Discover the publications from the Landry Lab
Preprints and submitted papers
BFG-PCA: tools and resources that expand the potential for binary protein interaction discovery
Evans-Yamamoto D, Rouleau FD, Nanda P, Makanae K, Liu Y, Després PC, Matsuo H, Seki M, Dubé AK, Ascencio D, Yachie N, and Landry CR
Barcode fusion genetics (BFG) utilizes deep sequencing to improve the throughput of protein-protein interaction (PPI) screening in pools. BFG has been implemented in Yeast two-hybrid (Y2H) screens (BFG-Y2H). While Y2H requires test protein pairs to localize in the nucleus for reporter reconstruction, Dihydrofolate Reductase Protein-Fragment Complementation Assay (DHFR-PCA) allows proteins to localize in broader subcellular contexts and proves to be largely orthogonal to Y2H. Here, we implemented BFG to DHFR-PCA (BFG-PCA). This plasmid-based system can leverage ORF collections across model organisms to perform comparative analysis, unlike the original DHFR-PCA that requires yeast genomic integration. The scalability and quality of BFG-PCA were demonstrated by screening human and yeast interactions of >11,000 protein pairs. BFG-PCA showed high-sensitivity and high-specificity for capturing known interactions for both species. BFG-Y2H and BFG-PCA capture distinct sets of PPIs, which can partially be explained based on the domain orientation of the reporter tags. BFG-PCA is a high-throughput protein interaction technology to interrogate binary PPIs that exploits clone collections from any species of interest, expanding the scope of PPI assays.
Heterogeneous mutation rates and spectra within and between species of yeast and their hybrids
Fijarczyk A, Hénault M, Marsit S, Charron G, and Landry CR
Mutation rates and spectra vary between species and among populations. Hybridization can contribute to this variation, but its role remains poorly understood. Estimating mutation rates requires controlled conditions where the effect of natural selection can be minimized. One way to achieve this is through mutation accumulation experiments coupled with genome sequencing. Here we investigate 400 mutation accumulation lines initiated from 11 genotypes spanning intra-lineage, inter-lineage and interspecific crosses of the yeasts Saccharomyces paradoxus and S. cerevisiae and propagated for 770 generations. We find significant differences in mutation rates and spectra among crosses, which are not related to the level of divergence of parental strains but are genotype specific. We find that departures from neutrality, differences in growth rate, ploidy and loss of heterozygosity only play a minor role as a source of variation and conclude that unique combinations of parental genotypes drive distinct rates and spectra in some crosses.
Mapping Gene-Microbe Interactions: Insights from Functional Genomics Co-culture Experiments between Saccharomyces cerevisiae and Pseudomonas spp
Nguyen Q G, Jain M, Landry CR and M Filteau
Microbial interactions contribute to shape ecosystems and their functions. The interplay between microorganisms also shapes the evolutionary trajectory of each species, by imposing metabolic and physiological selective pressures. The mechanisms underlying these interactions are thus of interest to improve our understanding of microbial evolution at the genetic level. Here we applied a functional genomics approach in the model yeast Saccharomyces cerevisiae to identify the fitness determinants of naïve biotic interactions. We used a barcoded prototroph yeast deletion collection to perform pooled fitness competitions in co-culture with seven Pseudomonas spp natural isolates. We found that co-culture had a positive impact on fitness profiles, as in general the deleterious effects of loss of function in our nutrient-poor media were mitigated. In total, 643 genes showed a fitness difference in co-culture, most of which can be explained by a media diversification procured by bacterial metabolism. However, a large fraction (36%) of gene-microbe interactions could not be recaptured in cell-free supernatant experiments, showcasing that feedback mechanisms or physical contacts modulate these interactions. Also, the gene list of some co-cultures was enriched with homologs in other eukaryote species, suggesting a variable degree of specificity underlying the mechanisms of biotic interactions and that these interactions could also exist in other organisms. Our results illustrate how microbial interactions can contribute to shape the interplay between genomes and species interactions, and that S. cerevisiae is a powerful model to study the impact of biotic interactions.
Published work in 2020 & 2021
The parasite Schistocephalus solidus secretes proteins with putative host manipulation functions
Berger CS, Laroche J, Maaroufi H, Martin H, Moon K-M, Landry CR, Foster LJ & N Aubin-Horth
Manipulative parasites are thought to liberate molecules in their external environment, acting as manipulation factors with biological functions implicated in their host’s physiological and behavioural alterations. These manipulation factors are part of a complex mixture called the secretome. While the secretomes of various parasites have been described, there is very little data for a putative manipulative parasite. It is necessary to study the molecular interaction between a manipulative parasite and its host to better understand how such alterations evolve. Here, we used proteomics to characterize the secretome of a model cestode with a complex life cycle based on trophic transmission. We studied Schistocephalus solidus during the life stage in which behavioural changes take place in its obligatory intermediate fish host, the threespine stickleback (Gasterosteus aculeatus). We produced a novel genome sequence and assembly of S. solidus to improve protein coding gene prediction and annotation for this parasite. We then described the whole worm’s proteome and its secretome during fish host infection using LC–MS/MS. A total of 2290 proteins were detected in the proteome of S. solidus, and 30 additional proteins were detected specifically in the secretome. We found that the secretome contains proteases, proteins with neural and immune functions, as well as proteins involved in cell communication. We detected receptor-type tyrosine-protein phosphatases, which were reported in other parasitic systems to be manipulation factors. We also detected 12 S. solidus-specific proteins in the secretome that may play important roles in host–parasite interactions. Our results suggest that S. solidus liberates molecules with putative host manipulation functions in the host and that many of them are species-specific.
Testing the Genomic Shock Hypothesis Using Transposable Element Expression in Yeast Hybrids
Drouin M, Hénault M, Hallin J, and CR Landry
Transposable element (TE) insertions are a source of structural variation and can cause genetic instability and gene expression changes. A host can limit the spread of TEs with various repression mechanisms. Many examples of plant and animal interspecific hybrids show disrupted TE repression leading to TE propagation. Recent studies in yeast did not find any increase in transposition rate in hybrids. However, this does not rule out the possibility that the transcriptional or translational activity of TEs increases following hybridization because of a disruption of the host TE control mechanisms. Thus, whether total expression of a TE family is higher in hybrids than in their parental species remains to be examined. We leveraged publically available RNA-seq and ribosomal profiling data on yeast artificial hybrids of the Saccharomyces genus and performed differential expression analysis of their LTR retrotransposons (Ty elements). Our analyses of total mRNA levels show that Ty elements are generally not differentially expressed in hybrids, even when the hybrids are exposed to a low temperature stress condition. Overall, only 2/26 Ty families show significantly higher expression in the S. cerevisiae × S. uvarum hybrids while there are 3/26 showing significantly lower expression in the S. cerevisiae x S. paradoxus hybrids. Our analysis of ribosome profiling data of S. cerevisiae × S. paradoxus hybrids shows similar translation efficiency of Ty in both parents and hybrids, except for Ty1_cer showing higher translation efficiency. Overall, our results do not support the hypothesis that hybridization could act as a systematic trigger of TE expression in yeast and suggest that the impact of hybridization on TE activity is strain and TE specific.
