Integrating perspectives in developing mycorrhizal trait databases: a call for inclusive and collaborative continental efforts.

Global assessments of mycorrhizal symbiosis present large sampling gaps in rich biodiversity regions. Filling these gaps is necessary to build large-scale, unbiased mycorrhizal databases to obtain reliable analyses and prevent misleading generalizations. Underrepresented regions in mycorrhizal research are mainly in Africa, Asia, and South America. Despite the high biodiversity and endemism in these regions, many groups of organisms remain understudied, especially mycorrhizal fungi. In this Viewpoint, we emphasize the importance of inclusive and collaborative continental efforts in integrating perspectives for comprehensive trait database development and propose a conceptual framework that can help build large mycorrhizal databases in underrepresented regions. Based on the four Vs of big data (volume, variety, veracity, and velocity), we identify the main challenges of constructing a large mycorrhizal dataset and propose solutions for each challenge. We share our collaborative methodology, which involves employing open calls and working groups to engage all mycorrhizal researchers in the region to build a South American Mycorrhizal Database. By fostering interdisciplinary collaborations and embracing a continental-scale approach, we can create robust mycorrhizal trait databases that provide valuable insights into the evolution, ecology, and functioning of mycorrhizal associations, reducing the geographical biases that are so common in large-scale ecological studies.

Mycorrhizas in South American Ericaceae.

Mycorrhizal symbioses (mycorrhizas) of Ericaceae, including ericoid mycorrhiza (ErM), have been mainly studied in the Northern Hemisphere, although the highest diversity of ericaceous plants is located in the Southern Hemisphere, where several regions remain largely unexplored. One of them is South America, which harbors a remarkably high diversity of Ericaceae (691 species and 33 genera) in a wide range of environmental conditions, and a specific mycorrhizal type called cavendishioid. In this review, we compile all available information on mycorrhizas of Ericaceae in South America. We report data on the mycorrhizal type and fungal diversity in 17 and 11 ericaceous genera, respectively. We show that South American Ericaceae exhibit a high diversity of habitats and life forms and that some species from typical ErM subfamilies may also host arbuscular mycorrhiza. Also, a possible geographical pattern in South American ErM fungal communities is suggested, with Sebacinales being the dominant mycorrhizal partners of the Andean clade species from tropical mountains, while archetypal ErM fungi are common partners in southern South America species. The gathered information challenges some common assumptions about ErM and suggests that focusing on understudied regions would improve our understanding of the evolution of mycorrhizal associations in this intriguing family.

Juvenile Plant-Microbe Interactions Modulate the Adaptation and Response of Forest Seedlings to Rapid Climate Change.

The negative impacts of climate change on native forest ecosystems have created challenging conditions for the sustainability of natural forest regeneration. These challenges arise primarily from abiotic stresses that affect the early stages of forest tree development. While there is extensive evidence on the diversity of juvenile microbial symbioses in agricultural and fruit crops, there is a notable lack of reports on native forest plants. This review aims to summarize the critical studies conducted on the diversity of juvenile plant-microbe interactions in forest plants and to highlight the main benefits of beneficial microorganisms in overcoming environmental stresses such as drought, high and low temperatures, metal(loid) toxicity, nutrient deficiency, and salinity. The reviewed studies have consistently demonstrated the positive effects of juvenile plant-microbiota interactions and have highlighted the potential beneficial attributes to improve plantlet development. In addition, this review discusses the beneficial attributes of managing juvenile plant-microbiota symbiosis in the context of native forest restoration, including its impact on plant responses to phytopathogens, promotion of nutrient uptake, facilitation of seedling adaptation, resource exchange through shared hyphal networks, stimulation of native soil microbial communities, and modulation of gene and protein expression to enhance adaptation to adverse environmental conditions.

The Waiting Room Hypothesis revisited by orchids: were orchid mycorrhizal fungi recruited among root endophytes?

BACKGROUND: As in most land plants, the roots of orchids (Orchidaceae) associate with soil fungi. Recent studies have highlighted the diversity of the fungal partners involved, mostly within Basidiomycotas. The association with a polyphyletic group of fungi collectively called rhizoctonias (Ceratobasidiaceae, Tulasnellaceae and Serendipitaceae) is the most frequent. Yet, several orchid species target other fungal taxa that differ from rhizoctonias by their phylogenetic position and/or ecological traits related to their nutrition out of the orchid roots (e.g. soil saprobic or ectomycorrhizal fungi). We offer an evolutionary framework for these symbiotic associations. SCOPE: Our view is based on the 'Waiting Room Hypothesis', an evolutionary scenario stating that mycorrhizal fungi of land flora were recruited from ancestors that initially colonized roots as endophytes. Endophytes biotrophically colonize tissues in a diffuse way, contrasting with mycorrhizae by the absence of morphological differentiation and of contribution to the plant's nutrition. The association with rhizoctonias is probably the ancestral symbiosis that persists in most extant orchids, while during orchid evolution numerous secondary transitions occurred to other fungal taxa. We suggest that both the rhizoctonia partners and the secondarily acquired ones are from fungal taxa that have broad endophytic ability, as exemplified in non-orchid roots. We review evidence that endophytism in non-orchid plants is the current ecology of many rhizoctonias, which suggests that their ancestors may have been endophytic in orchid ancestors. This also applies to the non-rhizoctonia fungi that were secondarily recruited by several orchid lineages as mycorrhizal partners. Indeed, from our review of the published literature, they are often detected, probably as endophytes, in extant rhizoctonia-associated orchids. CONCLUSION: The orchid family offers one of the best documented examples of the 'Waiting Room Hypothesis': their mycorrhizal symbioses support the idea that extant mycorrhizal fungi have been recruited among endophytic fungi that colonized orchid ancestors.

