From the Cover. Contents. July 23, 2013 u vol. 110 u no. 30 u OPINION THIS WEEK IN PNAS QNAS LETTERS (ONLINE ONLY) COMMENTARIES
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1 July 23, 2013 u vol. 110 u no. 30 u Cover image: Pictured is a close-up of a fluffy yeast colony growing on an agar plate. Fluffy yeast colonies contain complex multicellular features and exhibit properties similar to bacterial biofilms. Zhihao Tan et al. identified yeast strains capable of reversibly switching between fluffy and smooth colonies, and showed that a gain or loss of a single chromosome could cause the yeast to toggle between the two forms. The findings indicate that a change in chromosome number could provide a quick, heritable, and reversible mechanism by which organisms can switch between phenotypes. See the article by Tan et al. on pages Image courtesy of Zhihao Tan. From the Cover A multicellular phenotypic switch Using acoustics to reveal room shape How biopolymers adapt to recurring strains Isolating an abundant marine virus Dating endosymbiosis events Contents THIS WEEK IN PNAS OPINION Transdisciplinary electric power grid science Charles D. Brummitt, Paul D. H. Hines, Ian Dobson, Cristopher Moore, and Raissa M. D Souza In This Issue QNAS LETTERS (ONLINE ONLY) QnAs with Arthur Beaudet Prashant Nair E2748 E2749 E2750 E2751 Valuable oil sands environmental research raises several questions Steve E. Hrudey Reply to Hrudey: Tracking the extent of oil sands airborne pollution Joshua Kurek, Jane L. Kirk, Derek C. G. Muir, Xiaowa Wang, Marlene S. Evans, and John P. Smol Viral underpinning to the Austrian record of type 2 diabetes? William Klitz and Bo Niklasson Reply to Klitz and Niklasson: Can viral infections explain the cross-sectional Austrian diabetes data? Stefan Thurner, Peter Klimek, Michael Szell, Georg Duftschmid, Gottfried Endel, Alexandra Kautzky-Willer, and David C. Kasper Free online through the PNAS open access option. COMMENTARIES Hearing the shape of a room Mark D. Plumbley See companion article on page Adaptation of fibrous biopolymers to recurring increasing strains John W. Weisel and Rustem I. Litvinov See companion article on page Insight into the unknown marine virus majority Alexander I. Culley See companion article on page Anciently duplicated genes reduce uncertainty in molecular clock estimates Olga Zhaxybayeva See companion article on page PNAS u July 23, 2013 u vol. 110 u no. 30 u iii viii
2 PNAS PLUS SIGNIFICANCE STATEMENTS E2752 PHYSICAL SCIENCES APPLIED MATHEMATICS Single-photon sampling architecture for solid-state imaging sensors Ewout van den Berg, Emmanuel Candès, Garry Chinn, Craig Levin, Peter Demetri Olcott, and Carlos Sing-Long E2812 E2821 CELL BIOLOGY Ultrahigh-resolution imaging reveals formation of neuronal SNARE/Munc18 complexes in situ Alexandros Pertsinidis, Konark Mukherjee, Manu Sharma, Zhiping P. Pang, Sang Ryul Park, Yunxiang Zhang, Axel T. Brunger, Thomas C. Südhof, and Steven Chu EVOLUTION Evolutionary diversification of the multimeric states of proteins Michael Lynch E2812 APPLIED PHYSICAL SCIENCES Ultrahigh-resolution imaging reveals formation of neuronal SNARE/Munc18 complexes in situ Alexandros Pertsinidis, Konark Mukherjee, Manu Sharma, Zhiping P. Pang, Sang Ryul Park, Yunxiang Zhang, Axel T. Brunger, Thomas C. Südhof, and Steven Chu E2829 MICROBIOLOGY Structural insights into