%% Papers Published
@article{fds161166,
Author = {J. R. Buchler and N. E. Buchler},
Title = {BL Herculis model pulsations; III. Livermore
opacities},
Volume = {285},
Pages = {213-219},
Year = {1994},
Key = {fds161166}
}
@article{Buchler97,
Author = {Buchler, NEG and Zuiderweg, ERP and Wang, H and Goldstein,
RA},
Title = {Protein Heteronuclear NMR Assignments Using Mean-Field
Simulated Annealing},
Journal = {Journal of Magnetic Resonance},
Volume = {125},
Number = {1},
Pages = {34-42},
Organization = {Biophysics Research Division, University of Michigan, Ann
Arbor 48109-1055, USA.},
Institution = {Biophysics Research Division, University of Michigan, Ann
Arbor 48109-1055, USA.},
Year = {1997},
Keywords = {Computer Simulation Magnetic Resonance Spectroscopy/*methods
Molecular Weight Proteins/*chemistry},
Abstract = {A computational method for the assignment of the NMR spectra
of larger (21 kDa) proteins using a set of six of the most
sensitive heteronuclear multidimensional nuclear magnetic
resonance experiments is described. Connectivity data
obtained from HNCα, HN (CO) Cα, HN (Cα)Hα, and
Hα(CαCO)NH and spin-system identification data obtained
from CP-(H)CCH-TOCSY and CP-(H)C(CαCO)NH-TOCSY were used to
perform sequence-specific assignments using a mean-field
formalism and simulated annealing. This mean-field method
reports the resonance assignments in a probabilistic
fashion, displaying the certainty of assignments in an
unambiguous and quantitative manner. This technique was
applied to the NMR data of the 172-residue peptide-binding
domain of the E. coli heat-shock protein, DnaK. The method
is demonstrated to be robust to significant amounts of
missing, spurious, noisy, extraneous, and erroneous data. ©
1997 Academic Press.},
Key = {Buchler97}
}
@article{Buchler99,
Author = {Buchler, NEG and Goldstein, RA},
Title = {Effect of alphabet size and foldability requirements on
protein structure designability},
Journal = {Proteins: Structure, Function and Bioinformatics},
Volume = {34},
Number = {1},
Pages = {113-124},
Organization = {Biophysics Research Division, Ann Arbor, Michigan,
USA.},
Institution = {Biophysics Research Division, Ann Arbor, Michigan,
USA.},
Year = {1999},
ISSN = {0887-3585},
url = {http://dx.doi.org/10.1002/(SICI)1097-0134(19990101)34:1<113::AID-PROT9>3.0.CO;},
Keywords = {Amino Acids/*chemistry Kinetics *Models, Statistical Normal
Distribution Protein Conformation *Protein
Folding},
Abstract = {A number of investigators have addressed the issue of why
certain protein structures are especially common by
considering structure designability, defined as the number
of sequences that would successfully fold into any
particular native structure. One such approach, based on
foldability, suggested that structures could be classified
according to their maximum possible foldability and that
this optimal foldability would be highly correlated with
structure designability. Other approaches have focused on
computing the designability of lattice proteins written with
reduced two- letter amino acid alphabets. These different
approaches suggested contrasting characteristics of the most
designable structures. This report compares the
designability of lattice proteins over a wide range of amino
acid alphabets and foldability requirements. While all
alphabets have a wide distribution of protein
designabilities, the form of the distribution depends on how
protein 'viability' is defined. Furthermore, under
increasing foldability requirements, the change in
designabilities for all alphabets are in good agreement with
the previous conclusions of the foldability approach. Most
importantly, it was noticed that those structures that were
highly designable for the two-letter amino acid alphabets
are not especially designable with higher-letter
alphabets.},
Doi = {10.1002/(SICI)1097-0134(19990101)34:1<113::AID-PROT9>3.0.CO;},
Key = {Buchler99}
}
@article{fds228191,
Author = {Buchler, NEG and Goldstein, RA},
Title = {Universal correlation between energy gap and foldability for
the random energy model and lattice proteins},
Journal = {Journal of Chemical Physics},
Volume = {111},
Number = {14},
Pages = {6599-6609},
Year = {1999},
Abstract = {The random energy model, originally used to analyze the
physics of spin glasses, has been employed to explore what
makes a protein a good folder versus a bad folder. In
earlier work, the ratio of the folding temperature over the
glass-transition temperature was related to a statistical
measure of protein energy landscapes denoted as the
foldability F. It was posited and subsequently established
by simulation that good folders had larger foldabilities, on
average, than bad folders. An alternative hypothesis,
equally verified by protein folding simulations, was that it
is the energy gap Δ between the native state and the next
highest energy that distinguishes good folders from bad
folders. This duality of measures has led to some
controversy and confusion with little done to reconcile the
two. In this paper, we revisit the random energy model to
derive the statistical distributions of the various energy
gaps and foldability. The resulting joint distribution
allows us to explicitly demonstrate the positive correlation
between foldability and energy gap. In addition, we compare
the results of this analytical theory with a variety of
lattice models. Our simulations indicate that both the
individual distributions and the joint distribution of
foldability and energy gap agree qualitatively well with the
random energy model. It is argued that the universal
distribution of and the positive correlation between
foldability and energy gap, both in lattice proteins and the
random energy model, is simply a stochastic consequence of
the "thermodynamic hypothesis." © 1999 American Institute
of Physics.},
Key = {fds228191}
}
@article{fds228192,
Author = {Buchler, NEG and Goldstein, RA},
Title = {Surveying determinants of protein structure designability
across different energy models and amino-acid alphabets: A
consensus},
Journal = {Journal of Chemical Physics},
Volume = {112},
Number = {5},
Pages = {2533-2547},
Year = {2000},
Abstract = {A variety of analytical and computational models have been
proposed to answer the question of why some protein
structures are more "designable" (i.e., have more sequences
folding into them) than others. One class of analytical and
statistical-mechanical models has approached the
designability problem from a thermodynamic viewpoint. These
models highlighted specific structural features important
for increased designability. Furthermore, designability was
shown to be inherently related to thermodynamically relevant
energetic measures of protein folding, such as the
foldability ℱ and energy gap Δ10. However, many of these
models have been done within a very narrow focus: Namely,
pair-contact interactions and two-letter amino-acid
alphabets. Recently, two-letter amino-acid alphabets for
pair-contact models have been shown to contain designability
artifacts which disappear for larger-letter amino-acid
alphabets. In addition, a solvation model was demonstrated
to give identical designability results to previous
two-letter amino-acid alphabet pair-contact models. In light
of these discordant results, this report synthesizes a broad
consensus regarding the relationship between specific
structural features, foldability ℱ, energy gap Δ10, and
structure designability for different energy models
(pair-contact vs solvation) across a wide range of
amino-acid alphabets. We also propose a novel measure Zkd
which is shown to be well correlated to designability.
