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Review

TRENDS in Biotechnology

Vol.21 No.10 October 2003

433

Cultivation of edible ectomycorrhizal mushrooms
Ian R. Hall, Wang Yun1 and Antonella Amicucci2
1 2

New Zealand Institute for Crop and Food Research Limited, Invermay Agricultural Centre, Private Bag 50034, Mosgiel, New Zealand Istituto di Chimica Biologica, ‘G. Fornaini’, University of Urbino, via Saffi 2, Urbino (PU), Italy

The edible mycorrhizal mushrooms include some of the world’s most expensive foods and have a global market measured in US$ billions. Despite this, few have been cultivated with any degree of success, and certainly not in volumes that are likely to reverse the catastrophic declines in production that have occurred over the past 100 years. The main obstacles to their cultivation are their need to be associated with a host plant to successfully grow and fruit, contamination with other ectomycorrhizal fungi both before and after the establishment of plantations, and a general lack of understanding of each mushroom’s trophic relationships, and biotic, edaphic and climatic requirements. Mycorrhizas are ancient symbiotic associations between specialised fungi and the fine roots of the majority of species of higher plants [1–4] (see http://www.berkeley.edu/ news/media/releases/2000/09/14_funghi.html). By extending the absorptive area of the root system, mycorrhizas have their principal beneficial effect – increasing plant uptake of nutrients, in particular phosphorus [5,6]. In exchange, the host plant provides the generally obligate mycorrhizal fungus with carbohydrates and a place to live. The complexities of the mycorrhizal association have proved fertile ground for researchers, with a search of the CAB International database (http://www. cabi-publishing.org/Products/Database/Abstracts/Index.asp) finding . 20 000 scientific papers in the past 15 years alone. However, mycorrhizas, and in particular ectomycorrhizas, are also of considerable interest to the chef and the gourmet because some of the basidiomycetes and ascomycetes that form them produce edible mushrooms, some of which are among the world’s most expensive foods (Table 1) [7].

Falling harvests There has been a catastrophic decline in harvests of some edible mycorrhizal mushrooms over the past century. For ´ example, European Tuber melanosporum (Perigord black truffle) harvests have fallen from around 2000 tonnes at the beginning of the 20th century to rarely . 150 tonnes now [8,9]. The official figures for T. melanosporum production in France illustrate this trend well (Fig. 1) [10,11] (M. Courvoisier, personal communication). Harvests of the Japanese delicacy matsutake [12,13] and other important species of edible mushrooms that grow in the Northern Hemisphere [14] have also fallen, necessitating the introduction of rules and regulations aimed at preventing over-harvesting [13,15,16]. Reasons advanced to account for these declines include deforestation, the loss of host plants within forests because of pests or disease, changed forest management practices such as planting more densely than occur in natural forests, the replacement of natural forests with plantations of species that are poor hosts, global warming since the last ice age, soil compaction by hordes of pickers, acid rain and the loss of expertise during two World Wars as to where and how to harvest mushrooms, particularly truffles [7 –9,12– 16]. Although the decline in production has triggered research into devising methods for the cultivation of mycorrhizal mushrooms, the associated scientific literature remains modest compared with other areas of mycorrhizal research. This is partly because edible mycorrhizal mushrooms take many years to fruit and other areas of mycorrhizal research provide a quicker route to a publication record. Another significant factor is that some key scientists working towards the cultivation of these potentially lucrative crops are tied by confidentiality agreements and are not permitted to publish or patent

Table 1. Approximate market information on the most important of the edible mycorrhizal mushrooms
Botanical name Boletus edulis Cantharellus cibarius Tricholoma matsutake Tuber melanosporum Tuber magnatum Common name Porcini Chanterelle Matsutake Perigord black truffle ´ Italian white truffle Approximate in-season retail market US$ . 250 million 1.62 billion 500 million . 150 million . 150 million Estimated world production (t) 20 000 –100 000 200 000 2000 150 50 –200 Approximate wholesale prices US$/kg (first grade) 13 –198 8 –19 40 –500 250 –1200 1000 –13 000 Refs [37] [75] [12] [9] [38]

