Mycol. Res. 107 (11): 1249–1252 (November 2003). f The British Mycological Society
1249
Printed in the United Kingdom.
Mycological Research News1
This issue of Mycological Research News features : Davidiella, a new generic name for the teleomorph of Cladosporium
s. str.; Will European forest fires favour Neurospora ascomata? ; Programmed cell death alive and well in fungi ; and
Complex conidia as branched hyphal systems ; An obituary for Colin Booth (1924–2003), a leading authority on
Fusarium and a past-President of the British Mycological Society, is also presented.
A detailed review of chemical interactions between mycorrhizal fungi and toxic metal cations is followed by ten
original research papers. These consider the molecular phylogenetics of Caloplaca and Xanthoria, Termitomyces spp.
and related fungi, the separation of Linocarpon and Neolinocarpon spp. using ultrastructural features, the Leptosphaeria
maculans–L. biglobosa complex, diversity within Hyaloperonospora parasitica and Thanatephoriu cucumeris (anamorph
Rhizoctonia solani), the development of markers for studies within Phialocephala fortinii, host–parasite relationships in
Hypomyces spp., hypovirulence in Sclerotinia sclerotiorum, and airborne mould spores in apartments.
No new scientific names are introduced in this part.
DOI: 10.1017/S0953756203219158
IN THIS ISSUE
This issue starts with a review of the chemical basis of
interactions between mycorrhizal fungi and toxic metal
cations (pp. 1253–1265). Mycorrhizal fungi have long
been known to be able to grow in toxic chemical environments, but how this is achieved and the extent to
which the partner plants have enhanced resistance as a
result has only recently started to be studied in depth.
The evidence for adaptive mechanisms is analysed and
found to be lacking, but the ways the fungi respond are
diverse and perhaps best interpreted as the environment selecting for the fungal community most likely to
cope with the challenging environment.
Current classifications are continually being challenged by molecular phylogenetic studies. Now, the separation of two of the most familiar lichen genera is
called into question as a result of nuclear SSU and LSU
rDNA analysis, with different groups of Xanthoria
species being intermixed with others of Caloplaca (pp.
1266–1276) ; the traditional emphasis on thallus morphology as a generic criterion in these lichens has resulted in the recognition of polyphyletic genera. In the
case of Termitomyces, however, molecular studies show
that they are a strongly supported monophyletic group
with significant differences between material from
different continents, and that two segregate genera
proposed cannot be supported (pp. 1277–1286). The
1
Mycological Research News is compiled by David L. Hawksworth, Executive Editor Mycological Research, The Yellow House,
Calle Aguila 12, Colonia La Maliciosa, Mataelpino, E-28492 Madrid,
Spain (tel/fax: [+34] 91 857 3640; e-mail: myconova@terra.es), to
whom suggestions for inclusion and items for consideration should be
sent. Unsigned items are by the Executive Editor.
ascospore ultrastructure in species of Linocarpon and
Neolinocarpon has been examined, and while the ascospore appendages proved to be of value in species
separations, the recognition of two genera could not be
supported (pp. 1304–1312).
Within the Leptosphaeria maculans–L. globosa
species complex, which causes stem cankers in crucifers,
at least seven distinct groups could be recognized by
a combination of biochemical and molecular criteria,
generally correlated with different host plants and
geographical locations (pp. 1287–1303). Similarly,
Hyaloperonospora parasitica isolates from different
brassicaceous hosts fell into four distinct clades on ITS
rDNA sequence analysis, suggesting that a number of
additional species merit recognition (pp. 1313–1321).
In Thanatephorus cucumeris (anamorph Rhizoctonia
solani) isolates causing lesions on potato, ITS1 and
RAPD analyses showed all belonged to the same anastomosis group, although different ITS types could
occur in the same isolate (pp. 1322–1330). The significance of Phialocephala fortinii as a root endophyte has
been recognized relatively recently ; now, RFLP markers have been developed to facilitate studies at the
population level in this species which has a high genetic
diversity (pp. 1331–1340).
