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Edited by
Karl Esser
THE MYCOTA
A Comprehensive Treatise on Fungi
as Experimental Systems for Basic and Applied Research
Biology of the Fungal Cell

VIII
Third Edition
Dirk Hoffmeister
Markus Gressler
Volume Editors
The Mycota
Edited by
K. Esser
The Mycota
I Growth, Differentiation and Sexuality

1st edition ed. by J.G.H. Wessels and F. Meinhardt
2nd edition ed. by U. Kües and R. Fischer
3rd edition ed. by J. Wendland
II Genetics and Biotechnology
1st and 2nd edition ed. by U. Kück
III Biochemistry and Molecular Biology
1st and 2nd edition ed. by R. Brambl and G. Marzluf
3rd edition ed. by D. Hoffmeister
IV Environmental and Microbial Relationships
1st edition ed. by D. Wicklow and B. Söderström
2nd edition ed. by C.P. Kubicek and I.S. Druzhinina
3rd edition ed. by I.S. Druzhinina and C.P. Kubicek
V Plant Relationships
1st edition ed. by G. Carroll and P. Tudzynski
2nd edition ed. by H.B. Deising
VI Human and Animal Relationships
1st edition ed. by D.H. Howard and J.D. Miller
2nd edition ed. by A.A. Brakhage and P.F. Zipfel
VII Systematics and Evolution
1st edition ed. by D.J. McLaughlin, E.G. McLaughlin, and P.A. Lemke{
2nd edition ed. by D.J. McLaughlin and J.W. Spatafora
VIII Biology of the Fungal Cell
1st and 2nd edition ed. by R.J. Howard and N.A.R. Gow
3rd edition ed. by D. Hoffmeister and M. Gressler
IX Fungal Associations
1st and 2nd edition ed. by B. Hock
X Industrial Applications
1st edition ed. by H.D. Osiewacz
2nd edition ed. by M. Hofrichter
XI Agricultural Applications
1st and 2nd edition ed. by F. Kempken
XII Human Fungal Pathogens
1st edition ed. by J.E. Domer and G.S. Kobayashi
2nd edition ed. by O. Kurzai
XIII Fungal Genomics
1st edition ed. by A.J.P. Brown
2nd edition ed. by M. Nowrousian
XIV Evolution of Fungi and Fungal-Like Organisms
Ed. by S. Pöggeler and J. Wöstemeyer
XV Physiology and Genetics: Selected Basic and Applied Aspects
1st edition ed. by T. Anke and D. Weber
2nd edition ed. by T. Anke and A. Schüffler
The Mycota
A Comprehensive Treatise on Fungi as
Experimental Systems for Basic and Applied
Research
Edited by K. Esser
Biology of the Fungal Cell

VIII
Volume Editors:
3rd Edition
Dirk Hoffmeister and Markus Gressler

Series Editor
Professor Dr. Dr. h.c. mult. Karl Esser
Allgemeine Botanik
Ruhr-Universität
44780 Bochum, Germany
Tel.: +49 (234)32-22211
Fax.: +49 (234)32-14211
e-mail: Karl.Esser@rub.de
Volume Editors
Professor Dr. Dirk Hoffmeister

Friedrich-Schiller-Universität
Pharmazeutische Mikrobiologie
Winzerlaer Strasse 2
07745 Jena, Germany
Tel.: +49 (3641)949851
Fax: +49 (3641)949852
e-mail: dirk.hoffmeister@leibniz-hki.de
Dr. Markus Gressler

Friedrich-Schiller-Universität
Pharmazeutische Mikrobiologie
Winzerlaer Strasse 2
07745 Jena, Germany
Tel.: +49 (3641) 949855
e-mail: Markus.Gressler@leibniz-hki.de
ISBN 978-3-030-05446-5 ISBN 978-3-030-05448-9 (eBook)

https://doi.org/10.1007/978-3-030-05448-9
Library of Congress Control Number: 2019933208
# Springer Nature Switzerland AG 2001, 2007, 2019

This work is subject to copyright. All rights are reserved by the Publisher, whether the whole or part of the
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Karl Esser
(born 1924) is retired Professor of General Botany
and Director of the Botanical Garden at the Ruhr-
Universität Bochum (Germany). His scientific work
focused on basic research in classical and molecular
genetics in relation to practical application. His stud-
ies were carried out mostly on fungi. Together with
his collaborators he was the first to detect plasmids in
higher fungi. This has led to the integration of fungal
genetics in biotechnology. His scientific work was
distinguished by many national and international
honors, especially three honorary doctoral degrees.
Markus Gressler
(born 1984) gained a Ph.D. in biochemistry at the
Friedrich Schiller University and the Leibniz Institute
for Natural Product Research and Infection Biol-
ogy—Hans Knöll Institute (HKI) in Jena (Germany)
in 2015. From 2015 till 2017 he was a postdoctoral
fellow at Institut Pasteur, Paris, before he pursued his
research interests in 2017 at the Friedrich Schiller
University, Jena, addressing the biosynthesis and
the ecological aspects of polyketides and nonriboso-
mal peptides in fungi.
Dirk Hoffmeister
(born 1972) is a mycologist and Full Professor for
Pharmaceutical Microbiology at the Friedrich Schiller
University Jena (Germany). He is also affiliated with
the Leibniz Institute for Natural Product Research and
Infection Biology—Hans Knöll Institute (HKI). Partic-
ularly emphasizing the basidiomycetes, research in his
group is focused on the biochemical and genetic basis
underlying fungal natural product biosyntheses.
Series Preface
Mycology, the study of fungi, originated as a sub discipline of botany and was a
descriptive discipline, largely neglected as an experimental science until the early
years of this century. A seminal paper by Blakeslee in 1904 provided evidence for
self-incompatibility, termed “heterothallism,” and stimulated interest in studies
related to the control of sexual reproduction in fungi by mating-type
specificities. Soon to follow was the demonstration that sexually reproducing
fungi exhibit Mendelian inheritance and that it was possible to conduct formal
genetic analysis with fungi. The names Burgeff, Kniep and Lindegren are all
associated with this early period of fungal genetics research.
These studies and the discovery of penicillin by Fleming, who shared a Nobel
Prize in 1945, provided further impetus for experimental research with fungi.
Thus, began a period of interest in mutation induction and analysis of mutants
for biochemical traits. Such fundamental research, conducted largely with Neu-
rospora crassa, led to the one gene:one enzyme hypothesis and to a second Nobel
Prize for fungal research awarded to Beadle and Tatum in 1958. Fundamental
research in biochemical genetics was extended to other fungi, especially to
Saccharomyces cerevisiae, and by the mid-1960s fungal systems were much
favored for studies in eukaryotic molecular biology and were soon able to
compete with bacterial systems in the molecular arena.
The experimental achievements in research on the genetics and molecular
biology of fungi have benefited more generally studies in the related fields of
fungal biochemistry, plant pathology, medical mycology, and systematics. Today,
there is much interest in the genetic manipulation of fungi for applied research.
This current interest in biotechnical genetics has been augmented by the develop-
ment of DNA-mediated transformation systems in fungi and by an understanding
of gene expression and regulation at the molecular level. Applied research initia-
tives involving fungi extend broadly to areas of interest not only to industry but to
agricultural and environmental sciences as well.
It is this burgeoning interest in fungi as experimental systems for applied as
well as basic research that has prompted publication of this series of books under
the title The Mycota. This title knowingly relegates fungi into a separate realm,
distinct from that of either plants, animals, or protozoa. For consistency through-
out this series of volumes, the names adopted for major groups of fungi (repre-
sentative genera in parentheses) are as follows:
Pseudomycota
Division: Oomycota (Achlya, Phytophthora, Pythium)
Division: Hyphochytriomycota
viii Series Preface
Eumycota
Division: Chytridiomycota (Allomyces)
Division: Zygomycota (Mucor, Phycomyces, Blakeslea)
Division: Dikaryomycota
Subdivision: Ascomycotina
Class: Saccharomycetes (Saccharomyces, Schizosaccharomyces)
Class: Ascomycetes (Neurospora, Podospora, Aspergillus)
Subdivision: Basidiomycotina
Class: Heterobasidiomycetes (Ustilago, Tremella)
Class: Homobasidiomycetes (Schizophyllum, Coprinus)
We have made the decision to exclude from The Mycota the slime molds which,
although they have traditional and strong ties to mycology, truly represent
nonfungal forms insofar as they ingest nutrients by phagocytosis, lack a cell
wall during the assimilative phase, and clearly show affinities with certain proto-
zoan taxa.
The series throughout will address three basic questions: what are the fungi,
what do they do, and what is their relevance to human affairs? Such a focused and
comprehensive treatment of the fungi is long overdue in the opinion of the
editors.
A volume devoted to systematics would ordinarily have been the first to
appear in this series. However, the scope of such a volume, coupled with the
need to give serious and sustained consideration to any reclassification of major
fungal groups, has delayed early publication. We wish, however, to provide a
preamble on the nature of fungi, to acquaint readers who are unfamiliar with
fungi with certain characteristics that are representative of these organisms and
which make them attractive subjects for experimentation.
The fungi represent a heterogeneous assemblage of eukaryotic microorgan-
isms. Fungal metabolism is characteristically heterotrophic or assimilative for
organic carbon and some nonelemental source of nitrogen. Fungal cells charac-
teristically imbibe or absorb, rather than ingest, nutrients and they have rigid cell
walls. The vast majority of fungi are haploid organisms reproducing either
sexually or asexually through spores. The spore forms and details on their
method of production have been used to delineate most fungal taxa. Although
there is a multitude of spore forms, fungal spores are basically only of two types:
(1) asexual spores are formed following mitosis (mitospores) and culminate
vegetative growth, and (2) sexual spores are formed following meiosis (meios-
pores) and are borne in or upon specialized generative structures, the latter
frequently clustered in a fruit body. The vegetative forms of fungi are either
unicellular, yeasts are an example, or hyphal; the latter may be branched to
form an extensive mycelium.
Regardless of these details, it is the accessibility of spores, especially the direct
recovery of meiospores coupled with extended vegetative haploidy, that have
made fungi especially attractive as objects for experimental research.
The ability of fungi, especially the saprobic fungi, to absorb and grow on rather
simple and defined substrates and to convert these substances, not only into
essential metabolites but into important secondary metabolites, is also noteworthy.
The metabolic capacities of fungi have attracted much interest in natural products
Series Preface ix
chemistry and in the production of antibiotics and other bioactive compounds.

