November 14, 2017 u vol. 114 u no. 46

From the Cover

12243 Zinc and skin epidermis development E9802 Putative giant panda pheromones 12162 Handgun waiting periods and gun deaths 12202 Climate change and arctic fish biogeography 12338 Population growth and climate change policy

Contents

THIS WEEK IN PNAS Cover image: Pictured are epithelial 12087 In This Issue cells (green) and the zinc transporter protein ZIP10 (red) in skin from a two- day-old mouse. Bum-Ho Bin et al. found LETTERS (ONLINE ONLY) that ZIP10 is highly expressed in E9755 Better choices than optical angular momentum multiplexing epidermal hair follicles and that ZIP10- for communications mediated zinc influx is required for the David A. B. Miller activity of the epidermal development E9757 Reply to Miller: Misunderstanding and mix-up of acoustic and regulator p63. Further, deletion of the optical communications Zip10 gene in mice resulted in Chengzhi Shi and Xiang Zhang epidermal hypoplasia, indicating the E9759 Theory, simulations, and experiments show that proteins fold by significance of ZIP10 and zinc multiple pathways homeostasis to epidermal development. William A. Eaton and Peter G. Wolynes See the article by Bin et al. on pages 12243–12248. Image courtesy of Koh-ei E9761 Reply to Eaton and Wolynes: How do proteins fold? Toyoshima and Takashi Tsuji. S. Walter Englander and Leland Mayne E9763 Harmful algal blooms in the Eastern North Atlantic Ocean Paul Dees, Eileen Bresnan, Andrew C. Dale, Martin Edwards, David Johns, Beth Mouat, Callum Whyte, and Keith Davidson E9765 Reply to Dees et al.: Ocean warming promotes species-specific increases in the cellular growth rates of harmful algal blooms Christopher J. Gobler, Theresa K. Hattenrath-Lehmann, Owen M. Doherty, Andrew W. Griffith, Yoonja Kang, and R. Wayne Litaker

INNER WORKINGS—An over-the-shoulder look at at work 12089 Special relationship between fungi and plants may have spurred changes to ancient climate Amber Dance

CORE CONCEPTS—A brief introduction to emerging topics in science 12092 Tissue resident memory cells emerging as key player in health and disease Bob Roehr

COMMENTARIES 12094 Reverse chemical ecology at the service of conservation biology Walter S. Leal See companion article on page E9802

Free online through the PNAS open access option. PNAS u November 14, 2017 u vol. 114 u no. 46 u iii–vii Downloaded by guest on September 30, 2021 12097 Reducing gun violence in America 12190 Early T cell receptor signals globally modulate ligand: Jens Ludwig receptor affinities during antigen discrimination See companion article on page 12162 Rafal M. Pielak, Geoff P. O’Donoghue, Jenny J. Lin, Katherine N. Alfieri, Nicole C. Fay, Shalini T. Low-Nam, 12100 Climate warming drives large-scale changes in and Jay T. Groves ecosystem function Leif Christian Stige and Kristina Øie Kvile COMPUTER SCIENCES See companion article on page 12202 E9783 Combining disparate data sources for improved 12103 How population growth relates to climate change poverty prediction and mapping Wolfgang Lutz Neeti Pokhriyal and Damien Christophe Jacques See companion article on page 12338 EARTH, ATMOSPHERIC, AND PLANETARY SCIENCES PNAS PLUS 12144 Giant boulders and Last Interglacial storm intensity in the North Atlantic 12106 Significance Statements Alessio Rovere, Elisa Casella, Daniel L. Harris, Thomas Brief statements written by the authors about the significance of their Lorscheid, Napayalage A. K. Nandasena, Blake Dyer, papers. Michael R. Sandstrom, Paolo Stocchi, William J. D’Andrea, and Maureen E. Raymo

