Morphological, mycorrhizal and molecular characterization of Finnish truffles belonging to the Tuber anniae species-complex

Article (PDF Available)inFungal Ecology 6(4) · August 2013with 225 Reads
DOI: 10.1016/j.funeco.2013.03.002
Abstract
The truffle species Tuber anniae was originally described from the U.S. Pacific Northwest and is purported to be uncommon. Here, we report for the first time on the fruiting of closely related taxa in Baltic Rim countries. These truffles were found in a forest dominated by Scots pine in eastern Finland. Mycorrhizal analyses confirmed its symbiosis with Pinus sylvestris. Morphological observations of ascomata and mycorrhizae, and phylogenetic analyses confirmed that these white truffles belong within the group of Tuber puberulum (i.e., Puberulum clade). Further, they group in Clades II and III of the T. anniae species-complex. With the inclusion of sequences from GenBank we are able to demonstrate that the previously unnamed environmental clade (Clade II) has been found as ectomycorrhiza in symbiosis with pine, birch, oak, aspen and even orchids in Europe. Thus, the T. anniae species-complex as a whole (and two of the three clades within) exhibit considerable geographic disjuncts: Northwestern North America and the Baltic Rim of Europe. Clade II, which was collected in agricultural soils in Finland and along roadsides in Alaska, may also be adapted for colonization into new habitats. This may help to explain its presence in New Zealand (where Tuber is not native), which most likely resulted from human-mediated dispersal of these fungi through forestry or the nursery trade. Based on our results, we hypothesize that management practices such as organic and lime amendments, along with aeration, are beneficial to the fruiting of T. anniae. Further research is needed to determine the edibility of these species and whether commercial markets can be developed.
Morphological, mycorrhizal and molecular characterization of
Finnish truffles belonging to the Tuber anniae species-complex
Xiang-Hua WANG
a
, Gian Maria Niccol
o BENUCCI
b,
*, Xue-Dan XIE
a
, Gregory BONITO
c
,
Matti LEISOLA
d
, Pei-Gui LIU
a
, Salem SHAMEKH
d
a
Key Laboratory of Biodiversity and Biogeography, Kunming Institute of Botany, Chinese Academy of Sciences, Lanhei Road 132,
Kunming 650204, PR China
b
Department of Applied Biology, University of Perugia, Borgo XX Giugno 74, I-06121 Perugia, Italy
c
Department of Biology, Duke University, Durham, NC 27708, USA
d
Department of Biotechnology and Chemical Technology, University of Aalto, FI-00076 Aalto, Finland
article info
Article history:
Received 5 August 2012
Revision received 31 January 2013
Accepted 12 February 2013
Available online 30 April 2013
Corresponding editor:
Kabir Peay
Keywords:
Baltic Rim
Ectomycorrhiza
ITS-rDNA
Pinus sylvestris
Puberulum clade
Tuber anniae
White truffles
abstract
The truffle species Tuber anniae was originally described from the U.S. Pacific Northwest
and is purported to be uncommon. Here, we report for the first time on the fruiting of
closely related taxa in Baltic Rim countries. These truffles were found in a forest dominated
by Scots pine in eastern Finland. Mycorrhizal analyses confirmed its symbiosis with Pinus
sylvestris. Morphological observations of ascomata and mycorrhizae, and phylogenetic
analyses confirmed that these white truffles belong within the group of Tuber puberulum
(i.e., Puberulum clade). Further, they group in Clades II and III of the T. anniae species-
complex. With the inclusion of sequences from GenBank we are able to demonstrate
that the previously unnamed environmental clade (Clade II) has been found as ectomy-
corrhiza in symbiosis with pine, birch, oak, aspen and even orchids in Europe. Thus, the
T. anniae species-complex as a whole (and two of the three clades within) exhibit consid-
erable geographic disjuncts: Northwestern North America and the Baltic Rim of Europe.
Clade II, which was collected in agricultural soils in Finland and along roadsides in Alaska,
may also be adapted for colonization into new habitats. This may help to explain its pres-
ence in New Zealand (where Tuber is not native), which most likely resulted from human-
mediated dispersal of these fungi through forestry or the nursery trade. Based on our
results, we hypothesize that management practices such as organic and lime amendments,
along with aeration, are beneficial to the fruiting of T. anniae. Further research is needed to
determine the edibility of these species and whether commercial markets can be developed.
ª2013 Elsevier Ltd and The British Mycological Society. All rights reserved.
Introduction
Species of Tuber are distributed across Asia, Europe, North
Africa and North America (Jeandroz et al. 2008). Early studies by
Vittadini (Vittadini 1831) and the Tulasne brothers (Tulasne &
Tulasne 1862) documented high morphological diversity of
Tuber across Europe. Many of these species and others since
have been reported from Asia (Moreno et al. 1997;Liu et al. 2009;
Deng et al. 2012) and North America (Guevara et al. 2008;Bonito
et al. 2010b;Guevara et al. 2012). However, recent studies
incorporating molecular data show high levels of continental
endemism in Tuber and indicate that, in many cases, European
*Corresponding author. Tel.: þ39 (0) 755856433.
E-mail address: gian.benucci@gmail.com (G.M.N. Benucci).
available at www.sciencedirect.com
journal homepage: www.elsevier.com/locate/funeco
1754-5048/$ esee front matter ª2013 Elsevier Ltd and The British Mycological Society. All rights reserved.
http://dx.doi.org/10.1016/j.funeco.2013.03.002
fungal ecology 6 (2013) 269e280
  • ... Distribution and ecology. Wang et al. (2013) reported from Europe; Colgan and Trappe 1997; Bonito et al. (2010) reported in North America. Here, we ex- tended the distribution to central México (State of México and Tlaxcala). ...
    ... Here, we ex- tended the distribution to central México (State of México and Tlaxcala). In Finland, T. anniae has been confirmed to establish association with P. sylvestris L. ( Wang et al. 2013). In Washington, this species has been confirmed to establish association with Pseudotsuga menziesii (Mirbel) Franco (Bonito et al. 2010). ...
    ... The holotype (from Washington) and the other collections reported were from the Pacific Northwest in the US and reported co-occurring with P. menziesii. The T. anniae complex of species has been proposed based on phylogenetic analysis using ITS region ( Wang et al. 2013). The collection from México is very similar to the holotype collection, however, the lat- ter has a brown to dark olive-brown peridium and its spores have thicker (up to 5 µm) spore walls than the former. ...
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