Fungi, especially yeasts, are important in fermentation processes. Other fungi are
important in the production of enzymes, citric acid, and other organic compounds
as well as in the fermentation of foods.
Fungi have invaded every conceivable ecological niche. Saprobic forms
abound, especially in the decay of organic debris. Pathogenic forms exist with
both plant and animal hosts. Fungi even grow on other fungi. They are found in
aquatic as well as soil environments, and their spores may pollute the air. Some
are edible; others are poisonous. Many are variously associated with plants as
copartners in the formation of lichens and mycorrhizae, as symbiotic endophytes
or as overt pathogens. Association with animal systems varies; examples include
the predaceous fungi that trap nematodes, the microfungi that grow in the
anaerobic environment of the rumen, the many insect associated fungi, and the
medically important pathogens afflicting humans. Yes, fungi are ubiquitous and
important. There are many fungi, conservative estimates are in the order of
100,000 species, and there are many ways to study them, from descriptive
accounts of organisms found in nature to laboratory experimentation at the
cellular and molecular level. All such studies expand our knowledge of fungi
and of fungal processes and improve our ability to utilize and to control fungi for
the benefit of humankind.
We have invited leading research specialists in the field of mycology to
contribute to this series. We are especially indebted and grateful for the initiative
and leadership shown by the Volume Editors in selecting topics and assembling
the experts. We have all been a bit ambitious in producing these volumes on a
timely basis and therein lies the possibility of mistakes and oversights in this first
edition. We encourage the readership to draw our attention to any error, omis-
sion, or inconsistency in this series in order that improvements can be made in
any subsequent edition.
Finally, we wish to acknowledge the willingness of Springer-Verlag to host
this project, which is envisioned to require more than 5 years of effort and the
publication of at least nine volumes.
Bochum, Germany KARL ESSER

Auburn, AL, USA PAUL A. LEMKE
April 1994 Series Editors
Volume Preface
Since the turn of the twenty-first century, an exponential amount of fungal

genomes has been sequenced and analyzed and are now available online with
open access. However, it quickly turned out that the massive collection of in
silico-generated data is not sufficient for biotechnological downstream applica-
tion processes or for an in-depth understanding of interspecies cross-talks:
The current third edition of The Mycota VIII highlights aspects of fundamen-
tal fungal cell biology. The academic view on the field of fungal cell growth—long
time denounced as a traditional but outranged field of fungal biology—has
undergone a drastic change within the last 20 years. The arising need for fungal
products necessitates the optimization of large-scale fermentation techniques
which in turn requires a detailed knowledge in fungal development, cell division,
cell wall production, and intracellular signal transduction: In food and pharma-
ceutical industries, the production of medically important fungal metabolites or
food contaminants, such as the aflatoxins, is strictly dependent on the develop-
mental stage of the producing fungi. In addition, some immune-modulating
drugs are based on large fungal cell wall polysaccharides but due to their sticki-
ness, their production is highly energy-wasting and complicated. However, phe-
notypic switches from filamentous to yeast-like growth forms ease not only the
fermentation process but also the subsequent downstream processing of the
fungal material. In sum, extended knowledge in fungal cell biology enables
defined, precise cultivation conditions and therefore highly advances the white
biotechnology in pharmaceutical and food industry.
From the ecological point of view, fungi are indispensable symbionts of most
of higher plant roots supporting each other’s growth. The tight fungus–plant
interplay not only requires a shift of the fungal cellular shape, but also an adapted
metabolism in response to defined extracellular signals. The discovery of fungal
signal transduction pathways eases the understanding of the fine-tuned metabolic
cross-flow between both symbionts and is therefore of increased interest in
agriculture.
The editors are pleased to work with an enthusiastic group of international
experts on the field of fungal cell biology who collected and combined the current
knowledge, wrote the articles, and depicted main findings in illustrated figures. The
close collaboration with the editors enabled a holistic view on fungal cell division
and development covering the two most important divisions of fungi, ascomycetes
and basidiomycetes. The volume highlights further aspects of cell–cell connections,
cell shape switches, polarized growth, and protein transport within the cells. As a
special feature, the current volume spans the divide between fungal cell growth and
signal transmission/transduction and shows its interconnectivity.
xii Volume Preface
The editors thank Steven D. Harris, Ph.D., who initiated this volume. We also
cordially thank Dr. Andrea Schlitzberger of Springer Nature for the discussion
and coordination of this current volume of The Mycota. The editors are grateful
to benefit from the profound experience of Senior Editor, Professor Emeritus Karl
Esser, and thank him for his kind and encouraging advice.
Jena, Germany Markus Gressler

November 2018 Dirk Hoffmeister
Contents
Fungal Cell Growth
The Woronin Body: A Fungal Organelle Regulating Multicellularity . . . 3

JUN-ICHI MARUYAMA, KATSUHIKO KITAMOTO
Septum Formation and Cytokinesis in Ascomycete Fungi . . . . . . . . . . . . . . 15

STEPHAN SEILER, YVONNE HEILIG
The Cytoskeleton and Polarity Markers During Polarized Growth

of Filamentous Fungi . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 43
NORIO TAKESHITA, REINHARD FISCHER
Developmental Decisions in Aspergillus nidulans . . . . . . . . . . . . . . . . . . . . . . . . . . 63

HEE-SOO PARK, MI-KYUNG LEE, KAP-HOON HAN, MIN-JU KIM, JAE-HYUK YU
Signals and Development
Biomechanics of Hyphal Growth . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 83

ROGER R. LEW
Molecular Signalling During the Ectomycorrhizal Symbiosis . . . . . . . . . . . 95

CLÉMENT PELLEGRIN, FRANCIS MARTIN, CLAIRE VENEAULT-FOURREY
Calcium Cation Cycling and Signaling Pathways in Fungi . . . . . . . . . . . . . . 111

YUANWEI ZHANG, HECHUN JIANG, LING LU
Biosystematic Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 125
Subject Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 127

List of Contributors
REINHARD FISCHER
Department of Microbiology, Institute for Applied Biosciences, Karlsruhe
Institute of Technology (KIT), Karlsruhe, Germany
KAP-HOON HAN
Department of Pharmaceutical Engineering, Woosuk University, Wanju,
Republic of Korea
YVONNE HEILIG
Institute for Biology II – Molecular Plant Physiology, Albert-Ludwigs University
Freiburg, Freiburg, Germany
HECHUN JIANG
Jiangsu Key Laboratory for Microbes and Functional Genomics, Jiangsu
Engineering and Technology Research Center for Microbiology, College of Life
Sciences, Nanjing Normal University, Nanjing, China
MIN-JU KIM
School of Food Science and Biotechnology, Institute of Agricultural Science and
Technology, Kyungpook National University, Daegu, Republic of Korea
KATSUHIKO KITAMOTO
Department of Biotechnology, The University of Tokyo, Tokyo, Japan
MI-KYUNG LEE
Biological Resource Center (BRC), Korea Research Institute of Bioscience and
Biotechnology (KRIBB), Jeongeup-si, Republic of Korea
ROGER R. LEW
Department of Biology, York University, Toronto, Canada
LING LU
xvi List of Contributors
FRANCIS MARTIN
Laboratoire d’excellence ARBRE, Centre INRA de Nancy-Lorraine, UMR INRA/
Université de Lorraine 1136 ‘Interactions Arbres/Microorganismes’,
Champenoux, France
JUN-ICHI MARUYAMA
Department of Biotechnology, The University of Tokyo, Tokyo, Japan
HEE-SOO PARK
School of Food Science and Biotechnology, Institute of Agricultural Science and
Technology, Kyungpook National University, Daegu, Republic of Korea
CLÉMENT PELLEGRIN
Champenoux, France
STEPHAN SEILER
Institute for Biology II – Molecular Plant Physiology, Albert-Ludwigs University
Freiburg Institute for Advanced Studies (FRIAS), Albert-Ludwigs University
NORIO TAKESHITA
Faculty of Life and Environmental Sciences, University of Tsukuba, Tsukuba,
Japan
CLAIRE VENEAULT-FOURREY
Champenoux, France
JAE-HYUK YU
Department of Bacteriology, University of Wisconsin, Madison, WI, USA
Department of Systems Biotechnology, Konkuk University, Seoul, Republic of
Korea
YUANWEI ZHANG
Fungal Cell Growth
The Woronin Body: A Fungal Organelle Regulating Multicellularity
JUN-ICHI MARUYAMA1, KATSUHIKO KITAMOTO1
CONTENTS Edgerton-Morgan and Oakley 2012). However,

