全 文 ：Potential Problems Associated with the Cultivation and International
Trade in Edible Ectomycorrhizal Mushrooms
Hall Ian R . 1 * , Zambonelli Alessandra2
?
, Wang Yun3
( 1 Truffles & Mushrooms Ltd, P . O . Box 268 , Dunedin 9054 NEW ZEALAND; 2 Dipartimento di Protezione e
Valorizzazione AgroalimentareVia Fanin 40 , I 40127 Bologna, ITALY; 3 New Zealand Institute for
Plant & Food Research Limited Private Bag 4704 , Christchurch, NEW ZEALAND)
Abstract: There is considerable potential for the cultivation of ectomycorrhizal mushrooms in countries that are not tradi-
tional producers of edible ectomycorrhizal mushrooms . Those countries that are in the Southern Hemispheremay be able to
take advantage of out-of-season Northern Hemisphere markets . For example, they might produce Périgord black truffles
( Tuber melanosporum) at the height of the Northern Hemisphere′s summer tourist season or matsutake ( Tricholoma mat-
sutake) during the Japanese cherry blossom festival . There is also the possibility that Northern Hemisphere countries not
noted for exporting ectomycorrhizal mushrooms could cultivatethose species that are in short supply elsewhere . For exam-
ple, Chinamightwish to try and cultivate Caesar′s mushroom ( Amanita caesarea) and supplement dwindling supplies in
Europe . However, thereare risks in importing novel ectomycorrhizal fungi for research purposes and trade that go far be-
yond those associated with the importation of fresh saprobic mushrooms raised infactories . This paper discusses these risks
and points to potential hazards countries are exposed to when importing fresh ectomycorrhizal mushrooms or moving them
from one part of the country to another .
Key words: Ectomycorrhiza; Mushrooms; Export; Import; Cultivation; Soil ; Risks; Pathogens; Management
CLC number : S 646 Document Code : A Article ID: 0253 - 2700 ( 2009) Suppl.ⅩⅥ- 086 - 04
Introduction
There are commercial opportunities for cultivating
edible ectomycorrhizal mushrooms ( EEMM ) either to
supplement dwindling supplies harvested from the wild
or to take advantage of higher prices out-of-season
(Hall et al. , 2003; Wang and Hall , 2004 ) . For ex-
ample, truffles are already being cultivated in Southern
Hemisphere countries for Northern Hemisphere markets
during its summermonthswhilst porcini ( Boletusedulis
sensu lato) which grows wild in South Africa and New
Zealand might be exported fresh to Northern Hemi-
sphere countries . The motivator for cultivating truffles
in AustraliaandNew Zealand has undoubtedly been the
high prices paid for the Périgord black truffle andbian-
chetto truffle particularly at a time of year when the
only competition is preserved product fromthe Northern
Hemisphere ( Hall et al. , 2007 ) . Some growers have
also been particularly high in some successful truffières
with yields occasionally exceeding 300 kg?ha . Howev-
er, there are also considerable commercial benefits in
producing even modestly priced EEMM as secondary
crops in plantation forests which otherwise are largely a
financial drain for investors until the trees are felled
(Hall and Wang, 2000; Hall , 2008b) . An example
has been the cultivation of the saffron milk cap ( Lac-
tarius deliciosus (L . ex Fr .) S.F . Gray) on Pinus ra-
diata D . Don in New Zealand . This has been a suc-
cessful commercial venture for Hannes and Theres
Krummenacher since 2003 with current production av-
eraging 3 kg from each 7 year old productive tree
(Hall , 2008a) . Other possibilities might be the culti-
vation and harvest of matsutake ( Tricholoma matsutake
(S . Ito et Imai ) Sing .) in the Southern Hemisphere
during theJapanese cherry blossomtimeor the produc-
tionof an EEMM in one Northern Hemisphere country
to supplement dwindling supplies in another, for exam-
ple, the cultivation of Caesar′s mushroom ( Amanita
caesarea) in say China to supply European countries
云 南 植 物 研 究 2009 , Suppl . ⅩⅥ : 86～89
Acta Botanica Yunnanica
? ?Author for correspondence; E-mail : truffle1@ ihug. co. nz; zambonel@agrsci . unibo. it
where it is now red listed .
