Can Yeast (S. cerevisiae) Metabolic Volatiles Provide Polymorphic Signaling?

Chemical signaling between organisms is a ubiquitous and evolutionarily dynamic process that helps to ensure mate recognition, location of nutrients, avoidance of toxins, and social cooperation. Evolutionary changes in chemical communication systems progress through natural variation within the organism generating the signal as well as the responding individuals. A promising yet poorly understood system with which to probe the importance of this variation exists between D. melanogaster and S. cerevisiae. D. melanogaster relies on yeast for nutrients, while also serving as a vector for yeast cell dispersal. Both are outstanding genetic and genomic models, with Drosophila also serving as a preeminent model for sensory neurobiology. To help develop these two genetic models as an ecological model, we have tested if - and to what extent - S. cerevisiae is capable of producing polymorphic signaling through variation in metabolic volatiles. We have carried out a chemical phenotyping experiment for 14 diverse accessions within a common garden random block design. Leveraging genomic sequences for 11 of the accessions, we ensured a genetically broad sample and tested for phylogenetic signal arising from phenotypic dataset. Our results demonstrate that significant quantitative differences for volatile blends do exist among S. cerevisiae accessions. Of particular ecological relevance, the compounds driving the blend differences (acetoin, 2-phenyl ethanol and 3-methyl-1-butanol) are known ligands for D. melanogasters chemosensory receptors, and are related to sensory behaviors. Though unable to correlate the genetic and volatile measurements, our data point clear ways forward for behavioral assays aimed at understanding the implications of this variation.

[1]  J. Piškur,et al.  Yeast, not fruit volatiles mediate Drosophila melanogaster attraction, oviposition and development , 2012 .

[2]  Sergi Bermdez i Badia,et al.  A high-throughput behavioral paradigm for Drosophila olfaction - The Flywalk , 2012, Scientific Reports.

[3]  S. Rollmann,et al.  Genetic variation in odorant receptors contributes to variation in olfactory behavior in a natural population of Drosophila melanogaster. , 2012, Chemical senses.

[4]  Kevin R. Thornton,et al.  The Drosophila melanogaster Genetic Reference Panel , 2012, Nature.

[5]  A. Auton,et al.  Genome-wide patterns of genetic variation in worldwide Arabidopsis thaliana accessions from the RegMap panel , 2011, Nature Genetics.

[6]  Pavan Ramdya,et al.  Complementary Function and Integrated Wiring of the Evolutionarily Distinct Drosophila Olfactory Subsystems , 2011, The Journal of Neuroscience.

[7]  G. Ruxton,et al.  Plant-Animal Communication , 2011 .

[8]  Jing W. Wang,et al.  Presynaptic Facilitation by Neuropeptide Signaling Mediates Odor-Driven Food Search , 2011, Cell.

[9]  R. Benton,et al.  Acid sensing by the Drosophila olfactory system , 2010, Nature.

[10]  Joy Bergelson,et al.  Towards identifying genes underlying ecologically relevant traits in Arabidopsis thaliana , 2010, Nature Reviews Genetics.

[11]  R. Peakall,et al.  Pollinator specificity, floral odour chemistry and the phylogeny of Australian sexually deceptive Chiloglottis orchids: implications for pollinator-driven speciation. , 2010, The New phytologist.

[12]  M. Rausher,et al.  The pigment-scent connection: do mutations in regulatory vs. structural anthocyanin genes differentially alter floral scent production in Ipomoea purpurea? , 2010 .

[13]  R. Borges,et al.  Reducing the babel in plant volatile communication: using the forest to see the trees. , 2010, Plant biology.

[14]  David B. Witonsky,et al.  Using Environmental Correlations to Identify Loci Underlying Local Adaptation , 2010, Genetics.

[15]  L. Harmon,et al.  POOR STATISTICAL PERFORMANCE OF THE MANTEL TEST IN PHYLOGENETIC COMPARATIVE ANALYSES , 2010, Evolution; international journal of organic evolution.

[16]  Pavan Ramdya,et al.  Evolving olfactory systems on the fly. , 2010, Trends in genetics : TIG.

[17]  B. Hansson,et al.  Flying the Fly: Long-range Flight Behavior of Drosophila melanogaster to Attractive Odors , 2010, Journal of Chemical Ecology.

[18]  T. Yee The VGAM Package for Categorical Data Analysis , 2010 .

[19]  M. Knaden,et al.  Towards plant-odor-related olfactory neuroethology in Drosophila , 2009, Chemoecology.

[20]  A. Jürgens,et al.  Do carnivorous plants use volatiles for attracting prey insects , 2009 .

[21]  L. Macías-Rodríguez,et al.  The role of microbial signals in plant growth and development , 2009, Plant signaling & behavior.

