Current Status of Mycorrhizal Research: From Micro to Macro

Martin FM, Öpik M, Dickie IA. (2024). Mycorrhizal research now: from the micro- to the macro-scale. New Phytologist, 242(4): 1399-1403.

(Published on April 24, 2024, full translation as follows)

Mycorrhizal symbiosis is a complex relationship between plants and fungi that significantly impacts the dynamics and functions of ecosystems in terrestrial environments. These symbiotic interactions involve various fungal lineages, including the subphylum Mucoromycotina, subphylum Glomeromycotina, phylum Ascomycota, and phylum Basidiomycota, as well as various plant hosts, which are crucial for nutrient cycling, carbon sequestration, plant growth, and resistance of both partners to environmental stress. Recent advances in molecular biology, genetics, and ecosystem science have enhanced our understanding of mycorrhizal symbiosis and revealed the mechanisms governing these intricate interactions and their ecological impacts.

This special issue of New Phytologist focuses on the theme “Current Status of Mycorrhizal Research: From Micro to Macro,” where we have gathered a series of studies exploring various types of mycorrhizal relationships, such as arbuscular mycorrhiza, orchid mycorrhiza, ericoid mycorrhiza, and ectomycorrhizal relationships. These studies investigate the molecular, physiological, and ecological aspects of mycorrhizal interactions, revealing the complex dialogue between plants and fungi and clarifying their broader ecological implications. By integrating molecular, physiological, and ecological perspectives, this collection aims to unravel the multifaceted interactions between plants and fungi and their cascading effects on terrestrial ecosystems. By distilling the key insights from these diverse studies, our goal is to identify new themes and future directions in mycorrhizal research.

Molecular Insights into Mycorrhizal Symbiosis

Martin and van der Heijden (2024, pp. 1486-1506) review genomic studies that reveal genes associated with nutrient uptake and symbiotic development and discuss the adaptations critical to the evolution of mycorrhizal lifestyles. Their research combines genomics with ecological theory, deepening our understanding of the evolutionary dynamics and functional significance of mycorrhizal symbionts, including how mycorrhizal symbionts offer hope for sustainable agriculture and forestry by enhancing nutrient uptake and stress resistance. Ledford et al. (2024, pp. 1534-1544) provide new insights into the molecular mechanisms governing arbuscular mycorrhizal symbiosis through the elucidation of small RNA-mediated transcriptional regulation. The complex regulatory network of secreted effector proteins and small RNAs coordinates the symbiotic interaction, providing potential targets for manipulating symbiotic efficiency and enhancing plant productivity in agricultural and restoration environments. Giovannetti et al. (2024a) reveal the intricate communication networks between plants and arbuscular mycorrhizal fungi during symbiotic interactions. These findings offer new perspectives on the molecular communication of symbiotic and pathogenic signaling pathways, providing insights into the evolution of mutualistic relationships and the co-evolutionary struggles between plants and their microbial partners (Giovannetti et al., 2024b, see pp. 1404-1407 of this issue).

Nutrient Cycling

One of the core themes of mycorrhizal research is nutrient cycling; mycorrhizae play a vital role in nutrient mineralization and carbon transport in soil profiles (Mahmood et al., 2024, pp. 1545-1560). The use of molecular, isotopic, and ecological methods continually deepens our understanding. The resource exchange between plants and fungal symbionts is crucial for nutrient cycling (Zhao et al., 2024, pp. 1507-1522). Market theories of resource exchange have recently dominated the understanding of mycorrhizal interactions (Dickie et al., 2015). However, Bogar (2024, pp. 1523-1528) suggests a re-examination of market exchange theory, particularly regarding its predictions of short-term outcomes. The study by Corrêa et al. (2024, pp. 1561-1575) also supports this view, suggesting that nutrient exchange is driven by resource surplus, but they found no support for market theory in regulating interactions between arbuscular mycorrhiza and rice. Lekberg et al. (2024, pp. 1576-1588) found that at high phosphorus sites, mycorrhizae supply more nutrients to plants than at low phosphorus sites, which contradicts market theory expectations. Plett et al. (2024, pp. 1589-1602) also discovered that nitrogen transfer from ectomycorrhizal fungi to plants is associated with free amino acids in fungal hyphae, which may align with surplus-driven exchanges, while direct carbon-nitrogen exchanges are not supported.