the regulation of sialic acid catabolism by the Vibrio vulnificus transcriptional repressor NanR Jungwon Hwang, Byoung Sik Kim, Song Yee Jang, Jong Gyu Lim, Dong-Ju You, Hyun Suk Jung, Tae-Kwang Oh, Jie-Oh Lee, Sang Ho Choi, and Myung Hee Kim E2821 CHEMISTRY Evolutionary diversification of the multimeric states of proteins Michael Lynch E2838 Torins are potent antimalarials that block replenishment of Plasmodium liver stage parasitophorous vacuole membrane proteins Kirsten K. Hanson, Ana S. Ressurreição, Kathrin Buchholz, Miguel Prudêncio, Jonathan D. Herman-Ornelas, Maria Rebelo, Wandy L. Beatty, Dyann F. Wirth, Thomas Hänscheid, Rui Moreira, Matthias Marti, and Maria M. Mota E2762 EARTH, ATMOSPHERIC, AND PLANETARY SCIENCES Comparison of geomechanical deformation induced by megatonne-scale CO 2 storage at Sleipner, Weyburn, and In Salah James P. Verdon, J.-Michael Kendall, Anna L. Stork, R. Andy Chadwick, Don J. White, and Rob C. Bissell E2848 SYSTEMS BIOLOGY Geminin deploys multiple mechanisms to regulate Cdt1 before cell division thus ensuring the proper execution of DNA replication Andrea Ballabeni, Raffaella Zamponi, Jodene K. Moore, Kristian Helin, and Marc W. Kirschner E2772 E2782 E2792 E2802 BIOLOGICAL SCIENCES BIOCHEMISTRY Ex-527 inhibits Sirtuins by exploiting their unique NAD + -dependent deacetylation mechanism Melanie Gertz, Frank Fischer, Giang Thi Tuyet Nguyen, Mahadevan Lakshminarasimhan, Mike Schutkowski, Michael Weyand, and Clemens Steegborn BIOPHYSICS AND COMPUTATIONAL BIOLOGY Thermodynamic origins of protein folding, allostery, and capsid formation in the human hepatitis B virus core protein Crispin G. Alexander, Maike C. Jürgens, Dale A. Shepherd, Stefan M. V. Freund, Alison E. Ashcroft, and Neil Ferguson Deciphering the rules by which 5 -UTR sequences affect protein expression in yeast Shlomi Dvir, Lars Velten, Eilon Sharon, Danny Zeevi, Lucas B. Carey, Adina Weinberger, and Eran Segal Isolated pseudo RNA-recognition motifs of SR proteins can regulate splicing using a noncanonical mode of RNA recognition Antoine Cléry, Rahul Sinha, Olga Anczuków, Anna Corrionero, Ahmed Moursy, Gerrit M. Daubner, Juan Valcárcel, Adrian R. Krainer, and Frédéric H.-T. Allain INAUGURAL ARTICLE Maturation, not initiation, is the major roadblock during reprogramming toward pluripotency from human fibroblasts Koji Tanabe, Michiko Nakamura, Megumi Narita, Kazutoshi Takahashi, and Shinya Yamanaka See Profiles on page 9223 in issue 24 of volume 109 and on page 5740 in issue 15 of volume 110 PHYSICAL SCIENCES APPLIED MATHEMATICS The counterbend phenomenon in flagellar axonemes and cross-linked filament bundles Hermes Gadêlha, Eamonn A. Gaffney, and Alain Goriely Acoustic echoes reveal room shape Ivan Dokmanic, Reza Parhizkar, Andreas Walther, Yue M. Lu, and Martin Vetterli See Commentary on page APPLIED PHYSICAL SCIENCES Molecule-hugging graphene nanopores Slaven Garaj, Song Liu, Jene A. Golovchenko, and Daniel Branton iv u