Finally, we conclusively demonstrate that two-letter
amino-acid alphabets for pair-contact models appear to be
solvation models in disguise. © 2000 American Institute of
Physics.},
Key = {fds228192}
}
@article{Buchler03,
Author = {Buchler, NE and Gerland, U and Hwa, T},
Title = {On schemes of combinatorial transcription
logic},
Journal = {Proceedings of the National Academy of Sciences of the
United States of America},
Volume = {100},
Number = {9},
Pages = {5136-5141},
Organization = {Department of Physics and Center for Theoretical Biological
Physics, University of California at San Diego, La Jolla, CA
92093-0319, USA.},
Institution = {Department of Physics and Center for Theoretical Biological
Physics, University of California at San Diego, La Jolla, CA
92093-0319, USA.},
Year = {2003},
url = {http://dx.doi.org/10.1073/pnas.0930314100},
Keywords = {Bacteria/genetics Models, Genetic *Transcription,
Genetic},
Abstract = {Cells receive a wide variety of cellular and environmental
signals, which are often processed combinatorially to
generate specific genetic responses. Here we explore
theoretically the potentials and limitations of
combinatorial signal integration at the level of
cis-regulatory transcription control. Our analysis suggests
that many complex transcription-control functions of the
type encountered in higher eukaryotes are already
implementable within the much simpler bacterial
transcription system. Using a quantitative model of
bacterial transcription and invoking only specific
protein-DNA interaction and weak glue-like interaction
between regulatory proteins, we show explicit schemes to
implement regulatory logic functions of increasing
complexity by appropriately selecting the strengths and
arranging the relative positions of the relevant
protein-binding DNA sequences in the cis-regulatory region.
The architectures that emerge are naturally modular and
evolvable. Our results suggest that the transcription
regulatory apparatus is a "programmable" computing machine,
belonging formally to the class of Boltzmann machines.
Crucial to our results is the ability to regulate gene
expression at a distance. In bacteria, this can be achieved
for isolated genes via DNA looping controlled by the
dimerization of DNA-bound proteins. However, if adopted
extensively in the genome, long-distance interaction can
cause unintentional intergenic cross talk, a detrimental
side effect difficult to overcome by the known bacterial
transcription-regulation systems. This may be a key factor
limiting the genome-wide adoption of complex transcription
control in bacteria. Implications of our findings for
combinatorial transcription control in eukaryotes are
discussed.},
Doi = {10.1073/pnas.0930314100},
Key = {Buchler03}
}
@article{Bintu05,
Author = {Bintu, L and Buchler, NE and Garcia, HG and Gerland, U and Hwa, T and Kondev, J and Kuhlman, T and Phillips, R},
Title = {Transcriptional regulation by the numbers:
Applications},
Journal = {Current Opinion in Genetics and Development},
Volume = {15},
Number = {2},
Pages = {125-135},
Organization = {Physics Department, Brandeis University, Waltham, MA 02454,
USA.},
Institution = {Physics Department, Brandeis University, Waltham, MA 02454,
USA.},
Year = {2005},
url = {http://dx.doi.org/10.1016/j.gde.2005.02.006},
Keywords = {Animals Bacteria/genetics DNA/chemistry *Gene Expression
Regulation Humans *Models, Theoretical Promoter Regions,
Genetic/genetics Quantitative Trait Loci *Thermodynamics
*Transcription, Genetic Transcriptional Activation},
Abstract = {With the increasing amount of experimental data on gene
expression and regulation, there is a growing need for
quantitative models to describe the data and relate them to
their respective context. Thermodynamic models provide a
useful framework for the quantitative analysis of bacterial
transcription regulation. This framework can facilitate the
quantification of vastly different forms of gene expression
from several well-characterized bacterial promoters that are
regulated by one or two species of transcription factors; it
is useful because it requires only a few parameters. As
such, it provides a compact description useful for
higher-level studies (e.g. of genetic networks) without the
need to invoke the biochemical details of every component.
Moreover, it can be used to generate hypotheses on the
likely mechanisms of transcriptional control. © 2005
Elsevier Ltd. All rights reserved.},
Doi = {10.1016/j.gde.2005.02.006},
Key = {Bintu05}
}
@article{Buchler05,
Author = {Buchler, NE and Gerland, U and Hwa, T},
Title = {Nonlinear protein degradation and the function of genetic
circuits},
Journal = {Proceedings of the National Academy of Sciences of the
United States of America},
Volume = {102},
Number = {27},
Pages = {9559-9564},
Organization = {Center for Studies in Physics and Biology, The Rockefeller
University, New York, NY 10021, USA. buchler@rockefeller.edu},
Institution = {Center for Studies in Physics and Biology, The Rockefeller
University, New York, NY 10021, USA. buchler@rockefeller.edu},
Year = {2005},
url = {http://dx.doi.org/10.1073/pnas.0409553102},
Keywords = {Bacteria/genetics *Gene Expression Regulation *Models,
Biological Multiprotein Complexes/*metabolism Protein
Engineering/methods Protein Subunits/*metabolism
Proteins/*metabolism Transcription Factors/metabolism},
Abstract = {The functions of most genetic circuits require a sufficient
degree of cooperativity in the circuit components. Although
mechanisms of cooperativity have been studied most
extensively in the context of transcriptional initiation
control, cooperativity from other processes involved in the
operation of the circuits can also play important roles. In
this work, we examine a simple kinetic source of
cooperativity stemming from the nonlinear degradation of
multimeric proteins. Ample experimental evidence suggests
that protein subunits can degrade less rapidly when
associated in multimeric complexes, an effect we refer to as
"cooperative stability." For dimeric transcription factors,
this effect leads to a concentration-dependence in the
degradation rate because monomers, which are predominant at
low concentrations, will be more rapidly degraded. Thus,
cooperative stability can effectively widen the accessible
range of protein levels in vivo. Through theoretical
analysis of two exemplary genetic circuits in bacteria, we
show that such an increased range is important for the
robust operation of genetic circuits as well as their
evolvability. Our calculations demonstrate that a few-fold
difference between the degradation rate of monomers and
dimers can already enhance the function of these circuits
substantially. We discuss molecular mechanisms of
cooperative stability and their occurrence in natural or
