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W2900198287 abstract "Scientists working on plant symbioses have known for more than a century that mycorrhizal fungi take central stage in terrestrial ecosystems. Over the last 50 years, several leading scientists have clarified the nature of what is undoubtedly the most common, and the most important, mutualistic symbiosis in terrestrial ecosystems (Bonfante, 2018; in this issue of New Phytologist, pp. 982–995). Simply stated, nearly all families of land plants form root symbiotic organs, termed mycorrhizas, with soil fungi belonging to Glomeromycotina, Ascomycotina or Basidiomycotina. Within days of their emergence in the upper soil profiles, up to 95% of plant short roots are colonized by mycorrhizal fungi. The importance of this symbiosis in controlling plant nutrient status and growth, and its ecological relevance is now well established (van der Heijden et al., 2015). It is said that the relationship between mycorrhizal fungi and plants is a love story – although this metaphor is undoubtedly naive. This intimate association has its origins in an ancient and intricate relationship that allows both partners to thrive (Martin et al., 2017; Field & Pressel, 2018; in this issue of New Phytologist, pp. 996–1011; Pither et al., 2018; pp. 1148–1160; Strullu-Derrien et al., 2018; pp. 1012–1030; Zobel, 2018; pp. 947–949). The long relationship between New Phytologist and the mycorrhizal research community has also been described as a love story, and indeed the title of a 2013 Editorial by Selosse and Martin was ‘Mycorrhizas and New Phytologist: une vraie histoire d'amour’. From a recent Web of Science citation analysis, it is clear that mycorrhizal research still contributes greatly to the success of the journal; the most widely cited and influential article in recent years being the Tansley review by van der Heijden et al. (2015), which discusses the key biological and ecological roles of the different types of mycorrhizal symbioses. This long-standing and tight association is also reflected in the organization of symposia, associated with special issues of the journal, such as the recent 33rd New Phytologist Symposium ‘Networks of power and influence: ecology and evolution of symbioses between plants and mycorrhizal fungi’ (Bender et al., 2014). A particularly exciting aspect with mycorrhiza in the New Phytologist, for an Editor, but also as a reader, is the diversity of approaches covered, ranging from evolution, physiology or genomics, to molecular biology and ecology. The published papers offer the true picture of a very active research community investigating mycorrhizal symbioses in many directions and by many methods and disciplines. This paves the way for papers crossing the disciplinary borders, e.g. viewing genomic or physiological traits as a starting point to analyze evolutionary patterns (e.g. Delaux et al., 2012) or ecologically relevant questions (e.g. Bödeker et al., 2014), and producing elegant, highly-cited works. The present Editorial explores New Phytologist's rich history of publishing the best research on this most fascinating and complex series of interactions, and, happily, this ‘real love story’ continues to play out. Today, with the advent of new concepts and techniques, the possibility of integration across a wide range of disciplines from genomics to molecular ecology and field ecology is becoming a reality that is much encouraged by New Phytologist. Since Selosse and Martin's Editorial was published, further outstanding research in this field has appeared in the pages of the journal, including a special issue titled ‘Ecology and evolution of mycorrhizas’ in 2015 (see Dickie et al., 2015 for an overview), and we are proud to introduce the collection presented here, which includes some of the most recent research in the area. In this Editorial we will highlight some of the recent innovative mycorrhizal research published in the journal and look to future challenges that lie ahead. This theme is continued throughout the Forum of this issue, including Commentaries on selected papers and a series of Letters stimulated by discussions and the ideas exchanged at two conferences held in 2017, both of which the New Phytologist Trust was proud to support: the 9th International Congress on Mycorrhizas (ICOM), in Prague, Czech Republic (Waller et al., 2018), and the 3rd International Molecular Mycorrhiza Meeting (iMMM3; see Plett, 2018) in Toulouse, France. The broad scope and wide range of themes covered in these meetings illustrate how diverse mycorrhizal research is. This diversity is reflected in the Editorial board of New Phytologist, and below we offer some insights and reflections from Editors past and present on the articles presented herein. ‘Eighty percent and 400 million years’ – so starts every graduate student's lab meeting presentations, at least if your lab works on arbuscular mycorrhiza (AM). We encourage all those graduate students (and postdocs and principal investigators) to update their knowledge of the diversity of AM in the context of all