The extent to which mycoparasitic and other fungicolous fungi are host-specific is often uncertain. Now,
in the case of Hypomyces strains infecting boletes
in North America, AFLP analyses and ITS rDNA sequence data reveal that H. microspermus is host-specific
to the Xerocomus chrysenteron group, while H. chrysospermus is a more generalist pathogen (pp. 1341–1348).
Mycological Research News
Within the tan sclerotial race of Sclerotinia sclerotiorum, hypovirulence in isolates was found to be both
stable and transmissible (pp. 1349–1359).
Mould spore loads in human habitations have long
been of concern, but most studies have been limited in
the extent and period of sampling undertaken. Now, we
report a study involving 1165 matched pairs of indoor
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and outdoor measurements made in Leipzig over the
years 1998–2002 (pp. 1360–1370). Indoor- (e.g. Penicillium spp.) and outdoor- (e.g. Cladosporium spp.)
relevant groups of fungi could be distinguished, with
considerable year-to-year variation occurring in the
outdoor group.
DOI: 10.1017/S0953756203229154
D A V I D I E L L A, A N EW G E N E R I C N A M E F O R T H E T E L E O M O R P H OF
C L A D O S P O R I U M S. S T R.
Molecular phylogenetic studies using ITS, 5.8S and 18S
rRNA gene sequences show Cladosporium s. lat. to be
heterogeneous, but significantly place Cladosporium
s. str. (including the ubiquitous C. herbarum, the type
species of the genus) as a sister group to Mycosphaerella
s. str. (Braun et al. 2003). Cladosporium s. str. species
are characterized by coronate conidiogenous scars and
conidial hila as demonstrated using scanning electron
microscopy by David (1997), whose results are confirmed by the molecular analyses. However, the teleomorph of Cladosporium s. str. is indistinguishable
from Mycosphaerella except in the anamorph. Despite
this, and therefore somewhat controversially, the new
generic name Davidiella is introduced for the teleomorphs of Cladosporium s. str. and four combinations
made into the new genus; D. tassiana (syn. Sphaerella
tassiana, Mycosphaerella tassiana) is the name proposed
for the teleomorph of C. herbarum. C. cladosporioides
falls in the same clade but no teleomorph is recognized
for that species. It now remains to be seen whether
mycologists in general will take up these new concepts
or prefer to retain a broader concept of Mycosphaerella,
perhaps using some sectional or subgeneric name, as
otherwise it may not be possible to say whether a fungus
belongs to Davidiella or Mycosphaerella without either
the anamorph or sequence data.
Braun, U., Crous, P. W., Dugan, F., Groenewald, J. Z. & de Hoog,
G. S. (2003) Phylogeny and taxonomy of Cladosporium-like
hyphomycetes, including Davidiella gen. nov., the teleomorph of
Cladosporium s. str. Mycological Progress 2: 3–18.
David, J. C. (1997) A contribution to the systematics of Cladosporium: revision of the fungi previously referred to Heterosporium.
Mycological Papers 172: 1–157.
DOI: 10.1017/S0953756203239150
WILL EUROPEAN FOREST FIRES FAVOUR NEUROSPORA ASCOMATA?
Neurospora has great potential as a model system for
fungal ecology, population biology and evolution,
complementing its important model status in genetics
and molecular biology. Renewed interest in Neurospora
in the wild has followed its recent discovery colonizing
burned trees after forest fires in western North America
(Jacobson et al. 2003). The devastating forest fires that
engulfed Europe this past summer were the worst in a
generation. This tragedy, however, presents a unique
opportunity to initiate comparative studies of this
fungus in similar natural habitats a continent apart. A
group of European and American workers are surveying forest fire sites and collecting populations of Neurospora across southern Europe.
Other than its obvious adaptation to fire-killed
vegetation, little is known about the natural history of
Neurospora. Viable ascospores are present in soil
(Maheswari & Anthony 1974, Pandit & Maheshwari
1996) and preliminary studies have indicated that
sexual reproduction is important in the genetic structuring of Neurospora populations. However, sexual
fruit bodies have rarely been found in nature at forest
fire sites or elsewhere (Jacobson et al. 2003, Pandit &
Maheshwari 1996, Perkins 2002). The role of resistant
sexual ascospores in survival, dissemination, and mode
of colonization is far from clear.