Regrettably the cultivation of EEMM has been,
and still is, not without its risks . Thepotential for fail-
ure is highlightedby the fact that fewer than adozenof
the 1000 species of EEMM have been successfully cul-
tivated .Thepotential for disaster is also ever present in
an EEMM research programme that could have far
reaching consequences-risks that also apply to the trade
in EEMM . This paper briefly covers these risks and by
doing so reveals what measures might be taken to avoid
possible problems becoming realities .
Potential problems with the import?export of
EEMM
Inferior truffles contaminating shipments of higher
quality species
In Europe all that stands in theway of agood and
a bad buy in a trufflemarket is the experience and ho-
nesty of the seller and the ability of thebuyer to identi-
fy truffles without the aid of a microscope or a fully
equipped molecular biology laboratory, both of which
are hard to find in truffle markets . Identification can
also beparticularly difficult if thetruffles arevery small
or are very immature . Périgord black truffles ( Tuber
melanosporum) truffles might be confused with Chinese
truffles ( Tuber indicum) , winter truffle ( Tuber brum-
ale) , Burgundy truffle ( Tuber aestivum) and the
smoothblack truffle ( Tuber macrosporum) (Hall et al. ,
2007) . Similarly, Italian white truffles ( Tuber magna-
tum) might be confused with young, immature Tuber
maculatumor bianchetto truffles ( Tuber borchii) partic-
ularly at the start of the season ( Hall et al. , 2007 ) ,
and bianchetto with inferior species such as Tuber
dryophilum-a likely contaminant in bianchetto
truffières . While patience and using the axiom,“ if in
doubt, throw it out”, can reduce risk the chances of
mistakes being made there is always the possibility of
mistakes beingmade .
The inclusion of an inferior species of truffle in a
meal could ruin a special occasionbut its inclusion in a
batch of inoculumused to produce truffle infected trees
could have dire consequences . Until recently, when
new regulations were introduced in Europe (United Na-
tions, 2004; Vignaud, 2006) , truffles covered in soil
were a common sight in European marketplaces . This
was primarily because truffles last longer when stored in
this condition and deteriorate more quickly after wash-
ing . However, perhaps during the washing process
there is the possibility that small pieces of a contami-
nating truffle, could perhaps become hidden in a small
crack in the surface of the desired species during the
washing process-even a 1 mm3 can contain enough
spores to contaminate 100 plants . Indeed thismay have
been how the inferior truffle winter truffle became es-
tablished in Australian and New Zealand truffières in
the past (Hall et al . , 2008) .
Importation of pathogenic fungi in shipments of
truffles
If truffle spores measuring about 20 - 55μmof one
species can becomesecreted inside cracks in the surface
of another then thereis also the possibility that spores of
other fungi coulddo likewise . Somewill befamiliar with
mushroomcollectors who pull mushrooms fromthe forest
floor, dump them into a sack with a liberal coating of
soil and thengivethemagoodshakingon theway to the
marketplace . The result is soil in the pores and gills
that may also carry spores of pathogenic fungi . While
mushrooms obviously contaminated with soil would not
be allowed into a country with strict quarantine stan-
dards the contamination may be so little as to go unno-
ticed . Also there may be no regulations preventing soil
contaminated mushrooms being shipped to another part
of the country where a pathogenmay be absent .