mycorrhizas by reading Brundrett & Tedersoo (2018; in this issue of New Phytologist, pp. 1108–1115). These authors review the global diversity of mycorrhizal and nonmycorrhizal plants and present revised estimates of mycorrhizal status based on 135 years of data, summarized in a stunning figure that also illustrates nutritional/habitat specialisations of the 8% of nonmycorrhizal plants. AM is still the most abundant type of mycorrhiza at 71%! The Tansley insight also discusses evolutionary history outlining three waves of mycorrhizal evolution, which illustrates shifts in mycorrhizal status and the fairly frequent occurrence of plant families with multifunctional or dual ectomycorrhizal (ECM)–AM root systems. These dual systems have not yet received much attention at the physiological or molecular levels and with the availability of genomes for all partners (e.g. Populus / Laccaria/Rhizophagus and Eucalyptus/Pisolithus/Rhizophagus associations), these interesting multifunctional mycorrhizal roots are calling out for further investigation. The AM status of the plant hosts is well accepted, but by contrast some aspects of AM fungal biology provoke lively debate, which simply illustrates that our knowledge of their biology is very limited. The Viewpoint by Bruns et al. (2018; in this issue of New Phytologist, pp. 963–967) summarises the thought-provoking presentations and discussions from an ICOM9 workshop on species recognition in the Glomeromycotina. Initially elevated to their own phylum (Glomeromycota) and suggested to be asexual fungi and possibly heterokaryotic, it later became clear from multi-locus analyses that AM fungi classify within the Mucoromycota. Furthermore, the current genome sequences (Tisserant et al., 2013; Ropars et al., 2016; Chen et al., 2018; in this issue of New Phytologist, pp. 1161–1171) (and additional analyses) argue that these AM fungi are homokaryotic and likely sexual, even if it is a mystery as to how sex occurs. Thus, after a slight demotion, AM fungi appear somewhat more traditional than originally thought. Regardless, many aspects of their biology are still a mystery including extensive variation in their ability to promote plant growth, as pointed out in a Letter from Sanders (2018; in this issue of New Phytologist, pp. 968–970). One avenue to growth promotion is almost certainly via phosphate acquisition and transfer to the plant. Recent advances in phosphate metabolism, reviewed by Ezawa & Saito, 2018; in this issue of New Phytologist, pp. 1116–1121), report the identification of five secreted acid phosphatases expressed in the extracellular hyphae of Rhizophagus clarus. This is interesting because they may enable liberation of phosphate from organic sources, for which there is some biochemical evidence, but also some earlier debate (reviewed in Ezawa & Saito, 2018). Variation in genes such as these could potentially underlie variation in plant growth promotion among symbionts. Recent advances in our knowledge of carbon transfer to the AM fungi is among the topics discussed by Lanfranco et al. (2018; in this issue of New Phytologist, pp. 1031–1046; although it should be noted that this comprehensive Tansley review covers much more). With strong evidence that the AM fungi acquire glucose from the plant, it was a surprise when the AM fungal genome and transcriptome sequences predicted that AM fungi were fatty acid auxotrophs. Subsequent studies led to the conclusion that the colonized root cells hugely increase fatty acid biosynthesis and redirect their lipid metabolism to generate an esterified-C16 fatty acid which is subsequently provided to the fungus (references can be found in Lanfranco et al.). Considering that AM fungi are oleaginous, and store and transport lipids throughout their mycelium, their status as fatty acid auxotrophs is a surprise – perhaps they are not so traditional after all. Associations with ECM fungi are widespread on roots of tree species. They evolved from saprotrophic fungi with whom they still share a limited set of enzymes for degradation of organic materials such as cellulose, hemicelluloses, proteins, etc. (Martin et al., 2008, 2010; Kohler et al., 2015). These restricted abilities to decompose soil organic matter have been proposed to be important for their free lifestyle in absence of a host. In this special issue, Zhang et al. (2018; in this issue of New Phytologist, pp. 1309–1321) uncover a new function. They demonstrate that a distinct fungal endoglucanase (glycoside hydrolase family 5 (GH5), LbGH5-CBM1) is required for invasion of Laccaria bicolor into the apoplast of poplar roots, suggesting that LbGH5-CBM1 is an effector mediating fungal–host interaction. Host colonization and formation of the Hartig net were preceded by activities of this mycorrhiza-induced endocellulase, The Hartig net is the key interface for reciprocal nutrient exchange between both organisms. Here, Becquer et al. (2018; in this issue of New Phytologist, pp. 1185–1199) show that a fungal phosphate transporter (HcPT2), located in extramatrical mycelium and the Hartig net, is induced by the