engineered systems. Our results suggest that cooperative
stability needs to be considered explicitly and
characterized quantitatively in any systematic experimental
or theoretical study of gene circuits. © 2005 by The
National Academy of Sciences of the USA.},
Doi = {10.1073/pnas.0409553102},
Key = {Buchler05}
}
@article{Archambault05,
Author = {Archambault, V and Buchler, NE and Wilmes, GM and Jacobson, MD and Cross, FR},
Title = {Two-faced cyclins with eyes on the targets},
Journal = {Cell Cycle},
Volume = {4},
Number = {1},
Pages = {125-130},
Organization = {Rockefeller University, New York, New York,
USA.},
Institution = {Rockefeller University, New York, New York,
USA.},
Year = {2005},
Keywords = {Amino Acid Motifs Amino Acid Sequence Cell
Cycle/genetics/physiology Cyclin B/chemistry/genetics/*physiology
Cyclin-Dependent Kinases/genetics/physiology
Cyclins/genetics/physiology DNA Replication *Gene Expression
Regulation, Fungal Hydrophobicity Molecular Sequence Data
Origin Recognition Complex/chemistry/genetics/*physiology
Protein Structure, Tertiary Saccharomyces
cerevisiae/genetics/*physiology Saccharomyces cerevisiae
Proteins/chemistry/genetics/*physiology Signal
Transduction/genetics/physiology},
Abstract = {We recently reported that the 'hydrophobic patch' (HP) of
the Saccharomyces cerevisiae S-phase cyclin Clb5 facilitates
its interaction with Orco (via its Cy or RXL motif),
providing a mechanism that helps prevent rereplication from
individual origins. This is the first finding of a
biological function for an interaction between a cyclin and
a cyclin-binding motif (Cy or RXL motif) in a target protein
in Saccharomyces cerevisiae. It is also the first such
example involving a B-type cyclin in any organism. Yet, some
of our observations as well as work from other groups
suggest that HP-RXL interactions are functionally important
for cyclin-Cdk signaling to other targets. The evolutionary
conservation of the HP motif suggests that it allows cyclins
to carry out important and specialized functions. ©2005
Landes Bioscience.},
Key = {Archambault05}
}
@article{Bintu05a,
Author = {Bintu, L and Buchler, NE and Garcia, HG and Gerland, U and Hwa, T and Kondev, J and Phillips, R},
Title = {Transcriptional regulation by the numbers:
Models},
Journal = {Current Opinion in Genetics and Development},
Volume = {15},
Number = {2},
Pages = {116-124},
Organization = {Physics Department, Brandeis University, Waltham, MA 02454,
USA.},
Institution = {Physics Department, Brandeis University, Waltham, MA 02454,
USA.},
Year = {2005},
url = {http://dx.doi.org/10.1016/j.gde.2005.02.007},
Keywords = {*Gene Expression Regulation Humans *Models, Theoretical
*Thermodynamics *Transcription, Genetic},
Abstract = {The expression of genes is regularly characterized with
respect to how much, how fast, when and where. Such
quantitative data demands quantitative models. Thermodynamic
models are based on the assumption that the level of gene
expression is proportional to the equilibrium probability
that RNA polymerase (RNAP) is bound to the promoter of
interest. Statistical mechanics provides a framework for
computing these probabilities. Within this framework,
interactions of activators, repressors, helper molecules and
RNAP are described by a single function, the 'regulation
factor'. This analysis culminates in an expression for the
probability of RNA polymerase binding at the promoter of
interest as a function of the number of regulatory proteins
in the cell. © 2005 Elsevier Ltd. All rights
reserved.},
Doi = {10.1016/j.gde.2005.02.007},
Key = {Bintu05a}
}
@article{Fritz07,
Author = {Fritz, G and Buchler, NE and Hwa, T and Gerland, U},
Title = {Designing sequential transcription logic: A simple genetic
circuit for conditional memory},
Journal = {Systems and Synthetic Biology},
Volume = {1},
Number = {2},
Pages = {89-98},
Organization = {Institute for Theoretical Physics, Universitat zu Koln,
Zulpicher Str. 77, Koln, Germany, 50937.},
Institution = {Institute for Theoretical Physics, Universitat zu Koln,
Zulpicher Str. 77, Koln, Germany, 50937.},
Year = {2007},
ISSN = {1872-5325},
url = {http://dx.doi.org/10.1007/s11693-007-9006-8},
Abstract = {The ability to learn and respond to recurrent events depends
on the capacity to remember transient biological signals
received in the past. Moreover, it may be desirable to
remember or ignore these transient signals conditioned upon
other signals that are active at specific points in time or
in unique environments. Here, we propose a simple genetic
circuit in bacteria that is capable of conditionally
memorizing a signal in the form of a transcription factor
concentration. The circuit behaves similarly to a "data
latch" in an electronic circuit, i.e. it reads and stores an
input signal only when conditioned to do so by a "read
command." Our circuit is of the same size as the well-known
genetic toggle switch (an unconditional latch) which
consists of two mutually repressing genes, but is
complemented with a "regulatory front end" involving protein
heterodimerization as a simple way to implement conditional
control. Deterministic and stochastic analysis of the
circuit dynamics indicate that an experimental
implementation is feasible based on well-characterized genes
and proteins. It is not known, to which extent molecular
networks are able to conditionally store information in
natural contexts for bacteria. However, our results suggest
that such sequential logic elements may be readily
implemented by cells through the combination of existing
protein-protein interactions and simple transcriptional
regulation. © 2007 Springer Science + Business Media
B.V.},
Doi = {10.1007/s11693-007-9006-8},
Key = {Fritz07}
}
@article{fds228188,
Author = {Buchler, NE and Louis, M},
Title = {Molecular Titration and Ultrasensitivity in Regulatory
Networks},
Journal = {Journal of Molecular Biology},
Volume = {384},
Number = {5},
Pages = {1106-1119},
Year = {2008},
ISSN = {0022-2836},
url = {http://dx.doi.org/10.1016/j.jmb.2008.09.079},
Keywords = {Animals • Bacteria • Dimerization • Gene
Regulatory Networks* • Kinetics • Models,
Molecular* • Protein Processing, Post-Translational
• Saccharomyces cerevisiae • Transcription Factors
• metabolism},
Abstract = {Protein sequestration occurs when an active protein is
sequestered by a repressor into an inactive complex. Using
mathematical and computational modeling, we show how this
regulatory mechanism (called "molecular titration") can
generate ultrasensitive or "all-or-none" responses that are
equivalent to highly cooperative processes. The
ultrasensitive nature of the input-output response is mainly
determined by two parameters: the dimer dissociation
constant and the repressor concentration. Because in vivo