3 12197 Strain history dependence of the nonlinear stress response of fibrin and collagen networks Stefan Münster, Louise M. Jawerth, Beverly A. Leslie, Jeffrey I. Weitz, Ben Fabry, and David A. Weitz See Commentary on page Graphene microsheets enter cells through spontaneous membrane penetration at edge asperities and corner sites Yinfeng Li, Hongyan Yuan, Annette von dem Bussche, Megan Creighton, Robert H. Hurt, Agnes B. Kane, and Huajian Gao CHEMISTRY Spatiotemporal control and superselectivity in supramolecular polymers using multivalency Lorenzo Albertazzi, Francisco J. Martinez-Veracoechea, Christianus M. A. Leenders, Ilja K. Voets, Daan Frenkel, and E. W. Meijer Liquid liquid transition in supercooled water suggested by microsecond simulations Yaping Li, Jicun Li, and Feng Wang Quantitative trait analysis in sequencing studies under trait-dependent sampling Dan-Yu Lin, Donglin Zeng, and Zheng-Zheng Tang Biclustering with heterogeneous variance Guanhua Chen, Patrick F. Sullivan, and Michael R. Kosorok SOCIAL SCIENCES ENVIRONMENTAL SCIENCES Economic repercussions of fisheries-induced evolution Anne Maria Eikeset, Andries Richter, Erin S. Dunlop, Ulf Dieckmann, and Nils Chr. Stenseth SOCIAL SCIENCES Within-mother analysis of seasonal patterns in health at birth Janet Currie and Hannes Schwandt EARTH, ATMOSPHERIC, AND PLANETARY SCIENCES Universal fractal scaling in stream chemistry and its implications for solute transport and water quality trend detection James W. Kirchner and Colin Neal Downscaling CMIP5 climate models shows increased tropical cyclone activity over the 21st century Kerry A. Emanuel Evidence for a water system transition beneath Thwaites Glacier, West Antarctica Dustin M. Schroeder, Donald D. Blankenship, and Duncan A. Young ENGINEERING Recycling rice husks for high-capacity lithium battery anodes Dae Soo Jung, Myung-Hyun Ryou, Yong Joo Sung, Seung Bin Park, and Jang Wook Choi A small animal Raman instrument for rapid, wide-area, spectroscopic imaging Sarah E. Bohndiek, Ashwin Wagadarikar, Cristina L. Zavaleta, Dominique Van de Sompel, Ellis Garai, Jesse V. Jokerst, Siavash Yazdanfar, and Sanjiv S. Gambhir PHYSICS Universal sheet resistance and revised phase diagram of the cuprate high-temperature superconductors Neven Barisic, Mun K. Chan, Yuan Li, Guichuan Yu, Xudong Zhao, Martin Dressel, Ana Smontara, and Martin Greven STATISTICS Evaluation of mixed-source, low-template DNA profiles in forensic science David J. Balding BIOLOGICAL SCIENCES BIOCHEMISTRY Thermodynamic framework for identifying free energy inventories of enzyme catalytic cycles Stephen D. Fried and Steven G. Boxer Extrahelical (CAG)/(CTG) triplet repeat elements support proliferating cell nuclear antigen loading and MutLα endonuclease activation Anna Pluciennik, Vickers Burdett, Celia Baitinger, Ravi R. Iyer, Kevin Shi, and Paul Modrich Blasticidin S inhibits translation by trapping deformed trna on the ribosome Egor Svidritskiy, Clarence Ling, Dmitri N. Ermolenko, and Andrei A. Korostelev trna tk UUU,tQ UUG, and te UUC wobble position modifications fine-tune protein translation by promoting ribosome A-site binding Vanessa Anissa Nathalie Rezgui, Kshitiz Tyagi, Namit Ranjan, Andrey L. Konevega, Joerg Mittelstaet, Marina V. Rodnina, Matthias Peter, and Patrick G. A. Pedrioli BIOPHYSICS AND COMPUTATIONAL BIOLOGY The counterbend phenomenon in flagellar axonemes and cross-linked filament bundles Hermes Gadêlha, Eamonn A. Gaffney, and Alain Goriely Molecule-hugging graphene nanopores Slaven Garaj, Song Liu, Jene A. Golovchenko, and Daniel Branton Graphene microsheets enter cells through spontaneous membrane penetration at edge asperities and corner sites Yinfeng Li, Hongyan Yuan, Annette von dem Bussche, Megan Creighton, Robert H. Hurt, Agnes B. Kane, and Huajian Gao PNAS u July 23, 2013 u vol. 110 u no. 30 u v
