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March 25, 2008 兩 vol. 105 兩 no. 12 兩 4531– 4962

PNAS

Proceedings of the National Academy of Sciences of the United States of America

www.pnas.org

Cover image: Foraging Laysan Albatross (Phoebastria immutabilis). Albatrosses soar over vast expanses of the ocean to search for food. Large olfactory bulbs in the wandering albatross (Diomedea exulans) suggest that the birds locate prey and carrion by scent. In their article on pages 4576–4581, Nevitt et al. report how albatross flight paths, obtained by GPS tracking, and feeding logs, recorded by stomach temperature sensors, confirm the scent hypothesis. Image courtesy of David Liittschwager (freelance photographer).

From the Cover 4576 Scent cues on the open ocean 4685 Raw NMR protein structure 4868 Emergence of toxic E. coli 4928 The roots of root symbiosis

Contents THIS WEEK IN PNAS

CHEMICAL ECOLOGY SPECIAL FEATURE INTRODUCTORY PERSPECTIVE 4539 Chemical ecology in retrospect and prospect Jerrold Meinwald and Thomas Eisner

4531 In This Issue

PERSPECTIVES

LETTER (ONLINE ONLY) E16 Reply to Pape et al.: The phylogeography of HIV-1 group M subtype B Michael Worobey, Arthur E. Pitchenik, M. Thomas P. Gilbert, Gabriela Wlasiuk, and Andrew Rambaut

COMMENTARIES 4533 Local knowledge helps determine protein structures Michael R. Gryk and Jeffrey C. Hoch ➜ See companion article on page 4685 4535 The continuing evolution of a bacterial pathogen James B. Kaper and Mohamed A. Karmali ➜ See companion article on page 4868 4537 SYMRK, an enigmatic receptor guarding and guiding microbial endosymbioses with plant roots Marcelle Holsters ➜ See companion article on page 4928

Free online through the PNAS open access option.

4587 Biosynthetic origin of natural products isolated from marine microorganism–invertebrate assemblages T. Luke Simmons, R. Cameron Coates, Benjamin R. Clark, Niclas Engene, David Gonzalez, Eduardo Esquenazi, Pieter C. Dorrestein, and William H. Gerwick 4601 The evolution of gene collectives: How natural selection drives chemical innovation Michael A. Fischbach, Christopher T. Walsh, and Jon Clardy

RESEARCH ARTICLES 4541 The lost origin of chemical ecology in the late 19th century Thomas Hartmann 4547 Selection for chemical trait remixing in an invasive weed after reassociation with a coevolved specialist A. R. Zangerl, M. C. Stanley, and M. R. Berenbaum 4553 cis-Jasmone induces Arabidopsis genes that affect the chemical ecology of multitrophic interactions with aphids and their parasitoids Toby J. A. Bruce, Michaela C. Matthes, Keith Chamberlain, Christine M. Woodcock, Abdul Mohib, Ben Webster, Lesley E. Smart, Michael A. Birkett, John A. Pickett, and Johnathan A. Napier PNAS 兩 March 25, 2008 兩 vol. 105 兩 no. 12 兩 iii–x

4559 Herbivory-induced changes in the small-RNA transcriptome and phytohormone signaling in Nicotiana attenuata Shree P. Pandey, Priyanka Shahi, Klaus Gase, and Ian T. Baldwin 4565 Context- and scale-dependent effects of floral CO2 on nectar foraging by Manduca sexta Joaquín Goyret, Poppy M. Markwell, and Robert A. Raguso 4571 Seed odor mediates an obligate ant–plant mutualism in Amazonian rainforests Elsa Youngsteadt, Satoshi Nojima, Christopher Ha¨berlein, Stefan Schulz, and Coby Schal 4576 Evidence for olfactory search in wandering albatross, Diomedea exulans Gabrielle A. Nevitt, Marcel Losekoot, and Henri Weimerskirch 4582 Factors promoting marine invasions: A chemoecological approach Ernesto Mollo, Margherita Gavagnin, Marianna Carbone, Francesco Castelluccio, Ferdinando Pozone, Vassilios Roussis, Jose´ Templado, Michael T. Ghiselin, and Guido Cimino 4595 Evolution of polyketide synthases in bacteria Christian P. Ridley, Ho Young Lee, and Chaitan Khosla