Machine learning approach for discrimination of genotypes based on bright-field cellular images
Suzuki G, Saito Y, Seki M, Evans-Yamamoto D, Negishi M, Kakoi K, Kawai H, Landry CR, Yachie N, and Mitsuyama T
Morphological profiling is a combination of established optical microscopes and cutting-edge machine vision technologies, which stacks up successful applications in high-throughput phenotyping. One major question is how much information can be extracted from an image to identify genetic differences between cells. While fluorescent microscopy images of specific organelles have been broadly used for single-cell profiling, the potential ability of bright-field (BF) microscopy images of label-free cells remains to be tested. Here, we examine whether single-gene perturbation can be discriminated based on BF images of label-free cells using a machine learning approach. We acquired hundreds of BF images of single-gene mutant cells, quantified single-cell profiles consisting of texture features of cellular regions, and constructed a machine learning model to discriminate mutant cells from wild-type cells. Interestingly, the mutants were successfully discriminated from the wild type (area under the receiver operating characteristic curve = 0.773). The features that contributed to the discrimination were identified, and they included those related to the morphology of structures that appeared within cellular regions. Furthermore, functionally close gene pairs showed similar feature profiles of the mutant cells. Our study reveals that single-gene mutant cells can be discriminated from wild-type cells based on BF images, suggesting the potential as a useful tool for mutant cell profiling.
The neutral rate of whole-genome duplication varies among yeast species and their hybrids
Hybridization and polyploidization are powerful mechanisms of speciation. Hybrid speciation often coincides with whole-genome duplication (WGD) in eukaryotes. This suggests that WGD may allow hybrids to thrive by increasing fitness, restoring fertility and/or increasing access to adaptive mutations. Alternatively, it has been suggested that hybridization itself may trigger WGD. Testing these models requires quantifying the rate of WGD in hybrids without the confounding effect of natural selection. Here we show, by measuring the spontaneous rate of WGD of more than 1300 yeast crosses evolved under relaxed selection, that some genotypes or combinations of genotypes are more prone to WGD, including some hybrids between closely related species. We also find that higher WGD rate correlates with higher genomic instability and that WGD increases fertility and genetic variability. These results provide evidence that hybridization itself can promote WGD, which in turn facilitates the evolution of hybrids.
Yeast proteins do not practice social distancing as species hybridize
Berger CM, Landry CR
With the current COVID-19 pandemic, we all realized how important interactions are. Interactions are everywhere. At the cellular level, protein interactions play a key role and their ensemble, also called interactome, is often referred as the basic building blocks of life. Given its importance, the maintenance of the integrity of the interactome is a real challenge in the cell. Many events during evolution can disrupt interactomes and potentially result in different characteristics for the organisms. However, the molecular underpinnings of changes in interactions at the cellular level are still largely unexplored. Among the perturbations, hybridization puts in contact two different interactomes, which may lead to many changes in the protein interaction network of the hybrid, including gains and losses of interactions. We recently investigated the fate of the interactomes after hybridization between yeast species using a comparative proteomics approach. A large-scale conservation of the interactions was observed in hybrids, but we also noticed the presence of proteostasis-related changes. This suggests that, despite a general robustness, small differences may accumulate in hybrids and perturb their protein physiology. Here, we summarize our work with a broader perspective on the importance of interactions.
The challenges of predicting transposable element activity in hybrids
Transposable elements (TEs) are ubiquitous mobile genetic elements that hold both disruptive and adaptive potential for species. It has long been postulated that their activity may be triggered by hybridization, a hypothesis that received mixed support from studies in various species. While host defense mechanisms against TEs are being elucidated, the increasing volume of genomic data and bioinformatic tools specialized in TE detection enable in-depth characterization of TEs at the levels of species and populations. Here, I borrow elements from the genome ecology theory to illustrate how knowledge of the diversity of TEs and host defense mechanisms may help predict the activity of TEs in the face of hybridization, and how current limitations make this task especially challenging.
Protein context shapes the specificity of SH3 domain-mediated interactions in vivo
Dionne U, Bourgault E, Dubé AK, Bradley D, Chartier FJM, Dandage R, Dibyachintan S, Després PC, Gish GD, Hang Pham NT, Létourneau M, Lambert JP, Doucet N, Bisson N, and CR Landry
Protein–protein interactions (PPIs) between modular binding domains and their target peptide motifs are thought to largely depend on the intrinsic binding specificities of the domains. The large family of SRC Homology 3 (SH3) domains contribute to cellular processes via their ability to support such PPIs. While the intrinsic binding specificities of SH3 domains have been studied in vitro, whether each domain is necessary and sufficient to define PPI specificity in vivo is largely unknown. Here, by combining deletion, mutation, swapping and shuffling of SH3 domains and measurements of their impact on protein interactions in yeast, we find that most SH3s do not dictate PPI specificity independently from their host protein in vivo. We show that the identity of the host protein and the position of the SH3 domains within their host are critical for PPI specificity, for cellular functions and for key biophysical processes such as phase separation. Our work demonstrates the importance of the interplay between a modular PPI domain such as SH3 and its host protein in establishing specificity to wire PPI networks. These findings will aid understanding how protein networks are rewired during evolution and in the context of mutation-driven diseases such as cancer.
Expression attenuation as a mechanism of robustness against gene duplication
Many studies have focused on the mechanisms of long-term retention of gene duplicates, such as the gain of functions or reciprocal losses. However, such changes are more likely to occur if the duplicates are maintained for a long period. This time span will be short if duplication is immediately deleterious. We measured the distribution of fitness effects of gene duplication for 899 genes in budding yeast. We find that gene duplication is more likely to be deleterious than beneficial. However, contrary to previous models, in general, gene duplication does not affect fitness by altering the organization of protein complexes. We show that expression attenuation may protect complexes from the effects of gene duplication.
Frequent assembly of chimeric complexes in the protein interaction network of an interspecies yeast hybrid
Dandage R, Berger CM, Gagnon-Arsenault I, Moon KM, Stacey RG, Forster LJ and CR Landry
Hybrids between species often show extreme phenotypes, including some that take place at the molecular level. In this study, we investigated the phenotypes of an interspecies diploid hybrid in terms of protein-protein interactions inferred from protein correlation profiling. We used two yeast species, Saccharomyces cerevisiae and Saccharomyces uvarum, which are interfertile, but yet have proteins diverged enough to be differentiated using mass spectrometry. Most of the protein-protein interactions are similar between hybrid and parents, and are consistent with the assembly of chimeric complexes, which we validated using an orthogonal approach for the prefoldin complex. We also identified instances of altered protein-protein interactions in the hybrid, for instance in complexes related to proteostasis and in mitochondrial protein complexes. Overall, this study uncovers the likely frequent occurrence of chimeric protein complexes with few exceptions, which may result from incompatibilities or imbalances between the parental proteins.