The surveys of vegetative colonization and asexual
sporulation of Neurospora need to be supplemented
with later periodic surveys for ascomata. Unfortunately, we cannot yet predict the timing of sexual
development is nature. Perithecia were only found
months after a burn in the tropics, when vegetation was
decomposed (Pandit & Maheshwari 1994). Only one
Neurospora perithecium was found in casual surveys of
forest fire sites (Jacobson & Natvig, unpubl.). Conidial
blooms of Neurospora can remain viable over winter
under the bark of trees (Jacobson et al. 2003, and unpubl.), however, no perithecia were found associated
with those 9–10 month old colonies. Dead trees can
remain standing for a decade or more after a fire. We
cannot predict whether the European situation will
mirror that of North America. However, it is not likely
that perithecia will be found during the autumn 2003
surveys, but will develop much later.
Mycological Research News
European forest fire sites should favour Neurospora
ascomata. To find them and learn the dynamics of
Neurospora sexual reproduction will take a concerted
effort to survey sites repeatedly through 2004. All
mycologists living near or passing through burnt sites
are encouraged to search for Neurospora perithecia.
For additional information on the surveys underway,
contact either David Jacobson (djjacob@stanford.edu)
or Martha Merrow (martha.merrow@imp.med.unimuenchen.de).
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J. W. & Natvig, D. O. (2003) Neurospora in temperate forests of
western North America. Mycologia: in press.
Maheshwari, R. & Antony, A. (1974) A selective technique for the
isolation of Neurospora crassa from soil. Journal of General
Microbiology 81 : 505–507.
Pandit, A. & Maheshwari, R. (1994) Sexual reproduction by Neurospora in nature. Fungal Genetics Newsletter 41: 67–68.
Pandit, A. & Maheshwari, R. (1996) Life history of Neurospora
intermedia in a sugar cane field. Journal of Bioscience 21: 57–79.
Perkins, D. D. (2002) Neurospora perithecia: the first sighting. Fungal
Genetics Newsletter 49: 9–10.
David J. Jacobson
Jacobson, D. J., Powell, A. J., Dettman, J. R., Saenz, G. S., Barton,
M. M., Hiltz, M. D., Dvorachek, W. H. jr, Glass, N. L., Taylor,
Department of Biological Sciences, Stanford University,
371 Serra Mall, Stanford, CA 94305-5020.
E-mail : djjacob@leland.stanford.edu
DOI: 10.1017/S0953756203249157
PROGRAMMED CELL DEATH ALIVE AND WELL IN FUNGI
The Oxford Dictionary of Biochemistry and Molecular
Biology (Smith et al. 1997) defines apoptosis as ‘ cell
death _ used broadly to encompass all forms of _
normal or pathological cell death or may be confined to
those processes involving morphological changes such
as occur in normal animal development ’. Fine, but
does the lack of mention of fungi or plants mean that
they don’t go in for programmed cell death ? Or does it
reflect that regrettably frequent narrowness of mind
that leaves so many people thinking that only animals
matter ? It’s the latter, I’m afraid, because there’s no
doubt at all that plants use programmed cell death
(think of all the leaves falling from those deciduous
trees. _.) ; and fungi ? Ah well, as you might expect,
fungi are well versed in the sophisticated use of programmed cell death (PCD) ; they’ve been using it for a
long time. Some recent papers establish this point, but
we can find evidence for it in some of the classic literature, too. Mousavi & Robson (2003), for example, have
just demonstrated that cell death of Aspergillus fumigatus in the stationary phase depends on caspase-like
enzyme activity. This is similar to animal apoptosis,
where cysteine-proteinases known as caspases are
essential components of the apoptotic pathway. Similarly, Lu, Gallo & Kües (2003) present customarily
elegant cytological evidence for apoptotic DNA degradation in basidia of meiotic mutants of Coprinopsis
cinereus (syn. Coprinus cinereus). Again, there is a
compelling comparison with animal apoptosis where
specific DNA fragmentation is an essential component.