The chlamydospores and oospores of Phytophthora
can be about the same size (20 - 91μm, Dailey et al. ,
2004; Werres et al. , 2001) as trufflespores so perhaps
they too could ride piggyback on truffles from district to
district or country to country . P . ramosum oospores,
and thoseof other species, can betransmitted in avar-
iety of ways such as in soil on machinery and in water
and are highly resistant to heat surviving in leaves held
at 55℃ for 1 week, ( Central Science Laboratory,
2006; Turner et al. , 2006 ) . Phytophthora cinnamo-
mi , P . citricola, P . cambivora, P . ramorum and
P . kernoviaeand are widely distributed in Europe and
infect a wide range of truffle host plants such as everg-
78增刊ⅩⅥ Hall Ian R . et al. : Potential Problems Associated with the Cultivation and International Trade in . . .
reenoak ( Quercus ilex) , commonoak ( Q. robur) and
European beech ( Fagus sylvatica) ( Brasier, 2003;
California Oak Mortality Task Force, 2008; Central
Science Laboratory, 2006 , 2007; Forest Research,
2007; Scoop UK , 2008 ) . Phytophthora ramosum is
the cause of sudden oak death and kills a variety of
trees including Quercus and Fagus in the USA and
Europe while P . kernoviae continues its insidious
spread in the UK despite emergency measures having
been taken ( Central Science Laboratory, 2007; Scoop
UK , 2008) . Noneof these are pathogens that a coun-
try would want to risk importing .
Armillaria, Heterobasidium, Phellinus, Polyporus
and other pathogens of a wide variety of trees that are
host plants for EEMM have much smaller spores than
truffle ascospores and oospores of Phytophthora ( typi-
cally 2μm to 10μm) . Perhaps these too might ride
piggyback in shipments of EEMM .
Bacteria
Nitrogen fixing Azospirillumwas found in Hebelo-
ma crustuliniforme, Laccaria laccata and Rhizopogon
vinicolor fruitingbodiesmore than 20 years ago (Li and
Castellano, 1987 ) . Pseudomonas and other bacteria
are also routinely found in the fruiting bodies of Can-
tharellus cibarius and Tuber spp . andother mycorrhizal
fungi where they are either benign, appear to help the
mycorrhiza infect their host plant ( mycorrhiza helper
bacteria) , play an unknown role, or simply cause de-
cay ( Barbieri et al. , 2007; Cittario et al. , 1995;
Danell , 2000; Founoune et al. , 2002; Hall et al. ,
2007; Pacioni et al. , 2000; Sbrana et al. , 2002 ) .
Similarly, there seems to be a routine association of
Cytophaga-Flexibacter-Bacteroides phylum bacteria
within the mycelium of Tuber ( Barbieri et al. , 2002 ,
2005) . All of thesemight slip into a country in afruit-
ing body or maybe on a culture .
Fungal transmission of viruses
More than 30 viruseshavebeen found to be trans-
mitted by Olpidium, Plasmodiophora, Polymyxa,
Puccinia, and Spongospora subterranea to their host
plants . There appear to be no studies on the presence
of viral particles in EEMM or other ectomycorrhizal
fungi .
Transmission of pests in EEMM
Fly and beetle larvae are commonly found in fresh
truffles andmushrooms particularly duringwetyears . It
is not known whether the larvaethat havebeen found in
Australian and New Zealand T. melanosporum truffles
are thesamespecies as thosepresent in French, Italian
and Spanish truffières . If it is determined that they are
imports, perhaps using molecular techniques, then it
would be of concern as to how they managed to escape
the strict quarantine measures required by, for exam-
ple, the past and current New Zealand Import Health
Standard documents ( MAF Biosecurity, 2008 ) . On
the other hand if the larvae are local species then
it would be of interest to determine what their normal
diet is .
Discussion
If it is demonstrated that there is the potential for
movingdiseases and pests around the world in truffles
and mushrooms then countiesmaywell takethe inevita-
ble knee jerk reaction and ban their import . Such cont-
aminated truffles andmushroomswould present less of a
danger if they were eaten . Unfortunately, it would not
be possible to predict and guarantee exactly what a
mushroomor truffle would be used for after it had gone
through customs . Similarly, a chef may throw unco-
oked wasteonto a compost heapor truffles aimed at the
restaurant industry might be used as inoculuminstead .
However, all the above is simple speculation until a
great deal of work is doneto determine exactlywhat the
risks are .