The Physiological Effect of a Holoparasite Over a Cactus Along an Environmental Gradient.

Echinopsis chiloensis is an endemic cactus from Chile, distributed in a temperature and rainfall gradient between 30° and 35° South latitude, with mean temperatures increasing and precipitation decreasing toward the north. It is the main host of the mistletoe Tristerix aphyllus, a holoparasite completely dependent on the cactus for water, carbon, and minerals. In this study, we investigated the consequences of parasitism over the fitness and physiology of this cactus throughout its distribution range and how it is affected by the environment. We measured five functional traits in eight populations latitudinally distributed, the first three only for the host: reproductive fitness, stomatal traits (density and size), and photosynthesis (during winter and summer); and the last two for the host and parasite: stable isotopes (∂13C and ∂15N), and nutrients (carbon and nitrogen content). The results showed a negative effect of parasitism over fitness of infected cacti. However, the higher nitrogen concentrations in cactus tissues toward the south improved overall fitness. Regarding photosynthesis, we only observed a negative effect of parasitism during the dry season (summer), which is also negatively affected by the increase in summer temperatures and decrease in winter rainfall toward the north. There were no differences in nutrient concentration or in the isotopic signature of healthy and infected cacti. Conversely, we observed a higher carbon and lower nitrogen concentration in mistletoes than in cacti regardless of latitude. The loss of temperature seasonality toward the north increases the C:N ratio, and the values between the parasite and its host diverge. ∂15N was similar between parasites and hosts while ∂13C of the parasite was enriched when compared to its host. Overall, the infection by T. aphyllus affects Echinopsis chiloensis fitness but showed no strong effects over the cactus physiology, except for the summer photosynthesis. Therefore, our data revealed that E. chiloensis response to T. aphyllus infection is sensitive to environmental changes in a way that could be strongly impacted by the desertification projected for this area due to climate change.

Soil P reduces mycorrhizal colonization while favors fungal pathogens: observational and experimental evidence in Bipinnula (Orchidaceae).

Little is known about the soil factors influencing root-associated fungal communities in Orchidaceae. Limited evidence suggests that soil nutrients may modulate the association with orchid mycorrhizal fungi (OMF), but their influence on non-mycorrhizal fungi remains unexplored. To study how nutrient availability affects mycorrhizal and non-mycorrhizal fungi associated with the orchid Bipinnula fimbriata, we conducted a metagenomic investigation within a large population with variable soil conditions. Additionally, we tested the effect of phosphorus (P) addition on fungal communities and mycorrhizal colonization. Soil P negatively correlated with the abundance of OMF, but not with the abundance of non-mycorrhizal fungi. After fertilization, increments in soil P negatively affected mycorrhizal colonization; however, they had no effect on OMF richness or composition. The abundance and richness of pathotrophs were negatively related to mycorrhizal colonization and then, after fertilization, the decrease in mycorrhizal colonization correlated with an increase in pathogen richness. Our results suggest that OMF are affected by soil conditions differently from non-mycorrhizal fungi. Bipinnula fimbriata responds to fertilization by altering mycorrhizal colonization rather than by switching OMF partners in the short term, and the influence of nutrients on OMF is coupled with indirect effects on the whole fungal community and potentially on plant's health.

Relationship between soil nutrients and mycorrhizal associations of two Bipinnula species (Orchidaceae) from central Chile.

BACKGROUND AND AIMS: Mycorrhizal associations are influenced by abiotic and biotic factors, including climate, soil conditions and the identity of host plants. However, the effect of environmental conditions on orchid mycorrhizal associations remains poorly understood. The present study examined how differences in soil nutrient availability are related to the diversity and composition of mycorrhizal fungi associated with two terrestrial orchid species from central Chile. METHODS: For 12 populations of Bipinnula fimbriata and B. plumosa, OTU (operational taxonomic unit) richness, phylogenetic diversity and community composition of mycorrhizal fungi in root samples were estimated using internal transcribed spacer (ITS) sequences. Then, these mycorrhizal diversity variables were related to soil nutrients and host species using generalized linear models and non-metric multidimensional scaling. KEY RESULTS: Variation in OTU composition of mycorrhizal fungi among sites was explained mainly by orchid host species. Fungi in Tulasnellaceae and Ceratobasidiaceae were isolated from both orchid species, but the former were more frequent in B. fimbriata and the latter in B. plumosa. Soil nutrients and orchid host species had significant effects on OTU richness and phylogenetic diversity. Mycorrhizal diversity decreased in habitats with higher N in both species and increased with P availability only in B. fimbriata CONCLUSIONS: The results suggest that soil nutrient availability modulates orchid mycorrhizal associations and provide support for the hypothesis that specialization is favoured by higher soil nutrient availability. Inter-specific differences in mycorrhizal composition can arise due to a geographical pattern of distribution of orchid mycorrhizal fungi, host preferences for fungal partners or differential performance of mycorrhizal fungi under different nutrient availabilities. Further experiments are needed to evaluate these hypotheses.