I. Multicellularity of Filamentous Fungi . . . . . . 3 the septum does not completely separate
II. The Woronin Body, an Organelle Specific to hyphae due to the presence of a septal pore,
Pezizomycotina . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4 which is a perforated structure that allows the
III. Molecular Basis of Woronin Body exchange of the cytoplasmic constituents,
Structure . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
IV. Woronin Body Biogenesis from including organelles, between adjacent hyphal
Peroxisomes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7 cells (Lew 2005; Tey et al. 2005; Ng et al. 2009;
V. Septal Tethering of the Woronin body . . . . . . 7 Bleichrodt et al. 2015). Such cell-to-cell connec-
VI. Proteins Associated with the Woronin tivity resembles gap junctions in animal cells
Body . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10 and plasmodesmata in plant cells.
VII. Conclusions and Perspectives . . . . . . . . . . . . . . . 11
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12 Cell-to-cell connectivity through the septal
pore is associated with the catastrophic risk of
cytoplasmic loss by cells adjacent to individu-
ally damaged hyphae. This risk was demon-
I. Multicellularity of Filamentous strated by the physical damage of hyphae with
Fungi a razor blade (Trinci and Collinge 1974) or
pulse laser (Lichius et al. 2012), treatment
Filamentous fungi form straight hyphae via with cell wall-destabilizing reagents (Bowman
polarized tubular extension of the hyphal tip et al. 2002), and exposure to hypotonic shock
and consist of a network of straight primary (Fig. 1a) (Jedd and Chua 2000; Maruyama et al.
hyphae with the formation of branches. Hyphae 2005). Cell death is induced by aging and het-
are compartmentalized into distinct cells by the erokaryon incompatibility (Fleißner and Glass
formation of a septum, which is not frequently 2007). Despite such damage, the cytoplasm of
observed in early-diverging fungi, such as cells immediately adjacent to the wounded cell
members of the phyla Mucoromycota and Chy- is typically retained (Fig. 1b) (Jedd and Chua
tridiomycota, but is regularly found in later- 2000; Maruyama et al. 2005). The protected
diverging fungi belonging to the phyla Ascomy- cells then initiate regrowth of the mycelium by
cota and Basidiomycota (Jedd 2011). The sep- producing a new hyphal tip (Jedd and Chua
tum is proposed to increase the mechanical 2000; Maruyama et al. 2006; Maruyama and
integrity of hyphae and to divide the mycelium Kitamoto 2007; Lichius et al. 2012). These pro-
into sections of distinct growth states, such as cesses represent an inherent defense system for
mitotic and non-mitotic cells (Fiddy and Trinci promoting survival by preventing the simulta-
1976; Momany et al. 2002; Nayak et al. 2010; neous loss of cytoplasm from multiple cells
upon hyphal wounding. Hence, the septal pore
is an important subcellular structure for main-
taining the multicellularity of filamentous
1
Department of Biotechnology, The University of Tokyo, fungi.
Tokyo, Japan; e-mail: amarujun@mail.ecc.u-tokyo.ac.jp
Biology of the Fungal Cell, 3rd Edition

The Mycota VIII
D. Hoffmeister, M. Gressler (Eds.)
© Springer Nature Switzerland AG 2019
4 J. Maruyama and K. Kitamoto
Hypotonic
shock
1st cell 1st cell

2nd cell 2nd cell
Fig. 1 Hyphal wounding and the prevention of exces- upon hyphal wounding. The cytoplasm is labeled by
sive cytoplasmic loss. (a) Hyphal tip bursting upon expressing EGFP. An arrowhead and arrow indicate a
hypotonic shock. Hyphal tips at the margin of an A. burst hyphal tip and the adjacent septum, respectively.
oryzae colony grown on agar medium were observed by Note that the cell (2nd) adjacent to the lysed cell (1st)
differential interference contrast (DIC) microscopy retains its cytoplasmic constituents, as determined by
before and after flooding hyphae with water. Bar: DIC and fluorescence microcopy. Bar: 10 mm
50 mm. (b) Prevention of the excessive loss of cytoplasm
II. The Woronin Body, an Organelle (Markham and Collinge 1987), and Agaricomy-
Specific to Pezizomycotina cotina (Basidiomycota) have an endoplasmic
reticulum (ER)-related septal pore cap (Müller
et al. 1998). Woronin bodies were first identi-
Filamentous fungal species that form septa
fied as highly refractive particles located near
have evolved to possess specialized
the septum in the filamentous ascomycete Asco-
membrane-bound organelles located around
bolus pulcherrimus by the Russian mycologist
the septum; the Pezizomycotina (Ascomycota)
Michael Stepanovitch Woronin (Woronin
contain structures called the Woronin body
1864). The organelle was later named by Buller
The Woronin Body: A Fungal Organelle Regulating Multicellularity 5
A B
Fig. 2 Morphology of the Woronin body. (a) Transmis- image of a hexagonal Woronin body localized to the
sion electron microscopic observation of Woronin cell cortex in N. crassa. Woronin bodies are indicated
bodies (arrows) near the septum in A. oryzae. Bar: by arrows. Bar: 1 mm
500 nm. (b) Differential interference contrast (DIC)
(1933) in recognition of Woronin’s discovery are occasionally visible by light microscopy

and is restricted to Pezizomycotina species (Fig. 2b) (Markham 1994). By both electron
(Markham and Collinge 1987). The Woronin and light microscopy, Woronin bodies were
body has two morphologically distinct sub- observed to plug the septal pore upon hyphal
classes; it predominantly appears by transmis- wounding (Markham and Collinge 1987).
sion electron microscopy as a spherical Therefore, it was long suspected that the pri-
electron-dense structure near the septum mary function of Woronin bodies was the pre-
(Fig. 2a), although in a small number of spe- vention of excessive cytoplasmic loss from
cies, such as Neurospora crassa, Woronin bod- cells adjacent to damaged or lysed cells
ies form hexagonal crystalline structures that (Fig. 3a).
After hyphal
A B wounding
Normal condition
Woronin body
y
Hyphal
wounding
Fig. 3 Woronin body function. (a) Schematic represen- (right) hyphal wounding. Woronin bodies and septa
tation of the septal plugging function of Woronin bod- were labeled by DsRed2 and EGFP, respectively (Mar-
ies. (b) Confocal images of Woronin bodies (red, uyama et al. 2005). Bar: 2 mm
arrowheads) and septa (green) before (left) and after
III. Molecular Basis of Woronin Body was reported in several species, including Mag-
Structure naporthe grisea, Aspergillus oryzae, and Asper-
gillus fumigatus (Soundararajan et al. 2004;
Maruyama et al. 2005; Beck et al. 2013). Both
Although Woronin bodies were discovered
spliced and non-spliced transcripts yield two
approximately 150 years ago, the composition
polypeptides that sediment in high-density
of Woronin bodies long remained unclear. Pro-
protein fractions (Maruyama et al. 2005), sug-
tease digestion of ultrathin sections suggested
gesting that these peptides participate in the
that Woronin bodies contained proteinaceous
self-assembly and formation of the Woronin
materials (McKeen 1971; Mason and Crosse
body core matrix. Moreover, it was demon-
1975). Woronin bodies from N. crassa were
strated that a poly-histidine motif encoded
first purified in 2000 through differential and
within an alternatively spliced region targets
density gradient centrifugation, allowing for
Hex1 to the septal pore (Beck et al. 2013).
the identification of Hex1 as a major structural
Although the hexagonal crystal structure of
protein (Jedd and Chua 2000; Tenney et al.
the N. crassa Woronin body is easily observed
2000). Genes encoding Hex1 are conserved in
by light microscopy, the fusion of Hex1 with a
Pezizomycotina species (Jedd and Chua 2000;
fluorescent protein enables the septal plugging
Asiegbu et al. 2004; Curach et al. 2004; Soun-
activity of Woronin bodies to be visualized in
dararajan et al. 2004; Maruyama et al. 2005;
most Pezizomycotina species (Fig. 3b) (Mar-
Beck and Ebel 2013). Deletion of the hex1
uyama et al. 2005; Beck and Ebel 2013). Using
gene results in defective Woronin body forma-
this approach, Bleichrodt et al. (2012) reported
tion and severe cytoplasmic bleeding upon
that the Woronin body reversibly plugs the
hyphal wounding (Jedd and Chua 2000; Mar-
septal pore during normal growth, a character-
uyama et al. 2005; Beck and Ebel 2013). When
istic that contrasts the conventional view of this
the apical neighboring cell is selectively rup-
organelle functioning in wound healing. The
tured, the subapical cells reinitiate hyphal
analysis of gene expression activity for individ-
growth by producing a new branch, but dele-
ual hyphae revealed that although wild-type
tion of the hex1 gene severely reduces or
cells exhibited heterogeneous activity, cells
completely loses the activity of growth reinitia-
lacking Woronin bodies through deletion of
tion (Tegelaar and Wösten 2017).
hex1 (Dhex1 strain) displayed more uniform
Characterization of Hex1 protein revealed
gene expression activity (Bleichrodt et al.
that it spontaneously self-assembles to form a
2012). Thus, it was proposed that Woronin
solid core, thereby providing mechanical resis-
bodies contribute to the generation of hyphal
tance against the protoplasmic streaming pres-
populations with different cellular activities by
sure that is generated upon hyphal wounding
occasionally preventing cell-to-cell connectiv-
(Jedd and Chua 2000; Yuan et al. 2003). The
ity via the plugging of the septal pore. The
crystal structure of Hex1 consists of three inter-
generation of such colonial heterogeneity
molecular contacts that promote self-assembly
under normal growth conditions may protect
(Yuan et al. 2003). Interestingly, the structural
cells against environmental stresses, as evi-
properties of Hex1 resemble those of eukaryotic
denced by the sensitivity of the A. oryzae
translation initiation factor 5A (eIF5A) proteins
Dhex1 strain to heat stress (Bleichrodt et al.
(Kim et al. 1998; Peat et al. 1998), suggesting that
2012). Thus, it appears that Woronin bodies
the hex1 gene evolved from eIF-5A by gene
have a gatekeeper role in regulating cell-to-cell
duplication in the ancestor of Pezizomycotina.
channels by simple plugging of septal pore,
Phosphorylation of Hex1 also contributes to the
similar to that observed upon hyphal wounding
formation of the multimeric core of the Woro-
(Jedd and Pieuchot 2012).
nin body (Tenney et al. 2000; Juvvadi et al. 2007).
The N. crassa hex1 gene encodes a single In addition to septal plugging, Hex1 has other physio-
translational product (Jedd and Chua 2000), logical impacts at the cellular level. For example, dele-
although alternative splicing of the hex1 gene tion of the hex1 gene results in defective conidiation
(asexual spore formation) (Yuan et al. 2003; Son et al. Fam1 is specifically localized on the membrane
2013), impaired growth under nitrogen starvation of Woronin bodies, raising the possibility that
(Soundararajan et al. 2004), and increased sensitivity
to cell wall and membrane-destabilizing agents (Beck
recycling of PTS receptor occurs in Woronin
et al. 2013). In plant pathogenic fungi, Hex1 is also bodies (Kubo et al. 2015).
required for efficient pathogenesis and viral RNA accu- In addition, the budding of Woronin bodies
mulation (Soundararajan et al. 2004; Son et al. 2013). from peroxisomes appears to require dynamin-
These lines of evidence suggest additional physiological related proteins (Würtz et al. 2008). The perox-
functions of Woronin bodies, which need further inves-
tigation of the action mechanisms.
isome proliferator protein Pex11 is needed for
the differentiation of Woronin bodies from per-
oxisomes (Fig. 4b) and also affects the septal
plugging function of these organelles (Escaño
IV. Woronin Body Biogenesis from et al. 2009). The genetic screening of N. crassa
Peroxisomes mutants defective in Woronin body biogenesis
identified several peroxins and the Woronin
Electron microscopic studies examining the body sorting complex (WSC) protein that
subcellular origin of Woronin bodies demon- were critical for this process (Liu et al. 2008).
strated the inclusion of these organelles within WSC is a Pezizomycotina-specific protein that
microbodies (Wergin 1973; Camp 1977). This recruits the Hex1 assembly to the matrix side of
finding was supported by the specific binding the peroxisomal membrane and facilitates bud-
of antibodies against microbody-specific signal ding of the Woronin body (Fig. 4b) (Liu et al.
peptides to Woronin bodies (Keller et al. 1991). 2008). WSC belongs to the PMP22 (peroxisome
A relationship between peroxisomes and the membrane protein)/MPV17 (myeloprolifera-
Woronin body was clearly indicated by the tive leukemia virus 17) gene family and is pro-
finding that the C-terminus of Hex1 protein posed to have evolved to possess new
contains peroxisomal targeting signal sequence functional properties, including self-assembly
1 (PTS1) (Jedd and Chua 2000). In addition, and Hex1 binding, from ancestral PMP22
time-lapse imaging analysis revealed that Wor- (Jedd 2011).
onin bodies bud from peroxisomes (Tey et al. ApsB, a component of the microtubule-
2005). organizing center (MTOC) that has functional
Woronin body formation occurs at the peroxisomal targeting signal sequence
hyphal apex through a process involving api- 2 (PTS2), interacts with Hex1 (Zekert et al.
cally biased expression of the hex1 gene (Tey 2010). In addition, TmpL, a transmembrane
et al. 2005). Woronin body biogenesis requires protein involved in redox-related signal trans-
peroxins that mediate the import of peroxi- duction, is localized to Woronin bodies (Kim
somal matrix and membrane proteins et al. 2009). However, it is unclear how ApsB
(Fig. 4a) (Managadze et al. 2007; Liu et al. and TmpL are involved in Woronin body bio-
2008; Li et al. 2014). Specifically, Hex1 associ- genesis and function.
ates with Pex26, a peroxin that is enriched in
Woronin body-containing peroxisomes and
recruits the AAA ATPases Pex1 and Pex6 to V. Septal Tethering of the Woronin
the peroxisomal membrane for receptor recy- body
cling (Liu et al. 2011). The recruitment of
Pex26 leads to the formation of a parallel acti- In most Pezizomycotina species, Woronin bod-
vation loop for Pex5 recycling and Hex1 ies are typically tethered to the septum by a
import, allowing for the efficient biogenesis filament at a distance of 100–200 nm (Momany
of Woronin bodies. Fam1 was originally iden- et al. 2002; Maruyama et al. 2005). The tethering
tified in Colletotrichum orbiculare as a Pezizo- structure was shown to have elastic properties,
mycotina-specific ortholog of Pex22, which as demonstrated by the rapid return of the
functions in the recycling of PTS receptors Woronin bodies to the septum after physical
from peroxisomes to the cytosol (Fig. 4a). separation by laser trapping (Berns et al.
Peroxisomal
A membrane
protein
mPTS
Recognition
Recognition
Pex5
PTS1
Pex19
Oligomeric
cargo Receptor
Pex5
recycling
Pex1
Release
Cytosol Pex4 Pex6
Pex5 + 14
Pex22
Pex26
Pex14
Pex13
Pex10
Pex12
Pex2
Pex3
Peroxisomal
Matrix Pex8
Receptor
Translocation recycling
B
Self-
assembled Pex11
Peroxisome
Hex1
Woronin
WSC body
Fig. 4 Woronin body biogenesis from peroxisomes. (a) Woronin body function. PTS1 peroxisomal targeting
Schematic diagrams of the import machineries of per- signal 1, mPTS membrane peroxisome targeting signal.
oxisomal matrix and membrane proteins. Peroxins (b) Model of Woronin body biogenesis from
labeled in blue were reported to be involved in peroxisomes
1992). Moreover, Woronin bodies rapidly compartments via association with the cell cor-
insert into the septal pore upon hyphal wound- tex (Tey et al. 2005; Liu et al. 2008). During a
ing and also reversibly plug the septal pore screening for mutants that accumulate Woro-
during normal growth (Bleichrodt et al. 2012). nin bodies in the apical compartment, Ng et al.
These processes require the proper positioning (2009) identified the leashin locus, which is
of the Woronin body and sufficient flexibility of comprised of the adjacent genes lah-1 and lah-
the tethering linker. 2. The N-terminal region of LAH-1 binds to
In contrast, the Woronin bodies of a few Woronin bodies via the membrane protein
members of the genera Neurospora and Sor- WSC, whereas the C-terminal region mediates
daria are associated with the cortex in a delo- the association of Woronin bodies with the cell
calized pattern (Plamann 2009). In N. crassa, cortex (Fig. 5a) (Ng et al. 2009). In contrast,
newly synthesized Hex1 proteins are imported LAH-2, which localizes to the hyphal tip and
into peroxisomes in the apical compartment septum, is not involved in Woronin body func-
(Tey et al. 2005), and the newly formed Wor- tion (Fig. 5a). In N. crassa cells expressing an
onin bodies are then inherited into subapical LAH-1/LAH2 fusion construct, Woronin bodies
A B
WSC LAH
LAH-2
WSC Woronin
body
Woronin
body
Septum
Septum
Septal pore Septal pore