INAUGURAL ARTICLE ENGINEERING 12111 STAT5-mediated chromatin interactions in 12150 Direct observation of impact propagation and superenhancers activate IL-2 highly inducible genes: absorption in dense colloidal monolayers Functional dissection of the Il2ra gene locus Ivo Buttinoni, Jinwoong Cha, Wei-Hsun Lin, Ste´phane Job, Peng Li, Suman Mitra, Rosanne Spolski, Jangsuk Oh, Wei Liao, Chiara Daraio, and Lucio Isa Zhonghui Tang, Fei Mo, Xingwang Li, Erin E. West, Daniel Gromer, Jian-Xin Lin, Chengyu Liu, Yijun Ruan, ENVIRONMENTAL SCIENCES and Warren J. Leonard E9793 Enhanced antibacterial activity through the controlled alignment of graphene oxide nanosheets Xinglin Lu, Xunda Feng, Jay R. Werber, Chiheng Chu, PHYSICAL SCIENCES Ines Zucker, Jae-Hong Kim, Chinedum O. Osuji, and Menachem Elimelech 12344 White blood cell population dynamics for risk PHYSICS stratification of acute coronary syndrome Anwesha Chaudhury, Lorette Noiret, and John M. Higgins 12156 Catalysis of heat-to-work conversion in quantum machines A. Ghosh, C. L. Latune, L. Davidovich, and G. Kurizki APPLIED PHYSICAL SCIENCES E9767 Continuum limit of the vibrational properties of amorphous solids SOCIAL SCIENCES Hideyuki Mizuno, Hayato Shiba, and Atsushi Ikeda 12120 Sensing fluctuating airflow with spider silk ECONOMIC SCIENCES Jian Zhou and Ronald N. Miles 12162 Handgun waiting periods reduce gun deaths Michael Luca, Deepak Malhotra, and Christopher Poliquin AND COMPUTATIONAL BIOLOGY See Commentary on page 12097 12126 De novo prediction of human chromosome 12338 Impact of population growth and population ethics structures: Epigenetic marking patterns on climate change mitigation policy encode genome architecture Noah Scovronick, Mark B. Budolfson, Francis Dennig, Marc Michele Di Pierro, Ryan R. Cheng, Erez Lieberman Aiden, Fleurbaey, Asher Siebert, Robert H. Socolow, Dean Spears, Peter G. Wolynes, and Jose´ N. Onuchic and Fabian Wagner See Commentary on page 12103 CHEMISTRY E9775 Interplay of hemilability and redox activity in models PSYCHOLOGICAL AND COGNITIVE SCIENCES of hydrogenase active sites 12279 Using neurostimulation to understand the impact Shengda Ding, Pokhraj Ghosh, Marcetta Y. Darensbourg, of pre-morbid individual differences on and Michael B. Hall post-lesion outcomes E9838 Parsing the roles of neck-linker docking and tethered Anna M. Woollams, Gaston Madrid, head diffusion in the stepping dynamics of kinesin and Matthew A. Lambon Ralph Zhechun Zhang, Yonathan Goldtzvik, and D. Thirumalai 12132 Assembly of silver Trigons into a buckyball-like SUSTAINABILITY SCIENCE E9783 Combining disparate data sources for improved Ag180 nanocage Zhi Wang, Hai-Feng Su, Yuan-Zhi Tan, Stan Schein, Shui-Chao poverty prediction and mapping Lin, Wei Liu, Shu-Ao Wang, Wen-Guang Wang, Chen-Ho Tung, Neeti Pokhriyal and Damien Christophe Jacques Di Sun, and Lan-Sun Zheng 12333 Supply and demand drive a critical transition to 12138 Strong texturing of lithium metal in batteries dysfunctional fisheries Feifei Shi, Allen Pei, Arturas Vailionis, Jin Xie, Bofei Liu, Jie John M. Fryxell, Ray Hilborn, Carling Bieg, Katrine Turgeon, Zhao, Yongji Gong, and Yi Cui Amanda Caskenette, and Kevin S. McCann

