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Nicholas Putnam Assistant Professor Assistant Professor of Ecology and Evolutionary Biology e-mail:[email protected] Sc. B. Physics (1996) Brown University, Providence, RI Ph.D. Physics, with Designated Emphasis in Genomic and Computational Biology (2004) University of California, Berkeley, Berkeley, California Department Affiliations Institute of Biosciences and Bioengineering Websites Lab Website Research Areas Evolutionary Biology, Bioinformatics, Comparative Genomics Evolution of Genome Organization Research Vision After five hundred million years of independent evolution since their divergence in the Pre-Cambrian, metazoan genomes still retain recognizable similarities that allow the partial reconstruction not only of their common ancestors’ protein coding genes, but of its genomic organization (intron-exon structures, organization into chromosomes, and cisregulatory elements). Also, there is new evidence for very ancient conservation of elements of the gene networks controlling body plan and neural patterning. These recent developments, and the dramatic increase in metazoan diversity spanned by genomic data sets, make comparative genomics a promising approach to some of evolution and development's most important questions: How do novelty and complexity arise in evolution? What impact does evolutionary history have on the architecture, function, and future evolution of biological systems? Our research approaches these questions by coupling the development of novel computational analyses with genomic experiments designed to leverage them. Our goal is to reconstruct ancestral genomes, pathways, and regulatory networks, and use these reconstructions to test the predictions of models of evolution, and functional hypotheses. Projects: Evolution of Genome Organization It has recently been shown that the organization of animal genomes at the chromosomal scale is preserved in the human genome and in the genomes of very distantly-related animals in other phyla (sea anemones, mollusks, and others; but not in insects or nematodes), and is therefore a relic of, and allows us to reconstruct, the genome organization of ancient animal ancestors going back at least to the last common ancestor of all “eumetazoans” — all animals excluding sponges — and perhaps further. The biological explanation for this conservation is unknown, but there are two broad possibilities: either this organization is conserved because it has a role in an unknown mechanism for regulating the genome, or it has no functional importance to the animal, but changes much more slowly than was suggested by previously-available data. This project aims to answer this question, and investigate the mechanisms and dynamics of genome evolution. The primary method we employ is computational comparative genomics: we are building on methods developed by Dr. Putnam as a post-doc in Dan Rokhsar’s lab, comparing the largescale organization of sequenced genomes (and other genomic data sets) to theoretical models of genome evolution. Genome Structure Variation in a Natural Population The recentlypublished genome of the Florida lancelet, also commonly called amphioxus (Branchiostoma floridae) showed a very high degree of variation between the two copies of the genome sequenced (polymorphism). The source DNA for the project was taking from a single wildcaught animal, and therefore contained two copies of the genome: one inherited from each parent of that individual. The assembly of the genome was able to reconstruct both of these copies independently for many regions of the genome, providing a large data set in which to examine variations between the two sampled genotypes, including insertions (or deletions) in one relative to the other, and inversions. The distribution of sequence differences between the two genotypes is consistent with a very large population size, which has been free of dramatic bottlenecks for a long time, making it a potentially useful natural laboratory for studying the rates of various mutational processes, including those that produce