plant and its overexpression increases phosphate allocation to the host. When the phosphate transporter was suppressed by RNAi, root colonization was also reduced, suggesting that more beneficial fungal partners are preferred by the host plant. Nehls & Plassard (2018; in this issue of New Phytologist, pp. 1047–1058) provide a comprehensive overview on the functions of ectomycorrhiza for phosphorus (P) and nitrogen (N) nutrition. Under natural conditions, trees are colonized by a multitude of different ECM fungal species, which have distinctly different abilities for N acquisition, especially under drought stress (Pena & Polle, 2014). Here, Köhler et al. (2018; in this issue of New Phytologist, pp. 1200–1210) report that higher ECM fungal species richness supports higher P uptake of the host. They further show that interaction with drought or N decreased species richness of ECM fungi and P uptake of the host plant. Complex mycorrhizal fungal communities may, thus, be advantageous to minimize the risk for nutrient imbalances. Comprehensive ecological studies in drought-prone environments (Castaño et al., 2018; in this issue of New Phytologist, pp. 1211–1221) and after an unusually strong flooding event (Barnes et al., 2018; in this issue of New Phytologist, pp. 1172–1184; see also the Commentary by Johnson, 2018; in this issue of New Phytologist, pp. 950–951) highlight the sensitivity of ECM symbiosis to weather extremes. Climate change may therefore influence the dynamics of mycorrhizal fungal community assembly and thereby, impact biogeochemical cycles. The fire that new methods ignited in fungal ecology (Hibbett et al., 2009) has, undoubtedly, attracted a broad field of researchers to a rather narrow set of similar questions. With this special collection, understanding of the biodiversity of AM fungi gains a range of new insights with an interesting focus on grasslands (in this issue of New Phytologist, Jiang et al., 2018, pp. 1222–1235; Neuenkamp et al., 2018, pp. 1236–1247; Rasmussen et al., 2018, pp. 1248–1261; Van Geel et al., 2018, pp. 1262–1272). Grasslands are globally common habitats and provide important functions for humans as well as being essential parts of landscapes and biosphere. They also host diverse AM fungal communities (Pärtel et al., 2017). In many areas of the world most of the grasslands have experienced and continue to experience human impact, i.e. they are semi-natural habitats. However, such habitats may harbour a substantial part of regional biodiversity and can contribute to human well-being and ecosystem functioning in a non-redundant manner. Neuenkamp et al. (2018, pp. 1236–1247) demonstrate that abandonment of management in Estonian seminatural calcareous grasslands brings about concurrent shifts of both plant and associating AM fungal diversities, with a change in plant community functional composition. Namely, with shrub encroaching and final forest take-over, the proportion of plants, which are less dependent on AM symbiosis (facultatively mycorrhizal plants), increased. Drivers of AM fungal community assembly in grasslands were also explored across 46 sites in six European countries (Van Geel et al., 2018, pp. 1262–1272), across different spatial scales in Åland archipelago of Finland (Rasmussen et al., 2018, pp. 1248–1261) and in Tibetan alpine grasslands in China (Jiang et al., 2018, pp. 1222–1235). These papers are exemplary in the field of fungal community ecology, demonstrating how apparently descriptive data are providing invaluable insights into how nature operates. These papers also illustrate how very similar questions may receive apparently contradictory answers. Here, the main drivers behind AM fungal community patterns were in some cases mostly spatial, in others mostly environmental (edaphic and/or climatic), and in others biotic (host plant or non-AM fungi-related) (Caruso, 2018; in this issue of New Phytologist, pp. 954–956; Hempel, 2018, pp. 952–953). It is clear that there is substantial value in these biodiversity surveys – descriptive observations of community patterns in nature – to identify which mechanisms to explore and test experimentally. Questions around the causality behind correlations in plant–fungi–soil systems are increasingly popular, but driver–passenger relationships in mycorrhizal symbiosis remain elusive (Hempel, 2018, pp. 952–953). Often, however, there is a tendency to put the fungal symbionts in the back seat and focus on the relative importance of plants or soils as drivers. There is still a need to strengthen the ‘mycocentric perspective’ (Fitter et al., 2000), because specificity in fungal–plant interactions (e.g. Lofgren et al., 2018; in this issue of New Phytologist, pp. 1273–1284) work both ways. Although notoriously difficult to support empirically, it seems likely that mycorrhizal fungal community composition is a decisive factor during assembly of plant communities. Causal effects of mycorrhizal fungi, either on the host (Jiang et al., 2018, pp. 1222–1235; Köhler et al., 2018, pp. 1200–1210) or on the soil (Storer et al., 2018; in this issue of New