LAH-1
C Ancestral
LAH
Gene splitting
Cell cortex association in LAH-1
New promoter for LAH-2 expression
LAH-1 LAH-2
Fig. 5 Subcellular localization of Woronin bodies and tal tethering of Woronin bodies via LAH protein. (c)
tethering proteins. (a) Delocalized pattern of cortex- Illustration of the generation of two LAH proteins from
associated Woronin bodies via LAH-1 protein. (b) Sep- the ancestral LAH protein
accumulate at both sides of the septum, which Large LAH protein can be functionally
only has partial ability to prevent the excessive divided into conserved N- and C-terminal
loss of cytoplasm upon hyphal injury (Ng et al. regions and a non-conserved central region
2009). This finding indicates an additional (Beck et al. 2013; Han et al. 2014): The N-
requirement of the tethered Woronin bodies terminal region associates with Woronin bod-
for septal pore plugging. ies in a WSC-dependent manner, and the C-
Other species, such as A. fumigatus and A. terminal region containing a transmembrane
oryzae, with tethered Woronin bodies have spanning region mediates localization of LAH
large LAH proteins consisting of a single poly- to the septum (Fig. 5b) (Beck et al. 2013; Han
peptide of over 5000 amino acids (Beck et al. et al. 2014; Leonhardt et al. 2017). A truncated
2013; Han et al. 2014). LAH is required for the LAH protein consisting of only the N- and C-
tethering of Woronin bodies to the septum and terminal regions retains the ability to tether
is involved in the Woronin body function of Woronin bodies to the septum; however, the
preventing the excessive loss of cytoplasm but Woronin bodies are located closer (~50 nm)
to a lesser extent than the major Woronin body to the septum than those in wild-type cells
protein Hex1 (Han et al. 2014). This property (Han et al. 2014). This difference is roughly
may be explained by the fact that untethered consistent with the 70-nm length of the approx-
Woronin bodies are able to plug the septal pore, imately 2700-amino-acid central region of
but not as quickly as tethered ones. LAH, as was estimated based on the length
(1 mm) of the 4-mDa protein titin (Nave et al. Woronin bodies to the septum may have reduced
1989). The elasticity of the Woronin body the exchange of cytoplasm between adjacent cells, a
delocalized pattern of Woronin bodies with cortex
tether that was previously demonstrated by association may have been selected to support the
laser-capture experiments (Berns et al. 1992) rapid growth of these species.
is conferred by the central non-conserved
region of LAH (Han et al. 2014). The non-
conserved central region in LAH is predicted
to be disordered (Han et al. 2014) and presum- VI. Proteins Associated with the
ably functions as a molecular spring, similarly Woronin Body
to the muscle protein titin, which exhibits
molecular spring-like elasticity via its intrinsi- Through the purification of Woronin body-
cally disordered region (Li et al. 2001). More- associated proteins and bioinformatics
over, in cells expressing LAH protein lacking approaches for detecting proteins that contain
the central region, tethered Woronin bodies do intrinsically disordered regions, 17 septal pore-
not plug the septal pore, even after hyphal associated (SPA) proteins were identified in N.
wounding (Han et al. 2014). Collectively, effi- crassa (Lai et al. 2012). Intrinsically disordered
cient septal plugging requires not only that proteins range from partially to completely
Woronin bodies are tethered to the septum unstructured and lacking globular folds; how-
but also that the tether must have sufficient ever, these proteins are capable of folding upon
elasticity to allow for the relatively unrestricted binding to target molecules (Wright and Dyson
movement of Woronin bodies. The occasional 2009). The number of reports related to intrin-
observation that Woronin bodies from the rup- sically disordered proteins has increased signif-
tured cell side plug the septal pore suggests an icantly in recent years, and many biological
active mechanism of Woronin body movement functions of these proteins have been revealed
(Steinberg et al. 2017a). Surprisingly, ATP (Oldfield and Dunker 2014). The loss-of-func-
depletion by the respiration inhibitor carbonyl tion of several SPA proteins leads to excessive
cyanide m-chlorophenylhydrazine induces the septation, septal pore degeneration, and uncon-
translocation of Woronin bodies into the septal trolled Woronin body activation (Lai et al.
pore without cell wounding. This suggests that 2012). Spa10 protein is required for the locali-
ATP is required to prevent the septal plugging zation of LAH C-terminal region at the mature
by Woronin bodies, leading to the speculation septal pore, consequently stable tethering of
that ATP may bind to the tethering protein Woronin bodies to the septum (Leonhardt
LAH for preventing a conformational change et al. 2017). These findings suggest that the
and contraction of the protein (Steinberg et al. septal pore is a complex subcellular site for
2017b). the assembly of unstructured proteins, which
contribute to diverse states of cell-to-cell con-
The molecular origin of LAH remains elusive, but nectivity.
this protein first appeared in the clade of Pezizomy-
cotina species together with Woronin bodies (Jedd
The Pezizomycotina-specific protein SO,
2011). The ancestral lah gene encodes a single, large which was originally found in N. crassa and
polypeptide and was subsequently split into two was named based on the “soft” appearance of
genes, lah1 and lah2, in the Neurospora-Sordaria the mutant colony, is important for hyphal
clade. The lah1 gene acquired an early termination fusion and sexual reproduction (Fleißner et al.
sequence and a new cortex association domain at the
C-terminus and a new promoter controlled expres-
2005; Engh et al. 2007). SO protein consists of
sion of the downstream lah2 gene (Fig. 5c). Thus, as approximately 1200 amino acids and contains a
a result of the gene splitting of the lah gene, the single WW domain. Pro40, a Sordaria macro-
localization of the Woronin body was shifted from spora SO homolog, functions as a scaffold by
septal tethering to the cortex. N. crassa and Sordaria associating with protein kinases involved in cell
fimicola exhibit extensive cytoplasmic streaming
through septal pores (Lew 2005; Tey et al. 2005; Ng
wall integrity (Teichert et al. 2014). SO protein
et al. 2009) and have unusually rapid growth rates is dispersed throughout the cytoplasm under
(>1 mm/s) (Ryan et al. 1943). As the tethering of normal growth conditions but accumulates at
Woronin body *
SO protein
Hyphal Stress
wounding condition
Fig. 6 Accumulation of SO protein at the septal pore. body. (Right) SO also accumulates at the septal pore
SO localization was visualized by expressing as EGFP under stressed conditions. Asterisk indicates the sep-
fusion protein. (Left) Upon hyphal wounding, SO accu- tum, and the arrowhead indicates the accumulation of
mulates at the septal pore together with the Woronin SO protein at the septal pore. Bars: 5 mm
the septal pore adjacent to wounded cells Thus, SO protein may regulate cell-to-cell con-
(Fig. 6), as was reported in N. crassa and A. nectivity via the septal pore in a stress-
oryzae (Fleißner and Glass 2007; Maruyama dependent manner.
et al. 2010). S. macrospora Pro40 protein colo-
calizes with Woronin bodies (Engh et al. 2007). A study of Aspergillus nidulans revealed that mitosis
Deletion of the so gene delays septal plugging interrupts cell-to-cell connectivity through the septal
and reduces the number of hyphae that prevent pore (Shen et al. 2014). The mitotic NIMA kinase was
found to be localized to the septum during interphase
excessive cytoplasmic loss in N. crassa and A. and to contribute to keeping the septal pore open but is
oryzae (Fleißner and Glass 2007; Maruyama translocated into the nucleus to initiate mitosis, result-
et al. 2010). Taken together, these findings indi- ing in septal closure. Notably, however, the mitotic
cate that SO protein has septal plugging activity regulation of cell-to-cell connectivity is independent
by accumulating at the septal pore, similar to of Woronin bodies and SO protein. Identification of
the NIMA kinase substrate(s) may provide insight
the function of Woronin bodies. Additionally, into the molecular mechanisms underlying mitotic
SO protein accumulates at the septal pore in interruption of cell-to-cell connectivity.
aging hyphae (Fleißner and Glass 2007) and
under various stress conditions, including
low/high temperature, high acidity/alkalinity,
and nitrogen/carbon depletion (Fig. 6) (Mar- VII. Conclusions and Perspectives
uyama et al. 2010). In response to pulse laser
treatment, which physically stresses cells with- Despite the discovery of Woronin bodies over
out causing hyphal wounding, SO rapidly accu- 150 years ago, our understanding of these
mulates at the septal pore nearest to the unique fungal organelles was exclusively based
stressed hyphal area (Maruyama et al. 2010). on primitive microscopic studies conducted in
the twentieth century. However, in the past 20 Buller AHR (1933) The translocation of protoplasm
years, molecular structure and function of Wor- through septate mycelium of certain Pyrenomy-
cetes, Discomycetes and Hymenomycetes. In:
onin bodies have been largely elucidated. Geno- Researches on fungi, vol 5. Longmans, Green &
mic changes such as gene duplication and Co, London, pp 75–167
splitting generated and modified the Woronin Camp RR (1977) Association of microbodies, Woronin
body to allow for specific multicellular organiza- bodies, and septa in intercellular hyphae of Cym-
tion of individual Pezizomycotina species. adothea trifolii. Can J Bot 55:1856–1859
Curach NC, Te’o VS, Gibbs MD, Bergquist PL, Nevalai-
Although the primary function of Woronin bod- nen KM (2004) Isolation, characterization and
ies had long been thought to be wound healing, expression of the hex1 gene from Trichoderma
recent molecular studies have revealed new phys- reesei. Gene 331:133–140
iological functions of these organelles. To date, Edgerton-Morgan H, Oakley BR (2012) gamma-Tubulin
however, the molecular machineries controlling plays a key role in inactivating APC/C(Cdh1) at the
G(1)-S boundary. J Cell Biol 198:785–791
and mediating septal closure and cell repair Engh I, Würtz C, Witzel-Schlömp K, Zhang HY, Hoff B,
remain mostly unknown. Further investigations Nowrousian M, Rottensteiner H, Kück U (2007)
to functionally link Woronin bodies and related The WW domain protein PRO40 is required for
molecules in the vicinity of the septum will lead fungal fertility and associates with Woronin bod-
to a more comprehensive understanding of the ies. Eukaryot Cell 6:831–843
Escaño CS, Juvvadi PR, Jin FJ, Takahashi T, Koyama Y,
mechanisms regulating cell-to-cell connectivity Yamashita S, Maruyama J, Kitamoto K (2009) Dis-
and fungal multicellularity. ruption of the Aopex11-1 gene involved in peroxi-
some proliferation leads to impaired Woronin
body formation in Aspergillus oryzae. Eukaryot
References Cell 8:296–305
Fiddy C, Trinci AP (1976) Mitosis, septation, branching
and the duplication cycle in Aspergillus nidulans. J
Asiegbu FO, Choi W, Jeong JS, Dean RA (2004) Cloning, Gen Microbiol 97:169–184
sequencing and functional analysis of Magna- Fleißner A, Glass NL (2007) SO, a protein involved in
porthe grisea MVP1 gene, a hex-1 homolog encod- hyphal fusion in Neurospora crassa, localizes to
ing a putative “Woronin body” protein. FEMS septal plugs. Eukaryot Cell 6:84–94
Microbiol Lett 230:85–90 Fleißner A, Sarkar S, Jacobson DJ, Roca MG, Read ND,
Beck J, Ebel F (2013) Characterization of the major Glass NL (2005) The so locus is required for vege-
Woronin body protein HexA of the human patho- tative cell fusion and postfertilization events in
genic mold Aspergillus fumigatus. Int J Med Neurospora crassa. Eukaryot Cell 4:920–930
Microbiol 303:90–97 Han P, Jin FJ, Maruyama J, Kitamoto K (2014) A large
Beck J, Echtenacher B, Ebel F (2013) Woronin bodies, nonconserved region of the tethering protein Lea-
their impact on stress resistance and virulence of shin is involved in regulating the position, move-
the pathogenic mould Aspergillus fumigatus and ment, and function of Woronin bodies in
their anchoring at the septal pore of filamentous Aspergillus oryzae. Eukaryot Cell 13:866–877
Ascomycota. Mol Microbiol 89:857–871 Jedd G (2011) Fungal evo-devo: organelles and multi-
Berns MW, Aist JR, Wright WH, Liang H (1992) Optical cellular complexity. Trends Cell Biol 21:12–19
trapping in animal and fungal cells using a tun- Jedd G, Chua NH (2000) A new self-assembled peroxi-
able, near-infrared titanium-sapphire laser. Exp somal vesicle required for efficient resealing of the
Cell Res 198:375–378 plasma membrane. Nat Cell Biol 2:226–231
Bleichrodt RJ, van Veluw GJ, Recter B, Maruyama J, Jedd G, Pieuchot L (2012) Multiple modes for gatekeep-
Kitamoto K, Wösten HA (2012) Hyphal heteroge- ing at fungal cell-to-cell channels. Mol Microbiol