PHYSICAL SCIENCES APPLIED PHYSICAL SCIENCES 4609 Tug-of-war as a cooperative mechanism for bidirectional cargo transport by molecular motors ¨ller, Stefan Klumpp, and Reinhard Lipowsky Melanie J. I. Mu

CHEMISTRY 4582 Factors promoting marine invasions: A chemoecological approach Ernesto Mollo, Margherita Gavagnin, Marianna Carbone, Francesco Castelluccio, Ferdinando Pozone, Vassilios Roussis, Jose´ Templado, Michael T. Ghiselin, and Guido Cimino 4615 A two-step nucleotide-flipping mechanism enables kinetic discrimination of DNA lesions by AGT Jie Hu, Ao Ma, and Aaron R. Dinner 4621 Dipole tensor-based atomic-resolution structure determination of a nanocrystalline protein by solid-state NMR W. Trent Franks, Benjamin J. Wylie, Heather L. Frericks Schmidt, Andrew J. Nieuwkoop, Rebecca-Maria Mayrhofer, Gautam J. Shah, Daniel T. Graesser, and Chad M. Rienstra 4627 Incremental parameter evaluation from incomplete data with application to the population pharmacology of anticoagulants Marcel O. Vlad, Alexandru Dan Corlan, Federico Mora´n, Peter Oefner, and John Ross

COMPUTER SCIENCES 4633 Tracing information flow on a global scale using Internet chain-letter data David Liben-Nowell and Jon Kleinberg

SOCIAL SCIENCES ENVIRONMENTAL SCIENCES 4639 Modeling targeted layered containment of an influenza pandemic in the United States M. Elizabeth Halloran, Neil M. Ferguson, Stephen Eubank, Ira M. Longini, Jr., Derek A. T. Cummings, Bryan Lewis, Shufu Xu, Christophe Fraser, Anil Vullikanti, Timothy C. Germann, Diane Wagener, Richard Beckman, Kai Kadau, Chris Barrett, Catherine A. Macken, Donald S. Burke, and Philip Cooley

SOCIAL SCIENCES 4633 Tracing information flow on a global scale using Internet chain-letter data David Liben-Nowell and Jon Kleinberg

BIOLOGICAL SCIENCES ANTHROPOLOGY 4645 Close correspondence between quantitative- and molecular-genetic divergence times for Neandertals and modern humans Timothy D. Weaver, Charles C. Roseman, and Chris B. Stringer 4650 The Homo floresiensis cranium (LB1): Size, scaling, and early Homo affinities Adam D. Gordon, Lisa Nevell, and Bernard Wood

APPLIED BIOLOGICAL SCIENCES 4656 Immunization by a bacterial aerosol Lucila Garcia-Contreras, Yun-Ling Wong, Pavan Muttil, Danielle Padilla, Jerry Sadoff, Jessica DeRousse, Willem Andreas Germishuizen, Sunali Goonesekera, Katharina Elbert, Barry R. Bloom, Rich Miller, P. Bernard Fourie, Anthony Hickey, and David Edwards

BIOCHEMISTRY 4661 Molecular basis of thrombin recognition by protein C inhibitor revealed by the 1.6-Å structure of the heparin-bridged complex Wei Li, Ty E. Adams, Jyoti Nangalia, Charles T. Esmon, and James A. Huntington 4667 RNA-dependent lipid remodeling by bacterial multiple peptide resistance factors Herve´ Roy and Michael Ibba 4673 The structure of LepA, the ribosomal back translocase Robin N. Evans, Gregor Blaha, Scott Bailey, and Thomas A. Steitz

BIOPHYSICS 4609 Tug-of-war as a cooperative mechanism for bidirectional cargo transport by molecular motors ¨ller, Stefan Klumpp, and Reinhard Lipowsky Melanie J. I. Mu 4615 A two-step nucleotide-flipping mechanism enables kinetic discrimination of DNA lesions by AGT Jie Hu, Ao Ma, and Aaron R. Dinner PNAS 兩 March 25, 2008 兩 vol. 105 兩 no. 12 兩 v

