understanding of the mechanisms that drive soil carbon sequestration and nutrient cycling. The implications of this study for ecosystem management and climate change mitigation are significant. D. Wang et al.'s (2024, in this issue pp. 1825–1834) validation of metabarcoding data for quantitative assessments of orchid mycorrhizal fungal communities provides a methodological framework for analyzing the role of these poorly known associations, with implications for biodiversity conservation and ecosystem restoration. Feedback between plant and fungal diversity in mixed forest stands of different mycorrhizal types is an important topic for better understanding biodiversity patterns, ecosystem management, and biodiversity conservation. In a subtropical forest experimental system, Singavarapu et al. (2024, in this issue pp. 1691–1703) clarified how coexistence of arbuscular mycorrhizal and ectomycorrhizal trees shapes soil fungal communities and coexistence of fungi of different mycorrhizal types. Such systems are excellent for clarifying the gradients of host specificity of both arbuscular and ectomycorrhizal fungi, which, as proposed by Voller et al. (2024, in this issue pp. 1426–1435), might operate via four mechanistic filters: partner availability, signaling recognition, competition for colonization (space), and symbiotic function. The dynamics of coexisting plants of different mycorrhizal types can have important implications for ecosystem function, including the reduced recalcitrance of roots and leaves of both arbuscular and ectomycorrhizal plants (Xia et al., 2024, in this issue pp. 1476–1485). An appropriate experimental design is critical to avoid misinterpretation of results in plant removal experiments, as tested by Monteux et al. (2024, in this issue pp. 1835–1846) in an experiment with ecto- and ericoid mycorrhizal plants in Northern Sweden. Furthermore, Mujica et al. (2024, in this issue pp. 1436–1440) call for interdisciplinary collaborations with a continental-scale approach to mitigate geographical biases in the development of plant mycorrhizal trait databases. Global change includes various factors that affect ecosystems and their dynamics. Hewitt et al. (2024, in this issue pp. 1704–1716) investigated the effects of warming on tundra plant–mycorrhizal interactions, revealing complex responses with implications for carbon and nitrogen cycling. Their research elucidated the mechanisms driving plant–fungal interactions under climate change scenarios, enhancing our understanding of ecosystem dynamics in high-latitude regions and informing strategies for mitigating the impacts of climate change on biodiversity and ecosystem function. Elevated CO2 levels, another driver of global change, emphasize the importance of understanding mycorrhizal nutrient cycling. Using nearly 150 yr of herbarium collections, Michaud et al. (2024, in this issue pp. 1717–1724) demonstrated that increasing CO2 levels contribute to the declining nutrient status of all forests, regardless of mycorrhizal type and N deposition. Nitrogen deposition can significantly affect soil fungal communities, as suggested by a study by Jörgensen et al. (2024, in this issue pp. 1725–1738) on ectomycorrhizal fungi. Although ectomycorrhizal fungal biomass is high in natural high-N sites, Jörgensen et al. (2024) showed that N deposition causes a substantial decline in the ectomycorrhizal fungal biomass. Global climate change also restructures plant–fungal relationships, as demonstrated by Hewitt et al. (2024) for fungi associated with ericoid shrubs in tundra ecosystems. These studies underscore the need for mycorrhizal researchers to resolve the regulation of resource exchange as global temperatures and background levels of atmospheric CO2 and soil nutrients rapidly change. By integrating biogeography with microbial ecology, their research enhances our understanding of the factors shaping fungal biodiversity patterns and ecosystem functions across spatial scales, with implications for biodiversity conservation and ecosystem management. Global change also causes glacier retreat, opening new lands for ecosystem succession and providing natural model systems for fungal community development during primary succession. Carteron et al. (2024, in this issue pp. 1739–1752) explored how mycorrhizal fungal communities develop in 46 glacier retreats around the globe, finding fast (in ecological time) colonization by both arbuscular and ectomycorrhizal fungi. It is essential to understand the impact of global change on the community composition of fungi, as this drives mycorrhizal symbioses that are critical for ecosystem processes. Invasive ectomycorrhizal fungi, such as Amanita phalloides, are increasing in frequency, and their persistence is a cause for concern. Population genetics and genomics research by Golan et al. (2024, in this issue pp. 1753–1770) revealed that these invasive fungi are not just opportunistic but can establish large and persistent genets belowground. This study provides an opportunity to elucidate the adaptive strategies employed by invasive fungi to colonize new habitats and outcompete native species, although implications for ecosystem processes remain unclear. A study conducted by McPolin et al. (2024) emphasized the significance of nutrient traits and distribution patterns among endemic mycorrhizal fungi in rainforests, which are crucial for maintaining ecosystem function and resilience. Their research highlights the distinct contributions of indigenous fungal species to nutrient cycling and plant diversity, providing valuable insights into the development of conservation strategies aimed at preserving indigenous biodiversity and ecosystem services in the face of global environmental changes. The life history of arbuscular mycorrhizal fungi provides further insights. Sporulation of the model fungus Rhizophagus irregularis yields spores of two different morphologies, including those matching the phenotypes of Rhizophagus fasciculatus in the case of at least four isolates, as described by Kokkoris et al. (2024). Lofgren et al. (2024, in this issue pp. 1448–1475) provide a community resource on Suillus, with an overview of its phylogeny, genetics and genomics, mating