Interspecific hybrids show a reduced adaptive potential under DNA damaging conditions
Hybridization may increase the probability of adaptation to extreme stresses. This advantage could be caused by an increased genome plasticity in hybrids, which could accelerate the search for adaptive mutations. High ultraviolet (UV) radiation is a particular challenge in terms of adaptation because it affects the viability of organisms by directly damaging DNA, while also challenging future generations by increasing mutation rate. Here we test whether hybridization accelerates adaptive evolution in response to DNA damage, using yeast as a model. We exposed 180 populations of hybrids between species (Saccharomyces cerevisiae and Saccharomyces paradoxus) and their parental strains to UV mimetic and control conditions for approximately 100 generations. Although we found that adaptation occurs in both hybrids and parents, hybrids achieved a lower rate of adaptation, contrary to our expectations. Adaptation to DNA damage conditions comes with a large and similar cost for parents and hybrids, suggesting that this cost is not responsible for the lower adaptability of hybrids. We suggest that the lower adaptive potential of hybrids in this condition may result from the interaction between DNA damage and the inherent genetic instability of hybrids.
Closely related budding yeast species respond to different ecological signals for spore activation
Spore activation is one of the most important developmental decisions in fungi as it initiates the transition from dormant and stress‐resistant cells to vegetative cells. Because in many species mating follows spore activation and germination, signals that trigger this developmental transition can also contribute to species reproductive barriers. Here, we examine the biochemical signals triggering spore activation in a natural species complex of budding yeast, Saccharomyces paradoxus (lineages SpA, SpB, SpC and SpC*). We first demonstrate that we can quantitatively monitor spore activation in these closely related lineages. Second, we dissect the composition of culture media to identify components necessary and/or sufficient to activate spores in the four lineages. We show that, contrary to expectation, glucose is necessary but not sufficient to trigger spore activation. We also show that two of the North American lineages (SpC and SpC*) diverge from the other North American (SpB) and European (SpA) lineages in terms of germination signal as their spore activation requires inorganic phosphate. Our results show that the way budding yeast interpret environmental conditions during spore activation diverged among closely related and incipient species, which means that it may play a role in their ecological differentiation and reproductive isolation.
The BUBR1 pseudokinase domain promotes efficient kinetochore PP2A-B56 recruitment to regulate spindle silencing and chromosome alignment
Gama Braga L, Cisneros AF, Mathieu M, Clerc M, Garcia P, Lottin B, Garand C, Thebault P, Landry CR & S. Elowe
The balance of phospho-signaling at the outer kinetochore is critical for forming accurate attachments between kinetochores and the mitotic spindle and timely exit from mitosis. A major player in determining this balance is the PP2A-B56 phosphatase, which is recruited to the kinase attachment regulatory domain (KARD) of budding uninhibited by benzimidazole 1-related 1 (BUBR1) in a phospho-dependent manner. This unleashes a rapid, switch-like phosphatase relay that reverses mitotic phosphorylation at the kinetochore, extinguishing the checkpoint and promoting anaphase. Here, we demonstrate that the C-terminal pseudokinase domain of human BUBR1 is required to promote KARD phosphorylation. Mutation or removal of the pseudokinase domain results in decreased PP2A-B56 recruitment to the outer kinetochore attenuated checkpoint silencing and errors in chromosome alignment as a result of imbalance in Aurora B activity. Our data, therefore, elucidate a function for the BUBR1 pseudokinase domain in ensuring accurate and timely exit from mitosis.
The effect of hybridization on transposable element accumulation in an undomesticated fungal species
Hénault M, Marsit S, Charron G & CR Landry
Transposable elements (TEs) are mobile genetic elements that can profoundly impact the evolution of genomes and species. A long-standing hypothesis suggests that hybridization could deregulate TEs and trigger their accumulation, although it received mixed support from studies mostly in plants and animals. Here, we tested this hypothesis in fungi using incipient species of the undomesticated yeast Saccharomyces paradoxus. Population genomic data revealed no signature of higher transposition in natural hybrids. As we could not rule out the elimination of past transposition increase signatures by natural selection, we performed a laboratory evolution experiment on a panel of artificial hybrids to measure TE accumulation in the near absence of selection. Changes in TE copy numbers were not predicted by the level of evolutionary divergence between the parents of a hybrid genotype. Rather, they were highly dependent on the individual hybrid genotypes, showing that strong genotype-specific deterministic factors govern TE accumulation in yeast hybrids.
Purification of yeast spores to investigate their dynamics of activation
Plante S & CR Landry
Germination is an important developmental process that supports resumption of growth in dormant spores. The study of the mechanisms underlying germination requires a pure spore population devoid of other cell types. This article describes the sporulation of wild Saccharomyces cerevisiae and Saccharomyces paradoxus strains, and the isolation and purification of ascospores. We also describe a method to synchronously induce germination in a spore population as well as to measure spore activation. This procedure can be applied, for example, to the study of environmental conditions that trigger germination. © 2020 Wiley Periodicals LLC.
The genome sequence of the Jean-Talon strain, an archeological tetraploid beer yeast from Québec, reveals traces of adaptation to specific brewing conditions
Fijarczyk A, Hénault M, Marsit S, Charron G, Fischborn T, Nicole-Labrie L & CR Landry
The genome sequences of archeological Saccharomyces cerevisiae isolates can reveal insights about the history of human baking, brewing and winemaking activities. A yeast strain called Jean-Talon was recently isolated from the vaults of the Intendant’s Palace of Nouvelle France on a historical site in Québec City. This site was occupied by breweries from the end of the 17th century until the middle of the 20th century when poisoning caused by cobalt added to the beer led to a shutdown of brewing activities. We sequenced the genome of the Jean-Talon strain and reanalyzed the genomes of hundreds of strains to determine how it relates to other domesticated and wild strains. The Jean-Talon strain is most closely related to industrial beer strains from the beer and bakery genetic groups from the United Kingdom and Belgium. It has numerous aneuploidies and Copy Number Variants (CNVs), including the main gene conferring cobalt resistance in yeast. The Jean-Talon strain has indeed higher tolerance to cobalt compared to other yeast strains, consistent with adaptation to the most recent brewing activities on the site. We conclude from this that the Jean-Talon strain most likely derives from recent brewing activities and not from the original breweries of Nouvelle France on the site.