4 12301 Validated near-atomic resolution structure of bacteriophage epsilon15 derived from cryo-em and modeling Matthew L. Baker, Corey F. Hryc, Qinfen Zhang, Weimin Wu, Joanita Jakana, Cameron Haase-Pettingell, Pavel V. Afonine, Paul D. Adams, Jonathan A. King, Wen Jiang, and Wah Chiu Fast spatiotemporal correlation spectroscopy to determine protein lateral diffusion laws in live cell membranes Carmine Di Rienzo, Enrico Gratton, Fabio Beltram, and Francesco Cardarelli CELL BIOLOGY Maturation, not initiation, is the major roadblock during reprogramming toward pluripotency from human fibroblasts Koji Tanabe, Michiko Nakamura, Megumi Narita, Kazutoshi Takahashi, and Shinya Yamanaka See Profiles on page 9223 in issue 24 of volume 109 and on page 5740 in issue 15 of volume Phage ϕ29 protein p1 promotes replication by associating with the FtsZ ring of the divisome in Bacillus subtilis David Ballesteros-Plaza, Isabel Holguera, Dirk-Jan Scheffers, Margarita Salas, and Daniel Muñoz-Espín Genetic loss or pharmacological blockade of testes-expressed taste genes causes male sterility Bedrich Mosinger, Kevin M. Redding, M. Rockwell Parker, Valeriya Yevshayeva, Karen K. Yee, Katerina Dyomina, Yan Li, and Robert F. Margolskee CTGF antagonism with mab FG-3019 enhances chemotherapy response without increasing drug delivery in murine ductal pancreas cancer Albrecht Neesse, Kristopher K. Frese, Tashinga E. Bapiro, Tomoaki Nakagawa, Mark D. Sternlicht, Todd W. Seeley, Christian Pilarsky, Duncan I. Jodrell, Suzanne M. Spong, and David A. Tuveson Loss of corepressor PER2 under hypoxia up-regulates OCT1-mediated EMT gene expression and enhances tumor malignancy Wendy W. Hwang-Verslues, Po-Hao Chang, Yung-Ming Jeng, Wen-Hung Kuo, Pei-Hsun Chiang, Yi-Cheng Chang, Tsung-Han Hsieh, Fang-Yi Su, Liu-Chen Lin, Serena Abbondante, Cheng-Yuan Yang, Huan-Ming Hsu, Jyh-Cherng Yu, King-Jen Chang, Jin-Yuh Shew, Eva Y.-H. P. Lee, and Wen-Hwa Lee Activation loop phosphorylation of a protein kinase is a molecular marker of organelle size that dynamically reports flagellar length Muqing Cao, Dan Meng, Liang Wang, Shuqing Bei, William J. Snell, and Junmin Pan ECOLOGY Genome of a SAR116 bacteriophage shows the prevalence of this phage type in the oceans Ilnam Kang, Hyun-Myung Oh, Dongmin Kang, and Jang-Cheon Cho See Commentary on page ENVIRONMENTAL SCIENCES Universal fractal scaling in stream chemistry and its implications for solute transport and water quality trend detection James W. Kirchner and Colin Neal EVOLUTION Economic repercussions of fisheries-induced evolution Anne Maria Eikeset, Andries Richter, Erin S. Dunlop, Ulf Dieckmann, and Nils Chr. Stenseth DNA-binding specificity changes in the evolution of forkhead transcription factors So Nakagawa, Stephen S. Gisselbrecht, Julia M. Rogers, Daniel L. Hartl, and Martha L. Bulyk Primary endosymbiosis events date to the later Proterozoic with cross-calibrated phylogenetic dating of duplicated ATPase proteins Patrick M. Shih and Nicholas J. Matzke See Commentary on page GENETICS Evaluation of mixed-source, low-template DNA profiles in forensic science David J. Balding Quantitative trait analysis in sequencing studies under trait-dependent sampling Dan-Yu Lin, Donglin Zeng, and Zheng-Zheng Tang Biclustering with heterogeneous variance Guanhua Chen, Patrick