concentrations are tunable through a variety of mechanisms,
molecular titration represents a flexible mechanism for
generating ultrasensitivity. Using physiological parameters,
we report how details of in vivo protein degradation affect
the strength of the ultrasensitivity at steady state. Given
that developmental systems often transduce signals into
cell-fate decisions on timescales incompatible with steady
state, we further examine whether molecular titration can
produce ultrasensitive responses within physiologically
relevant time intervals. Using Drosophila somatic sex
determination as a developmental paradigm, we demonstrate
that molecular titration can generate ultrasensitivity on
timescales compatible with most cell-fate decisions. Gene
duplication followed by loss-of-function mutations can
create dominant negatives that titrate and compete with the
original protein. Dominant negatives are abundant in gene
regulatory circuits, and our results suggest that molecular
titration might be generating an ultrasensitive response in
these networks. © 2008 Elsevier Ltd. All rights
reserved.},
Language = {eng},
Doi = {10.1016/j.jmb.2008.09.079},
Key = {fds228188}
}
@article{fds228189,
Author = {Buchler, NE and Cross, FR},
Title = {Protein sequestration generates a flexible ultrasensitive
response in a genetic network},
Journal = {Molecular systems biology},
Volume = {5},
Pages = {272},
Year = {2009},
ISSN = {1744-4292},
url = {http://dx.doi.org/10.1038/msb.2009.30},
Keywords = {Basic-Leucine Zipper Transcription Factors • Fungal
Proteins • Gene Expression Regulation, Fungal •
Gene Regulatory Networks* • Genes, Dominant •
Genetic Engineering • Models, Genetic* • Mutation
• Saccharomycetales • Trans-Activators •
Transcription, Genetic • genetics • metabolism
• metabolism* • methods*},
Abstract = {Ultrasensitive responses are crucial for cellular
regulation. Protein sequestration, where an active protein
is bound in an inactive complex by an inhibitor, can
potentially generate ultrasensitivity. Here, in a synthetic
genetic circuit in budding yeast, we show that sequestration
of a basic leucine zipper transcription factor by a
dominant-negative inhibitor converts a graded
transcriptional response into a sharply ultrasensitive
response, with apparent Hill coefficients up to 12. A simple
quantitative model for this genetic network shows that both
the threshold and the degree of ultrasensitivity depend upon
the abundance of the inhibitor, exactly as we observed
experimentally. The abundance of the inhibitor can be
altered by simple mutation; thus, ultrasensitive responses
mediated by protein sequestration are easily tuneable. Gene
duplication of regulatory homodimers and loss-of-function
mutations can create dominant negatives that sequester and
inactivate the original regulator. The generation of
flexible ultrasensitive responses is an unappreciated
adaptive advantage that could explain the frequent
evolutionary emergence of dominant negatives.© 2009 EMBO
and Macmillan Publishers Limited. All rights
reserved.},
Language = {eng},
Doi = {10.1038/msb.2009.30},
Key = {fds228189}
}
@article{fds228179,
Author = {Cross, FR and Buchler, NE and Skotheim, JM},
Title = {Evolution of networks and sequences in eukaryotic cell cycle
control},
Journal = {Philosophical Transactions B},
Volume = {366},
Number = {1584},
Pages = {3532-3544},
Year = {2011},
ISSN = {0962-8436},
url = {http://hdl.handle.net/10161/9350 Duke open
access},
Keywords = {Amino Acid Sequence • Animals • Cell Cycle
Checkpoints* • Cell Cycle Proteins • Conserved
Sequence • Eukaryota • Evolution, Molecular*
• Mammals • Phylogeny • Plant Cells •
Plants • Sequence Alignment • Yeasts •
classification • cytology • cytology* •
genetics • genetics* • metabolism},
Abstract = {The molecular networks regulating the G1-S transition in
budding yeast and mammals are strikingly similar in network
structure. However, many of the individual proteins
performing similar network roles appear to have unrelated
amino acid sequences, suggesting either extremely rapid
sequence evolution, or true polyphyly of proteins carrying
out identical network roles. A yeast/mammal comparison
suggests that network topology, and its associated dynamic
properties, rather than regulatory proteins themselves may
be the most important elements conserved through evolution.
However, recent deep phylogenetic studies show that fungal
and animal lineages are relatively closely related in the
opisthokont branch of eukaryotes. The presence in plants of
cell cycle regulators such as Rb, E2F and cyclins A and D,
that appear lost in yeast, suggests cell cycle control in
the last common ancestor of the eukaryotes was implemented
with this set of regulatory proteins. Forward genetics in
non-opisthokonts, such as plants or their green algal
relatives, will provide direct information on cell cycle
control in these organisms, and may elucidate the
potentially more complex cell cycle control network of the
last common eukaryotic ancestor. © 2011 The Royal
Society.},
Language = {eng},
Doi = {10.1098/rstb.2011.0078},
Key = {fds228179}
}
@article{fds228180,
Author = {Buchler, NE and Bai, L},
Title = {Chromatin: Bind at your own RSC},
Journal = {Current Biology},
Volume = {21},
Number = {6},
Pages = {R223-R225},
Year = {2011},
ISSN = {0960-9822},
url = {http://hdl.handle.net/10161/9351 Duke open
access},
Keywords = {Chromatin • DNA-Binding Proteins • Galactokinase
• Gene Expression Regulation, Fungal • Nucleosomes
• Promoter Regions, Genetic • Saccharomyces
cerevisiae Proteins • Transcription Factors •
genetics • metabolism • metabolism* •
physiology*},
Abstract = {Recent work has identified a novel RSC-nucleosome complex
that both strongly phases flanking nucleosomes and presents
regulatory sites for ready access. These results challenge
several widely held views. © 2011 Elsevier Ltd All rights
reserved.},
Language = {eng},
Doi = {10.1016/j.cub.2011.01.060},
Key = {fds228180}
}
@article{fds228178,
Author = {Tanouchi, Y and Pai, A and Buchler, NE and You, L},
Title = {Programming stress-induced altruistic death in engineered
bacteria.},
Journal = {Molecular systems biology},
Volume = {8},
Pages = {626},
Year = {2012},
ISSN = {1744-4292},
url = {http://www.ncbi.nlm.nih.gov/pubmed/23169002},
Keywords = {Apoptosis* • Escherichia coli • Genetic
Engineering* • Microbial Viability* • Models,
Biological • Reproducibility of Results • Stress,
Physiological* • cytology* • growth &
development},
Abstract = {Programmed death is often associated with a bacterial stress
response. This behavior appears paradoxical, as it offers no
benefit to the individual. This paradox can be explained if
the death is 'altruistic': the killing of some cells can
benefit the survivors through release of 'public goods'.