The Canadian Fungal Research Network: Current Challenges and Future Opportunities
Horianopoulos L, Gluck-Thaler E, Benoit Gelber I , Cowen LE, Geddes-McAlister J, Landry CR, Schwartz IS, Scott JA, Sellam A, Sheppard DC, Spribille T, Subramaniam R,Walker AK, Harris SD, Shapiro RS & AC. Gerstein
Fungi critically impact the health and function of global ecosystems and economies. In Canada, fungal researchers often work within silos defined by subdiscipline and institutional type, complicating the collaborations necessary to understand the impacts fungi have on the environment, economy, and plant and animal health. Here, we announce the establishment of the Canadian Fungal Research Network (CanFunNet, https://fungalresearch.ca), whose mission is to strengthen and promote fungal research in Canada by facilitating dialogue among scientists. We summarize the challenges and opportunities for Canadian fungal research that were discussed at CanFunNet’s inaugural meeting in 2019, and identify 4 priorities for our community: (i) increasing collaboration among scientists, (ii) studying diversity in the context of ecological disturbance, (iii) preserving culture collections in the absence of sustained funding, and (iv) leveraging diverse expertise to attract trainees. We have gathered additional information to support our recommendations, including a survey identifying underrepresentation of fungal-related courses at Canadian universities, a list of Canadian fungaria and culture collections, and a case study of a human fungal pathogen outbreak. We anticipate that these discussions will help prioritize fungal research in Canada, and we welcome all researchers to join this nationwide effort to enhance knowledge dissemination and funding advocacy.
Perturbing proteomes at single residue resolution using base editing
Després PC, Dubé AK, Seki M, Yachie N and CR Landry
Base editors derived from CRISPR-Cas9 systems and DNA editing enzymes offer an unprecedented opportunity for the precise modiﬁcation of genes, but have yet to be used at a genome-scale throughput. Here, we test the ability of the Target-AID base editor to systematically modify genes genome-wide by targeting yeast essential genes. We mutate around 17,000 individual sites in parallel across more than 1500 genes. We identify over 700 sites at which mutations have a signiﬁcant impact on ﬁtness. Using previously determined and preferred Target-AID mutational outcomes, we ﬁnd that gRNAs with signiﬁcant effects on ﬁtness are enriched in variants predicted to be deleterious based on residue conservation and predicted protein destabilization. We identify key features inﬂuencing effective gRNAs in the context of base editing. Our results show that base editing is a powerful tool to identify key amino acid residues at the scale of proteomes.
Similarities in biological processes can be used to bridge ecology and molecular biology
Hallin J, Cisneros AF, Hénault M, Fijarczyk A, Dandage R, Bautista C and CR Landry
Much of the research in biology aims to understand the origin of diversity. Naturally, ecological diversity was the first object of study, but we now have the necessary tools to probe diversity at molecular scales. The inherent differences in how we study diversity at different scales caused the disciplines of biology to be organized around these levels, from molecular biology to ecology. Here, we illustrate that there are key properties of each scale that emerge from the interactions of simpler components and that these properties are often shared across different levels of organization. This means that ideas from one level of organization can be an inspiration for novel hypotheses to study phenomena at another level. We illustrate this concept with examples of events at the molecular level that have analogs at the organismal or ecological level and vice versa. Through these examples, we illustrate that biological processes at different organization levels are governed by general rules. The study of the same phenomena at different scales could enrich our work through a multidisciplinary approach, which should be a staple in the training of future scientists.
Hybridization and introgression drive genome evolution of the Dutch Elm Disease pathogens
Hessenauer P*, Fijarczyk A*, Martin H, Prunier J, Charron G, Chapuis J, Bernier L, Tanguay P, Hamelin RC and CR Landry
Hybridization and the resulting introgression can drive the success of invasive species via the rapid acquisition of adaptive traits. The Dutch elm disease pandemics in the past 100 years were caused by three fungal lineages with permeable reproductive barriers: Ophiostoma ulmi, Ophiostoma novo-ulmi subspecies novo-ulmi and Ophiostoma novo-ulmi subspecies americana. Using whole-genome sequences and growth phenotyping of a worldwide collection of isolates, we show that introgression has been the main driver of genomic diversity and that it impacted fitness-related traits. Introgressions contain genes involved in host–pathogen interactions and reproduction. Introgressed isolates have enhanced growth rate at high temperature and produce different necrosis sizes on an in vivo model for pathogenicity. In addition, lineages diverge in many pathogenicity-associated genes and exhibit differential mycelial growth in the presence of a proxy of a host defence compound, implying an important role of host trees in the molecular and functional differentiation of these pathogens.
Competition experiments in soil reveal the impact of genetic and biotic factors on natural yeast populations
Bleuven C, Nguyen G, Despres PC, Filteau M and CR Landry
The ability to measure microbial fitness directly in natural conditions and in interaction with other microbes is a challenge that needs to be overcome if we want to gain a better understanding of microbial fitness determinants in nature. Here we investigate the influence of the natural microbial community on the relative fitness of the North American populations SpB, SpC and SpC* of the wild yeast Saccharomyces paradoxus using DNA barcodes and a soil microcosm derived from soil associated with oak trees. We find that variation in fitness among these genetically distinct groups is influenced by the microbial community. Altering the microbial community load and diversity with an irradiation treatment significantly diminishes the magnitude of fitness differences among populations. Our findings suggest that microbial interactions could affect the evolution of yeast lineages in nature by modulating variation in fitness.
Diverse perspectives on interdisciplinarity from the Members of the College of The Royal Society of Canada
Cooke, S.J., V.M. Nguyen, D. Anastakis, S.D. Scott, M.R. Turetsky, A. Amirfazli, A. Hearn, C.E. Milton, L. Loewen, E.E. Smith, D.R. Norris, K.L. Lavoie, A. Aiken, D. Ansari, A.N. Antle, M. Babel, J. Bailey, D.M. Bernstein, R. Birnbaum, C. Bourassa, A. Calcagno, A. Campana, B. Chen, K. Collins, C.E. Connelly, M. Denov, B. Dupont, E. George, I. Gregory-Eaves, S. High, J.M. Hill, P.L. Jackson, N. Jette, M. Jurdjevic, A. Kothari, P. Khairy, S.A. Lamoureux, K. Ladner, C.R. Landry, F. Légaré, N. Lehoux, C. Leuprecht, A.R. Lieverse, A. Luczak, M.L. Mallory, E. Manning, A. Mazalek, S.J. Murray, L.L. Newman, V. Oosterveld, P. Potvin, S. Reimer-Kirkham, J. Rowsell, D. Stacey, S.L. Tighe, D.J. Vocadlo, A.E. Wilson and A. Woolford. 2020
Various multiple-disciplinary terms and concepts (although most commonly “interdisciplinarity,” which is used herein) are used to frame education, scholarship, research, and interactions within and outside academia. In principle, the premise of interdisciplinarity may appear to have many strengths; yet, the extent to which interdisciplinarity is embraced by the current generation of academics, the benefits and risks for doing so, and the barriers and facilitators to achieving interdisciplinarity, represent inherent challenges. Much has been written on the topic of interdisciplinarity, but to our knowledge there have been few attempts to consider and present diverse perspectives from scholars, artists, and scientists in a cohesive manner. As a team of 57 members from the Canadian College Cooke of New Scholars, Artists, and Scientists of the Royal Society of Canada (the College) who self-identify as being engaged or interested in interdisciplinarity, we provide diverse intellectual, cultural, and social perspectives. The goal of this paper is to share our collective wisdom on this topic with the broader community and to stimulate discourse and debate on the merits and challenges associated with interdisciplinarity. Perhaps the clearest message emerging from this exercise is that working across established boundaries of scholarly communities is rewarding, necessary, and is more likely to result in impact. However, there are barriers that limit the ease with which this can occur (e.g., lack of institutional structures and funding to facilitate cross-disciplinary exploration). Occasionally, there can be significant risk associated with doing interdisciplinary work (e.g., lack of adequate measurement or recognition of work by disciplinary peers). Solving many of the world’s complex and pressing problems (e.g., climate change, sustainable agriculture, the burden of chronic disease, and aging populations) demands thinking and working across long-standing, but in some ways restrictive, academic boundaries. Academic institutions and key support structures, especially funding bodies, will play an important role in helping to realize what is readily apparent to all who contributed to this paper—that interdisciplinarity is essential for solving complex problems; it is the new norm. Failure to empower and encourage those doing this research will serve as a great impediment to training, knowledge, and addressing societal issues.