Phytologist, pp. 1285–1295), are often discussed in terms of ‘functionality’ (in this issue of New Phytogist, Hazard & Johnson, 2018, pp. 1122–1128; Lekberg & Helgason, 2018, pp. 957–962; Powell & Rillig, 2018, pp. 1059–1075). Powell & Rillig (2018, pp. 1059–1075) provide a comprehensive review on AM fungal (functional) diversity, and in particular, indicate research directions, questions, experiments and approaches to reach understanding on how AM fungal diversity is related to ecosystem function. They propose to consider biological stoichiometry as a conceptual framework for designing further studies disentangling diversity–function relationships. Along the same lines, Lekberg & Helgason (2018, pp. 957–962) discuss approaches to study mycorrhizal functioning in the actual field conditions, rather than in the controlled environment, and how to consider multiple mycorrhizal types simultaneously (Lekberg et al., 2018, pp. 971–976). The study by Jiang et al. (2018, pp. 1222–1235) provides a good example by manipulating AM fungal communities in the field and testing the response of fungi to nutrient addition. However, it is important to consider that ‘functional’ interactions between mycorrhizal fungi, plants and soils in most cases will turn out to be bi-directional. Systems with bi-directional dependencies are characterized by strong feedbacks, implying that mycorrhizal interactions may act to stabilize ecosystems, if negative feedbacks prevail, or to destabilize ecosystems and propel directional changes, if positive feed-backs are common (e.g. Corrales et al., 2018; in this issue of New Phytologist, pp. 1076-1091). The increasing realization of the importance of plant–soil feedbacks in ecosystem dynamics puts mycorrhizal symbiosis in focus of the much wider research community interested in global change and land use. Of course, the relationship between mycorrhizal symbiosis and global change is also bidirectional (Barnes et al., 2018; in this issue of New Phytologist, pp. 1172–1184; Castaño et al., 2018, pp. 1211-1221; Köhler et al., 2018, pp. 1200–1210) with obvious risk scenarios of accelerating global change, but also possibilities for mitigation by well-informed land-use management. A cross-cutting theme joining several areas of mycorrhizal research included in this special collection, is the question of what is a species, and how to delimit and recognise (identify) species to enable best research on genomics, physiology or any other field requiring that the targeted organisms are consistently named (Bruns et al., 2018, pp. 963–967; Mathieu et al., 2018, pp. 1129–1134; Sanders, 2018, pp. 968–970). The issue of optimal selection of approaches for detection (and identification) of fungi and mycorrhizal fungi in natural samples is further tackled by Lekberg et al. (2018, pp. 971–976). An area where consistent and easy-to-communicate naming is required is the application of AM fungi. Ryan & Graham (2018; in this issue of New Phytologist, pp. 1092–1107) provoke the research community to take a fresh look on what is known about functional roles of AM fungi in agroecosystems and what would the crop growers need from scientists to be able to harness the potential of soil biodiversity for more environment-friendly and sustainable crop production, but also for minimizing destruction of natural habitats. Certainly, this subject continues to receive attention from scientists, farmers, inoculum and biofertiliser producers as well as policy makers. Rivero et al. (2018; in this issue of New Phytologist, pp. 1322–1336) examine plant metabolic plasticity in stressed tomato plants, and note that AM symbioses can help plants deal with this stress, and the Tansley insight by Sawers et al. (2018; in this issue of New Phytologist, pp. 1135–1140) examines AM symbiosis in light of domestication and crop improvement in cereals. A formidable challenge faced by our community is to identify the functions played by the assemblages of mycorrhizal fungi in situ. As a prerequisite of such large-scale functional ecology studies, we now need to accelerate the discovery of factors (e.g. gene networks) controlling the development and functioning of the various types of mycorrhizal symbioses. The fitness of the mycorrhizal symbioses is thought to be caused by interaction of hundreds of symbiosis-related genes and symbiont environment. By characterizing and manipulating patterns of gene expression, we should be able to identify the genetic hubs regulating the mycorrhizal fungal response to changing host physiology, and better understand how these interactions control ecosystem function. Critical in this endeavor will be the use of genomic information on the recently sequenced mycorrhizal fungi (Kohler et al., 2015; Martino et al., 2018; Chen et al., 2018, pp. 1161–1171; see also Perotto et al., 2018, pp. 1141–1147). The completion or impending completion of 100+ genome sequences of mycorrhizal fungi (see the Mycorrhizal Fungi page at the MycoCosm database, https://genome.jgi.doe.gov/Mycorrhizal_fungi/Mycorrhizal_fungi.info.html) provides an unprecedented opportunity