Understanding resource exchange between plants and fungi in mycorrhizae is a complex challenge requiring community-level studies. Lekberg et al. (2024) argue that using soil inocula from entire communities can explain the discrepancies between their observations and previous experiments with single fungal species controls. Moreover, the nutrient acquisition characteristics of fungi may be habitat-specific, as local ectomycorrhizal fungi have higher nutrient concentrations than cosmopolitan fungi (McPolin et al., 2024, pp. 1603-1613). Plant communities, particularly mycorrhizal strategies, also play a key role in nutrient cycling. The study by Bönisch et al. (2024, pp. 1614-1629) shows that multiple mycorrhizal strategies are a key driver of plant diversity effects. Additionally, Gille et al. (2024, pp. 1630-1644) reveal the intricate interactions between mycorrhizal and non-mycorrhizal plants in terrestrial ecosystems. Non-mycorrhizal plant species, such as sedges, are cosmopolitan and exist in various ecosystems, thus necessitating a deeper understanding of their roles. Zhang et al. (2024, pp. 1645-1660) conducted a study exploring the molecular mechanisms associated with mycorrhizal-assisted iron uptake in plants, finding a trade-off between symbiosis and plant growth. This research provides insights into strategies for enhancing plant nutrition and stress resistance in agricultural and natural ecosystems. Perotto and Balestrini (2024, pp. 1408-1416) studied nutrient transfer mechanisms in arbuscular mycorrhiza and orchid mycorrhiza, identifying conserved traits of symbiotic interactions. By clarifying the structural and functional similarities of various mycorrhizal types, these researchers made significant contributions to establishing a unified framework that aids in understanding the evolutionary trajectories and ecological significance of mycorrhizal symbiosis.

Kakouridis et al. (2024, pp. 1661-1675) explored the fate of mycorrhizal carbon in food webs. They utilized nanoSIMS imaging and isotope ratio mass spectrometry (IRMS) to trace labeled carbon, discovering that carbon is fractionally enriched in soil aggregates and specific bacterial communities derived from arbuscular mycorrhizal fungi. Similarly, L. Wang et al. (2024, pp. 1529-1533) summarized how core mycobiomes influence mycorrhizal nutrient cycling and the functioning of mycorrhizal holobionts.

Community Ecology and Functional Groups

Auer et al. (2024, pp. 1676-1690) elucidated the role of fungal communities in soil function, carbon stabilization, and overall ecosystem resilience, emphasizing the delicate balance within soil microbial communities and its impact on ecosystem function and stability. Pioneering metatranscriptomic work highlights the importance of under-researched soil fungal populations (such as Mucoromycota, especially the genus Mucor) and demonstrates the value of using minimal amplification of fungal transcriptomes to gain insights into interactions between mycorrhizal and saprotrophic fungi in ecosystems. Similarly, Wu et al. (2024, pp. 1417-1425) proposed a conceptual framework outlining four pathways through which arbuscular mycorrhizal fungi influence soil organic matter dynamics. This framework integrates microbial community ecology with biogeochemical cycling, enhancing our understanding of soil carbon sequestration and nutrient cycling mechanisms. This research holds significant implications for ecosystem management and climate change mitigation. D. Wang et al. (2024, pp. 1825-1834) validated the macro-barcoding data used for quantitative assessment of orchid mycorrhizal fungal communities, providing a methodological framework for analyzing the roles of these lesser-known associations, which is crucial for biodiversity conservation and ecosystem restoration.

The feedback between plant and fungal diversity in mixed forests 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, pp. 1691-1703) elucidated how the coexistence of arbuscular mycorrhizal and ectomycorrhizal trees affects soil fungal communities and the coexistence of different mycorrhizal type fungi. As proposed by Voller et al. (2024, pp. 1426-1435), these systems may filter through four mechanisms: partner availability, signal recognition, colonization competition (spatial), and symbiotic function. The dynamics of coexistence among plants of different mycorrhizal types can significantly impact ecosystem functions, including reducing stress resistance in roots and leaves of arbuscular and ectomycorrhizal plants (Xia et al., 2024, pp. 1476-1485). As tested by Monteux et al. (2024, pp. 1835-1846) in an experiment on ectomycorrhizal and arbuscular mycorrhizal plants in northern Sweden, appropriate experimental design is crucial to avoid misinterpretation of plant removal experiment results. Additionally, Mujica et al. (2024, pp. 1436-1440) call for interdisciplinary collaboration, employing a continental-scale approach to reduce geographic biases in the development of plant mycorrhizal trait databases.