4621 Dipole tensor-based atomic-resolution structure determination of a nanocrystalline protein by solid-state NMR W. Trent Franks, Benjamin J. Wylie, Heather L. Frericks Schmidt, Andrew J. Nieuwkoop, Rebecca-Maria Mayrhofer, Gautam J. Shah, Daniel T. Graesser, and Chad M. Rienstra 4679 Reassessing a sparse energetic network within a single protein domain ¨m, Yao Shi, Tord Sna¨ll, Celestine N. Chi, Lisa Elfstro ¨m, and Per Jemth Åke Engstro 4685 Consistent blind protein structure generation from NMR chemical shift data Yang Shen, Oliver Lange, Frank Delaglio, Paolo Rossi, James M. Aramini, Gaohua Liu, Alexander Eletsky, Yibing Wu, Kiran K. Singarapu, Alexander Lemak, Alexandr Ignatchenko, Cheryl H. Arrowsmith, Thomas Szyperski, Gaetano T. Montelione, David Baker, and Ad Bax ➜ See Commentary on page 4533

4739 Inositol trisphosphate 3-kinase B (InsP3KB) as a physiological modulator of myelopoiesis Yonghui Jia, Fabien Loison, Hidenori Hattori, Yitang Li, Christophe Erneux, Shin-Young Park, Chong Gao, Li Chai, Leslie E. Silberstein, Stephane Schurmans, and Hongbo R. Luo 4745 PHDs overactivation during chronic hypoxia ‘‘desensitizes’’ HIF␣ and protects cells from necrosis Amandine Ginouve`s, Karine Ilc, Nuria Maci´as, Jacques Pouysse´gur, and Edurne Berra 4751 Heparan sulfate biosynthesis enzymes EXT1 and EXT2 affect NDST1 expression and heparan sulfate sulfation Jenny Presto, Maria Thuveson, Pernilla Carlsson, Marta Busse, Maria Wile´n, Inger Eriksson, Marion Kusche-Gullberg, and Lena Kjelle´n 4757 ATP-dependent activation of p21WAF1/CIP1-associated Cdk2 by Cdc6 Qiuming Kan, Shigeki Jinno, Hanako Yamamoto, Kohei Kobayashi, and Hiroto Okayama

DEVELOPMENTAL BIOLOGY 4691 Myosin V and Kinesin act as tethers to enhance each others’ processivity M. Yusuf Ali, Hailong Lu, Carol S. Bookwalter, David M. Warshaw, and Kathleen M. Trybus 4697 Unilamellar vesicle formation and encapsulation by microfluidic jetting Jeanne C. Stachowiak, David L. Richmond, Thomas H. Li, Allen P. Liu, Sapun H. Parekh, and Daniel A. Fletcher 4703 Monolayer purification: A rapid method for isolating protein complexes for single-particle electron microscopy Deborah F. Kelly, Danijela Dukovski, and Thomas Walz

CELL BIOLOGY 4709 X-inactivation in female human embryonic stem cells is in a nonrandom pattern and prone to epigenetic alterations Yin Shen, Youko Matsuno, Shaun D. Fouse, Nagesh Rao, Sierra Root, Renhe Xu, Matteo Pellegrini, Arthur D. Riggs, and Guoping Fan 4715 Transposition of a reconstructed Harbinger element in human cells and functional homology with two transposon-derived cellular genes Ludivine Sinzelle, Vladimir V. Kapitonov, Dawid P. Grzela, Tobias Jursch, Jerzy Jurka, Zsuzsanna Izsva´k, and Zolta´n Ivics 4721 Gene expression-based screening identifies microtubule inhibitors as inducers of PGC-1␣ and oxidative phosphorylation Zoltan Arany, Bridget K. Wagner, Yanhong Ma, Jessica Chinsomboon, Dina Laznik, and Bruce M. Spiegelman 4727 Protein phosphatase 2A controls the activity of histone deacetylase 7 during T cell apoptosis and angiogenesis Maud Martin, Michael Potente, Veerle Janssens, Didier Vertommen, Jean-Claude Twizere, Mark H. Rider, Jozef Goris, Stefanie Dimmeler, Richard Kettmann, and Franck Dequiedt 4733 Splicing mediates the activity of four putative cellular internal ribosome entry sites Brian T. Baranick, Nathan A. Lemp, Jill Nagashima, Kei Hiraoka, Noriyuki Kasahara, and Christopher R. Logg