These days there are other risks that researchers
must consider before embarking on a potentially long
research programme . The most important of these is
that a funding body may discontinue support before the
research is complete ( Hall , 2008a; Hall et al. , 2007
p . 10 and 228 - 229) . Another possibility is that com-
mercial interests brought in to help fund aproject could
stifle publications to ensure maximum return on their
investment . The result might be that a researchers′
publication record and their desirability as a future em-
ployee could be adversely affectedwith potentially trag-
ic consequences (Danell , pers . comm .) .
88 云 南 植 物 研 究 增刊ⅩⅥ
References:
Barb ?ieri E , Bertini L , Rossi I et al. , 2005 . New evidence for bacterial
diversity in the ascoma of the ectomycorrhizal fungus Tuber borchii
Vittad [ J ] . FEMS MicrobiologyLetters, 247: 23—35
Barb ?ieri E , Guidi C , Bertaux J et al. , 2007 . Occurrence and diversity of
bacterial communities in Tuber magnatum during truffle maturation
[ J ] . Environmental Microbiology, 9 : 2234—2246
Barb ?ieri E , Riccioni G, Pisano A et al. , 2002 . Competitive PCR for
quantification of a Cytophaga-Flexibacter-Bacteroides phylum bacteri-
umassociatedwith Tuber borchii Vittad . mycelium [ J ] . Applied En-
vironmental Microbiology, 68 : 6421—6424
Bras ?ier C, 2003 . Phytophthoras in European forests: their rising signifi-
cance . Sudden Oak Death Online Symposium . www. apsnet. org?on-
line?SOD (website of The American Phytopathological Society) . doi :
10 . 1094?SOD-2003-CB
Cali ?forniaOak Mortality Task Force, 2008 . Study identifies sudden oak
death introduction points into California′s forests, and finds pathogen
is evolving . http:??nature.berkeley. edu?comtf?pdf?Press?4 .16 .08 %
20Release .% 20Study% 20Identifies% 20SOD% 20Introduction%
20Points% 20Into% 20CA— Forests— and— Finds— Pathogen— isEvolv-
ing. pdf
Cent ?ral Science Laboratory, 2006 . Detection of Phytophthora ramorum in
water courses . DEFRA Research Project Final Report PH0317 . http:
??www.defra.gov. uk?science?Project— Data?DocumentLibrary?
PH0317?PH0317— 4587— FRP .pdf
Cent ?ral Science Laboratory, 2007 . Investigation of eradication and control
strategies for Phytophthorakernoviae ( PtC) in natural environments .
DEFRA Research Project Final Report PH0318 . http:? randd.d-
efra. gov. uk?Document. aspx ? Document = PH0318— 6338— FRP .pdf
Citterio B, Cardoni P , Potenza L et al. , 1995 . Isolation of bacteria from
sporocarps of Tuber magnatum Pico, Tuber borchii Vitt . and Tuber
maculatum Vitt .: identification and characterization [ A ] . In: Stocchi
V , Bonfante P, Nuti M, Biotechnology of ectomycorrhizae: molecular
approaches [M ] . New York: Plenum, 241—248
Dail ?ey A , Toohey M, Parke J et al. , 2004 . Phytophthora ramorum, a
guide for Washington nurseries . Oregon State University Extension
Service
Dane +ll E , 2000 . Cantharellus [ A ] . In: Ectomycorrhizal fungi: key gen-
era in profile . Cairney JWG, Chambers SM eds, [ M ] . New York:
Springer-Verlag, 253—267
Fore ?st Research, 2007 . Datasheet for Phytophthoraramorum . PPP 11824
and PPP 12421 . http:??www. defra.gov. uk?planth?pra?pram.pdf
Foun &oune H , Duponnois R, BaAM et al. , 2002 . Mycorrhizahelper bac-