[22]  Leonid Kruglyak,et al.  Comprehensive polymorphism survey elucidates population structure of Saccharomyces cerevisiae , 2009, Nature.

[23]  G. Franz,et al.  Conditional embryonic lethality to improve the sterile insect technique in Ceratitis capitata (Diptera: Tephritidae) , 2009, BMC Biology.

[24]  L. Vosshall,et al.  Variant Ionotropic Glutamate Receptors as Chemosensory Receptors in Drosophila , 2009, Cell.

[25]  R. Raguso,et al.  Geographic divergence in floral morphology and scent in Linanthus dichotomus (Polemoniaceae). , 2008, American journal of botany.

[26]  R. Raguso Wake Up and Smell the Roses: The Ecology and Evolution of Floral Scent , 2008 .

[27]  Robert P. Davey,et al.  Population genomics of domestic and wild yeasts , 2008, Nature.

[28]  J. Carlson,et al.  A Regulatory Code for Neuron-Specific Odor Receptor Expression , 2008, PLoS biology.

[29]  D. Goldstein,et al.  Which evolutionary processes influence natural genetic variation for phenotypic traits? , 2007, Nature Reviews Genetics.

[30]  Anne-Béatrice Dufour,et al.  The ade4 Package: Implementing the Duality Diagram for Ecologists , 2007 .

[31]  E. Pichersky,et al.  Scent engineering: toward the goal of controlling how flowers smell. , 2007, Trends in biotechnology.

[32]  G. Bell,et al.  Increased outbreeding in yeast in response to dispersal by an insect vector , 2007, Current Biology.

[33]  T. C. Turlings,et al.  Advances and challenges in the identification of volatiles that mediate interactions among plants and arthropods. , 2006, The Analyst.

[34]  R. Agarwala,et al.  Composition-based statistics and translated nucleotide searches: Improving the TBLASTN module of BLAST , 2006, BMC Biology.

[35]  J. W. Valentine,et al.  Out of the Tropics: Evolutionary Dynamics of the Latitudinal Diversity Gradient , 2006, Science.

[36]  Manfred Forstreuter,et al.  Behavioral responses of Drosophila to biogenic levels of carbon dioxide depend on life-stage, sex and olfactory context , 2006, Journal of Experimental Biology.

[37]  B. Potts,et al.  A framework for community and ecosystem genetics: from genes to ecosystems , 2006, Nature Reviews Genetics.

[38]  Pardis C Sabeti,et al.  Positive Natural Selection in the Human Lineage , 2006, Science.

[39]  John R. Carlson,et al.  Coding of Odors by a Receptor Repertoire , 2006, Cell.

[40]  S. Olsson,et al.  The chemosensory basis for behavioral divergence involved in sympatric host shifts II: olfactory receptor neuron sensitivity and temporal firing pattern to individual key host volatiles , 2006, Journal of Comparative Physiology A.

[41]  Shivani J Patel,et al.  Regulation of the human LAT gene by the Elf-1 transcription factor , 2006, BMC Molecular Biology.

[42]  D. Huson,et al.  Application of phylogenetic networks in evolutionary studies. , 2006, Molecular biology and evolution.

[43]  R. Raguso,et al.  When Flowers Smell Fermented: The Chemistry and Ontogeny of Yeasty Floral Scent in Pawpaw (Asimina triloba: Annonaceae) , 2006, International Journal of Plant Sciences.

[44]  Jihong Wang,et al.  The biosynthesis and regulation of biosynthesis of Concord grape fruit esters, including 'foxy' methylanthranilate. , 2005, The Plant journal : for cell and molecular biology.

[45]  R. Raguso,et al.  Chemistry and geographic variation of floral scent in Yucca filamentosa (Agavaceae). , 2005, American journal of botany.

[46]  Martin J. Mueller,et al.  Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. , 2005, Molecular plant-microbe interactions : MPMI.

[47]  C. Montell Drosophila TRP channels , 2005, Pflügers Archiv.

[48]  J. Cornuet,et al.  Assortative Mating in Sympatric Host Races of the European Corn Borer , 2005, Science.

[49]  Jeremy Schmutz,et al.  Widespread Parallel Evolution in Sticklebacks by Repeated Fixation of Ectodysplasin Alleles , 2005, Science.

[50]  D. Suckling,et al.  Volatile constituents of fermented sugar baits and their attraction to lepidopteran species. , 2005, Journal of agricultural and food chemistry.

[51]  N. Rosenberg distruct: a program for the graphical display of population structure , 2003 .

[52]  D. McKey,et al.  Protective ant-plant interactions as model systems in ecological and evolutionary research. , 2003 .

[53]  J. Feder,et al.  Fruit odor discrimination and sympatric host race formation in Rhagoletis , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[54]  M. Stephens,et al.  Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. , 2003, Genetics.

