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Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis

Abstract

A comprehensive appraisal of the mycorrhizal literature provides data for 336 plant families representing 99% of flowering plants, with regard to mycorrhizas and other nutritional adaptations. In total, arbuscular (AM), orchid, ectomycorrhizas (EM) and ericoid mycorrhizas and nonmycorrhizal (NM) roots occur in 74%, 9%, 2%, 1% and 6% of Angiosperm species respectively. Many families of NM plants have alternative nutritional strategies such as parasitism, carnivory, or cluster roots. The remaining angiosperms (8%) belong to families reported to have both AM and NM species. These are designated as NM-AM families here and tend to occur in habitats considered non-conducive to mycorrhizal fungi, such as epiphytic, aquatic, extremely cold, dry, disturbed, or saline habitats. Estimated numbers of species in each category of mycorrhizas is presented with lists of NM and EM families. Evolutionary trends are also summarised by providing data on all clades and orders of flowering and non-flowering vascular plants on a global scale. A case study of Western Australian plants revealed that plants with specialised nutritional modes such as carnivory, cluster roots, or EM were much more diverse in this ancient landscape with infertile soils than elsewhere. Detailed information on the mycorrhizal diversity of plants presented here is linked to a website (mycorrhizas.info) to allow data to remain current. Over a century of research effort has resulted in data on mycorrhizal associations of >10,000 plant species that are of great value, but also somewhat of a liability due to conflicting information about some families and genera. It is likely that these conflicts result in part from misdiagnosis of mycorrhizal associations resulting from a lack of standardisation in criteria used to define them. Families that contain both NM and AM species provide a second major source of inconsistency, but even when these are excluded there is a ∼10% apparent error rate in published lists of mycorrhizal plants. Arbuscules are linked to AM misdiagnosis since they are used less often than vesicles to recognise AM associations in roots and apparently occur sporadically in NM plants. Key issues with the diagnosis of mycorrhizal plants are discussed using the Cyperaceae as a case study. Detailed protocols designed to consistently distinguish AM from endophytic Glomeromycotan Fungus Colonisation (GFC) are provided. This review aims to stimulate debate and provide advice to researchers delving into root biology.

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Abbreviations

AM:

arbuscular mycorrhizas (vesicular-arbuscular mycorrhizas VAM)

NM:

nonmycorrhizal plants

EM:

ectomycorrhizas (ECM)

NM-AM:

plants with variable AM or NM roots

GFC:

endophytic or unspecified colonisation by Glomeromycotan Fungi

RLC:

root length colonised

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Acknowledgements

I would especially like to thank my wife Karen Clarke for her endless patience while this review was compiled. This review would not have been possible without the support of Lotterywest and the School of Plant Biology at The University of Western Australia. I am also very grateful to Hans Lambers for suggesting this data be made available and providing detailed comments.

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Correspondence to Mark C. Brundrett.

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Responsible Editor: Yongguan Zhu.

Appendices

Appendix 1

List of relevant tables and other data with direct links

Information Link
Ectomycorrhizal families and genera http://mycorrhizas.info/ecm.html#hosts/
Nonmycorrhizal families http://mycorrhizas.info/nmplants.html/
Mycorrhizas of primitive plants http://mycorrhizas.info/evol.html/
Methods for identifying mycorrhizas http://mycorrhizas.info/method.html/
Ectomycorrhizal fungi http://mycorrhizas.info/ecmf.html#list/
Arbuscular mycorrhizal fungi (Arthur Schüßler's site) http://www.lrz-muenchen.de/×schuessler/amphylo/

Appendix 2

Practical advice for the diagnosis of mycorrhizal associations

Processes required to obtain, process and evaluate samples for accurate mycorrhizal diagnosis are listed in Table 5. It is advisable to use several criteria to identify mycorrhizal associations, especially when roots are of unknown age (field collected). The first criteria (presence of a mycorrhizal interface) should always be used, as it provides the most reliable evidence, but should not be the only evidence required for diagnosis. Consistency of colonisation is another key criteria. If interface hyphae (arbuscules, Hartig net, or coils) were not observed in roots, reliable identification mycorrhizas may not be possible and it should be stated that further sampling is required for that species. It is important to clearly state which criteria were used in diagnosis in published reports. Lists of mycorrhizal species should be organised into plant families to allow comparison with other studies.

Table 5 Stages in the process of accurately identifying mycorrhizal associations

A protocol for diagnosis of AM or NM roots is presented in Fig. 16. Many mycorrhizal studies are already at least partially compliant with these requirements if they include data that allows multiple evidence of diagnosis (e.g. arbuscules, vesicles and colonisation levels). It is most difficult to distinguish functional AM from endophytic root colonisation, especially in extreme habitats where mycorrhizal activity may be suppressed. These habitats usually require more samples or sampling times to determine if plants are mycorrhizal. In some cases it will not be possible to conclusively state if samples are mycorrhizal or not—in which case sparse associations are likely to be of minor importance.

Fig. 16
figure 16

Flowchart presenting recommended protocol for diagnosis of AM or NM roots

Diagnosis becomes easier with experience. It is unrealistic to expect accurate diagnosis without experience or guidance from an experience mycorrhizologists. Accuracy in mycorrhizal diagnosis is linked to the following factors:

  • Experience and training.

  • Sampling intensity.

  • Use of standard diagnosis criteria.

  • Adequate samples with sufficient replication that include young roots.

  • Higher sampling intensity in habitats where NM-AM plants are common.

  • Minimising cross contamination of roots by different plant species, but acknowledging it may still occur, especially with fine-rooted species.

  • Acknowledging when diagnosis cannot be resolved by GFC designation. It is better to err on the side of caution rather than publish an incorrect diagnosis.

Table 6 lists categories of data that should be used to diagnose AM associations. It is best to list all data and protocols used for diagnosis in publications. Protocols used to diagnose AM should be fully explained in the methods section. Detailed information can be presented as supplemental data if not included in the main document. Arbuscule density information is especially important if plants belong to families suspected to have NM-AM roots, have NM roots with some GFC, or are from habitats where NM plants tend to occur. However, in many cases a statement that plants designated as AM contained typical associations with many arbuscules in their roots will be sufficient to confirm diagnosis.

Table 6 Mycorrhizal data categories used for AM diagnosis

A similar process to that described above can be used to present data used to support diagnosis of EM associations (see Table 4), but usually is not required unless associations are atypical, or occur in an unexpected host plant. Table 3 also provides criteria that could be used for the diagnosis of ericoid or orchid mycorrhizas.

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Brundrett, M.C. Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320, 37–77 (2009). https://doi.org/10.1007/s11104-008-9877-9

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Keywords

  • Arbuscular mycorrhiza
  • Ectomycorrhiza
  • Roots
  • Plant diversity and evolution
  • Glomeromycotan fungus colonisation
  • Symbiotic diagnosis