systems and partner specificity, environmental preferences and invasion, including a SuilluScope database of isolates with the phenotypic and genome information, and a range of protocols. This resource is of massive help to anyone working with Suillus or other ectomycorrhizal plant–fungus systems. Moreno Jiménez et al. (2024, in this issue pp. 1441–1447) employed a dual method that encompasses molecular mechanisms and microbiome management. The approach capitalizes on collaborative efforts between plants and beneficial microorganisms to provide innovative solutions for improving agricultural sustainability and food security amidst climate change. The findings of L. Wang et al. (2024) shed light on the role of the core microbiome in mycorrhizal phosphorus uptake and plant–fungal interactions. This study elucidates the functional significance of microbial consortia associated with fungal hyphae and provides insights into the mechanisms driving nutrient cycling and ecosystem resilience in diverse ecosystems, which have implications for microbial ecology and biogeochemistry. This study has important implications for agricultural sustainability, food security, and ecosystem resilience. Spores of arbuscular mycorrhizal fungi harbor endobacteria. Based on field-collected spores, it appears that endobacterial communities inside individual fungal spores can be diverse, and a remarkable number of different bacteria can be found within Glomeromycotina spores (Lastovetsky et al., 2024, in this issue pp. 1785–1797). Clearly, it is necessary to learn more about the natural distribution of bacterial endosymbionts and hyphae-associating bacteria and to determine their role in mycorrhizal functioning and nutrient cycling in ecosystems (L. Wang et al., 2024). Peng et al.'s (2024, in this issue pp. 1798–1813) comparative examination of low-input and conventional farming methods illuminates their varying effects on arbuscular mycorrhizal symbiosis and soil ecosystem functions. In doing so, their research revealed the trade-offs between intensive agricultural practices and symbiotic interactions, which can inform strategies for sustainable agriculture and soil management. These findings have significant implications for enhancing ecosystem resilience and ensuring long-term sustainability of the food system. By elucidating the factors influencing microbial community dynamics in urban environments, Metzler et al. (2024, in this issue pp. 1814–1824) provided strategies for enhancing urban ecosystem resilience and sustainability, with implications for green infrastructure development and urban planning. Ranging from molecular signaling pathways to ecosystem-scale dynamics, these investigations offer a multifaceted understanding of the mechanisms underlying symbiotic interactions and their broader ecological implications. Considering the composite insights gained from these diverse studies, several key themes have surfaced, shedding light on potential avenues for future research and informing sustainable ecosystem management strategies. First, molecular dialogues between plants and fungi represent a rich frontier for exploration. Unraveling the genomic blueprints of an increasing number of mycorrhizal symbionts and the intricate signaling networks that govern symbiotic interactions holds promise for enhancing our understanding of mutualistic associations and their adaptive significance. Future research in this area may delve deeper into the genomic and transcriptomic landscapes of symbiotic partners, to elucidate the genetic basis of symbiotic development and nutrient exchange dynamics. Second, the ecological consequences of mycorrhizal symbioses extend far beyond individual interactions and influence ecosystem functioning and resilience. Integrating ecological theory with empirical studies can provide insights into the mechanisms that drive nutrient cycling, carbon sequestration, and community dynamics mediated by mycorrhizal fungi. Future research should focus on scaling up local interactions to ecosystem-level processes, incorporating global surveys, landscape-scale analyses, and modeling approaches to predict the impacts of environmental change on mycorrhizal functioning and ecosystem services. Third, the practical applications of mycorrhizal research hold immense potential for sustainable agriculture, ecosystem restoration, and climate change mitigation. Harnessing the beneficial traits of mycorrhizal fungi, such as nutrient acquisition efficiency and stress tolerance, can inform strategies to enhance crop productivity, soil fertility, and ecosystem resilience. Future research may explore innovative approaches for harnessing mycorrhizal symbioses in diverse contexts, from agroecosystems to urban green spaces, and fostering collaboration between scientists, practitioners, and policymakers to translate research findings into actionable solutions. In conclusion, the collective insights derived from recent studies on mycorrhizal symbioses underscore the importance of interdisciplinary collaboration and holistic approaches for understanding and harnessing the ecological and agricultural potential of these symbiotic associations. This diverse range of approaches demonstrates the dedication of the research community to exploring mycorrhizal symbioses from multiple perspectives and disciplines. By addressing knowledge gaps, embracing emerging technologies, and fostering cross-disciplinary dialogue, future research can unlock new frontiers in mycorrhizal ecology, paving the way for sustainable and resilient ecosystems in a rapidly changing world. FMM's research was supported by the Agence Nationale de la Recherche (Laboratoire d'Excellence ARBRE (ANR-11-LABX-0002-01)) and the Huazhong Agricultural University, Wuhan, China. IAD's research supported by BioProtection Aotearoa. MÖ was supported by the Estonian Research Council grant no. 1789 (project FUNFARM). We would like to thank Dr Holly Slater for her support in assembling this Special Issue. Editorial Office Note: We apologize to readers that Giovannetti et al. (2024a) is not included in this issue of the journal. This was due to an Editorial Office oversight.

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