iv u www.pnas.org Contents Downloaded by guest on September 30, 2021 12190 Early T cell receptor signals globally modulate ligand: BIOLOGICAL SCIENCES receptor affinities during antigen discrimination APPLIED BIOLOGICAL SCIENCES Rafal M. Pielak, Geoff P. O’Donoghue, Jenny J. Lin, – Katherine N. Alfieri, Nicole C. Fay, Shalini T. Low-Nam, 12166 High-throughput characterization of protein protein and Jay T. Groves interactions by reprogramming yeast mating David Younger, Stephanie Berger, David Baker, CELL BIOLOGY and Eric Klavins E9863 Sequences flanking the transmembrane segments facilitate mitochondrial localization and BIOCHEMISTRY membrane fusion by mitofusin E9802 Reverse chemical ecology: Olfactory proteins from the Xiaofang Huang, Xin Zhou, Xiaoyu Hu, Amit S. Joshi, giant panda and their interactions with putative Xiangyang Guo, Yushan Zhu, Quan Chen, William A. Prinz, pheromones and bamboo volatiles and Junjie Hu Jiao Zhu, Simona Arena, Silvia Spinelli, Dingzhen Liu, Guiquan E9873 Intercellular mRNA trafficking via membrane Zhang, Rongping Wei, Christian Cambillau, Andrea Scaloni, nanotube-like extensions in mammalian cells Guirong Wang, and Paolo Pelosi Gal Haimovich, Christopher M. Ecker, Margaret C. Dunagin, See Commentary on page 12094 Elliott Eggan, Arjun Raj, Jeffrey E. Gerst, and Robert H. Singer E9811 Molecular basis of the 14-3-3 protein-dependent E9883 Probing and manipulating intracellular membrane activation of yeast neutral trehalase Nth1 traffic by microinjection of artificial vesicles Miroslava Alblova, Aneta Smidova, Vojtech Docekal, Jan Seiichi Koike and Reinhard Jahn Vesely, Petr Herman, Veronika Obsilova, and Tomas Obsil E9893 Patterns of conserved gp120 epitope presentation E9821 Role of the nucleotidyl cyclase helical domain in on attached HIV-1 virions catalytically active dimer formation Meron Mengistu, Ai-hui Tang, James S. Foulke Jr., Thomas A. Irene Vercellino, Lenka Rezabkova, Vincent Olieric, Yevhen Blanpied, Mileidy W. Gonzalez, John L. Spouge, Robert C. Polyhach, Tobias Weinert, Richard A. Kammerer, Gunnar Gallo, George K. Lewis, and Anthony L. DeVico Jeschke, and Volodymyr M. Korkhov E9903 A vimentin binding small molecule leads to mitotic E9829 Protocadherin cis-dimer architecture and disruption in mesenchymal cancers recognition unit diversity Michael J. Bollong, Mika Pietila¨, Aaron D. Pearson, Tapasree Kerry M. Goodman, Rotem Rubinstein, Hanbin Dan, Fabiana Roy Sarkar, Insha Ahmad, Rama Soundararajan, Costas A. Bahna, Seetha Mannepalli, Go¨ran Ahlse´n, Chan Aye Thu, Lyssiotis, Sendurai A. Mani, Peter G. Schultz, Rosemary V. Sampogna, Tom Maniatis, Barry Honig, and Luke L. Lairson and Lawrence Shapiro 12196 DsbA-L prevents obesity-induced inflammation and 12172 Mechanism of RNA polymerase II stalling by insulin resistance by suppressing the mtDNA DNA alkylation release-activated cGAS-cGAMP-STING pathway Stefano Malvezzi, Lucas Farnung, Claudia M. N. Aloisi, Todor Juli Bai, Christopher Cervantes, Juan Liu, Sijia He, Haiyan Zhou, Angelov, Patrick Cramer, and Shana J. Sturla Bilin Zhang, Huan Cai, Dongqing Yin, Derong Hu, Zhi Li, 12178 Large domain movements upon UvrD dimerization Hongzhi Chen, Xiaoli Gao, Fang Wang, Jason C. O’Connor, and helicase activation Yong Xu, Meilian Liu, Lily Q. Dong, and Feng Liu Binh Nguyen, Yerdos Ordabayev, Joshua E. Sokoloski, Elizabeth Weiland, and Timothy M. Lohman DEVELOPMENTAL BIOLOGY 12184 Inhibition of curli assembly and Escherichia coli E9913 Relevance of iPSC-derived human PGC-like cells at biofilm formation by the human systemic the surface of embryoid bodies to prechemotaxis amyloid precursor transthyretin migrating PGCs Neha Jain, Jo¨rgen A˚de´n, Kanna Nagamatsu, Margery L. Shino Mitsunaga, Junko Odajima, Shiomi Yawata, Keiko Evans, Xinyi Li, Brennan McMichael, Magdalena I. Shioda, Chie Owa, Kurt J. Isselbacher, Jacob H. Hanna, Ivanova, Fredrik Almqvist, Joel N. Buxbaum, and Toshi Shioda and Matthew R. Chapman ECOLOGY BIOPHYSICS AND COMPUTATIONAL BIOLOGY 12202 Climate-driven changes in functional biogeography E9838 Parsing the roles of neck-linker docking and tethered of Arctic marine fish communities head diffusion in the stepping dynamics of kinesin Andre´ Frainer, Raul Primicerio, Susanne Kortsch, Magnus Aune, Andrey V. Dolgov, Maria Fossheim, Zhechun Zhang, Yonathan Goldtzvik, and D. Thirumalai and Michaela M. Aschan E9846 Probing the cooperativity of Thermoplasma See Commentary on page 12100 acidophilum proteasome core particle 12208 Pathogen-mediated selection in free-ranging elk gating by NMR spectroscopy populations infected by chronic wasting disease Rui Huang, Felipe Pe´rez, and Lewis E. Kay Ryan J. Monello, Nathan L. Galloway, Jenny G. Powers, Sally A. E9855 Binding kinetics and substrate selectivity in HIV-1 Madsen-Bouterse, William H. Edwards, Mary E. Wood, protease−Gag interactions probed at atomic Katherine I. O’Rourke, and Margaret A. Wild resolution by chemical exchange NMR Lalit Deshmukh, Vitali Tugarinov, John M. Louis, ENVIRONMENTAL SCIENCES and G. Marius Clore E9923 Contaminants of emerging concern affect Trichoplusia 12126 De novo prediction of human chromosome ni growth and development on artificial diets and structures: Epigenetic marking patterns a key host plant encode genome architecture Marcus J. Pennington, Jason A. Rothman, Stacia L. Dudley, Michele Di Pierro, Ryan R. Cheng, Erez Lieberman Aiden, Michael B. Jones, Quinn S. McFrederick, Jay Gan, Peter G. Wolynes, and Jose´ N. Onuchic and John T. Trumble