F. Sullivan, and Michael R. Kosorok Functional genomic screen of human stem cell differentiation reveals pathways involved in neurodevelopment and neurodegeneration Ying Zhang, Vincent P. Schulz, Brian D. Reed, Zheng Wang, Xinghua Pan, Jessica Mariani, Ghia Euskirchen, Michael P. Snyder, Flora M. Vaccarino, Natalia Ivanova, Sherman M. Weissman, and Anna M. Szekely Aneuploidy underlies a multicellular phenotypic switch Zhihao Tan, Michelle Hays, Gareth A. Cromie, Eric W. Jeffery, Adrian C. Scott, Vida Ahyong, Amy Sirr, Alexander Skupin, and Aimée M. Dudley Male-specific region of the bovine Y chromosome is gene rich with a high transcriptomic activity in testis development Ti-Cheng Chang, Yang Yang, Ernest F. Retzel, and Wan-Sheng Liu IMMUNOLOGY Zinc-finger antiviral protein mediates retinoic acid inducible gene I like receptor-independent antiviral response to murine leukemia virus Hanna Lee, Jun Komano, Yasunori Saitoh, Shoji Yamaoka, Tatsuya Kozaki, Takuma Misawa, Michihiro Takahama, Takashi Satoh, Osamu Takeuchi, Naoki Yamamoto, Yoshiharu Matsuura, Tatsuya Saitoh, and Shizuo Akira vi u
5 12385 Osteoclast precursors in murine bone marrow express CD27 and are impeded in osteoclast development by CD70 on activated immune cells Yanling Xiao, Ji-Ying Song, Teun J. de Vries, Christien Fatmawati, Diana B. Parreira, Geerling E. J. Langenbach, Nikolina Bąbała, Martijn A. Nolte, Vincent Everts, and Jannie Borst Modulation of natural killer cell antitumor activity by the aryl hydrocarbon receptor June Ho Shin, Luhua Zhang, Oihana Murillo-Sauca, Junmo Kim, Holbrook E. K. Kohrt, Jack D. Bui, and John B. Sunwoo Intracellular antibody receptor TRIM21 prevents fatal viral infection Marina Vaysburd, Ruth E. Watkinson, Helen Cooper, Martin Reed, Kevin O Connell, Jackie Smith, James Cruickshanks, and Leo C. James CD22 ligand-binding and signaling domains reciprocally regulate B-cell Ca 2+ signaling Jennifer Müller, Ingrid Obermeier, Miriam Wöhner, Carolin Brandl, Sarah Mrotzek, Sieglinde Angermüller, Palash C. Maity, Michael Reth, and Lars Nitschke MEDICAL SCIENCES A small animal Raman instrument for rapid, wide-area, spectroscopic imaging Sarah E. Bohndiek, Ashwin Wagadarikar, Cristina L. Zavaleta, Dominique Van de Sompel, Ellis Garai, Jesse V. Jokerst, Siavash Yazdanfar, and Sanjiv S. Gambhir Dissection of TBK1 signaling via phosphoproteomics in lung cancer cells Jae-Young Kim, Eric A. Welsh, Umut Oguz, Bin Fang, Yun Bai, Fumi Kinose, Crystina Bronk, Lily L. Remsing Rix, Amer A. Beg, Uwe Rix, Steven A. Eschrich, John M. Koomen, and Eric B. Haura PTEN loss defines a PI3K/AKT pathway-dependent germinal center subtype of diffuse large B-cell lymphoma Matthias Pfeifer, Michael Grau, Dido Lenze, Sören-Sebastian Wenzel, Annette Wolf, Brigitte Wollert-Wulf, Kerstin Dietze, Hendrik Nogai, Benjamin Storek, Hannelore Madle, Bernd Dörken, Martin Janz, Stephan Dirnhofer, Peter Lenz, Michael Hummel, Alexandar Tzankov, and Georg Lenz Targeted genetic dependency screen facilitates identification of actionable mutations in FGFR4, MAP3K9, and PAK5 in lung cancer Shameem Fawdar, Eleanor W. Trotter, Yaoyong Li, Natalie L. Stephenson, Franziska Hanke, Anna A. Marusiak, Zoe C. Edwards, Sara Ientile, Bohdan Waszkowycz, Crispin J. Miller, and John Brognard Abl kinases are required for vascular function, Tie2 expression, and angiopoietin-1 mediated survival Elizabeth