neity in Aspergillus oryzae is the result of dynamic 86:1291–1294
closure of septa by Woronin bodies. Mol Micro- Juvvadi PR, Maruyama J, Kitamoto K (2007) Phosphor-
biol 86:1334–1344 ylation of the Aspergillus oryzae Woronin body
Bleichrodt RJ, Hulsman M, Wösten HA, Reinders MJ protein, AoHex1, by protein kinase C: evidence
(2015) Switching from a unicellular to multicellu- for its role in the multimerization and proper
lar organization in an Aspergillus niger hypha. localization of the Woronin body protein. Bio-
MBio 6:e00111 chem J 405:533–540
Bowman JC, Scott Hicks P, Kurtz MB, Rosen H, Schmatz Keller GA, Krisans S, Gould SJ, Sommer JM, Wang CC,
DM, Liberator PA, Douglas CM (2002) The antifun- Schliebs W, Kunau W, Brody S, Subramani S (1991)
gal echinocandin caspofungin acetate kills growing Evolutionary conservation of a microbody targeting
cells of Aspergillus fumigatus in vitro. Antimicrob signal that targets proteins to peroxisomes, glyoxy-
Agents Chemother 46:3001–3012 somes, and glycosomes. J Cell Biol 114:893–904
Kim KK, Hung LW, Yokota H, Kim R, Kim SH (1998) Markham P (1994) Occlusions of septal pores in fila-
Crystal structures of eukaryotic translation initia- mentous fungi. Mycol Res 98:1089–1106
tion factor 5A from Methanococcus jannaschii at Markham P, Collinge AJ (1987) Woronin bodies of
1.8 A resolution. Proc Natl Acad Sci USA filamentous fungi. FEMS Microbiol Rev 46:1–11
95:10419–10424 Maruyama J, Kitamoto K (2007) Differential distribu-
Kim KH, Willger SD, Park SW, Puttikamonkul S, Grahl tion of the endoplasmic reticulum network in fila-
N, Cho Y, Mukhopadhyay B, Cramer RA Jr, Lawr- mentous fungi. FEMS Microbiol Lett 272:1–7
ence CB (2009) TmpL, a transmembrane protein Maruyama J, Juvvadi PR, Ishi K, Kitamoto K (2005)
required for intracellular redox homeostasis and Three-dimensional image analysis of plugging at
virulence in a plant and an animal fungal patho- the septal pore by Woronin body during hypo-
gen. PLoS Pathog 5:e1000653 tonic shock inducing hyphal tip bursting in the
Kubo Y, Fujihara N, Harata K, Neumann U, Robin GP, filamentous fungus Aspergillus oryzae. Biochem
O’Connell R (2015) Colletotrichum orbiculare Biophys Res Commun 331:1081–1088
FAM1 encodes a novel Woronin body-associated Maruyama J, Kikuchi S, Kitamoto K (2006) Differential
Pex22 peroxin required for appressorium- distribution of the endoplasmic reticulum network
mediated plant infection. MBio 6:e01305–e01315 as visualized by the BipA-EGFP fusion protein in
Lai J, Koh CH, Tjota M, Pieuchot L, Raman V, Chan- hyphal compartments across the septum of the
drababu KB, Yang D, Wong L, Jedd G (2012) filamentous fungus, Aspergillus oryzae. Fungal
Intrinsically disordered proteins aggregate at fun- Genet Biol 43:642–654
gal cell-to-cell channels and regulate intercellular Maruyama J, Escaño CS, Kitamoto K (2010) AoSO protein
connectivity. Proc Natl Acad Sci USA 109:15781– accumulates at the septal pore in response to various
15786 stresses in the filamentous fungus Aspergillus ory-
Leonhardt Y, Kakoschke SC, Wagener J, Ebel F (2017) zae. Biochem Biophys Res Commun 391:868–873
Lah is a transmembrane protein and requires Mason PJ, Crosse R (1975) Crystalline inclusions in
Spa10 for stable positioning of Woronin bodies hyphae of the glaucus group of Aspergilli. Trans
at the septal pore of Aspergillus fumigatus. Sci Br Mycol Soc 65:129–134
Rep 7:44179 McKeen WE (1971) Woronin bodies in Erysiphe grami-
Lew RR (2005) Mass flow and pressure-driven hyphal nis DC. Can J Microbiol 17:1557–1560
extension in Neurospora crassa. Microbiology Momany M, Richardson EA, Van Sickle C, Jedd G
151:2685–2692 (2002) Mapping Woronin body position in Asper-
Li H, Oberhauser AF, Redick SD, Carrion-Vazquez M, gillus nidulans. Mycologia 94:260–266
Erickson HP, Fernandez JM (2001) Multiple con- Müller WH, Montijn RC, Humbel BM, van Aelst AC,
formations of PEVK proteins detected by single- Boon EJ, van der Krift TP, Boekhout T (1998)
molecule techniques. Proc Natl Acad Sci USA Structural differences between two types of basid-
98:10682–10686 iomycete septal pore caps. Microbiology 144:1721–
Li L, Wang J, Zhang Z, Wang Y, Liu M, Jiang H, Chai R, 1730
Mao X, Qiu H, Liu F, Sun G (2014) MoPex19, Nave R, Fürst DO, Weber K (1989) Visualization of the
which is essential for maintenance of peroxisomal polarity of isolated titin molecules: a single globu-
structure and Woronin bodies, is required for lar head on a long thin rod as the M band anchor-
metabolism and development in the rice blast fun- ing domain? J Cell Biol 109:2177–2187
gus. PLoS One 9:e85252 Nayak T, Edgerton-Morgan H, Horio T, Xiong Y, De
Lichius A, Yáñez-Gutiérrez ME, Read ND, Castro- Souza CP, Osmani SA, Oakley BR (2010) Gamma-
Longoria E (2012) Comparative live-cell imaging tubulin regulates the anaphase-promoting com-
analyses of SPA-2, BUD-6 and BNI-1 in Neuros- plex/cyclosome during interphase. J Cell Biol
pora crassa reveal novel features of the filamentous 190:317–330
fungal polarisome. PLoS One 7:e30372 Ng SK, Liu F, Lai J, Low W, Jedd G (2009) A tether for
Liu F, Ng SK, Lu Y, Low W, Lai J, Jedd G (2008) Making Woronin body inheritance is associated with evo-
two organelles from one: Woronin body biogene- lutionary variation in organelle positioning. PLoS
sis by peroxisomal protein sorting. J Cell Biol Genet 5:e1000521
180:325–339 Oldfield CJ, Dunker AK (2014) Intrinsically disordered
Liu F, Lu Y, Pieuchot L, Dhavale T, Jedd G (2011) proteins and intrinsically disordered protein
Import oligomers induce positive feedback to pro- regions. Annu Rev Biochem 83:553–584
mote peroxisome differentiation and control Peat TS, Newman J, Waldo GS, Berendzen J, Terwilliger
organelle abundance. Dev Cell 21:457–468 TC (1998) Structure of translation initiation factor
Managadze D, Würtz C, Sichting M, Niehaus G, Veen- 5A from Pyrobaculum aerophilum at 1.75 A reso-
huis M, Rottensteiner H (2007) The peroxin PEX14 lution. Structure 6:1207–1214
of Neurospora crassa is essential for the biogenesis Plamann M (2009) Cytoplasmic streaming in Neuros-
of both glyoxysomes and Woronin bodies. Traffic pora: disperse the plug to increase the flow? PLoS
8:687–701 Genet 5:e1000526
Ryan FJ, Beadle GW, Tatum EL (1943) The tube method unique to filamentous fungi, encodes the major
of measuring the growth rate of Neurospora. Am J protein of the Woronin body and functions as a
Bot 30:784–799 plug for septal pores. Fungal Genet Biol 31:205–217
Shen KF, Osmani AH, Govindaraghavan M, Osmani SA Tey WK, North AJ, Reyes JL, Lu YF, Jedd G (2005)
(2014) Mitotic regulation of fungal cell-to-cell con- Polarized gene expression determines Woronin
nectivity through septal pores involves the NIMA body formation at the leading edge of the fungal
kinase. Mol Biol Cell 25:763–775 colony. Mol Biol Cell 16:2651–2659
Son M, Lee KM, Yu J, Kang M, Park JM, Kwon SJ, Kim Trinci APJ, Collinge AJ (1974) Occlusion of the septal
KH (2013) The HEX1 gene of Fusarium grami- pores of damaged hyphae of Neurospora crassa by
nearum is required for fungal asexual reproduc- hexagonal crystals. Protoplasma 80:57–67
tion and pathogenesis and for efficient viral RNA Wergin WP (1973) Development of Woronin bodies
accumulation of Fusarium graminearum virus 1. J from microbodies in Fusarium oxysporum f. sp.
Virol 87:10356–10367 lycopersici. Protoplasma 76:249–260
Soundararajan S, Jedd G, Li X, Ramos-Pamploña M, Woronin M (1864) Zur Entwicklungsgeschichte der
Chua NH, Naqvi NI (2004) Woronin body function Ascobolus pulcherrimus Cr und eigiger Pezizen.
in Magnaporthe grisea is essential for efficient Abh Senkenb Naturforsch Ges 5:333–344
pathogenesis and for survival during nitrogen Wright PE, Dyson HJ (2009) Linking folding and bind-
starvation stress. Plant Cell 6:1564–1574 ing. Curr Opin Struct Biol 19:31–38
Steinberg G, Schuster M, Hacker C, Kilaru S, Correia A Würtz C, Schliebs W, Erdmann R, Rottensteiner H
(2017a) ATP prevents Woronin bodies from seal- (2008) Dynamin-like protein-dependent forma-
ing septal pores in unwounded cells of the fungus tion of Woronin bodies in Saccharomyces cerevi-
Zymoseptoria tritici. Cell Microbiol 19:e12764 siae upon heterologous expression of a single
Steinberg G, Harmer NJ, Schuster M, Kilaru S (2017b) protein. FEBS J 275:2932–2941
Woronin body-based sealing of septal pores. Fun- Yuan P, Jedd G, Kumaran D, Swaminathan S, Shio H,
gal Genet Biol 109:53–55 Hewitt D, Chua NH, Swaminathan K (2003) A
Tegelaar M, Wösten HAB (2017) Functional distinction HEX-1 crystal lattice required for Woronin body
of hyphal compartments. Sci Rep 7:6039 function in Neurospora crassa. Nat Struct Biol
Teichert I, Steffens EK, Schnaß N, Fränzel B, Krisp C, (4):264–270
Wolters DA, Kück U (2014) PRO40 is a scaffold Zekert N, Veith D, Fischer R (2010) Interaction of the
protein of the cell wall integrity pathway, linking Aspergillus nidulans microtubule-organizing cen-
the MAP kinase module to the upstream activator ter (MTOC) component ApsB with gamma-tubulin
protein kinase C. PLoS Genet 10:e1004582 and evidence for a role of a subclass of peroxi-
Tenney K, Hunt I, Sweigard J, Pounder JI, McClain C, somes in the formation of septal MTOCs. Eukaryot
Bowman EJ, Bowman BJ (2000) Hex-1, a gene Cell 9:795–805
Septum Formation and Cytokinesis in Ascomycete Fungi
STEPHAN SEILER1,2, YVONNE HEILIG1
CONTENTS I. Introduction
I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15
II. Spatial Cues: Mechanisms Specifying the Cell division is a fundamental cellular process
Position of the Division Plane . . . . . . . . . . . . . . . 16 that is essential for proliferation of unicellular
A. Positioning the Cell Division Plane in as well as multicellular organisms. It reflects the
Unicellular Yeasts . . . . . . . . . . . . . . . . . . . . . . . . . 16
final stage of the cell cycle, during which a cell is
B. Septum Placement in Filamentous
Ascomycete Fungi . . . . . . . . . . . . . . . . . . . . . . . . . 18
physically divided into two daughter cells that
C. Signal Integration by Anillin-Type
contain a full set of chromosomes and other
Landmark Proteins . . . . . . . . . . . . . . . . . . . . . . . . 19 cellular organelles. Cytokinesis can be divided
III. Temporal Cue(s): Coordination of Cell Cycle into several general steps that apply to most
Progression and Septation Initiation . . . . . . . . 21 eukaryotic cells (Barr and Gruneberg 2007;
A. Coordination of Mitotic Exit and Initiation Eggert et al. 2006): (1) the selection of the future
of Septation in Unicellular Yeasts . . . . . . . . . 21 cell division plane based on spatial as well as
B. The Septation Initiation Network in the temporal cues, (2) the assembly of a cortical
Pezizomycotina Fungi . . . . . . . . . . . . . . . . . . . . . 23 actomyosin ring (CAR) at this site, and (3) its
C. Coordination of Nuclear Behavior and constriction coupled with membrane invagi-
Septum Formation in Pezizomycotina nation. In general, the formation of the CAR
Fungi . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 24
and its subsequent constriction is tightly cou-
IV. Assembly and Regulation of the Contractile
Actomyosin Ring (CAR) . . . . . . . . . . . . . . . . . . . . . 26
pled to the cell cycle to ensure that cell separ-
A. CAR Assembly in Budding and Fission
ation does not occur prior to chromosome
Yeast . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 26 segregation. (4) The formation of an extra-
B. CAR Assembly in the Pezizomycotina . . . . . 27 cellular cell wall, the septum, composed of glu-
C. Crosstalk Between the SIN and the MOR cans, chitin, and other polysaccharides in fungi
Pathways for CAR Regulation . . . . . . . . . . . . . 28 further requires coordination of CAR constric-
V. Cell Wall Biogenesis and Cell Division . . . . . . 29 tion with secretion of cell wall biosynthetic and
A. Cell Wall Biogenesis . . . . . . . . . . . . . . . . . . . . . . . 29 remodeling enzymes to build the extracellular
B. Septum Formation and Cell Division During septum. (5) This primary septum is covered by
Fungal Development . . . . . . . . . . . . . . . . . . . . . . 30 additional layers of cell wall material that form
C. Septal Pore-Associated Functions in the secondary septum and is finally degraded
Filamentous Ascomycete Fungi . . . . . . . . . . . 32 by secreted hydrolytic enzymes in the uni-
VI. Conclusions and Perspectives . . . . . . . . . . . . . . . 33 cellular yeasts and during sexual development of
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 33 filament-forming molds to allow detachment of
the two cells.
1
Institute for Biology II – Molecular Plant Physiology, Albert- Several overviews have recently summar-
Ludwigs University Freiburg, Freiburg, Germany; e-mail: Ste- ized the mechanistic principles underlying cell
phan.Seiler@biologie.uni-freiburg.de; polarization and division in budding yeast and
2
Freiburg Institute for Advanced Studies (FRIAS), Albert-Lud- fission yeast, two unicellular fungi that consis-
wigs University Freiburg, Freiburg, Germany
Biology of the Fungal Cell, 3rd Edition