to identify the key components of interspecific and organism–environment interactions (Martin et al., 2017). There is no doubt that large-scale genome sequencing of mycorrhizal fungi, endophytes and related soil saprotrophs will be fertile ground for novel hypotheses about how mycorrhizal symbioses evolved in the different plant families and drive present ecosystems (van der Heijden et al., 2015; Brundrett & Tedersoo, 2018, pp. 1108–1115). The scientific rewards from comprehensive research programs on mycorrhizal symbioses include a greater fundamental understanding of the interactions between organisms at the community level and benefits for sustainable agriculture and forestry. A deeper understanding of the complex array of factors affecting host–fungus interactions and co-evolution could indeed ensure efficient selection of fungal symbionts for large-scale inoculation methods in forest and agricultural ecosystems, although all scientists are not so optimistic (Ryan & Graham, 2018, pp. 1092–1107). This will require a tighter collaboration with agronomists and foresters. Through the application of the advanced omics approaches at several levels – genomics, transcriptomics, proteomics and metabolomics – remarkable progress has been made in understanding the mechanisms that control the development and functioning of mycorrhizal symbioses. However, most of these studies have been carried out in simple experimental settings, such as growth chambers. Understanding how these mutualistic associations adapt and respond to changes in the biological, chemical and physical properties of agro- and natural ecosystems therefore remains a significant challenge for plant and microbial biologists. Combined community structure and function studies applying both molecular ecology and in situ transcriptomics and proteomics may, in the future, significantly promote our understanding of the interactions between mycorrhizal fungal species with their hosts and with their biotic and abiotic environment. Future research on mycorrhizal symbioses would thus greatly benefit from a comprehensive approach bridging genetics, molecular biology, physiology, field ecology and agronomy. Unfortunately, the community of scientists working on mycorrhizas is partly fragmented with molecular biologists attending iMMM conferences and field ecologists gathering mainly at ICOMs. Recently, Ferlian et al. (2018) pointed out that ‘this historic partitioning [iMMM / ICOM] into separate fields sometimes hinders a comprehensive understanding of how mycorrhizae function’. In the future, we should explore ways to re-unify our community to better integrate the molecular knowledge with field ecology and provide opportunities to early career researchers to embrace all the facets of the complex mycorrhizal associations. The lack of a unified research community may lead to a lack of encouragement for students to enter into this world. As a more optimistic note, readers in this special collection can also find two Profiles that highlight individuals who have made an enormous impact on the field of mycorrhizal research. Prof. Alastair Fitter (pp. 977-978) was a long-standing Editor of New Phytologist; and served on the board of the New Phytologist Trust. The second Profile features Prof. Paola Bonfante (pp. 979-981), again, another leader in the field with long-standing connections to the journal, Paola currently serves as a member of our Advisory Board. She also contributes to the collection via two articles (Bonfante, 2018, pp. 982–995; Chialva et al., 2018, pp. 1296–1308), including a Tansley review which once again mines the fascinating history of mycorrhizal research. Despite this look to the past this review, and the collection as a whole, has a focus firmly on the future. The Royal Botanic Gardens, Kew recently released a report titled State of the World's Fungi (Willis, 2018). This report is the first to summarize the current status of this immensely important group of organisms, and needless to say the mycorrhizal symbiosis is given great prominence. State of the World's Fungi highlights the importance of Fungi to life on Earth, and how it must be conserved and protected; our aim for this collection is to also highlight this importance, and to showcase the outstanding research that is contributing to our understanding of these important plant–fungal interactions. We would like to thank the organizers of ICOM9 and iMMM3 for their outstanding service to the community. The research in FMM's lab is funded through the Laboratory of Excellence Advanced Research on the Biology of Tree and Forest Ecosystems (ANR-11-LABX 0002 01). MÖ is supported by the Estonian Research Council (IUT20-28), the European Regional Development Fund (Centre of Excellence EcolChange) and ERA-NET Cofund BiodivERsA3 (SoilMan). We would also like to thank Ian A. Dickie for his contribution to the editorial process." @default.
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W2900198287 title "Cross-scale integration of mycorrhizal function" @default.
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