Contents PNAS u November 14, 2017 u vol. 114 u no. 46 u v Downloaded by guest on September 30, 2021 12261 O2 availability impacts iron homeostasis in E9932 Seasonally fluctuating selection can maintain Escherichia coli polymorphism at many loci via segregation lift Nicole A. Beauchene, Erin L. Mettert, Laura J. Moore, Su¨ndu¨z ş Meike J. Wittmann, Alan O. Bergland, Marcus W. Feldman, Kele , Emily R. Willey, and Patricia J. Kiley Paul S. Schmidt, and Dmitri A. Petrov 12267 Phytopathogenic fungus hosts a plant virus: 12213 Estimating mobility using sparse data: Application to A naturally occurring cross-kingdom viral infection human genetic variation Ida Bagus Andika, Shuang Wei, Chunmei Cao, Lakha Salaipeth, Liisa Loog, Marta Mirazo´n Lahr, Mirna Kovacevic, Andrea Hideki Kondo, and Liying Sun Manica, Anders Eriksson, and Mark G. Thomas 12273 Replication of early and recent Zika virus isolates 12219 Testing the neutral hypothesis of throughout mouse brain development phenotypic evolution Amy B. Rosenfeld, David J. Doobin, Audrey L. Warren, Wei-Chin Ho, Yoshikazu Ohya, and Jianzhi Zhang Vincent R. Racaniello, and Richard B. Vallee