structural variation. We are using this resource to identify structural variants in the data, which serve as the starting point for sampling from the B. floridae population in the Gulf of Mexico. Teaching Areas Bioinformatics, Phylogenetics, Evolutionary Biology, Computational Biology Selected Publications Refereed articles Sucgang, R., Kuo, A., Tian, X., Salerno, W., Parikh, A., Feasley, C., Dalin, E., Tu, H., Huang, E., Barry, K., Lindquist, E., Shapiro, H., Bruce, D., Schmutz, J., Salamov, A., Fey, P., Gaudet, P., Anjard, A., Babu, M., Basu, S., Bushmanova, Y., van der Wel, H., Katoh-Kurasawa, M., Dinh, C., Coutinho, P., Saito, S., Elias, M., Schaap, P., Kay, R., Henrissat, B., Eichinger, L., Rivero, F., Putnam, N., West, C., Loomis, W., Chisholm, R., Shaulsky, G., Strassmann, J., Queller, D., Kuspa, A., and Grigoriev, I. 2011. Comparative genomics of the social amoebae Dictyostelium discoideum and Dictyostelium purpureum. Genome Biology 12:R20 Chapman JA, Kirkness EF, Simakov O, Hampson SE, Mitros T, Weinmaier T, Rattei T, Balasubramanian PG, Borman J, Busam D, Disbennett K, Pfannkoch C, Sumin N, Sutton GG, Viswanathan LD, Walenz B, Goodstein DM, Hellsten U, Kawashima T, Prochnik SE, Putnam NH, Shu S, Blumberg B, Dana CE, Gee L, Kibler DF, Law L, Lindgens D, Martinez DE, Peng J, Wigge PA, Bertulat B, Guder C, Nakamura Y, Ozbek S, Watanabe H, Khalturin K, Hemmrich G, Franke A, Augustin R, Fraune S, Hayakawa E, Hayakawa S, Hirose M, Hwang JS, Ikeo K, Nishimiya-Fujisawa C, Ogura A, Takahashi T, Steinmetz PR, Zhang X, Aufschnaiter R, Eder MK, Gorny AK, Salvenmoser W, Heimberg AM, Wheeler BM, Peterson KJ, Böttger A, Tischler P, Wolf A, Gojobori T, Remington KA, Strausberg RL, Venter JC, Technau U, Hobmayer B, Bosch TC, Holstein TW, Fujisawa T, Bode HR, David CN, Rokhsar DS, Steele RE. "The dynamic genome of Hydra." Nature, 464 (2010) : 592-6. Articles David M Goodstein, Shengqiang Shu, Russell Howson, Rochak Neupane, Richard D Hayes, Joni Fazo, Therese Mitros, William Dirks, Uffe Hellsten, Nicholas Putnam, Daniel S Rokhsar "Phytozome: a comparative platform for green plant genomics." Nucleic acids research (2012/1/1) Oleg Simakov, Ferdinand Marletaz, Sung-Jin Cho, Eric Edsinger-Gonzales, Paul Havlak, Uffe Hellsten, Dian-Han Kuo, Tomas Larsson, Jie Lv, Detlev Arendt, Robert Savage, Kazutoyo Osoegawa, Pieter de Jong, Jane Grimwood, Jarrod A Chapman, Harris Shapiro, Andrea Aerts, Robert P Otillar, Astrid Y Terry, Jeffrey L Boore, Igor V Grigoriev, David R Lindberg, Elaine C Seaver, David A Weisblat, Nicholas H Putnam, Daniel S Rokhsar "Insights into bilaterian evolution from three spiralian genomes." Nature (2012/12/19) Hellsten U, Harland RM, Gilchrist MJ, Hendrix D, Jurka J, Kapitonov V, Ovcharenko I, Putnam NH, Shu S, Taher L, Blitz IL, Blumberg B, Dichmann DS, Dubchak I, Amaya E, Detter JC, Fletcher R, Gerhard DS, Goodstein D, Graves T, Grigoriev IV, Grimwood J, Kawashima T, Lindquist E, Lucas SM, Mead PE, Mitros T, Ogino H, Ohta Y, Poliakov AV, Pollet N, Robert J, Salamov A, Sater AK, Schmutz J, Terry A, Vize PD, Warren WC, Wells D, Wills A, Wilson RK, Zimmerman LB, Zorn AM, Grainger R, Grammer T, Khokha MK, Richardson PM, Rokhsar DS. "The genome of the Western clawed frog Xenopus tropicalis.." Science, 328 (2010) : 633-6. Srivastava M, Simakov O, Chapman J, Fahey B, Gauthier ME, Mitros T, Richards GS, Conaco C, Dacre M, Hellsten U, Larroux C, Putnam NH, Stanke M, Adamska M, Darling A, Degnan SM, Oakley TH, Plachetzki DC, Zhai Y, Adamski M, Calcino A, Cummins SF, Goodstein DM, Harris C, Jackson DJ, Leys SP, Shu S, Woodcroft BJ, Vervoort M, Kosik KS, Manning G, Degnan BM, Rokhsar DS. "The Amphimedon queenslandica genome and the evolution of animal complexity.." Nature, 466 (2010) : 720-6. Takeshi Kawashima, Shuichi Kawashima, Chisaki Tanaka, Miho Murai, Masahiko Yoneda, Nicholas H. Putnam, Daniel S. Rokhsar, Minoru Kanehisa, Nori Satoh and Hiroshi Wada "Domain shuffling and the evolution of vertebrates." Genome Research, 19 (2009) : 13931403. Martinez et al. Genome sequencing and analysis of the biomass-degrading fungus Trichoderma reesei (syn. Hypocrea jecorina). Nat Biotechnol (2008) vol. 26 (5) pp. 553-60 Holland et al. The amphioxus genome illuminates vertebrate origins and cephalochordate biology. Genome Res (2008) vol. 18 (7) pp. 1100-11 Srivastava et al. The Trichoplax genome and the nature of placozoans. Nature (2008) vol. 454 (7207) pp. 955-60 Putnam et al. The amphioxus genome and the evolution of the chordate karyotype. Nature (2008) vol. 453 (7198) pp. 1064-71 King et al. The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature (2008) vol. 451 (7180) pp. 783-8 Conference papers Lv, J, Havlak, P, and Putnam, N. 2011. Constraints on genes shape long-term conservation of macro-synteny in metazoan genomes. BMC Bioinformatics 12:S11 Presentations Invited Talks "Reconstructing ancient transitions in metazoan genome organization." Developmental Biology of the Sea Urchin XVIII, Woods Hole, MA. (April 24 2008) Keynote Speaker "Long time scale evolution of metazoan genome organization. ." Eighth Annual RECOMB Satellite Workshop on Comparative Genomics, Ottawa, Canada. (October 11, 2010) Posters "Testing for the action of selection on genome rearrangement dynamics deep in the metazoan tree. ." Society for Integrative and Comparative Biology, Seattle, Washington. (1/4/2010) Seminar Speaker Lv, J., Havlak, P, and Putnam, N. 2011. Constraints on genes shape long-term conservation of macro-synteny in metazoan genomes. Ninth Annual RECOMB Conference on Comparative Genomics. Oct. 7-10, 2011. Galway, Ireland. Putnam, N. 2011. Selective constraints on the evolution of metazoan genome organization. Society for Molecular Biology and Evolution (SMBE) conference. July 26-30, 2011. Kyoto, Japan "Reconstructing ancient transitions in metazoan genome evolution.." Okinawa Institute of Science and Technology, Okinawa, Japan. (3/19/09) "Reconstructing ancient transitions in metazoan genome evolution.." University of Houston, Department of Biology, Houston, TX. (10/7/09) "Reconstructing ancient transitions in metazoan genome evolution.." Rice University Institute of Biosciences and Bioengineering Symposium, Houston, TX. (7/15/09) "Reconstructing ancient transitions in metazoan genome evolution.." University of Pittsburgh, Department of Biology, Pittsburgh, PA. (11/23/09) "Reconstructing ancient transitions in metazoan genome evolution.." Dept. Marine Biology and Oceanography, Texas A&M University, Galveston, TX. (2/3/09) Supervised Theses & Dissertations Xiaoyun "Sean" Liao, PhD Evolution of Altruism and Eusociality: Fitness Cost and Benefit, Genetic Relatedness. (2012) (Committee Member) Shuwei Li, PhD Network-guided population genomics of warfarin resistant rats (Rattus norvegicus) . (2015) (Committee Member) Ching-Hua Shih, PhD Exploration of some effects genetic interactions have on polyphorism and divergence. (2015) (Committee Member) Jie Lv, PhD Functional constraints on genes shape long-term conservation of synteny in metazoan genomes. (2017) (Thesis or Dissertation Director) Juan Diaz, PhD Testing models of adaptive trait evolution: Studies of convergent evolution, ancestral standing variation and de novo mutation in candidate genes underlying rodenticide resistance and coat color variation in rats. (2018) (Committee Member) Jiaxing Yue, PhD Population Genomics of Amphioxus. (2018) (Thesis or Dissertation Director) Kimberly Vincent, PhD The role of chromosomal inversions in the adaptation of an invasive species, Aedes albopictus. (Thesis or Dissertation Director) Kimberly Y Vincent, Ph.D. The role of CCAT2 in miRNA expression and processing. (Thesis or Dissertation Director) Jie Lv, Ph.D. TBD. (Thesis or Dissertation Director) Shuwei Li, Ph.D. Detecting selection on genetic network components using population genetic statistics. (Committee Member) Ching-Hua Shih, Ph.D. The speciation and comparative genomics of genetic barriers to gene flow. (Committee Member) Chandra Jack, Ph.D. Kin discrimination in Dictyostelium. (Committee Member) Awards, Prizes, & Fellowships Kavli Fellow, National Academy of Science (2011) Beckman Young Investigator Award, Arnold and Mabel Beckman Foundation (August 2009)