However, the conditions where bacterial programmed death
becomes advantageous have not been unambiguously
demonstrated experimentally. Here, we determined such
conditions by engineering tunable, stress-induced altruistic
death in the bacterium Escherichia coli. Using a
mathematical model, we predicted the existence of an optimal
programmed death rate that maximizes population growth under
stress. We further predicted that altruistic death could
generate the 'Eagle effect', a counter-intuitive phenomenon
where bacteria appear to grow better when treated with
higher antibiotic concentrations. In support of these
modeling insights, we experimentally demonstrated both the
optimality in programmed death rate and the Eagle effect
using our engineered system. Our findings fill a critical
conceptual gap in the analysis of the evolution of bacterial
programmed death, and have implications for a design of
antibiotic treatment.},
Language = {eng},
Doi = {10.1038/msb.2012.57},
Key = {fds228178}
}
@article{fds228177,
Author = {Mazo-Vargas, A and Park, H and Aydin, M and Buchler,
NE},
Title = {Measuring fast gene dynamics in single cells with time-lapse
luminescence microscopy.},
Journal = {Molecular Biology of the Cell},
Volume = {25},
Number = {22},
Pages = {3699-3708},
Year = {2014},
Month = {November},
ISSN = {1059-1524},
url = {http://hdl.handle.net/10161/9353 Duke open
access},
Keywords = {Animals • Beetles • Cell Cycle • Cell Cycle
Proteins • Fireflies • Gene Expression Regulation,
Fungal* • Insect Proteins • Luciferases •
Luminescent Measurements • Microfluidic Analytical
Techniques • Microscopy, Fluorescence •
Saccharomyces cerevisiae • Saccharomyces cerevisiae
Proteins • Single-Cell Analysis • Time-Lapse
Imaging • chemistry • enzymology • genetics
• genetics* • metabolism •
methods},
Abstract = {Time-lapse fluorescence microscopy is an important tool for
measuring in vivo gene dynamics in single cells. However,
fluorescent proteins are limited by slow chromophore
maturation times and the cellular autofluorescence or
phototoxicity that arises from light excitation. An
alternative is luciferase, an enzyme that emits photons and
is active upon folding. The photon flux per luciferase is
significantly lower than that for fluorescent proteins. Thus
time-lapse luminescence microscopy has been successfully
used to track gene dynamics only in larger organisms and for
slower processes, for which more total photons can be
collected in one exposure. Here we tested green, yellow, and
red beetle luciferases and optimized substrate conditions
for in vivo luminescence. By combining time-lapse
luminescence microscopy with a microfluidic device, we
tracked the dynamics of cell cycle genes in single yeast
with subminute exposure times over many generations. Our
method was faster and in cells with much smaller volumes
than previous work. Fluorescence of an optimized reporter
(Venus) lagged luminescence by 15-20 min, which is
consistent with its known rate of chromophore maturation in
yeast. Our work demonstrates that luciferases are better
than fluorescent proteins at faithfully tracking the
underlying gene expression.},
Language = {eng},
Doi = {10.1091/mbc.e14-07-1187},
Key = {fds228177}
}
@article{fds228175,
Author = {Zhou, M and Wang, W and Karapetyan, S and Mwimba, M and Marqués, J and Buchler, NE and Dong, X},
Title = {Redox rhythm reinforces the circadian clock to gate immune
response.},
Journal = {Nature},
Volume = {523},
Number = {7561},
Pages = {472-476},
Year = {2015},
Month = {July},
ISSN = {0028-0836},
url = {http://hdl.handle.net/10161/10230 Duke open
access},
Abstract = {Recent studies have shown that in addition to the
transcriptional circadian clock, many organisms, including
Arabidopsis, have a circadian redox rhythm driven by the
organism's metabolic activities. It has been hypothesized
that the redox rhythm is linked to the circadian clock, but
the mechanism and the biological significance of this link
have only begun to be investigated. Here we report that the
master immune regulator NPR1 (non-expressor of
pathogenesis-related gene 1) of Arabidopsis is a sensor of
the plant's redox state and regulates transcription of core
circadian clock genes even in the absence of pathogen
challenge. Surprisingly, acute perturbation in the redox
status triggered by the immune signal salicylic acid does
not compromise the circadian clock but rather leads to its
reinforcement. Mathematical modelling and subsequent
experiments show that NPR1 reinforces the circadian clock
without changing the period by regulating both the morning
and the evening clock genes. This balanced network
architecture helps plants gate their immune responses
towards the morning and minimize costs on growth at night.
Our study demonstrates how a sensitive redox rhythm
interacts with a robust circadian clock to ensure proper
responsiveness to environmental stimuli without compromising
fitness of the organism.},
Language = {ENG},
Doi = {10.1038/nature14449},
Key = {fds228175}
}
@article{fds228176,
Author = {Tanouchi, Y and Pai, A and Park, H and Huang, S and Stamatov, R and Buchler, NE and You, L},
Title = {A noisy linear map underlies oscillations in cell size and
gene expression in bacteria.},
Journal = {Nature},
Volume = {523},
Number = {7560},
Pages = {357-360},
Year = {2015},
Month = {July},
ISSN = {0028-0836},
url = {http://hdl.handle.net/10161/10801 Duke open
access},
Abstract = {During bacterial growth, a cell approximately doubles in
size before division, after which it splits into two
daughter cells. This process is subjected to the inherent
perturbations of cellular noise and thus requires regulation
for cell-size homeostasis. The mechanisms underlying the
control and dynamics of cell size remain poorly understood
owing to the difficulty in sizing individual bacteria over
long periods of time in a high-throughput manner. Here we
measure and analyse long-term, single-cell growth and
division across different Escherichia coli strains and
growth conditions. We show that a subset of cells in a
population exhibit transient oscillations in cell size with
periods that stretch across several (more than ten)
generations. Our analysis reveals that a simple law
governing cell-size control-a noisy linear map-explains the
origins of these cell-size oscillations across all strains.