Drivers of Global Change

Global change encompasses various factors influencing ecosystems and their dynamics. Hewitt et al. (2024, pp. 1704-1716) studied the effects of climate warming on tundra plant-mycorrhizal interactions, revealing complex responses that impact carbon and nitrogen cycling. Their research elucidates the driving mechanisms of plant-fungal interactions under climate change scenarios, deepening our understanding of ecosystem dynamics in high-latitude regions and providing references for mitigating the impacts of climate change on biodiversity and ecosystem function. Rising carbon dioxide levels are another driver of global change, underscoring the importance of understanding mycorrhizal nutrient cycling. Michaud et al. (2024, pp. 1717-1724) utilized nearly 150 years of herbarium collections to demonstrate that elevated carbon dioxide levels lead to declines in nutrient status across all forest types, regardless of mycorrhizal type and nitrogen deposition. As shown in Jörgensen et al. (2024), nitrogen deposition severely impacts soil fungal communities. Although the biomass of ectomycorrhizal fungi is high in naturally high-nitrogen areas, the study by Jörgensen et al. (2024) indicates that nitrogen deposition leads to a significant decrease in the biomass of ectomycorrhizal fungi. Global climate change can also reshape the relationships between plants and fungi; Hewitt et al. (2024) studied fungi associated with rhododendron shrubs in tundra ecosystems. These studies highlight the need for mycorrhizal researchers to address the regulatory issues of resource exchange as global temperatures and atmospheric carbon dioxide and soil nutrient background levels change rapidly. By integrating biogeography with microbial ecology, their research deepens our understanding of the factors influencing fungal biodiversity patterns and ecosystem function across spatial scales, thereby impacting biodiversity conservation and ecosystem management.

Global change also leads to glacial retreat, opening new lands for ecosystem succession and providing natural model systems for the development of fungal communities during primary succession. Carteron et al. (2024, pp. 1739-1752) explored the development processes of mycorrhizal fungal communities in 46 glacial retreat areas worldwide, finding that both arbuscular mycorrhizal fungi and ectomycorrhizal fungi can rapidly (within ecological time frames) colonize.

(Invasive) Mycorrhizal Fungi Life History Traits

Understanding the impacts of global change on fungal community composition is crucial, as this will drive mycorrhizal symbioses that are critical to ecosystem processes. The increasing frequency of invasive ectomycorrhizal fungi (such as the death cap Amanita phalloides) is concerning due to their persistence. Population genetics and genomics studies by Golan et al. (2024, pp. 1753-1770) found that these invasive fungi are not only opportunistic but can also establish large and persistent genomes underground. This research provides opportunities to elucidate the adaptive strategies employed by invasive fungi to settle in novel habitats and outcompete local species, although their impacts on ecosystem processes remain unclear. McPolin et al. (2024) emphasize the importance of nutrient traits and distribution patterns of endemic mycorrhizal fungi in rainforests, which are critical for maintaining ecosystem function and resilience. Their research highlights the unique contributions of native fungal species to nutrient cycling and plant diversity, offering valuable insights for developing conservation strategies aimed at protecting native biodiversity and ecosystem services in the face of global environmental changes.

The life history of arbuscular mycorrhizal fungi provides further insights. As described by Kokkoris et al. (2024), the model fungus Rhizophagus irregularis produces two different types of spores, with at least four isolates’ spores being consistent with the phenotype of Rhizophagus fasciculatus.

Lofgren et al. (2024, pp. 1448-1475) provide a resource on the genus Suillus, outlining its phylogeny, genetics, genomics, mating systems, partner specificity, environmental preferences, and invasiveness, including a database of isolates with phenotypic and genomic information, along with a series of protocols. This material is highly beneficial for those studying the genus Suillus or other ectomycorrhizal plant fungi systems.