As Money (2003) has commented, such a process in a
mushroom may well be a matter of resource conservation (the Coprinopsis mutants cannot complete meiosis so there is presumably some value in recycling the
contents of the defective basidia). However, constant
comparison with apoptosis in complex animals may
well be diverting us from appreciation of the several
roles for programmed cell death in fungi that have been
known for many years. The point is that most research
is done (for obvious reasons) on vertebrate animals in
which a primary ‘ design requirement’ is that as the cell
dies release of antigens must be avoided to protect the
animal against autoimmunity. This has resulted in
development of a highly sophisticated cell destruction
process that takes place inside an intact cell membrane,
so that the cell remnants remain separated from the
immune system until they are engulfed by phagocytes.
This seems to be the system with which everything else
is compared, but it is a highly adapted system, and even
in animals there are many examples of ‘partial apoptotic ’ systems which, nevertheless, accomplish programmed removal of cells in a controlled and specific
manner (Lockshin, Zakeri & Tilly 1998). So, the message is that a cell death programme will be adapted to its
function, and, unless it happens in an organism with an
active immune system, it’s unlikely to feature all the
events that can be recognised in vertebrates. So where
do you look for programmed cell death in fungi ? First,
look at all those subterminal cells that are sacrificed
to release the terminal spore – if their death is not programmed, then what is ? Cell death is a common occurrence in various structures starting to differentiate,
for example the formation of gill cavities in Agaricus
bisporus (Umar & van Griensven 1997, 1998). These
authors point out that specific timing and positioning
imply that cell death is part of the differentiation process and that fungal PCD could play a role at many
stages in the development of many species. Individual
hyphal compartments can be sacrificed to trim hyphae
to create particular tissue shapes. PCD is used, therefore, to sculpture the shape of the fruit body from
the raw material provided by the hyphal mass of the
fruit body initial and primordium (Moore et al. 1998).
Several examples detailed by Umar & van Griensven
(1998) feature a PCD programme that involves the
sacrificed cells over-producing mucilaginous materials
Mycological Research News
that are released by cell lysis. Evidently, in fungal PCD,
the cell contents that are released when the sacrificed
cells die could be specialised to particular functions too.
But don’t run away with the idea that you only have to
go back ten years to find examples of PCD in fungi. To
my mind, the most obvious example of fungal PCD is
the autolysis that occurs in the later stages of development of fruit bodies of many species of Coprinopsis and
Coprinus. So dip into the 30-year old literature and
you’ll find that autolysis involves specifically-timed
production and organised release of a range of lytic
enzymes (Iten 1970, Iten & Matile 1970) and is clearly
a programmed enzymatic cell death. Allegedly, the
phrase programmed cell death was first used in a doctoral thesis dealing with insect development (Lockshin
1963). But over 30 years before that date, Buller (1924,
1931) interpreted autolysis in coprinoid fungi as part
of the developmental programme of the fruit body
(specifically : autolysis removes gill tissue from the bottom of the cap to avoid interference with spore discharge from regions above). I consider that Reginald
deserves a healthy slice of any credit that might be
handed out for introducing this concept into biology.
He should appear in future editions of the Oxford
Dictionary of Biochemistry and Molecular Biology.
Buller, A. H. R. (1924) Researches on Fungi. Vol. 3. Longmans Green,
London.
Buller, A. H. R. (1931) Researches on Fungi. Vol. 4. Longmans Green,
London.
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Iten, W. (1970) Zur Funktion hydrolytischer Enzyme bei der
Autolysate von Coprinus. Berichte der Schweitzerische Botanische
Gesellschaft 79: 175–198.
Iten, W. & Matile, P. (1970) Role of chitinase and other lysosomal
enzymes of Coprinus lagopus in the autolysis of fruiting bodies.