This noisy linear map implements a negative feedback on
cell-size control: a cell with a larger initial size tends
to divide earlier, whereas one with a smaller initial size
tends to divide later. Combining simulations of cell growth
and division with experimental data, we demonstrate that
this noisy linear map generates transient oscillations, not
just in cell size, but also in constitutive gene expression.
Our work provides new insights into the dynamics of
bacterial cell-size regulation with implications for the
physiological processes involved.},
Language = {ENG},
Doi = {10.1038/nature14562},
Key = {fds228176}
}
@article{fds228174,
Author = {Rienzo, A and Poveda-Huertes, D and Aydin, S and Buchler, NE and Pascual-Ahuir, A and Proft, M},
Title = {Different Mechanisms Confer Gradual Control and Memory at
Nutrient- and Stress-Regulated Genes in Yeast.},
Journal = {Molecular and Cellular Biology},
Volume = {35},
Number = {21},
Pages = {3669-3683},
Year = {2015},
Month = {November},
ISSN = {0270-7306},
url = {http://hdl.handle.net/10161/10648 Duke open
access},
Abstract = {Cells respond to environmental stimuli by fine-tuned
regulation of gene expression. Here we investigated the
dose-dependent modulation of gene expression at high
temporal resolution in response to nutrient and stress
signals in yeast. The GAL1 activity in cell populations is
modulated in a well-defined range of galactose
concentrations, correlating with a dynamic change of histone
remodeling and RNA polymerase II (RNAPII) association. This
behavior is the result of a heterogeneous induction delay
caused by decreasing inducer concentrations across the
population. Chromatin remodeling appears to be the basis for
the dynamic GAL1 expression, because mutants with impaired
histone dynamics show severely truncated dose-response
profiles. In contrast, the GRE2 promoter operates like a
rapid off/on switch in response to increasing osmotic
stress, with almost constant expression rates and
exclusively temporal regulation of histone remodeling and
RNAPII occupancy. The Gal3 inducer and the Hog1
mitogen-activated protein (MAP) kinase seem to determine the
different dose-response strategies at the two promoters.
Accordingly, GAL1 becomes highly sensitive and dose
independent if previously stimulated because of residual
Gal3 levels, whereas GRE2 expression diminishes upon
repeated stimulation due to acquired stress resistance. Our
analysis reveals important differences in the way dynamic
signals create dose-sensitive gene expression
outputs.},
Doi = {10.1128/mcb.00729-15},
Key = {fds228174}
}
@article{fds300277,
Author = {Schaap, P and Barrantes, I and Minx, P and Sasaki, N and Anderson, RW and Bénard, M and Biggar, KK and Buchler, NE and Bundschuh, R and Chen, X and Fronick, C and Fulton, L and Golderer, G and Jahn, N and Knoop, V and Landweber, LF and Maric, C and Miller, D and Noegel, AA and Peace, R and Pierron, G and Sasaki, T and Schallenberg-Rüdinger, M and Schleicher, M and Singh, R and Spaller, T and Storey, KB and Suzuki, T and Tomlinson, C and Tyson, JJ and Warren, WC and Werner, ER and Werner-Felmayer, G and Wilson, RK and Winckler, T and Gott, JM and Glöckner, G and Marwan, W},
Title = {The Physarum polycephalum Genome Reveals Extensive Use of
Prokaryotic Two-Component and Metazoan-Type Tyrosine Kinase
Signaling.},
Journal = {Genome Biology and Evolution},
Volume = {8},
Number = {1},
Pages = {109-125},
Year = {2015},
Month = {November},
url = {http://hdl.handle.net/10161/11511 Duke open
access},
Abstract = {Physarum polycephalum is a well-studied microbial eukaryote
with unique experimental attributes relative to other
experimental model organisms. It has a sophisticated life
cycle with several distinct stages including amoebal,
flagellated, and plasmodial cells. It is unusual in
switching between open and closed mitosis according to
specific life-cycle stages. Here we present the analysis of
the genome of this enigmatic and important model organism
and compare it with closely related species. The genome is
littered with simple and complex repeats and the coding
regions are frequently interrupted by introns with a mean
size of 100 bases. Complemented with extensive transcriptome
data, we define approximately 31,000 gene loci, providing
unexpected insights into early eukaryote evolution. We
describe extensive use of histidine kinase-based
two-component systems and tyrosine kinase signaling, the
presence of bacterial and plant type photoreceptors
(phytochromes, cryptochrome, and phototropin) and of
plant-type pentatricopeptide repeat proteins, as well as
metabolic pathways, and a cell cycle control system
typically found in more complex eukaryotes. Our analysis
characterizes P. polycephalum as a prototypical eukaryote
with features attributed to the last common ancestor of
Amorphea, that is, the Amoebozoa and Opisthokonts.