Corresponding author: Ian R. Hall (halli@crop.cri.nz).
http://tibtec.trends.com 0167-7799/$ - see front matter q 2003 Elsevier Ltd. All rights reserved. doi:10.1016/S0167-7799(03)00204-X

temperature. During Talon’s lifetime this ‘dirty technique’ became the mainstay of the truffle industry and continued to be used until the 1970s.myk opat. He discovered that if ´ self-sown seedlings growing under Perigord black truffleproducing oaks were used to establish truffle plantations ` (truffieres). Gutierrez. Tuber melanosporum and Tuber brumale truffle production in France 1903– 2001 (from Refs [10. such as Thelephora spp. Similar techniques were also used to cultivate Tuber uncinatum (Burgundy truffle) [17] and the Japanese delicacy honshimeji (Lyophyllum shimeji) [18]. Considerable effort has been devoted to devising quality control standards (see http://www.se/mycorrhiza/edible/proceed/ bencivenga.html) [27.slu. As Hall and Wang point out. But despite these successes. remain trade secrets [24. that compete with the truffle mycelium for space on the host’s roots in the greenhouse and later in the http://tibtec.com field. there is an important difference between inoculating a plant (i. and this includes important commercial species such as Boletus edulis [37]. light levels. such as Scleroderma. but their implementation has been limited.e. their research findings for fear that vital intellectual property will be lost. 5 to 20 years later these plantations would also produce truffles.HTML).html) [7]. mykopat.29] or pure cultures prepared either from fruiting bodies [30] or mycorrhizal root tips [22] have led to the formation of edible mycorrhizal mushroom fruiting bodies in the field. poor seedling quality remains a serious problem in Tuber-inoculated plants (see http:// www. Although dozens of nurseries around the world now produce seedlings inoculated with T. Sphaerosporella brunnea and Pulvinula constellatio. Courvoisier. Consequently. Talon’s technique produces plants contaminated by other soil flora and fauna.38].17. Cultivation of other species Plants infected following inoculation with sporal suspensions [24. in greenhouses either with spores [19 – 22] or segments of infected root [22] (and I.se/mycorrhiza/edible/proceed/ chevalier. potting medium formulation and pH.jp/KansaiWindowhtml/ News/1996-e/19961119_NEWS. Rhizopogon rubescens [31]. many of the resulting trees never produced truffles and the technique was considered unreliable (see G. Despite these problems. Lyophyllum shimeji (‘Kyoto scientists grow hon-shimeji mushrooms’.kippo. who lived in France during the first part of the 18th Century.32].or. uncinatum [17]. Another crucial factor is the control of contaminating saprobic and ectomycorrhizal fungi. many details that ensure success. supplies of most commercially important edible mycorrhizal mushrooms are still restricted to those that can be harvested from the wild during autumn or winter. devised the first method for cultivating an edible mycorrhizal mushroom [7].21 No.25]. applying the inoculum to the roots) and producing a plant well-infected solely with the correct ectomycorrhizal fungus [24]. including other potentially competing ectomycorrhizal fungi.trends.434 Review TRENDS in Biotechnology Vol. unpublished) [33] and various species of Tuber. uncinatum [7–9. Tricholoma matsutake [13] and the Italian white truffle (Tuber magnatum) [26.28]. Terfezia (A.slu. http://www.mykopat. melanosporum truffles are now harvested from artificial plantations.slu. more than half of all T. T.R. borchii (bianchetto) [34]. fertilisation. Consequently. Hall. including Lactarius deliciosus [31.html) [26]. However. unpublished data based on [21]).se/mycorrhiza/edible/proceed/chevalier. Consequently.8] and T. personal communication). melanosporum [7.11] and M. such as the amount. melanosporum and T.. quality and treatment of inocula as well as watering. Cultivation of Tuber spp Joseph Talon. For these we are left to speculate on the reasons why we have not . and possibly pathogens. Suillus granulatus [32]. However.10 October 2003 1200 1000 800 600 400 200 0 1900 Production (t) 1910 1920 1930 1940 1950 Year 1960 1970 1980 1990 2000 TRENDS in Biotechnology Fig. nematodes and insect pests. 1. Chevalier. fewer than a dozen of the many hundreds of edible mycorrhizal mushrooms have ever been cultivated with any degree of success [36]. beginning in the late 1960s and early 1970s more reliable methods were devised to artificially infect plants with Tuber spp. http://www. including T. Danell and Camacho also produced Cantharellus cibarius in pots in the greenhouse [35].23].