GENETICS 12225 DNA–RNA interactions are critical for chromosome NEUROSCIENCE condensation in Escherichia coli E9952 Visual experience sculpts whole-cortex spontaneous Zhong Qian, Victor B. Zhurkin, and Sankar Adhya infraslow activity patterns through an 12231 Genomic features shaping the landscape of meiotic Arc-dependent mechanism double-strand-break hotspots in maize Andrew W. Kraft, Anish Mitra, Adam Q. Bauer, Abraham Z. Snyder, Marcus E. Raichle, Joseph P. Culver, and Jin-Moo Lee Yan He, Minghui Wang, Stefanie Dukowic-Schulze, Adele Zhou, Choon-Lin Tiang, Shay Shilo, Gaganpreet K. Sidhu, E9962 Electrical synapses mediate synergism Steven Eichten, Peter Bradbury, Nathan M. Springer, between pheromone and food odors in Edward S. Buckler, Avraham A. Levy, Qi Sun, Jaroslaw Pillardy, Drosophila melanogaster Penny M. A. Kianian, Shahryar F. Kianian, Changbin Chen, Sudeshna Das, Federica Trona, Mohammed A. Khallaf, and Wojciech P. Pawlowski Elisa Schuh, Markus Knaden, Bill S. Hansson, and Silke Sachse IMMUNOLOGY AND INFLAMMATION E9942 The immunopeptidomic landscape of E9972 Silent memory engrams as the basis for ovarian carcinomas retrograde amnesia Dheeraj S. Roy, Shruti Muralidhar, Lillian M. Smith, Heiko Schuster, Janet K. Peper, Hans-Christian Bo¨smu¨ller, and Susumu Tonegawa Kevin Ro¨hle, Linus Backert, Tatjana Bilich, Britta Ney, Markus W. Lo¨ffler, Daniel J. Kowalewski, Nico Trautwein, 12279 Using neurostimulation to understand the impact Armin Rabsteyn, Tobias Engler, Sabine Braun, Sebastian P. of pre-morbid individual differences on Haen, Juliane S. Walz, Barbara Schmid-Horch, Sara Y. Brucker, post-lesion outcomes Diethelm Wallwiener, Oliver Kohlbacher, Falko Fend, Anna M. Woollams, Gaston Madrid,  Hans-Georg Rammensee, Stefan Stevanovic, Annette and Matthew A. Lambon Ralph Staebler, and Philipp Wagner 12285 Facephenes and rainbows: Causal evidence for 12111 STAT5-mediated chromatin interactions in functional and anatomical specificity of face superenhancers activate IL-2 highly inducible genes: and color processing in the human brain Functional dissection of the Il2ra gene locus Gerwin Schalk, Christoph Kapeller, Christoph Peng Li, Suman Mitra, Rosanne Spolski, Jangsuk Oh, Wei Liao, Guger, Hiroshi Ogawa, Satoru Hiroshima, Rosa Zhonghui Tang, Fei Mo, Xingwang Li, Erin E. West, Daniel Lafer-Sousa, Zeynep M. Saygin, Kyousuke Kamada, Gromer, Jian-Xin Lin, Chengyu Liu, Yijun Ruan, and Nancy Kanwisher and Warren J. Leonard 12291 The human visual cortex response to melanopsin- MEDICAL SCIENCES directed stimulation is accompanied by a 12237 Dynamics of cell transformation in culture and its distinct perceptual experience significance for tumor development in animals Manuel Spitschan, Andrew S. Bock, Jack Ryan, Giulia Frazzetta, Harry Rubin David H. Brainard, and Geoffrey K. Aguirre 12243 Requirement of zinc transporter ZIP10 for epidermal 12297 Human hippocampal theta power indicates development: Implication of the ZIP10–p63 axis in movement onset and distance travelled epithelial homeostasis Daniel Bush, James A. Bisby, Chris M. Bird, Stephanie Gollwitzer, Roman Rodionov, Beate Diehl, Andrew W. McEvoy, Bum-Ho Bin, Jinhyuk Bhin, Mikiro Takaishi, Koh-ei Toyoshima, Matthew C. Walker, and Neil Burgess Saeko Kawamata, Kana Ito, Takafumi Hara, Takashi Watanabe, Tarou Irie´, Teruhisa Takagishi, Su-Hyon Lee, Haeng-Sun Jung, 12303 Cooperative cortical network for categorical Sangchul Rho, Juyeon Seo, Dong-Hwa Choi, Daehee Hwang, processing of Chinese lexical tone Haruhiko Koseki, Osamu Ohara, Shigetoshi Sano, Takashi Xiaopeng Si, Wenjing Zhou, and Bo Hong Tsuji, Kenji Mishima, and Toshiyuki Fukada 12249 PRC2-mediated repression of SMARCA2 predicts EZH2 inhibitor activity in SWI/SNF mutant tumors PHARMACOLOGY Thomas Januario, Xiaofen Ye, Russell Bainer, Bruno Alicke, 12309 Endosomal signaling of the receptor for Tunde Smith, Benjamin Haley, Zora Modrusan, Stephen Gould, calcitonin gene-related peptide mediates and Robert L. Yauch pain transmission Rebecca E. Yarwood, Wendy L. Imlach, TinaMarie Lieu, MICROBIOLOGY Nicholas A. Veldhuis, Dane D. Jensen, Carmen Klein 12255 Rewriting nature’s assembly manual for Herenbrink, Luigi Aurelio, Zhijian Cai, MacDonald J. Christie, a ssRNA virus Daniel P. Poole, Christopher J. H. Porter, Peter McLean, Nikesh Patel, Emma Wroblewski, German Leonov, Simon E. V. Gareth A. Hicks, Pierangelo Geppetti, Michelle L. Halls, Phillips, Roman Tuma, Reidun Twarock, and Peter G. Stockley Meritxell Canals, and Nigel W. Bunnett