Specifically, the presence of tyrosine kinases in
Acanthamoeba and Physarum as representatives of two
distantly related subdivisions of Amoebozoa argues against
the later emergence of tyrosine kinase signaling in the
opisthokont lineage and also against the acquisition by
horizontal gene transfer.},
Doi = {10.1093/gbe/evv237},
Key = {fds300277}
}
@article{fds302226,
Author = {Karapetyan, S and Buchler, NE},
Title = {Role of DNA binding sites and slow unbinding kinetics in
titration-based oscillators.},
Journal = {Physical Review E - Statistical, Nonlinear, and Soft Matter
Physics},
Volume = {92},
Number = {6},
Pages = {062712},
Year = {2015},
Month = {December},
ISSN = {1539-3755},
url = {http://hdl.handle.net/10161/11506 Duke open
access},
Abstract = {Genetic oscillators, such as circadian clocks, are
constantly perturbed by molecular noise arising from the
small number of molecules involved in gene regulation. One
of the strongest sources of stochasticity is the binary
noise that arises from the binding of a regulatory protein
to a promoter in the chromosomal DNA. In this study, we
focus on two minimal oscillators based on activator
titration and repressor titration to understand the key
parameters that are important for oscillations and for
overcoming binary noise. We show that the rate of unbinding
from the DNA, despite traditionally being considered a fast
parameter, needs to be slow to broaden the space of
oscillatory solutions. The addition of multiple, independent
DNA binding sites further expands the oscillatory parameter
space for the repressor-titration oscillator and lengthens
the period of both oscillators. This effect is a combination
of increased effective delay of the unbinding kinetics due
to multiple binding sites and increased promoter
ultrasensitivity that is specific for repression. We then
use stochastic simulation to show that multiple binding
sites increase the coherence of oscillations by mitigating
the binary noise. Slow values of DNA unbinding rate are also
effective in alleviating molecular noise due to the
increased distance from the bifurcation point. Our work
demonstrates how the number of DNA binding sites and slow
unbinding kinetics, which are often omitted in biophysical
models of gene circuits, can have a significant impact on
the temporal and stochastic dynamics of genetic
oscillators.},
Doi = {10.1103/physreve.92.062712},
Key = {fds302226}
}
@article{fds228173,
Author = {Burnetti, AJ and Aydin, M and Buchler, NE},
Title = {Cell cycle Start is coupled to entry into the yeast
metabolic cycle across diverse strains and growth
rates.},
Journal = {Molecular Biology of the Cell},
Volume = {27},
Number = {1},
Pages = {64-74},
Year = {2016},
Month = {January},
ISSN = {1059-1524},
url = {http://hdl.handle.net/10161/11291 Duke open
access},
Abstract = {Cells have evolved oscillators with different frequencies to
coordinate periodic processes. Here we studied the
interaction of two oscillators, the cell division cycle
(CDC) and the yeast metabolic cycle (YMC), in budding yeast.
Previous work suggested that the CDC and YMC interact to
separate high oxygen consumption (HOC) from DNA replication
to prevent genetic damage. To test this hypothesis, we grew
diverse strains in chemostat and measured DNA replication
and oxygen consumption with high temporal resolution at
different growth rates. Our data showed that HOC is not
strictly separated from DNA replication; rather, cell cycle
Start is coupled with the initiation of HOC and catabolism
of storage carbohydrates. The logic of this YMC-CDC coupling
may be to ensure that DNA replication and cell division
occur only when sufficient cellular energy reserves have
accumulated. Our results also uncovered a quantitative
relationship between CDC period and YMC period across
different strains. More generally, our approach shows how
studies in genetically diverse strains efficiently identify
robust phenotypes and steer the experimentalist away from
strain-specific idiosyncrasies.},
Doi = {10.1091/mbc.e15-07-0454},
Key = {fds228173}
}
@article{fds315378,
Author = {Medina, EM and Turner, JJ and Gordân, R and Skotheim, JM and Buchler,
NE},
Title = {Punctuated evolution and transitional hybrid network in an
ancestral cell cycle of fungi.},
Journal = {eLife},
Volume = {5},
Number = {MAY2016},
Year = {2016},
Month = {May},
url = {http://hdl.handle.net/10161/12000 Duke open
access},
Abstract = {Although cell cycle control is an ancient, conserved, and
essential process, some core animal and fungal cell cycle
regulators share no more sequence identity than
non-homologous proteins. Here, we show that evolution along
the fungal lineage was punctuated by the early acquisition
and entrainment of the SBF transcription factor through
horizontal gene transfer. Cell cycle evolution in the fungal
ancestor then proceeded through a hybrid network containing
both SBF and its ancestral animal counterpart E2F, which is
still maintained in many basal fungi. We hypothesize that a
virally-derived SBF may have initially hijacked cell cycle
control by activating transcription via the cis-regulatory
elements targeted by the ancestral cell cycle regulator E2F,
much like extant viral oncogenes. Consistent with this
hypothesis, we show that SBF can regulate promoters with E2F
binding sites in budding yeast.},
Doi = {10.7554/elife.09492},
Key = {fds315378}
}
@article{fds325578,
Author = {Tanouchi, Y and Pai, A and Park, H and Huang, S and Buchler, NE and You,
L},
Title = {Long-term growth data of Escherichia coli at a single-cell
level.},
Journal = {Scientific Data},
Volume = {4},
Pages = {170036},
Year = {2017},
Month = {March},
url = {http://dx.doi.org/10.1038/sdata.2017.36},
Abstract = {Long-term, single-cell measurement of bacterial growth is
extremely valuable information, particularly in the study of
homeostatic aspects such as cell-size and growth rate
control. Such measurement has recently become possible due
to the development of microfluidic technology. Here we
present data from single-cell measurements of Escherichia
coli growth over 70 generations obtained for three different
growth conditions. The data were recorded every minute, and
contain time course data of cell length and fluorescent
intensity of constitutively expressed yellow fluorescent
protein.},
Doi = {10.1038/sdata.2017.36},
Key = {fds325578}
}
@article{fds326156,
Author = {Liban, TJ and Medina, EM and Tripathi, S and Sengupta, S and Henry, RW and Buchler, NE and Rubin, SM},
Title = {Conservation and divergence of C-terminal domain structure
in the retinoblastoma protein family.},
Journal = {Proceedings of the National Academy of Sciences of
USA},
Volume = {114},
Number = {19},
Pages = {4942-4947},
Year = {2017},
Month = {May},
url = {http://dx.doi.org/10.1073/pnas.1619170114},
Abstract = {The retinoblastoma protein (Rb) and the homologous pocket
proteins p107 and p130 negatively regulate cell
proliferation by binding and inhibiting members of the E2F
transcription factor family. The structural features that
distinguish Rb from other pocket proteins have been unclear
but are critical for understanding their functional
diversity and determining why Rb has unique tumor suppressor
activities. We describe here important differences in how
the Rb and p107 C-terminal domains (CTDs) associate with the