teria stimulated ectomycorrhizal symbiosis of Acacia holosericea with
Pisolithus alba [ J ] . New Phytologist, 153: 81—89
Hall &IR , 2008a . Editorial : Research funding in New Zealand . Dunedin,
Truffles & Mushrooms ( Consulting ) Ltd . http:?www. tru-
fflesandmushrooms. co. nz?page16 . html , http:??www. trufflesandmu-
shrooms. co.nz?Science% 20Funding% 20 in% 20New% 20Ze-
aland.pdf
Hall ?IR , 2008b . Cultivation of the saffron milk cap as a secondary crop in
pine plantations . Dunedin, Truffles & Mushrooms (Consulting) Ltd
Hall ?IR , BrownG, Zambonelli A , 2007 . Taming the truffle: thehistory,
lore, and scienceof the ultimate mushroom . Portland: Timber Press
Hall ?IR , Stephenson SL , Buchanan PK et al. , 2003 . Edible and poison-
ous mushrooms of theworld . Portland: Timber Press
Hall ?IR , Wang Y , 2000 . Edible mushrooms as secondary crops in forests
[ J ] . Quarterly J ournal of Forestry, 94 : 299—304
Hall ?IR , Zambonelli A , Nelson P, 2008 . Distinguishing the Périgord
black truffle from thewinter truffle and other look-alikes . Dunedin,
Truffles & Mushrooms ( Consulting ) Ltd . http:?www. tru-
fflesandmushrooms. co.nz?Distinguishing% 20the% 20Perigord%
20black% 20truffle% 20from% 20 look-alikes. pdf (1150k pdf file)
Li C ?Y , Castellano MA , 1987 . Azospirillum isolated from within sporo-
carps of the mycorrhizal fungi Hebeloma crustuliniforme, Laccaria
laccata and Rhizopogon vinicolor [ J ] . Transactionsof the British My-
cological Society, 88 : 563—565
MAF ?Biosecurity, 2008 . BNZ-IMP- Tuber: Importation into New Zealand
of specified fresh and frozen Tuber species ( truffles) . Biosecurity
New Zealand standard . www. biosecurity. govt. nz?files?ihs?bnz-imp-
tuber.pdf
Paci ?oni G, Comandini O, 2000 . Tuber [ A ] . In: Ectomycorrhizal fungi :
key genera in profile . Cairney JWG, Chambers SM eds . [M ] . New
York: Springer-Verlag, 63—186
Sbra ?na C, Agnolucci M, Bedini S et al. , 2002 . Diversity of culturable
bacterial populations associated to Tuber borchii ectomycorrhizas and
their activity on T. borchii mycelial growth [ J ] . FEMS Microbiology
Letters, 211 (2 ) : 195—201
Scoo ?p UK , 2008 . Consultation on the future management of Phytophthora
ramorum and Phytophthora kernoviae . http:??www. scoop. co. nz?sto-
ries?WO0807?S00429 . htm
Turn ?er JA , J ennings P, McDonough S, 2006 . Investigation of dry-heat
treatment methods for sanitisation of P . ramorum and P . kernoviae
on?in plants . Internal quarterly reports1 and 2 . Defra Project . See:
http:??www. defra.gov. uk?planth?pra?pram.pdf , 54
Werr ?es S, Marwitz R , Manintveld WA et al. , 2001 . Phytophthora ramo-
rum sp . nov ., a new pathogen on Rhododendron and Viburnum
[ J ] . Mycological Research, 105 : 1155—1165
Wang ?Y , Hall IR , 2004 . Edible mycorrhizal mushrooms: challenges and
achievements [ J ] . Canadian J ournal of Botany, 82 : 1063—1073
Unit ?ed Nations, 2004 . UNECE Recommendation FFV-53 concerning the
marketing and commercial quality control of fresh truffles ( Tuber ) .
Based on document TRADE?WP. 7?GE. 1?2004?INF . 19 . www.unece.
org?trade?agr?meetings?ge. 01?document?2004— 25— a08 .pdf
Vign ?audG, 2006 . La nouvelle norme“ truffes fra?ches”. Le Trufficult-
eur . October-November-December , 11—14
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