vi u www.pnas.org Contents Downloaded by guest on September 30, 2021 12315 NOX4-dependent neuronal autotoxicity and BBB E10018 Global analysis of ribosome-associated noncoding breakdown explain the superior sensitivity of RNAs unveils new modes of translational regulation the brain to ischemic damage Je´re´mie Bazin, Katja Baerenfaller, Sager J. Gosai, Brian D. Ana I. Casas, Eva Geuss, Pamela W. M. Kleikers, Stine Mencl, Gregory, Martin Crespi, and Julia Bailey-Serres Alexander M. Herrmann, Izaskun Buendia, Javier Egea, 12321 COP1 mediates dark-specific degradation of Sven G. Meuth, Manuela G. Lopez, Christoph Kleinschnitz, microtubule-associated protein WDL3 in regulating and Harald H. H. W. Schmidt Arabidopsis hypocotyl elongation Na Lian, Xiaomin Liu, Xiaohong Wang, Yangyang Zhou, Hong PHYSIOLOGY Li, Jigang Li, and Tonglin Mao E9980 Active site voltage clamp fluorometry of the sodium 12327 Two rice receptor-like kinases maintain male fertility glucose cotransporter hSGLT1 under changing temperatures Edurne Gorraitz, Bruce A. Hirayama, Aviv Paz, Ernest M. Junping Yu, Jiaojiao Han, Yu-Jin Kim, Ming Song, Zhen Yang, Wright, and Donald D. F. Loo Yi He, Ruifeng Fu, Zhijing Luo, Jianping Hu, Wanqi Liang, E9989 Transcriptomes of major renal collecting and Dabing Zhang duct cell types in mouse identified by single-cell RNA-seq POPULATION BIOLOGY Lihe Chen, Jae Wook Lee, Chung-Lin Chou, Anil V. Nair, 12333 Supply and demand drive a critical transition to Maria A. Battistone, Teodor G. Paunescu,˘ Maria Merkulova, dysfunctional fisheries Sylvie Breton, Jill W. Verlander, Susan M. Wall, Dennis Brown, John M. Fryxell, Ray Hilborn, Carling Bieg, Katrine Turgeon, Maurice B. Burg, and Mark A. Knepper Amanda Caskenette, and Kevin S. McCann

SUSTAINABILITY SCIENCE PLANT BIOLOGY 12338 Impact of population growth and population ethics E9999 Genome diversity of tuber-bearing Solanum uncovers on climate change mitigation policy complex evolutionary history and targets of Noah Scovronick, Mark B. Budolfson, Francis Dennig, Marc domestication in the cultivated potato Fleurbaey, Asher Siebert, Robert H. Socolow, Dean Spears, Michael A. Hardigan, F. Parker E. Laimbeer, Linsey and Fabian Wagner Newton, Emily Crisovan, John P. Hamilton, Brieanne See Commentary on page 12103 Vaillancourt, Krystle Wiegert-Rininger, Joshua C. Wood, David S. Douches, Eva M. Farre´, Richard E. Veilleux, SYSTEMS BIOLOGY and C. Robin Buell 12344 White blood cell population dynamics for risk E10009 MPSR1 is a cytoplasmic PQC E3 ligase for stratification of acute coronary syndrome eliminating emergent misfolded proteins Anwesha Chaudhury, Lorette Noiret, and John M. Higgins in Arabidopsis thaliana Jong Hum Kim, Seok Keun Cho, Tae Rin Oh, Moon Young Ryu, Seong Wook Yang, and Woo Taek Kim ix Subscription Form

Contents PNAS u November 14, 2017 u vol. 114 u no. 46 u vii Downloaded by guest on September 30, 2021