Journal of General Microbiology 61 : 301–309.
Lockshin, R. A. (1963) Programmed cell death in an insect. PhD
thesis, Harvard University.
Lockshin, R. A., Zakeri, Z. & Tilly, J. L. (1998) When Cells Die. John
Wiley & Sons, New York.
Lu, B. C., Gallo, N. & Kües, U. (2003) White-cap mutants and
meiotic apoptosis in the basidiomycete Coprinus cinereus. Fungal
Genetics and Biology 39: 82–93.
Money, N. P. (2003) Suicidal mushroom cells. Nature 423: 26.
Moore, D., Chiu, S. W., Umar, M. H. & Sánchez, C. (1998) In the
midst of death we are in life: further advances in the study of higher
fungi. Botanical Journal of Scotland 50: 121–135.
Mousavi, S. A. A. & Robson, G. D. (2003) Entry into the stationary
phase is associated with a rapid loss of viability and an apoptoticlike phenotype in the opportunistic pathogen Aspergillus fumigatus.
Fungal Genetics and Biology 39: 221–229.
Smith, A. D., Datta, S. P., Smith, G. H., Campbell, P. N., Bentley, R.
& McKenzie, H. A. (1997) Oxford Dictionary of Biochemistry and
Molecular Biology. Oxford University Press, Oxford.
Umar, M. H. & van Griensven, L. J. L. D. (1997) Morphogenetic cell
death in developing primordia of Agaricus bisporus. Mycologia 89:
274–277.
Umar, M. H. & van Griensven, L. J. L. D. (1998) The role of
morphogenetic cell death in the histogenesis of the mycelial cord
of Agaricus bisporus and in the development of macrofungi.
Mycological Research 102: 719–735.
David Moore
School of Biological Sciences, University of Manchester,
Stopford Building, Oxford Road, Manchester M13 9PT, UK.
E-mail: david.moore@man.ac.uk
DOI: 10.1017/S0953756203259153
COMPLEX CONIDIA AS BRANCHED HYPHAL SYSTEMS
Bryce Kendrick has been studying hyphomycetes for
almost 50 years, since he first discovered several previously undescribed genera and species in the course of
his PhD studies at the University of Liverpool in the
late 1950s. He was one of the strongest advocates of the
need to take a fresh look at approaches to the classification of asexual fungi and their integration into ‘whole
fungus ’ systems through the international Kananaskis
workshops of 1969 and 1977 of which he was the driving
force (Kendrick 1971, 1979). He has now taken a fresh
look at the problem, analysing types of conidiophore
morphogenesis and condium types (Kendrick 2003).
Most importantly, he endeavours to explain complex
conidia, especially staurosporous (e.g. branched) types
as condensed or otherwise ‘unorthodox ’ branching
hyphal systems (e.g. Desmidiospora, Gyoerffiella, Tetracladium, Tricladium, Uvarispora, Varicosporium),
and(or) analogues of colony development (e.g. Flabellospora, Petrakia, Psammina). More than 150 genera
are considered as forming conidia that are interpretable
as branched hyphal systems. This novel approach to
the interpretation of complex conidia transcends
current thinking (Kirk et al. 2001) and demands a reappraisal of how complex conidia are described and
pertinent conidial fungal genera are separated. All concerned with systems of hyphomycetes need to reflect on
the fundamental importance of the interpretations
suggested here.
Kendrick, B. (ed.) (1971) Taxonomy of Fungi Imperfecti. University of
Toronto Press, Toronto.
Kendrick, B. (ed.) (1979) The Whole Fungus. 2 vols. National
Museum of Natural Sciences, Ottawa.
Kendrick, B. (2003) Analysis of morphogenesis in hyphomycetes:
new characters derived from considering some conidiophores and
conidia as condensed hyphal systems. Canadian Journal of Botany
81: 75–100.
Kirk, P. M., Cannon, P. F., David, J. C. & Stalpers, J. A. (2001)
Ainsworth & Bisby’s Dictionary of the Fungi. 9th edn. CABI
Publishing, Wallingford.