Hallin J & CR Landry. Regulation plays a multifaceted role in the retention of gene duplicates. PLOS Biology https://doi.org/10.1371/journal.pbio.3000519
Dandage R. & Landry CR. Paralog dependency indirectly affects the robustness of human cells. Molecular Systems Biology 15:e8871 (2019)
Charron G, Marsit S, Henault M, Martin H & CR Landry. Spontaneous whole-genome duplication restores fertility in interspecific hybrids. Nature Communications 10: 4126 (2019)
Marchant A*, Cisneros AF*, Dubé AK, Gagnon-Arsenault I, Ascencio D, Jain HA, Aubé S, Eberlein C, Evans-Yamamoto D, Yachie N & CR Landry. The role of structural pleiotropy and regulatory evolution in the retention of heteromers of paralogs. eLife 2019;8:e46754 (2019)
Nielly-Thibault L & CR Landry, Differences between the de novo proteome and its non-functional precursor can result from neutral constraints on its birth process, not necessarily from natural selection alone. Genetics 10.1534/genetics.119.302187 (2019)
Dandage R, Després PC, Yachie N & CR Landry, beditor: A computational workflow for designing libraries of guide RNAs for CRISPR base editing. Genetics 212(2):377-385 (2019)
Durand E, Gagnon-Arsenault I, Hallin I, Nielly-Thibault L, Namy O & CR Landry, The high turnover of ribosome-associated transcripts from de novo ORFs produces gene-like characteristics available for de novo gene emergence in wild yeast populations. Genome Research 29(6):932-943 (2019)
Eberlein C, Hénault M, Fijarczyk A, Charron G, Bouvier M, Kohn L, Anderson J, Landry CR. Hybridization is a recurrent evolutionary stimulus in wild yeast speciation. Nature Communications 10, Article number: 923 (2019)
Bleuven C, Dubé AK, N’guyen GQ, Gagnon-Arsenault I, Martin H & Landry CR,
A collection of barcoded natural isolates of Saccharomyces paradoxus to study microbial evolutionary ecology. MicrobiologyOpen accepted https://doi.org/10.1002/mbo3.773 (2018)
N’guyen GQ, Martin N, Jain M, Lagace L, Landry CR & Filteau M, A systems biology approach to explore the impact of maple tree dormancy release on sap variation and maple syrup quality. Scientific Reports, 8:14658 (2018)
Despres PC, Dube AK, Nielly-Thibault L, Yachie N & Landry CR, Double Selection Enhances the Efficiency of Target-AID and Cas9-Based Genome Editing in Yeast. G3
Dionne U, Chartier FJM, de los Santos YL, Lavoie N, Bernard DN, Banerjee SL, Otis F, Jacquet K, Tremblay MG, Jain M, Bourassa S, Gish GD, Gagné JP, Poirier GG, Laprise P, Voyer N, Landry CR, Doucet N & Bisson N, Direct phosphorylation of SRC Homology 3 domains by tyrosine kinase receptors disassembles ligand-induced signalling networks. Molecular Cell 70:1-13 (2018)
Wolters JF, Charron G, Gaspary A, Landry CR, Fiumera AC & Fiumera HI, Mitochondrial recombination reveals mito-mito epistasis in yeast. Genetics 209:307-319 (2018)
Chrétien AE, Gagnon-Arsenault I, Dubé AK, Barbeau X, Després PC, Lamothe C, Dion-Côté AM, Lagüe P & Landry CR, Extended linkers improve the detection of protein-protein interactions (PPIs) by dihydrofolate reductase protein-fragment complementation assay (DHFR PCA) in living cells. Molecular & Cellular Proteomics 17:373-383 (2018)
Hénault M*, Eberlein C*, Charron G, Durand E, Nielly-Thibault L, Martin H & Landry CR, Yeast population genomics goes wild: the case of Saccharomyces paradoxus. In: Polz M, Rajora OP (eds) Population genomics: microorganisms. Springer (2017)
Samandi S, Roy AV, Delcourt V, Lucier JF, Gagnon J, Beaudoin MC, Vanderperre B, Breton MA, Motard J, Jacques JF, Brunelle M, Gagnon-Arsenault I, Fournier I, Ouangraoua A, Hunting DJ, Cohen AA, Landry CR, Scott MS & Roucou X, Deep transcriptome annotation enables the discovery and functional characterization of cryptic small proteins. eLife 6:e27860 (2017)
Landry CR & Diss G, Molecular dependency impacts on the compensating ability of paralogs: a response to Veitia. Trends in Genetics 33:657-658 (2017)
Leducq JB*, Henault M*, Charron G, Nielly-Thibault L, Terrat Y, Fiumera HL, Shapiro BJ & Landry CR, Mitochondrial recombination and introgression during speciation by hybridization. Molecular Biology and Evolution 34:1947-1959 (2017)
Eberlein C, Nielly-Thibault L, Maaroufi H, Dubé AK, Leducq JB, Charron G & Landry CR, The rapid evolution of an ohnolog contributes to the ecological specialization of incipient yeast species. Molecular Biology and Evolution 34:2173-2186 (2017)
Charron G & Landry CR, No evidence for extrinsic post-zygotic isolation in a wild Saccharomyces yeast system. Biology Letters 13:20170197 (2017)
Marsit S, Leducq JB, Durand E, Marchant A, Filteau M & Landry CR, Evolutionary biology through the lens of budding yeast comparative genomics. Nature Reviews Genetics 18:581-598 (2017)
Peris D, Moriarty RV, Alexander WG, Baker EC, Sylvester K, Sardi M, Langdon QK, Libkind D, Wang QM, Bai FY, Leducq JB, Charron G, Landry CR, Sampaio JP, Gonçalves P, Hyma KE, Fay JC, Sato TK & Hittinger CT, Hybridization and adaptive evolution of diverse Saccharomyces species for cellulosic biofuel production. Biotechnology for Biofuels 10:78 (2017)
Diss G, Gagnon-Arsenault I, Dion-Coté AM, Vignaud H, Ascencio DI, Berger CM & Landry CR, Gene duplication can impart fragility, not robustness, in the yeast protein interaction network. Science 355:630-634 (2017)
Hébert FO, Grambauer S, Barber I, Landry CR & Aubin-Horth N, Major host transitions are modulated through transcriptome-wide reprogramming events in Schistocephalus solidus, a threespine stickleback parasite. Molecular Ecology 26:1118–1130 (2017)
Xia W, Nielly-Thibault L, Charron G, Landry CR, Kasimer D, Anderson JB & Kohn LM, Population genomics reveals structure at the individual, host-tree scale and persistence of genotypic variants of the undomesticated yeast Saccharomyces paradoxus in a natural woodland. Molecular Ecology 26:995–1007 (2017)