The Mycota VIII
D. Hoffmeister, M. Gressler (Eds.)
© Springer Nature Switzerland AG 2019
16 S. Seiler and Y. Heilig
tently serve as conceptual framework for the the Schizosaccharomycetes and other early
analysis of fungal as well as higher eukaryotic diverging lineages and is primarily represented
cell biology (Pollard and Wu 2010; Bi and Park by Schizosacchomyces pombe. The monophy-
2012; Weiss 2012; Martin and Arkowitz 2014). letic origin of this subphylum is still under
However, the vast majority of fungi forms debate, but most recent data support the mono-
mycelial colonies that consist of networks of phyly of the taxon (James et al. 2006). Both
branched hyphe. These cells grow by tip growth filaments and yeasts are found in this subphy-
and are compartmentalized by septum that par- lum, suggesting that both morphologies are
tition cellular environments within the hypha. ancestral in Ascomycota.
In contrast to the unicellular yeasts, not every Despite the importance of septum for
nuclear division triggers the formation of a new hyphae, proliferation, and differentiation in fil-
septum in mycelial fungi, and thus hyphal com- amentous fungi, our understanding of septum
partments are generally multinucleate. More- formation and its regulation is highly fragmen-
over, a small septal pore is retained in higher tary (Harris 2001; Seiler and Justa-Schuch 2010;
fungi to enable intercellular communication Mourino-Perez and Riquelme 2013). In this
and transport of cytoplasm and organelles review, we will focus on recent progress that
between adjacent hyphal compartments. This confirms the use of conserved molecular mod-
controlled segmentation of hyphal units ules during cell division in the unicellular
through septal cross walls in a multicellular yeasts and during septum formation in the fila-
mycelium is the basis for the morphological mentous fungi. However, it is also becoming
complexity achieved by the fungi during vege- apparent that proper placement and regulated
tative growth, differentiation, and infection formation and function of septa in the different
processes and is thus a prerequisite for the phylogenetic groups of Ascomycota requires
evolutionary success of the fungal kingdom significant rewiring and species-specific adap-
(Gull 1978; Pringle and Taylor 2002; Blackwell tation of these conserved modules (Gu et al.
2011). 2015).
The phylum Ascomycota comprises three
major subphyla: Taphrinomycotina, Saccharo-
mycotina, and Pezizomycotina (McLaughlin
et al. 2009; Stajich et al. 2009). The subphylum II. Spatial Cues: Mechanisms
of the Pezizomycotina contains over 90% of the Specifying the Position of the
Ascomycota species. Almost all species of this Division Plane
clade generate multinuclear hyphae that are
compartmentalized by septa and include the A. Positioning the Cell Division Plane in
model molds Aspergillus nidulans and Neuro- Unicellular Yeasts
spora crassa. The Saccharomycotina contain the
industrial yeasts and parasitic Canidida spec. The regulatory pathways that control the spatial
species, dimorphic fungi that can switch aspects to place the future cell division plane
between yeast and mycelial states (Sudbery are poorly conserved among different eukary-
2011). Most members of the Saccharomycotina otic organisms despite the high importance of a
are unicellular, but this group also includes fila- tight coordination of cytokinesis with chromo-
mentous forms, such as Ashbya gossypii. This some and organelle segregation. For example,
species is very closely related to Saccharomyces the two model yeasts S. cerevisiae and S. pombe
cerevisiae, and more than 90% of the genes are have developed fundamentally distinct
highly conserved in the two fungi (Dietrich et al. mechanisms to control the spatial aspects for
2004; Wendland and Walther 2005), but the two placing the future cell division plane (Fig. 1a,
species have developed dramatically different b). The bud-site selection system of budding
growth forms: constitutive multinucleate tip yeast relies on cortical cues of the previous
growth in A. gossypii versus unicellular growth cell division cycle in order to redirect the divid-
in S. cerevisiae. The third subphylum includes ing nucleus to the bud neck, while the position
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134.2 Rev. P. Dehon, S.J., “Religion and Customs of the Uraons,”
Memoirs of the Asiatic Society of Bengal, vol. i. No. 9 (Calcutta,
1906), pp. 139 sq.
134.3 Lieut.-Colonel H. W. G. Cole, “The Lushais,” in Census of
India, 1911, vol. iii. Assam, Part I. (Shillong, 1912) p. 140.