before finally exhibiting some saprobic ability by continuing to live in the host tissues perhaps even after its host tree has been milled for timber [12. However. for example Suillus bovinus and Rhizopogon with Gomphidius roseus. Similarly. a close relative of T. Many mycorrhizal fungi exhibit marked saprobic abilities [43].g. New Zealand. saprobes (those that live in dead animal or plant remains). Symbionts. Complex biotic interactions Bacteria. Some mycorrhizal fungi can also maintain infections and fruit in soils containing high concentrations of available phosphorus [17. muscaria or A. are also routinely found in the fruiting bodies of Cantharellus cibarius. . against fungal contaminants from ascocarps of Tuber borchii [53]. sometimes completely destroying the root cortex. Sweden and USA. edulis hyphae and rhizomorphs were often closely B. Even ‘typical’ mycorrhizal fungi such as Tuber melanosporum and T. as the flow of nutrients seems to be in the direction of the host [6. Wang. matsutake. do not occupy precise zones within the triangle defined by these terms. whereas Lactarius Mycorrhizal deliciosus can invade host cortical cells (Y. In some cases these zones might shift depending on the phase in the life cycle of a fungus. or why fruiting bodies simply fail to form. excelsa Cortex Stele A. saprobes and pathogens One possible reason why we have been unsuccessful in cultivating some ‘mycorrhizal’ species is because we simply assume that they are mycorrhizal when their relationship with their hosts is more complicated. Several ectomycorrhizal fungi are also regularly found associated with saprobic [56] or other ectomycorrhizal fungi.com Fig. can be intimately associated with ectomycorrhizas and appear to aid the infection process. 3. producing the ‘burnt’ ˆ ´ area known as the brule [7. on closer inspection some fungi do not fit neatly into these man-made categories and instead a continuous gradation of behaviour can be seen [39. excelsa and B. although its role has yet to be determined [55]. 2. Although many fungi fit neatly into the terms ‘saprobe’. 2) (Y. Boletus edulis is regularly found in the same locations and at the same time of year as Amanita muscaria or Amanita excelsa in Austria. Bacteria. Italy. the ‘mycorrhizas’ of non-photosynthetic plants hardly seem to fit the classical functional definition of mycorrhiza. http://tibtec. although they do not seem to be mycorrhiza helper bacteria in this situation [50].53]. although initially appearing to be mycorrhizal on young roots. suggesting that they might have a role in ascocarp development and in the formation of mycorrhizas. [57 –59]. they have been referred to as ‘mycorrhiza helper bacteria’ [47 – 49]. with many fungi occupying zones within the triangle defined by the terms ‘symbiont’. with Chroogomphus spp. unpublished) found that A.21 No. in particular Pseudomonas spp. T. Bacteria.13]. In this work some of the bacteria tested were observed to release metabolites that affected the growth of T. many pathogens such as Armillaria mellea. particularly Pseudomonas. Mycologists classify fungi as symbionts (e. ‘saprobe’ and ‘pathogen’ (Fig. why what appear to be adequate infections subsequently fail or are displaced by other ectomycorrhizal fungi.trends. including some ‘mycorrhizal’ fungi.Review TRENDS in Biotechnology Vol. Wang and Stringer (A. again typically Pseudomonas. Stringer.44].10 October 2003 435 been able to establish viable infections on a suitable host plant. borchii mycelia also contain a Cytophaga-Flexibacter-Bacteroides phylogroup bacterium. ‘pathogen’ or ‘mycorrhizal’. England. have also been isolated from Tuber fruiting bodies [51. unpublished). which would markedly depress the growth of other mycorrhizal fungi [4]. As a consequence. and the ‘mycorrhizal’ fungus Tricholoma matsutake.52].45.. and pathogens (those that gain their nutrition from living plants or animals). and are involved in the suppression of competing ectomycorrhizal fungi [25. Suillus spp. soon becomes pathogenic. Most interesting is the antimycotic activity of Pseudomonas spp. lichens and mycorrhizas). edulis B. unpublished) [12]. The sometimes intimate association between species of mycorrhizal fungi is illustrated by this transverse section of a Pinus radiata mycorrhiza in New Zealand formed by Amanita excelsa and Boletus edulis. uncinatum will kill all the vegetation around the host tree. By contrast. For example.42]. borchii mycelia and morphogenesis in culture [54]. and Boletus parasiticus with Scleroderma citrinum [60]. can live on in the host tissues long after the host has died. excelsa Saprobe Pathogen TRENDS in Biotechnology TRENDS in Biotechnology Fig.41. Following closer investigation. others. edulis rhizomorph A.46].40]. Wang.