coiled-coil and marked-box domains (CMs) of E2Fs. We find
that although CTD-CM binding is conserved across protein
families, Rb and p107 CTDs show clear preferences for
different E2Fs. A crystal structure of the p107 CTD bound to
E2F5 and its dimer partner DP1 reveals the molecular basis
for pocket protein-E2F binding specificity and how
cyclin-dependent kinases differentially regulate pocket
proteins through CTD phosphorylation. Our structural and
biochemical data together with phylogenetic analyses of Rb
and E2F proteins support the conclusion that Rb evolved
specific structural motifs that confer its unique capacity
to bind with high affinity those E2Fs that are the most
potent activators of the cell cycle.},
Doi = {10.1073/pnas.1619170114},
Key = {fds326156}
}
@article{fds326543,
Author = {Hendler, A and Medina, EM and Kishkevich, A and Abu-Qarn, M and Klier,
S and Buchler, NE and de Bruin, RAM and Aharoni, A},
Title = {Gene duplication and co-evolution of G1/S transcription
factor specificity in fungi are essential for optimizing
cell fitness.},
Journal = {PLoS genetics},
Volume = {13},
Number = {5},
Pages = {e1006778},
Year = {2017},
Month = {May},
url = {http://dx.doi.org/10.1371/journal.pgen.1006778},
Abstract = {Transcriptional regulatory networks play a central role in
optimizing cell survival. How DNA binding domains and
cis-regulatory DNA binding sequences have co-evolved to
allow the expansion of transcriptional networks and how this
contributes to cellular fitness remains unclear. Here we
experimentally explore how the complex G1/S transcriptional
network evolved in the budding yeast Saccharomyces
cerevisiae by examining different chimeric transcription
factor (TF) complexes. Over 200 G1/S genes are regulated by
either one of the two TF complexes, SBF and MBF, which bind
to specific DNA binding sequences, SCB and MCB,
respectively. The difference in size and complexity of the
G1/S transcriptional network across yeast species makes it
well suited to investigate how TF paralogs (SBF and MBF) and
DNA binding sequences (SCB and MCB) co-evolved after gene
duplication to rewire and expand the network of G1/S target
genes. Our data suggests that whilst SBF is the likely
ancestral regulatory complex, the ancestral DNA binding
element is more MCB-like. G1/S network expansion took place
by both cis- and trans- co-evolutionary changes in closely
related but distinct regulatory sequences. Replacement of
the endogenous SBF DNA-binding domain (DBD) with that from
more distantly related fungi leads to a contraction of the
SBF-regulated G1/S network in budding yeast, which also
correlates with increased defects in cell growth, cell size,
and proliferation.},
Doi = {10.1371/journal.pgen.1006778},
Key = {fds326543}
}
@article{fds328789,
Author = {Gómez-Schiavon, M and Chen, L-F and West, AE and Buchler,
NE},
Title = {BayFish: Bayesian inference of transcription dynamics from
population snapshots of single-molecule RNA FISH in single
cells.},
Journal = {Genome Biology: biology for the post-genomic
era},
Volume = {18},
Number = {1},
Pages = {164},
Year = {2017},
Month = {September},
url = {http://dx.doi.org/10.1186/s13059-017-1297-9},
Abstract = {Single-molecule RNA fluorescence in situ hybridization
(smFISH) provides unparalleled resolution in the measurement
of the abundance and localization of nascent and mature RNA
transcripts in fixed, single cells. We developed a
computational pipeline (BayFish) to infer the kinetic
parameters of gene expression from smFISH data at multiple
time points after gene induction. Given an underlying model
of gene expression, BayFish uses a Monte Carlo method to
estimate the Bayesian posterior probability of the model
parameters and quantify the parameter uncertainty given the
observed smFISH data. We tested BayFish on synthetic data
and smFISH measurements of the neuronal activity-inducible
gene Npas4 in primary neurons.},
Doi = {10.1186/s13059-017-1297-9},
Key = {fds328789}
}
@article{fds332834,
Author = {Lin, YT and Buchler, NE},
Title = {Efficient analysis of stochastic gene dynamics in the
non-adiabatic regime using piecewise deterministic Markov
processes.},
Journal = {Journal of the Royal Society Interface},
Volume = {15},
Number = {138},
Year = {2018},
Month = {January},
url = {http://dx.doi.org/10.1098/rsif.2017.0804},
Abstract = {Single-cell experiments show that gene expression is
stochastic and bursty, a feature that can emerge from slow
switching between promoter states with different activities.
In addition to slow chromatin and/or DNA looping dynamics,
one source of long-lived promoter states is the slow binding
and unbinding kinetics of transcription factors to
promoters, i.e. the non-adiabatic binding regime. Here, we
introduce a simple analytical framework, known as a
piecewise deterministic Markov process (PDMP), that
accurately describes the stochastic dynamics of gene
expression in the non-adiabatic regime. We illustrate the
utility of the PDMP on a non-trivial dynamical system by
analysing the properties of a titration-based oscillator in
the non-adiabatic limit. We first show how to transform the
underlying chemical master equation into a PDMP where the
slow transitions between promoter states are stochastic, but
whose rates depend upon the faster deterministic dynamics of
the transcription factors regulated by these promoters. We
show that the PDMP accurately describes the observed periods
of stochastic cycles in activator and repressor-based
titration oscillators. We then generalize our PDMP analysis
to more complicated versions of titration-based oscillators
to explain how multiple binding sites lengthen the period
and improve coherence. Last, we show how noise-induced
oscillation previously observed in a titration-based
oscillator arises from non-adiabatic and discrete binding
events at the promoter site.},
Doi = {10.1098/rsif.2017.0804},
Key = {fds332834}
}
@article{fds328227,
Author = {Hendler, A and Medina, EM and Buchler, NE and de Bruin, RAM and Aharoni,
A},
Title = {The evolution of a G1/S transcriptional network in
yeasts.},
Journal = {Current Genetics},
Volume = {64},
Number = {1},
Pages = {81-86},
Year = {2018},
Month = {February},
url = {http://dx.doi.org/10.1007/s00294-017-0726-3},
Abstract = {The G1-to-S cell cycle transition is promoted by the
periodic expression of a large set of genes. In
Saccharomyces cerevisiae G1/S gene expression is regulated
by two transcription factor (TF) complexes, the MBF and SBF,
which bind to specific DNA sequences, the MCB and SCB,
respectively. Despite extensive research little is known
regarding the evolution of the G1/S transcription regulation
including the co-evolution of the DNA binding domains with
their respective DNA binding sequences. We have recently
examined the co-evolution of the G1/S TF specificity through
the systematic generation and examination of chimeric
Mbp1/Swi4 TFs containing different orthologue DNA binding
domains in S. cerevisiae (Hendler et al. in PLoS Genet
13:e1006778. doi: 10.1371/journal.pgen.1006778 , 2017).
Here, we review the co-evolution of G1/S transcriptional
network and discuss the evolutionary dynamics and
specificity of the MBF-MCB and SBF-SCB interactions in
different fungal species.},
Doi = {10.1007/s00294-017-0726-3},
Key = {fds328227}
}