Hénault M & CR Landry. When nuclear-encoded proteins and mitochondrial RNAs do not get along, species split apart. EMBO Reports 18:8–10 (2017)
Caron D, Byrne DP, Thebault P, Soulet D, Landry CR, Eyers PA & Elowe S, Mitotic phosphotyrosine network analysis reveals that tyrosine phosphorylation regulates Polo-like kinase 1 (PLK1). Science Signaling 9:rs14 (2016)
Filteau M, Charron G & Landry CR, Identification of the fitness determinants of budding yeast on a natural substrate. The ISME Journal 11:959–971 (2016)
Bleuven C & Landry CR, Molecular and cellular bases of adaptation to a changing environment in microorganisms. Proceedings of the Royal Society B 283:20161458 (2016)
Peris D, Langdon QK, Moriarty RV, Sylvester K, Bontrager M, Charron G, Leducq JB, Landry CR, Libkind D & Hittinger CT, Complex ancestries of lager-brewing hybrids were shaped by standing variation in the wild yeast Saccharomyces eubayanus. PLoS Genetics 12:e1006155 (2016)
Hébert FO, Grambauer S, Barber I, Landry CR & Aubin-Horth N, Transcriptome sequences spanning key developmental states as a resource for the study of the cestode Schistocephalus solidus, a threespine stickleback parasite. GigaScience 5:24 (2016)
Leducq JB*, Nielly-Thibault L*, Charron G*, Eberlein C, Verta JP, Samani P, Sylvester K, Hittinger CT, Bell G & Landry CR, Speciation driven by hybridization and chromosomal plasticity in a wild yeast. Nature Microbiology 1:15003 (2016)
Landry CR, Analysis of biological systems. Invited book review for The Quarterly Review of Biology (2016)
Verta JP, Landry CR & Mackay J, Dissection of expression-quantitative trait locus and allele specificity using a haploid/diploid plant system – insights into compensatory evolution of transcriptional regulation within populations. New Phytologist 211:159–171 (2016)
Barbosa R, Almeida P, Safar SVB, Santos RO, Morais PB, Nielly-Thibault L, Leducq JB, Landry CR, Gonçalves P, Rosa CA & Sampaio JP, Evidence of natural hybridization in Brazilian wild lineages of Saccharomyces cerevisiae. Genome Biology and Evolution 18:317–329 (2016)
Filteau M, Hamel V & Landry CR, La levure à vin – Modèle d’étude des gènes et des maladies humaines dans un contexte personnalisé. Médecine/Sciences 32:332–334 (2016)
Michnick SW, Landry CR, Levy ED, Diss G, Ear PH, Kowarzyk J, Malleshaiah MK, Messier V & Tchekanda E, Protein-fragment complementation assays for large-scale analysis, functional dissection, and spatiotemporal dynamic studies of protein-protein interactions in living cells. Cold Spring Harbor Protocol (2016)
Michnick SW, Levy ED, Landry CR, Kowarzyk J & Messier V, The dihydrofolate reductase protein-fragment complementation assay: a survival-selection assay for large-scale analysis of protein-protein interactions. Cold Spring Harbor Protocol (2016)
Diss G & Landry CR, Combining the dihydrofolate reductase protein-fragment complementation assay with gene deletions to establish genotype-to-phenotype maps of protein complexes and interaction networks. Cold Spring Harbor Protocol (2016)
Filteau M, Hamel V, Pouliot MC, Gagnon-Arsenault I, Dubé AK & Landry CR, Evolutionary rescue by compensatory mutations is constrained by genomic and environmental backgrounds. Molecular Systems Biology 11:832 (2015)
Filteau M, Vignaud H, Rochette S, Diss G, Chrétien AE, Berger CM & Landry CR, Multi-scale perturbations of protein interactomes reveal their mechanisms of regulation, robustness and insights into genotype-phenotype maps. Briefings in Functional Genomics 15:130–137 (2015)
Eberlein C, Leducq JB & Landry CR, The genomics of wild yeast populations sheds lights on the domestication of man’s best (micro) friend. Molecular Ecology 24:5309-5311 (2015)
Nigg M, Laroche J, Landry CR & Bernier L, RNAseq analysis highlights specific transcriptome signatures of yeast and mycelial growth phases in the Dutch elm disease fungus Ophiostoma novo-ulmi. G3: Genes|Genomes|Genetics 5:2487-2495 (2015)
Torres-Quiroz F, Filteau M & Landry CR, Feedback regulation between autophagy and PKA. Autophagy 11:1181-1183 (2015)
Freel KC, Charron G, Leducq JB, Landry CR & Schacherer J, Lachancea quebecensis sp. nov., a yeast species consistently isolated from the tree bark in the Canadian province of Quebec. International Journal of Systematic and Evolutionary Microbiology 65:3392-3399 (2015)
Filteau M, Diss G, Torres-Quiroz F, Dubé AK, Schraffl A, Bachmann VA, Gagnon-Arsenault I, Chrétien AE, Steunou AL, Dionne U, Côté J, Bisson N, Stefan E & Landry CR, Systematic identification of signal integration by protein kinase A. PNAS 112:4501-4506 (2015)
Hebert FO, Phelps L, Samonte I, Panchal M, Grambauer S, Barber I, Kalbe M, Landry CR & Aubin-Horth N, Identification of candidate mimicry proteins involved in parasite-driven phenotypic changes. Parasites & Vectors 8:225 (2015)
Landry CR, Zhong X, Nielly-Thibault L & Roucou X, Found in translation: functions and evolution of a recently discovered alternative proteome. Current Opinion in Structural Biology 32:74–80 (2015)
Boutchueng-Djidjou M, Collard-Simard G, Fortier S, Hébert SS, Kelly I, Landry CR & Faure RL, The last enzyme of the de novo purine synthesis pathway 5-aminoimidazole-4-carboxamide ribonucleotide formyltransferase/IMP cyclohydrolase (ATIC) plays a central role in insulin signalling and the Golgi/endosomes protein network. Molecular and Cellular Proteomics 14:1079-1092 (2015)
Stockwell SR, Landry CR & Rifkin SA, The yeast galactose network as a quantitative model for cellular memory. Molecular BioSystems 11:28-37 (2015)
Samani P, Low-Decarie E, McKelvey K, Bell T, Burt A, Koufopanou V, Landry CR & Bell G, Metabolic variation in natural populations of wild yeast. Ecology and Evolution 5:722-732 (2015)
Rochette S*, Diss G*, Filteau M, Leducq JB, Dubé AK & Landry CR, Genome-wide protein-protein interaction screening by Protein-fragment Complementation Assay (PCA) in living cells. Journal of Visualized Experiments 97:e52255 (2015)