4763 Zebrafish early cardiac connexin, Cx36.7/Ecx, regulates myofibril orientation and heart morphogenesis by establishing Nkx2.5 expression Naznin Sultana, Kakon Nag, Kazuyuki Hoshijima, Dale W. Laird, Atsushi Kawakami, and Shigehisa Hirose

ECOLOGY 4541 The lost origin of chemical ecology in the late 19th century Thomas Hartmann 4559 Herbivory-induced changes in the small-RNA transcriptome and phytohormone signaling in Nicotiana attenuata Shree P. Pandey, Priyanka Shahi, Klaus Gase, and Ian T. Baldwin 4565 Context- and scale-dependent effects of floral CO2 on nectar foraging by Manduca sexta Joaquín Goyret, Poppy M. Markwell, and Robert A. Raguso 4571 Seed odor mediates an obligate ant–plant mutualism in Amazonian rainforests Elsa Youngsteadt, Satoshi Nojima, Christopher Ha¨berlein, Stefan Schulz, and Coby Schal 4576 Evidence for olfactory search in wandering albatross, Diomedea exulans Gabrielle A. Nevitt, Marcel Losekoot, and Henri Weimerskirch 4582 Factors promoting marine invasions: A chemoecological approach Ernesto Mollo, Margherita Gavagnin, Marianna Carbone, Francesco Castelluccio, Ferdinando Pozone, Vassilios Roussis, Jose´ Templado, Michael T. Ghiselin, and Guido Cimino 4595 Evolution of polyketide synthases in bacteria Christian P. Ridley, Ho Young Lee, and Chaitan Khosla 4769 Mapping H5N1 highly pathogenic avian influenza risk in Southeast Asia Marius Gilbert, Xiangming Xiao, Dirk U. Pfeiffer, M. Epprecht, Stephen Boles, Christina Czarnecki, Prasit Chaitaweesub, Wantanee Kalpravidh, Phan Q. Minh, M. J. Otte, Vincent Martin, and Jan Slingenbergh PNAS 兩 March 25, 2008 兩 vol. 105 兩 no. 12 兩 vii

ENVIRONMENTAL SCIENCES 4775 Photosynthetic maximum quantum yield increases are an essential component of the Southern Ocean phytoplankton response to iron Michael R. Hiscock, Veronica P. Lance, Amy M. Apprill, Robert R. Bidigare, Zackary I. Johnson, B. Greg Mitchell, Walker O. Smith, Jr., and Richard T. Barber

EVOLUTION 4547 Selection for chemical trait remixing in an invasive weed after reassociation with a coevolved specialist A. R. Zangerl, M. C. Stanley, and M. R. Berenbaum 4781 Evolution of malaria parasite plastid targeting sequences Christopher J. Tonkin, Bernardo J. Foth, Stuart A. Ralph, Nicole Struck, Alan F. Cowman, and Geoffrey I. McFadden 4786 Increasing morphological complexity in multiple parallel lineages of the Crustacea Sarah J. Adamowicz, Andy Purvis, and Matthew A. Wills 4792 Rapid large-scale evolutionary divergence in morphology and performance associated with exploitation of a different dietary resource Anthony Herrel, Katleen Huyghe, Bieke Vanhooydonck, Thierry Backeljau, Karin Breugelmans, Irena Grbac, Raoul Van Damme, and Duncan J. Irschick

IMMUNOLOGY 4796 HDAC inhibitor reduces cytokine storm and facilitates induction of chimerism that reverses lupus in anti-CD3 conditioning regimen Nainong Li, Dongchang Zhao, Mark Kirschbaum, Chunyan Zhang, Chia-Lei Lin, Ivan Todorov, Fouad Kandeel, Stephen Forman, and Defu Zeng 4802 Maintenance of the plasma cell pool is independent of memory B cells Anupama Ahuja, Shannon M. Anderson, Ashraf Khalil, and Mark J. Shlomchik 4808 Role of the Akt pathway in mRNA translation of interferon-stimulated genes Surinder Kaur, Antonella Sassano, Blazej Dolniak, Sonali Joshi, Beata Majchrzak-Kita, Darren P. Baker, Nissim Hay, Eleanor N. Fish, and Leonidas C. Platanias 4814 Chemokine receptor CXCR3 and its ligands CXCL9 and CXCL10 are required for the development of murine cerebral malaria Gabriele S. V. Campanella, Andrew M. Tager, Joseph K. El Khoury, Seddon Y. Thomas, Tabitha A. Abrazinski, Lindsay A. Manice, Richard A. Colvin, and Andrew D. Luster