135.1 Mrs. Leslie Milne, Shans at Home (London, 1910), p. 96. The
custom of carrying the dead out of the house by a special opening,

which is then blocked up to prevent the return of the ghost, has been
observed by many peoples in many parts of the world. For examples
see The Belief in Immortality and the Worship of the Dead, i. 452
sqq.
136.1 Ch. Gilhodes, “Naissance et Enfance chez les Katchins
(Birmanie),” Anthropos, vi. (1911) pp. 872 sq.
136.2 Van Schmidt, “Aanteekeningen nopens de zeden, etc., der
bevolking van de eilanden Saparoea, etc.,” Tijdschrift voor
Neêrlands Indie, v. Tweede Deel (Batavia, 1843), pp. 528 sqq.; G.
Heijmering, “Zeden en gewoonten op het eiland Timor,” Tijdschrift
voor Neerlands Indië, vii. Negende Aflevering (Batavia, 1845), pp.
278 sq., note; B. F. Matthes, Bijdragen tot de Ethnologie van Zuid-
Celebes (The Hague, 1875), p. 97; W. E. Maxwell, “Folk-lore of the
Malays,” Journal of the Straits Branch of the Royal Asiatic Society,
No. 7 (June 1881), p. 28; W. W. Skeat, Malay Magic (London, 1900),
p. 325; J. G. F. Riedel, De sluik- en kroesharige rassen tusschen
Selebes en Papua (The Hague, 1886), p. 81; B. C. A. J. van Dinter,
“Eenige geographische en ethnographische aanteekeningen
betreffende het eiland Siaoe,” Tijdschrift voor Indische Taal- Land-
en Volkenkunde, xli. (1899) p. 381; A. C. Kruijt, “Eenige
ethnografische aanteekeningen omtrent de Toboengkoe en de
Tomori,” Mededeelingen van wege het Nederlandsche
Zendelinggenootschap, xliv. (Rotterdam, 1900) p. 218; id., Het
Animisme in den Indischen Archipel (The Hague, 1906), p. 252; G.
A. Wilken, Handleiding voor de vergelijkende Volkenkunde van
Nederlandsch-Indië (Leyden, 1893), p. 559; J. H. Meerwaldt,
“Gebruiken der Bataks in het maatschappelijk leven,”
Mededeelingen van wege het Nederlandsche
Zendelineggnootschap, xlix. (1905) p. 113. The common name for
these dreaded ghosts is pontianak. For a full account of them see A.
C. Kruijt, Het Animisme in den Indischen Archipel, pp. 245 sqq.
137.1 J. Perham, “Sea Dyak Religion,” Journal of the Straits Branch
of the Royal Asiatic Society, No. 14 (Singapore, 1885), pp. 291 sq.
137.2 W. W. Skeat and C. O. Blagden, Pagan Races of the Malay
Peninsula (London, 1906), ii. 109.

137.3 T. de Pauly, Description ethnographique des peuples de la
Russie (St. Petersburg, 1862), Peuples ouralo-altaïques, p. 71.
137.4 A. W. Howitt, Native Tribes of South-East Australia (London,
1904), p. 474.
137.5 A. W. Howitt, op. cit. p. 473.
137.6 H. Zimmer, Altindisches Leben (Berlin, 1879), p. 402.
138.1 Rev. Father Julius Jetté, “On the Superstitions of the Ten’a
Indians,” Anthropos, vi. (1911) p. 707.