Nguyen Ba AN, Strome B, Hua JJ, Desmond J, Gagnon-Arsenault I, Weiss EL, Landry CR & Moses AM, Detecting functional divergence after gene duplication through evolutionary changes in posttranslational regulatory sequences. PLoS Computational Biology 12:e1003977 (2014)
Charron G*, Leducq JB* & Landry CR, Chromosomal variation segregates within incipient species and correlates with reproductive isolation. Molecular Ecology 23:4362-4372 (2014)
Landry CR, Freschi L, Zarin T & Moses AM, Turnover of protein phosphorylation evolving under stabilizing selection. Frontiers in Genetics 5:245 (2014)
Goldman A, Roy J, Bodenmiller B, Wanka S, Landry CR, Aebersold R & Cyert MS, The calcineurin signaling network evolves via conserved kinase-phosphatase modules that transcend substrate identity. Molecular Cell 55:422-435 (2014)
Leducq JB*, Charron G*, Samani P, Dubé AK, Sylvester K, James B, Almeida P, Sampaio JP, Hittinger CT, Bell G & Landry CR, Local climatic adaptation in a widespread microorganism. Proceedings of the Royal Society B 281:20132472 (2014)
Freschi L, Osseni M & Landry CR, Functional divergence and evolutionary turnover in mammalian phosphoproteomes. PLoS Genetics 10:e1004062 (2014)
Landry CR & Aubin-Horth N, Recent advances in ecological genomics: from phenotypic plasticity to convergent and adaptive evolution and speciation. In: Landry C, Aubin-Horth N (eds) Ecological Genomics. Advances in Experimental Medicine and Biology, 781. Springer, Dordrecht (2014)
Rochette S, Gagnon-Arsenault I, Diss G & Landry CR, Modulation of the yeast protein interactome in response to DNA damage. Journal of Proteomics 100:25-36 (2014)
Diss G, Ascencio D, DeLuna A & Landry CR, Molecular mechanisms of paralogous compensation and the robustness of cellular networks. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution 322:488-499 (2014)
Charron G, Leducq JB, Bertin C, Dubé AK & Landry CR, Exploring the northern limit of the distribution of Saccharomyces cerevisiae and Saccharomyces paradoxus in North America. FEMS Yeast Research 14:281-288 (2014)
Landry CR*, Levy ED*, Abd Rabbo D, Tarassov K & Michnick SW, Extracting insight from noisy cellular networks. Cell 155:983–989 (2013)
Diss G, Dubé AK, Boutin J, Gagnon-Arsenault I & Landry CR, A systematic approach for the genetic dissection of protein complexes in living cells. Cell Reports 3:2155–2167 (2013)
See also Nature Methods 10:821 (2013)
Diss G, Filteau M, Freschi L, Leducq JB, Rochette S, Torres-Quiroz F & Landry CR, Integrative avenues for exploring the dynamics and evolution of protein interaction networks. Current Opinion in Biotechnology 24:775-783 (2013)
Verta JP, Landry CR & Mackay JJ, Are long-lived trees poised for evolutionary change? Single locus effects in the evolution of gene expression networks in spruce. Molecular Ecology 22:23692379 (2013)
Gagnon-Arsenault I, Marois Blanchet FC, Rochette S, Diss G, Dubé AK & Landry CR, Transcriptional divergence plays a role in the rewiring of protein interaction networks after gene duplication. Journal of Proteomics 81:112-125 (2013)
Freschi L, Torres-Quiroz F, Dubé AK & Landry CR, qPCA: a scalable assay to measure the perturbation of protein-protein interactions in living cells. Molecular BioSystems 9:36-43 (2013)
Leducq JB, Charron G, Diss G, Gagnon-Arsenault I, Dubé AK & Landry CR, Evidence for the robustness of protein complexes to inter-species hybridization. PLoS Genetics 8:e1003161 (2012)
Goyette G*, Boulais J*, Carruthers NJ, Landry CR, Jutras I, Duclos S, Dermine JF, Michnick SW, LaBoissière S, Lajoie G, Barreiro L, Thibault P & Desjardins M, Proteomic characterization of phagosomal membrane microdomains during phagolysosome biogenesis and evolution. Molecular & Cellular Proteomics 11:1365-1377 (2012)
Pavey SA, Bernatchez L, Aubin-Horth N & Landry CR, What is needed for next-generation ecological and evolutionary genomics? Trends in Ecology and Evolution 27:673-678 (2012)
Landry CR & Rifkin SA, The genotype-phenotype maps of systems biology and quantitative genetics: distinct and complementary. In: Soyer O (eds) Evolutionary Systems Biology. Advances in Experimental Medicine and Biology, 751. Springer, New York (2012)
Diss G, Freschi L & Landry CR, Where do phosphosites come from and where do they go after gene duplication? International Journal of Evolutionary Biology 2012:843167 (2012)
Levy ED, Michnick SW & Landry CR, Protein abundance is key to distinguish promiscuous from functional phosphorylation based on evolutionary information. Philosophical Transactions of The Royal Society B Biological Sciences 367:2594-606 (2012)
Lee S, Thebault P, Freschi L, Beaufils S, Blundell TL, Landry CR, Bolanos-Garcia VM & Elowe S, Characterization of spindle checkpoint kinase Mps1 reveals a domain with functional and structural similarities to tetratricopeptide repeat motifs of the Bub1 and BubR1 checkpoint kinases. The Journal of Biological Chemistry 287:5988-6001 (2012)
Landry CR, A cellular roadmap for the plant kingdom. Science 333:532-533 (2011)
Freschi L, Courcelles M, Thibault P, Michnick SW & Landry CR, Phosphorylation network rewiring by gene duplication. Molecular Systems Biology 7:504 (2011)
Michnick SW, Ear PH, Landry C, Malleshaiah MK & Messier V, Protein-fragment complementation assays for large-scale analysis, functional dissection and dynamic studies of protein-protein interactions in living cells. In: Luttrell L, Ferguson S (eds) Signal transduction protocols. Methods in Molecular Biology 756. Humana Press, Totowa NJ (2011)
2001 - 2010
Landry CR & Rifkin SA, Chromatin regulators shape the genotype-phenotype map. Molecular Systems Biology 6:434 (2010)
Boulais J, Trost M, Landry CR, Dieckmann R, Levy ED, Soldati T, Michnick SW, Thibault P & Desjardins M, Molecular characterization of the evolution of phagosomes. Molecular Systems Biology 6:423 (2010)