MEDICAL SCIENCES 4627 Incremental parameter evaluation from incomplete data with application to the population pharmacology of anticoagulants Marcel O. Vlad, Alexandru Dan Corlan, Federico Mora´n, Peter Oefner, and John Ross

4820 X-chromosome inactivation and epigenetic fluidity in human embryonic stem cells Susana S. Silva, Rebecca K. Rowntree, Shila Mekhoubad, and Jeannie T. Lee 4826 Dissection of mechanisms of Chinese medicinal formula Realgar-Indigo naturalis as an effective treatment for promyelocytic leukemia Lan Wang, Guang-Biao Zhou, Ping Liu, Jun-Hong Song, Yang Liang, Xiao-Jing Yan, Fang Xu, Bing-Shun Wang, Jian-Hua Mao, Zhi-Xiang Shen, Sai-Juan Chen, and Zhu Chen 4832 Decay dynamics of HIV-1 depend on the inhibited stages of the viral life cycle Ahmad R. Sedaghat, Jason B. Dinoso, Lin Shen, Claus O. Wilke, and Robert F. Siliciano 4838 Hedgehog signaling overrides p53-mediated tumor suppression by activating Mdm2 Yoshinori Abe, Eri Oda-Sato, Kei Tobiume, Keiko Kawauchi, Yoichi Taya, Koji Okamoto, Moshe Oren, and Nobuyuki Tanaka 4844 Cytosine methylation profiling of cancer cell lines Mathias Ehrich, Julia Turner, Peter Gibbs, Lara Lipton, Mara Giovanneti, Charles Cantor, and Dirk van den Boom 4850 Netrin-1 expression confers a selective advantage for tumor cell survival in metastatic breast cancer Julien Fitamant, Ce´line Guenebeaud, Marie-May Coissieux, Catherine Guix, Isabelle Treilleux, Jean-Yves Scoazec, Thomas Bachelot, Agne`s Bernet, and Patrick Mehlen 4856 Linking Notch signaling to ischemic stroke Joseph F. Arboleda-Velasquez, Zhipeng Zhou, Hwa Kyoung Shin, Angeliki Louvi, Hyung-Hwan Kim, Sean I. Savitz, James K. Liao, Salvatore Salomone, Cenk Ayata, Michael A. Moskowitz, and Spyros Artavanis-Tsakonas 4862 Activation of Trk neurotrophin receptors by glucocorticoids provides a neuroprotective effect Freddy Jeanneteau, Michael J. Garabedian, and Moses V. Chao

MICROBIOLOGY 4868 Variation in virulence among clades of Escherichia coli O157:H7 associated with disease outbreaks Shannon D. Manning, Alifiya S. Motiwala, A. Cody Springman, Weihong Qi, David W. Lacher, Lindsey M. Ouellette, Janice M. Mladonicky, Patricia Somsel, James T. Rudrik, Stephen E. Dietrich, Wei Zhang, Bala Swaminathan, David Alland, and Thomas S. Whittam ➜ See Commentary on page 4535 4874 RXLR effector reservoir in two Phytophthora species is dominated by a single rapidly evolving superfamily with more than 700 members Rays H. Y. Jiang, Sucheta Tripathy, Francine Govers, and Brett M. Tyler 4880 Temperature-induced switch to the pathogenic yeast form of Histoplasma capsulatum requires Ryp1, a conserved transcriptional regulator Van Q. Nguyen and Anita Sil PNAS 兩 March 25, 2008 兩 vol. 105 兩 no. 12 兩 ix