M. Chislock, Colleen Ring, and Ann Marie Pendergast MICROBIOLOGY Molecular architecture of the uncleaved HIV-1 envelope glycoprotein trimer Youdong Mao, Liping Wang, Christopher Gu, Alon Herschhorn, Anik Désormeaux, Andrés Finzi, Shi-Hua Xiang, and Joseph G. Sodroski A mechanism for induction of a hypoxic response by vaccinia virus Michela Mazzon, Nicholas E. Peters, Christoph Loenarz, Ewelina M. Krysztofinska, Stuart W. J. Ember, Brian J. Ferguson, and Geoffrey L. Smith Rapid evolution of the human gut virome Samuel Minot, Alexandra Bryson, Christel Chehoud, Gary D. Wu, James D. Lewis, and Frederic D. Bushman NEUROSCIENCE Very long-term memories may be stored in the pattern of holes in the perineuronal net Roger Y. Tsien Cognitive and motivational deficits together with prefrontal oxidative stress in a mouse model for neuropsychiatric illness Alexander W. Johnson, Hanna Jaaro-Peled, Neelam Shahani, Thomas W. Sedlak, Sandra Zoubovsky, Daniel Burruss, Francesco Emiliani, Akira Sawa, and Michela Gallagher Transducin translocation contributes to rod survival and enhances synaptic transmission from rods to rod bipolar cells Anurima Majumder, Johan Pahlberg, Kimberly K. Boyd, Vasily Kerov, Saravanan Kolandaivelu, Visvanathan Ramamurthy, Alapakkam P. Sampath, and Nikolai O. Artemyev PHARMACOLOGY Tumor-derived hydrogen sulfide, produced by cystathionine-β-synthase, stimulates bioenergetics, cell proliferation, and angiogenesis in colon cancer Csaba Szabo, Ciro Coletta, Celia Chao, Katalin Módis, Bartosz Szczesny, Andreas Papapetropoulos, and Mark R. Hellmich PHYSIOLOGY Fat cells directly sense temperature to activate thermogenesis Li Ye, Jun Wu, Paul Cohen, Lawrence Kazak, Melin J. Khandekar, Mark P. Jedrychowski, Xing Zeng, Steven P. Gygi, and Bruce M. Spiegelman Induced fit substrate binding to an archeal glutamate transporter homologue David Ewers, Toni Becher, Jan-Philipp Machtens, Ingo Weyand, and Christoph Fahlke PLANT BIOLOGY Perception of conserved pathogen elicitors at the plasma membrane leads to relocalization of the Arabidopsis PEN3 transporter William Underwood and Shauna C. Somerville PNAS u July 23, 2013 u vol. 110 u no. 30 u vii
6 CORRECTIONS PHYSICS Elasto-inertial turbulence Devranjan Samanta, Yves Dubief, Markus Holzner, Christof Schäfer, Alexander N. Morozov, Christian Wagner, and Björn Hof ANTHROPOLOGY Beginning of viniculture in France Patrick E. McGovern, Benjamin P. Luley, Nuria Rovira, Armen Mirzoian, Michael P. Callahan, Karen E. Smith, Gretchen R. Hall, Theodore Davidson, and Joshua M. Henkin MEDICAL SCIENCES Genetic confirmation for a central role for TNFα in the direct action of thyroid stimulating hormone on the skeleton Li Sun, Ling-Ling Zhu, Ping Lu, Tony Yuen, Jianhua Li, Risheng Ma, Ramkumari Baliram, Surinder S. Moonga, Peng Liu, Alberta Zallone, Maria I. New, Terry F. Davies, and Mone Zaidi MICROBIOLOGY IKK epsilon kinase is crucial for viral G protein-coupled receptor tumorigenesis Yi Wang, Xiaolu Lu, Lining Zhu, Yan Shen, Shylet Chengedza, Hao Feng, Laiyee Wang, Jae U. Jung, Julio S. Gutkind, and Pinghui Feng ix Subscription Form viii u
No. Name College Major Email 1 Ke Yang Chuan College of Science Chemistry key@cup.edu.cn 2 Wang Li Qun College of Science Mathematics wliqunhmily@gmail.com 3 Xu Tao College of Science Mathematics xutao@cup.edu.cn
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