Landry CR & Aubin-Horth N, Gene network architecture as a canvas for the interpretation of ecological genomics investigations. Molecular Ecology 19:5084-5085 (2010)
Moses AM & Landry CR, Moving from transcriptional to phospho-evolution: generalizing regulatory evolution? Trends in Genetics 26:462-467 (2010)
Di Poi C, Diss G & Freschi L, Biodiversity matters in a changing world. Biology Letters 7:4-6 (2010) **Student initiative**
Levy ED*, Landry CR* & Michnick SW, Signaling through cooperation. Science 328:983-984 (2010)
Michnick SW, Ear PH, Landry CR, Malleshaiah MK & Messier V, A toolkit of protein-fragment complementation assays for studying and dissecting large-scale and dynamic protein-protein interactions in living cells. In: Weissman J, Guthrie C, Fink G (eds.) Guide to yeast genetics: functional genomics, proteomics and other systems analysis. Methods in Enzymology 470. Elsevier Press, New York USA (2010)
Fontanillas P, Landry CR, Wittkopp PJ, Russ C, Gruber JD, Nusbaum C & Hartl DL, Key considerations for measuring allelic expression on a genomic scale using high-throughput sequencing. Molecular Ecology 19:212–227 (2010)
Landry CR*, Levy ED* & Michnick SW, Weak functional constraints on phosphoproteomes. Trends in Genetics 25:193-197 (2009)
Levy ED*, Landry CR* & Michnick SW, How perfect can protein interactomes be? Science Signalling 2:pe11 (2009)
Landry CR, Systems biology spins off a new model for the study of canalization. Trends in Ecology and Evolution 24:63-66 (2009)
Cheung V, Chua G, Batada NN, Landry CR, Michnick SW, Hughes TR & Winston F, Chromatin- and transcription-related factors repress transcription from within coding regions throughout the Saccharomyces cerevisiae genome. PloS Biology 6:e277 (2008)
Tarassov K*, Messier V*, Landry CR*, Radinovic S*, Serna Molina MM, Shames I, Malitskaya Y, Vogel J, Bussey H & Michnick SW, An in vivo map of the yeast protein interactome. Science 320:1465-1479 (2008)
Lynch M, Sung W, Morris K, Coffey N, Landry CR, Dopman EB, Dickinson WJ, Okamoto K, Kulkarni S, Hartl DL & Thomas WK, A Genome-wide view of the spectrum of spontaneous mutations in yeast. Proceedings of the National Academy of Sciences of the United States of America 105:9272-9277 (2008)
Brown KM, Landry CR, Hartl DL & Cavalieri D, Cascading transcriptional effects of a naturally occurring frameshift mutation in Saccharomyces cerevisiae. Molecular Ecology 17:2985-2997 (2008)
Stefan E, Aquin S, Berger N, Landry CR, Nyfeler B, Bouvier M & Michnick SW, Quantification of dynamic protein complexes using Renilla luciferase-fragment complementation applied to protein kinase A activities in vivo. Proceedings of the National Academy of Sciences of the United States of America 104:16916-16921 (2007)
Landry CR*, Lemos B*, Rifkin SA, Dickinson WJ & Hartl DL, Genetic properties influencing the evolvability of gene expression. Science 317:118-121 (2007)
Landry CR, Castillo-Davis CI, Ogura A, Liu JS & Hartl DL, Systems-level analysis and evolution of the Drosophila phototransduction cascade. Proceedings of the National Academy of Sciences of the United States of America 104:3283-3288 (2007)
Landry CR & Aubin-Horth N, Ecological annotation of genes and genomes through ecological genomics. Molecular Ecology 16:4419-4421 (2007)
Landry CR, Hartl DL & Ranz JM, Genome clashes in hybrids: insights from gene expression. Heredity 99:483-493 (2007)
Lemos B, Landry CR, Fontanillas P, Renn SP, Kulathinal R, Brown KM & Hartl DL, Evolution of Genomic Expression. In Pagel M, Pomiankowski A (eds) Evolutionary genomics and proteomics. Sinauer Associates, Sunderland, MA (2007)
Salathia N, Lee HN, Sangster TA, Morneau K, Landry CR, Schellenberg K, Behere AS, Gunderson KL, Cavalieri D, Jander G & Queitsch C, Indel array: an affordable alternative for genotyping. Plant Journal 51:727-737 (2007)
Landry CR, Townsend JP, Hartl DL & Cavalieri D, Ecological and evolutionary genomics of Saccharomyces cerevisiae. Molecular Ecology 15:575-591 (2006)
Landry CR, Oh J, Hartl DL & Cavalieri D, Genome-wide scan reveals that genetic variation for transcriptional plasticity in yeast is biased towards multi-copy and dispensable genes. Gene 366:343-351 (2006)
Landry CR, Wittkopp PJ, Taubes CH, Ranz JM, Clark AG & Hartl DL, Compensatory cis-trans evolution and the dysregulation of gene expression in interspecific hybrids of Drosophila. Genetics 171:1813-1822 (2005)
Giuntini E, Mengoni A, De Filippo C, Cavalieri D, Aubin-Horth N, Landry CR, Becker A & Bazzicalupo M, Large-scale genetic variation of the symbiosis-required megaplasmid pSymA revealed by comparative genomic analysis of Sinorhizobium meliloti natural strains. BMC Genomics 6: 158 (2005)
Aubin-Horth N, Landry CR, Letcher BH & Hofmann HA, Alternative life-histories shape brain gene expression profiles in males of the same population. Proceedings of the Royal Society B 272:1655-1662 (2005)
Landry C, Geyer LB, Arakaki Y, Uehara T & Palumbi SR, Recent speciation in the Indo-West Pacific: rapid evolution of gamete recognition and sperm morphology in cryptic species of sea urchin. Proceedings of the Royal Society B 270:1839-1847 (2003)
Bernatchez L & Landry C, MHC studies in nonmodel vertebrates: what have we learned about natural selection in 15 years? Journal of Evolutionary Biology 16:363-377 (2003)
Landry C & Bernatchez L, Comparative analysis of population structure across environments and geographic scales at major histocompatibility complex and microsatellite Atlantic salmon (Salmo salar). Molecular Ecology 10:2525-2540 (2001)
Landry C, Garant D, Duchesne P & Bernatchez L, “Good genes as heterozygosity”: the major histocompatibility complex and mate choice in Atlantic salmon (Salmo salar). Proceedings of the Royal Society B 268:1279-1285 (2001)