[55]  B. Birren,et al.  Sequencing and comparison of yeast species to identify genes and regulatory elements , 2003, Nature.

[56]  J. Tumlinson,et al.  Differential volatile emissions and salicylic acid levels from tobacco plants in response to different strains of Pseudomonas syringae , 2003, Planta.

[57]  T. Baker,et al.  Identification of Odors from Overripe Mango That Attract Vinegar Flies, Drosophila melanogaster , 2003, Journal of Chemical Ecology.

[58]  Pierre Taberlet,et al.  Landscape genetics: combining landscape ecology and population genetics , 2003 .

[59]  Bill S Hansson,et al.  Novel natural ligands for Drosophila olfactory receptor neurones , 2003, Journal of Experimental Biology.

[60]  Robert P. Adams,et al.  Identification of essential oil components by gas chromatography/quadrupole mass spectroscopy , 2001 .

[61]  P. Donnelly,et al.  Inference of population structure using multilocus genotype data. , 2000, Genetics.

[62]  Balasubramanian Narasimhan,et al.  Dynamic Display of Changing Posterior in Bayesian Survival Analysis: The Software , 1999 .

[63]  C. Wild,et al.  Vector Generalized Additive Models , 1996 .

[64]  P. Legendre,et al.  Comparison tests for dendrograms: A comparative evaluation , 1995 .

[65]  W. T. Starmer,et al.  Coadaptation ofDrosophila and yeasts in their natural habitat , 1986, Journal of Chemical Ecology.

[66]  W. T. Starmer,et al.  Comparisons of yeast florae from natural substrates and larval guts of southwestern Drosophila , 1982, Oecologia.

[67]  Anthony A. Williams,et al.  The gas chromatographic-mass spectrometric examination of the volatiles produced by the fermentation of a sucrose solution , 1981 .

[68]  A. R. Williams,et al.  Determination of methyl anthranilate in grape beverages by high-pressure liquid chromatography and fluorescence , 1977 .

[69]  M. W. Miller,et al.  The ecology of yeast flora associated with cactiphilic Drosophila and their host plants in the Sonoran desert , 1976, Microbial Ecology.

[70]  P. Schreier,et al.  Über die Biosynthese von Aromastoffen durch Mikroorganismen , 1975 .

[71]  P. O'donald,et al.  Evolution and the Genetics of Populations. Volume 2. The theory of gene frequencies . By Sewall Wright. Pp. 511. (University of Chicago Press, London 1970.) Price £6·75. , 1972, Journal of Biosocial Science.

[72]  G. Bush SYMPATRIC HOST RACE FORMATION AND SPECIATION IN FRUGIVOROUS FLIES OF THE GENUS RHAGOLETIS (DIPTERA, TEPHRITIDAE) , 1969, Evolution; international journal of organic evolution.

[73]  P. Raven,et al.  BUTTERFLIES AND PLANTS: A STUDY IN COEVOLUTION , 1964 .

[74]  Sandra L. Lindsay Food Preferences of Drosophila larvae , 1958, The American Naturalist.

[75]  M. Miller,et al.  Yeasts Found in the Alimentary Canal of Drosophila , 1956 .

[76]  E. Mrak,et al.  INTESTINAL YEAST FLORAS OF SUCCESSIVE POPULATIONS OF DROSOPHILA , 1952 .

[77]  T. Dobzhansky,et al.  ON FOOD PREFERENCES OF SYMPATRIC SPECIES OF DROSOPHILA , 1951 .

[78]  T. Dobzhansky Genetics and the Origin of Species , 1937 .

[79]  A. Bennett The Origin of Species by means of Natural Selection; or the Preservation of Favoured Races in the Struggle for Life , 1872, Nature.

[80]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[81]  G. Poppy,et al.  Why plant volatile analysis needs bioinformatics--detecting signal from noise in increasingly complex profiles. , 2008, Plant biology.

[82]  S. Zheng,et al.  Update on Ecological Genomics of Plant-Insect Interactions Ecological Genomics of Plant-Insect Interactions : From Gene to Community 1 [ C ] , 2008 .

[83]  Anupama Dahanukar,et al.  Insect odor and taste receptors. , 2006, Annual review of entomology.

[84]  Pardis C Sabeti,et al.  Positive Natural Selection in the Human , 2006 .

[85]  K. R. Clarke,et al.  Change in marine communities : an approach to statistical analysis and interpretation , 2001 .

[86]  J. Barker,et al.  Attraction of Larvae of Drosophila-Buzzatii and Drosophila-Aldrichi to Yeast Species Isolated From Their Natural-Environment , 1988 .

[87]  H. L. Carson,et al.  The Genetics and Biology of Drosophila , 1976, Heredity.