50].trends. Part 5. If these complex tripartite relationships are essential then it will be necessary to ensure that all the components are present to ensure stable infections of some edible ectomycorrhizal mushrooms on their host plant. and Read.J. The RAPD technique provides DNA fingerprints from which it is possible to select and sequence fragments to use as SCAR markers.com Molecular tools Whether the starting point in the cultivation of an edible mycorrhizal mushroom is a pure culture.. (2002) Fall mushrooms. (2003) Edible and Poisonous Mushrooms of the World. (2000) Glomalean fungi from the Ordovician. Even so. 467– 475 2 Le Page. Balkema 10 Courvoisier. for example. Am. ed. 3) similar to those described by Agerer for Suillus bovinus and Rhizopogon with Gomphidius roseus [58]. unpublished) Wang envisaged. It is also capable of fruiting under similar conditions or.21 No. the fungus survives rapid diurnal swings in temperature and fluctuating soil moisture [46]. perhaps in long-term experiments in which. 16. S. 410 – 412 3 Redecker. L.. Evol. This fungus then disappears once its pioneer host plant begins to succumb to competition from trees later in the succession [12]. monitor the effect of changing environmental conditions on mycorrhizal community structures [66]. Le Trufficulteur Francais 13. using specific oligonucleotides deduced from internal transcribed spacer regions [68.W.). as they offer the opportunity of establishing the full necessary biota required for an edible mycorrhizal fungus to infect and fruit perhaps long before we understand the intricate biotic interactions involved. Mushrooms: the journal of wild mushroom collecting 20.R. the degree of competition from contaminant mycorrhizas. and initiation of fruiting [74].62] or immunological techniques [63]. pH.). 1920– 1921 4 Smith.E. Some useful tools that could be used to investigate this further would be in situ DNA hybridisation [61. Le Trufficulteur Francais 10. One way such potential problems could be overcome would be to use ‘dirty’ techniques similar to those developed by Talon for Tuber melanosporum. (1995) La production et les cours de la truffe d’hiver 1903– 1995.38. borchii and other Tuber species belonging to the group of the so-called ‘bianchetti’ (whitish truffles) [70]. their relationship with other belowground organisms [43]. R. Wang. soil composition. D. unpublished) [12. the published information is rarely complete and for T. D. Bot. Trends Ecol. Acta Hortic 9 Olivier. 8 – 9 ¸ 11 Courvoisier. et al. et al.G. and identify the factors required to trigger fruiting [46]. 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Academic Press 5 Landeweert. apart from T.69] and sequence characterised amplified region (SCAR) markers obtained from the random amplified polymorphic DNA (RAPD) technique [70 –72]. account for the collapse of Boletus edulis ectomycorrhizas when wellinfected plants are transferred into open pots in the greenhouse (Y. uncinatum [7.10 October 2003 interwoven and formed composite mycorrhizas (Fig. 10 – 11 ¸ . 11 – 16 7 Hall.R. et al. our understanding of the ecological conditions favoured by edible ectomycorrhizal mushroom is restricted to a handful of fungi and a paucity of publications (A. melanosporum. (2000) Evolution of mycorrhiza systems. M. T. B.8. and a definition revisited. J. Timber Press 8 Lefevre. so it is likely that their use will soon become widespread. C. et al. 84. browsing by insects. (2000) Progress in the cultivation of truffles. Gutierrez. 248 – 254 6 Trudell.A. (1997) Fossil ectomycorrhizae from the Middle Eocene.D. References 1 Cairney. 513– 520. This might. (1995) La production et les cours de la truffe d’hiver 1903– 1995. pp.J. T. Wang. melanosporum truffiere. where there is little or no canopy cover. By contrast. I. Tricholoma matsutake does not appear in Pinus densiflora stands until the trees are 20-years-old and there is 75% canopy cover. S. Mycorrhizas.L. presence of hyperparasites. In Mushroom Science XV: Science and Cultivation of Edible Fungi (Vol. J. I. Naturwissenschaften 87.M. (2001) Linking plants to rocks. uncinatum [17] and L. the use of molecular tools is almost essential to ensure that the inoculum used is of the correct species and avoid the problems that have been encountered in attempts to cultivate Tuber magnatum [26]. These tools can also be used to detect contaminant species [67] as well as the persistence on a plant of an inoculant fungus. The molecular strategies developed in recent years for edible mycorrhizal mushrooms are primarily PCR-based.65]. moisture and temperature are varied. However. http://tibtec. Clearly the relationships between some edible ectomycorrhizal mushrooms and other ectomycorrhizal fungi and bacteria are anything but casual. Molecular tools provide more accurate methods for identification than the few characters afforded by traditional morphological features. and Hall. (2001) In The global status of truffle cultivation. M. Clearly there is a need for considerable study in this area to determine whether an edible mycorrhizal mushroom is found on young or old trees – so-called early or late-stage mushrooms [64. ectomycorrhizal fungi mobilize nutrients from minerals.A. unpublished).17]. The use of molecular strategies will be crucial in following the survival of inoculant fungi. These and other edible mycorrhizal mushrooms have a distinct set of edaphic and climatic conditions that they will either tolerate or require to both survive in the soil and ultimately fruit.436 Review TRENDS in Biotechnology Vol. Science 289. in particular multiplex PCR [73]. S. 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