138.2 T. de Pauly, Description ethnographique des peuples de la
Russie (St. Petersburg, 1862), Peuples ouralo-altaïques, p. 71.

138.3 (Sir) H. H. Risley, The Tribes and Castes of Bengal,
Ethnographic Glossary, ii. (Calcutta, 1891) pp. 75 sq. Compare E. T.

Atkinson, The Himalayan Districts of the North-Western Provinces of
India, ii. (Allahabad, 1884) p. 832; W. Crooke, Popular Religion and
Folk-lore of Northern India (Westminster, 1896), ii. 57.
139.1 Rev. G. Whitehead, “Notes on the Chins of Burma,” Indian
Antiquary, xxxvi. (1907) pp. 214 sq.
139.2 Relations des Jésuites, 1639, p. 44 (Canadian reprint,
Quebec, 1858).
140.1 Rev. Peter Jones, History of the Ojebway Indians (London,
N.D.), pp. 99 sq.

141.1 “Sitten und Gebräuche der Lengua-Indianer, nach
Missionsberichten von G. Kurze,” Mitteilungen der geographischen
Gesellschaft zu Jena, xxiii. (1905) pp. 17 sq., 19 sq., 21 sq. The
Cross River natives of Southern Nigeria, like the Lengua Indians, cut
off the diseased members of a corpse, in the belief that if they did
not do so the person would suffer from the same disease at his next
reincarnation. See Charles Partridge, Cross River Natives (London,
1905), pp. 238 sq.
142.1 Charles A. Sherring, Western Tibet and the British Borderland
(London, 1906), pp. 127-132.
142.2 Lieutenant Herold, “Bericht betreffend religiöse
Anschauungen und Gebräuche der deutschen Ewe-Neger,”
Mitteilungen von Forschungsreisenden und Gelehrten aus den
deutschen Schutzgebieten, v. Heft 4 (Berlin, 1892), p. 155; H. Klose,
Togo unter deutscher Flagge (Berlin, 1899), p. 274.
143.1 Franz Boas, in Sixth Report on the North-Western Tribes of
Canada, p. 92 (Report of the British Association for the
Advancement of Science, Leeds, 1890, separate reprint).
143.2 Franz Boas, in Tenth Report on the North-Western Tribes of
Canada, p. 45 (Report of the British Association for the
Advancement of Science, Ipswich, 1895, separate reprint).
144.1 Franz Boas, in Sixth Report on the North-Western Tribes of
Canada, pp. 23 sq. (Report of the British Association for the
Advancement of Science, Leeds, 1890, separate reprint).
144.2 Franz Boas, in Seventh Report on the North-Western Tribes
of Canada, p. 13 (Report of the British Association for the
Advancement of Science, Cardiff, 1891, separate reprint).
145.1 James Teit, “The Thompson Indians of British Columbia,” pp.
332 sq. (The Jesup North Pacific Expedition, Memoir of the

American Museum of Natural History, April, 1900).
146.1 James Teit, “The Lillooet Indians” (Leyden and New York,
1906), p. 271 (The Jesup North Pacific Expedition, Memoir of the

American Museum of Natural History).
147.1 Franz Boas, in Fifth Report on the North-Western Tribes of
Canada, pp. 43 sq. (Report of the British Association for the

Advancement of Science, Newcastle-upon-Tyne, 1889, separate
reprint).
148.1 Father Guis (de la Congrégation du Sacré-Cœur d’Issoudun,
Missionnaire en Nouvelle-Guinée), “Les Canaques, mort-deuil,” Les
Missions catholiques, xxxiv. (Lyons, 1902) pp. 208 sq.
149.1 Elsewhere I have illustrated the fear of the dead as it is
displayed in funeral customs (“On certain Burial Customs as
illustrative of the Primitive Theory of the Soul,” Journal of the
Anthropological Institute, xv. (1886) pp. 64 sqq.).
150.1 J. J. M. de Groot, The Religious System of China, iv. (Leyden,
1901) pp. 436 sqq., especially pp. 450, 464.
150.2 J. J. M. de Groot, The Religious System of China, iv. 450 sq.
151.1 J. J. M. de Groot, The Religious System of China, iv. 457-
460.
151.2 The Greek orator Antiphon observes that the presence of a
homicide pollutes the whole city and brings the curse of barrenness
on the land (Antiphon, ed. F. Blass, Leipsic, 1871, pp. 13, 15, 30).
See further L. R. Farnell, The Evolution of Religion (London, 1905),
pp. 139 sqq.
Chapter VI Notes
156.1 Lucian, Hermotimus, 64, κατὰ τοὺς Ἀρεοπαγίτας αὐτὸ
ποιοῦντα, οἳ ἐν νυκτὶ καὶ σκότῳ δικάζουσιν, ὡς μὴ ἐς τοὺς λέγοντας,
ἀλλ᾽ ἐς τὰ λεγόμενα ἀποβλέποιεν: id., De domo, 18, εἰ μὴ τύχοι τις
παντελῶς τυφλὸς ὢν ἢ ἐν νυκτὶ ὥσπερ ἡ ἐξ Ἀρείου πάγου βουλὴ
ποιοῖτο τὴν ἀκρόασιν.
The Scope of Social Anthropology Notes
166.1 This happened at Ballyvadlea, in the county of Tipperary, in
March 1895. For details of the evidence given at the trial of the
murderers, see “The ‘Witch-burning’ at Clonmel,” Folk-lore, vi. (1895)
pp. 373-384.
166.2 This happened at Norwich in June 1902. See The People’s
Weekly Journal for Norfolk, July 19, 1902, p. 8.

167.1 I say “an enlightened minority,” because in any large
community there are always many minorities, and some of them are
very far from enlightened. It is possible to be below as well as above
the average level of our fellows.
170.1 E. Renan et M. Berthelot, Correspondance (Paris, 1898), pp.
75 sq.
173.1 J. Boswell, Life of Samuel Johnson9 (London, 1822), iv. 315.
174.1
“In boundless oceans, never to be passed

By navigators uninform’d as they,
Or plough’d perhaps by British bark again.”
The Task, book i. 629 sqq.
TRANSCRIBER’S NOTES
Page numbers are given in {curly} brackets.
Plain text version only: endnote markers and sidenotes are given
in [square] brackets, with the latter prefixed with “Sidenote:”.
Minor spelling inconsistencies (e.g. blood-covenant/blood
covenant, childbed/child-bed, etc.) are preserved.
Alterations to the text:
Convert footnotes to endnotes, relabel note markers (append the
original note number to the page number), and add a corresponding
entry to the TOC.
[Chapter IV]
Change “The Blu- u Kayans, another tribe in the interior of Borneo”
to Blu-u.
(‘Give me,’ said Cairbre’s druid, that Corc there…) add left single
quotation mark before that.
[Chapter V]
(In China respect for human life in enforced by fear of ghosts.) to
is.
[Endnotes]
Fix a few missing periods.
(p. 46, note 3) “Tijdschrift van het Nederlandsch Aaardrijkskundig”
to Aardrijkskundig.
[End of text]
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Biology of the Fungal Cell Dirk

Biochemistry and Molecular Biology 3rd Edition Dirk

Developments in Fungal Biology and Applied Mycology 1st

Essential Cell Biology Fifth Edition Alberts

Cell Biology of Herpes Viruses 1st Edition Klaus

Neural cell biology 1st Edition Cheng Wang

BRS Cell Biology Histology Leslie P. Gartner

Essential Cell Biology 5th Edition Bruce Alberts

Essential Cell Biology 5th Edition Bruce Alberts

Biology of the Fungal Cell

I Growth, Differentiation and Sexuality

Biology of the Fungal Cell

Dirk Hoffmeister and Markus Gressler

Professor Dr. Dirk Hoffmeister

Dr. Markus Gressler

ISBN 978-3-030-05446-5 ISBN 978-3-030-05448-9 (eBook)

Library of Congress Control Number: 2019933208

# Springer Nature Switzerland AG 2001, 2007, 2019

chemistry and in the production of antibiotics and other bioactive compounds.

Bochum, Germany KARL ESSER

Since the turn of the twenty-first century, an exponential amount of fungal

Jena, Germany Markus Gressler

Fungal Cell Growth

The Woronin Body: A Fungal Organelle Regulating Multicellularity . . . 3

Septum Formation and Cytokinesis in Ascomycete Fungi . . . . . . . . . . . . . . 15

The Cytoskeleton and Polarity Markers During Polarized Growth

Developmental Decisions in Aspergillus nidulans . . . . . . . . . . . . . . . . . . . . . . . . . . 63

Signals and Development

Biomechanics of Hyphal Growth . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 83

Molecular Signalling During the Ectomycorrhizal Symbiosis . . . . . . . . . . . 95

Calcium Cation Cycling and Signaling Pathways in Fungi . . . . . . . . . . . . . . 111

Biosystematic Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 125

Subject Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 127

JUN-ICHI MARUYAMA1, KATSUHIKO KITAMOTO1

CONTENTS Edgerton-Morgan and Oakley 2012). However,

Biology of the Fungal Cell, 3rd Edition

1st cell 1st cell

(1933) in recognition of Woronin’s discovery are occasionally visible by light microscopy

Septal pore Septal pore

STEPHAN SEILER1,2, YVONNE HEILIG1

Biology of the Fungal Cell, 3rd Edition

India, 1911, vol. iii. Assam, Part I. (Shillong, 1912) p. 140.

custom of carrying the dead out of the house by a special opening,

Peninsula (London, 1906), ii. 109.

Indians,” Anthropos, vi. (1911) p. 707.

Russie (St. Petersburg, 1862), Peuples ouralo-altaïques, p. 71.

Ethnographic Glossary, ii. (Calcutta, 1891) pp. 75 sq. Compare E. T.

N.D.), pp. 99 sq.

332 sq. (The Jesup North Pacific Expedition, Memoir of the

1906), p. 271 (The Jesup North Pacific Expedition, Memoir of the

Canada, pp. 43 sq. (Report of the British Association for the

Weekly Journal for Norfolk, July 19, 1902, p. 8.

“In boundless oceans, never to be passed

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