4886 Rifamycin antibiotic resistance by ADP-ribosylation: Structure and diversity of Arr Jennifer Baysarowich, Kalinka Koteva, Donald W. Hughes, Linda Ejim, Emma Griffiths, Kun Zhang, Murray Junop, and Gerard D. Wright

NEUROSCIENCE 4892 Ischemic preconditioning blocks BAD translocation, Bcl-xL cleavage, and large channel activity in mitochondria of postischemic hippocampal neurons Takahiro Miyawaki, Toshihiro Mashiko, Dimitry Ofengeim, Richard J. Flannery, Kyung-Min Noh, Sho Fujisawa, Laura Bonanni, Michael V. L. Bennett, R. Suzanne Zukin, and Elizabeth A. Jonas 4898 Light deprivation damages monoamine neurons and produces a depressive behavioral phenotype in rats M. M. C. Gonzalez and G. Aston-Jones 4904 Chemical transmission between dopaminergic neuron pairs Marie Vandecasteele, Jacques Glowinski, Jean-Michel Deniau, and Laurent Venance 4910 Motion vision is independent of color in Drosophila Satoko Yamaguchi, Reinhard Wolf, Claude Desplan, and Martin Heisenberg 4916 Loss of the inactive myotubularin-related phosphatase Mtmr13 leads to a Charcot–Marie–Tooth 4B2-like peripheral neuropathy in mice Fred L. Robinson, Ingrid R. Niesman, Kristina K. Beiswenger, and Jack E. Dixon 4922 Vesicle association and exocytosis at ribbon and extraribbon sites in retinal bipolar cell presynaptic terminals David Zenisek

4928 SymRK defines a common genetic basis for plant root endosymbioses with arbuscular mycorrhiza fungi, rhizobia, and Frankia bacteria Hassen Gherbi, Katharina Markmann, Sergio Svistoonoff, Joan Estevan, Daphne´ Autran, Gabor Giczey, Florence Auguy, Benjamin Pe´ret, Laurent Laplaze, Claudine Franche, Martin Parniske, and Didier Bogusz ➜ See Commentary on page 4537 4933 Three thioredoxin targets in the inner envelope membrane of chloroplasts function in protein import and chlorophyll metabolism Sandra Bartsch, Julie Monnet, Kristina Selbach, Franc¸oise Quigley, John Gray, Diter von Wettstein, Steffen Reinbothe, and Christiane Reinbothe 4939 Systems approach identifies an organic nitrogenresponsive gene network that is regulated by the master clock control gene CCA1 Rodrigo A. Gutie´rrez, Trevor L. Stokes, Karen Thum, Xiaodong Xu, Mariana Obertello, Manpreet S. Katari, Milos Tanurdzic, Alexis Dean, Damion C. Nero, C. Robertson McClung, and Gloria M. Coruzzi 4945 Involvement of Arabidopsis HOS15 in histone deacetylation and cold tolerance Jianhua Zhu, Jae Cheol Jeong, Yanmei Zhu, Irina Sokolchik, Saori Miyazaki, Jian-Kang Zhu, Paul M. Hasegawa, Hans J. Bohnert, Huazhong Shi, Dae-Jin Yun, and Ray A. Bressan 4951 Genome-wide analysis for discovery of rice microRNAs reveals natural antisense microRNAs (nat-miRNAs) Cheng Lu, Dong-Hoon Jeong, Karthik Kulkarni, Manoj Pillay, Kan Nobuta, Rana German, Shawn R. Thatcher, Christopher Maher, Lifang Zhang, Doreen Ware, Bin Liu, Xiaofeng Cao, Blake C. Meyers, and Pamela J. Green

POPULATION BIOLOGY PLANT BIOLOGY 4553 cis-Jasmone induces Arabidopsis genes that affect the chemical ecology of multitrophic interactions with aphids and their parasitoids Toby J. A. Bruce, Michaela C. Matthes, Keith Chamberlain, Christine M. Woodcock, Abdul Mohib, Ben Webster, Lesley E. Smart, Michael A. Birkett, John A. Pickett, and Johnathan A. Napier

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4957 Population genomics of the wild yeast Saccharomyces paradoxus: Quantifying the life cycle Isheng J. Tsai, Douda Bensasson, Austin Burt, and Vassiliki Koufopanou xi–xii Author Index xiii Subscription Form