Mycorrhizal Microbiomes

Moreno Jiménez et al. (2024, pp. 1441-1447) adopted a dual approach encompassing molecular mechanisms and microbiome management. This approach utilizes the cooperation between plants and beneficial microbes to provide innovative solutions for enhancing agricultural sustainability and food security in the context of climate change. L. Wang et al. (2024) elucidated the role of core microbiomes in mycorrhizal phosphorus uptake and plant-fungal interactions. This research clarifies the functional significance of microbial symbionts associated with fungal hyphae and delves into the driving mechanisms of nutrient cycling and ecosystem resilience in diversified ecosystems, holding significant implications for microbial ecology and biogeochemistry. This research is crucial for agricultural sustainability, food security, and ecosystem resilience.

Arbuscular mycorrhizal fungal spores contain endobacteria. Based on field-collected spores, the endobacterial communities within individual fungal spores can be diverse, and a large number of different bacteria can be found within spores of the subphylum Glomeromycotina (Lastovetsky et al., 2024, pp. 1785-1797). Clearly, more understanding is needed regarding the natural distribution of endobacterial and hyphal-associated bacteria and their roles in mycorrhizal function and ecosystem nutrient cycling (L. Wang et al., 2024).

Arbuscular Mycorrhizal Fungi in Agricultural Ecosystems and Urban Environments

Peng et al. (2024, pp. 1798-1813) conducted a comparative study of low-input and traditional farming methods, revealing their differing impacts on arbuscular mycorrhizal symbiosis and soil ecosystem functions. In this process, their research unveiled the trade-offs between intensive agricultural practices and symbiotic interactions, providing references for sustainable agriculture and soil management strategies. These findings are significant for enhancing ecosystem resilience and ensuring the long-term sustainability of food systems. By clarifying the factors influencing microbial community dynamics in urban environments, Metzler et al. (2024, pp. 1814-1824) provide strategies to enhance urban ecosystem resilience and sustainability, which are crucial for green infrastructure development and urban planning.

The Future of Mycorrhizal Research: From Micro to Macro Scales

From molecular signaling pathways to ecosystem-scale dynamics, these investigations provide a multifaceted understanding of symbiotic interactions and their broader ecological significance. Considering the integrated insights gained from these diverse studies, several key themes emerge, revealing potential directions for future research and providing guidance for sustainable ecosystem management strategies.

Firstly, the molecular dialogue between plants and fungi represents a rich frontier for exploration. Unraveling the increasingly intricate genetic blueprints of mycorrhizal symbionts and mastering the complex signaling networks governing symbiotic interactions promises to enhance our understanding of mutualistic unions and their adaptive significance. Future research in this area may delve into the genomic and transcriptomic landscapes of symbiotic partners to elucidate the genetic basis of symbiotic development and nutrient exchange dynamics.

Secondly, the ecological consequences of mycorrhizal symbiosis extend far beyond individual interactions and affect ecosystem functions and stability. Combining ecological theory with empirical research can provide insights into the mechanisms of nutrient cycling, carbon fixation, and community dynamics mediated by mycorrhizal fungi. Future research should focus on extending local interactions to ecosystem-level processes, integrating global surveys, landscape-scale analyses, and modeling approaches to predict the impacts of environmental changes on mycorrhizal function and ecosystem services.

Thirdly, the practical applications of mycorrhizal research hold immense potential for sustainable agriculture, ecological restoration, and climate change mitigation. Leveraging the beneficial traits of mycorrhizal fungi, such as nutrient acquisition efficiency and stress resistance, can guide strategies for enhancing crop yield, soil fertility, and ecosystem stability. Future research could explore innovative ways to utilize mycorrhizal symbiosis across diverse contexts, from agricultural ecosystems to urban green spaces, and promote collaboration between scientists, practitioners, and policymakers to translate research findings into viable solutions.

In summary, the integrated insights gained from recent research on mycorrhizal symbiosis highlight the importance of interdisciplinary collaboration and holistic approaches for understanding and harnessing the ecological and agricultural potential of these symbiotic relationships. This diverse range of approaches showcases the dedication of the research community to exploring mycorrhizal symbiosis from multiple perspectives and disciplines. By addressing knowledge gaps, embracing emerging technologies, and fostering interdisciplinary dialogue, future research can pave the way for new frontiers in mycorrhizal ecology, laying the groundwork for sustainable and resilient ecosystems in a rapidly changing world.

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