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April 7, 2015 u vol. 112 u no. 14 u 4183–4506

Cover image: Pictured is zebrafish visceral adipose tissue containing lipid droplets (green), plasma membranes (magenta), and collagen (blue). Using genetic analysis and in vivo imag- ing of fluorescently labeled adipocytes, James E. N. Minchin et al. observed lipid deposition patterns in zebrafish. Fish deficient in Plxnd1, a transmembrane receptor that controls the migration of different cell types, displayed altered visceral body fat distribution and were protected from insulin resistance induced by a high-fat diet. The results suggest that Plxnd1 regulates the distribution and morphology of adipose tissue and may have implications in the treatment of metabolic disease. See the article by Minchin et al. on pages 4363–4368. Image courtesy of James E. N. Minchin. From the Cover

4363 Regulation of body fat distribution 4214 Jupiter and evolution of the Solar System 4352 Improving luminescence imaging 4381 Phosphorus sequestration in marine sponges 4459 Evolution of leprosy

Contents SCIENCE AND CULTURE—How science intersects with culture 4185 Science and Culture: Using fiction to make the case for basic research Joel Shurkin THIS WEEK IN PNAS

4183 In This Issue COMMENTARIES

4187 Systems approach to metal-based pharmacology LETTERS (ONLINE ONLY) Isolda Romero-Canelón and Peter J. Sadler See companion article on page 3211 in issue 11 of volume 112 E1693 Loss of HtrA1-induced attenuation of TGF-β signaling 4189 Jupiter’s role in sculpting the early Solar System in fibroblasts might not be the main mechanism Smadar Naoz of CARASIL pathogenesis See companion article on page 4214 Ju Liu, Fengyun Dong, and Josephine Hoh 4191 Sponge symbionts and the marine P cycle E1694 Reply to Liu et al.: Loss of TGF-β signaling in Albert S. Colman CARASIL pathogenesis See companion article on page 4381 Nathalie Beaufort, Eva Scharrer, Vanda Lux, Michael Ehrmann, Christof Haffner, and Martin Dichgans PNAS PLUS E1695 Highly productive sown biodiverse pastures with low invasion risk Vânia Proença, Carlos Aguiar, and Tiago Domingos 4193 Significance Statements Brief statements written by the authors about the significance of E1696 Reply to Proença et al.: Sown biodiverse pastures their papers. are not a universal solution to invasion risk Don A. , Jane A. Catford, Jacob N. , Philip E. Hulme, Inderjit, Tara G. Martin, Aníbal INAUGURAL ARTICLE Pauchard, Petr Pysek, M. Richardson, Sophie Riley, and Vernon Visser 4195 Candidate ionotropic taste receptors in the Drosophila larva Shannon Stewart, Tong-Wey Koh, Arpan C. Ghosh, Free online through the PNAS open access option. and John R. Carlson

PNAS u April 7, 2015 u vol. 112 u no. 14 u iii–vii Downloaded by guest on September 30, 2021 ENVIRONMENTAL SCIENCES PHYSICAL SCIENCES 4251 Trichodesmium genome maintains abundant, widespread noncoding DNA in situ, despite APPLIED MATHEMATICS oligotrophic lifestyle 4202 Using wavelength and slope to infer the historical Nathan Walworth, Ulrike Pfreundt, William C. Nelson, origin of semiarid vegetation bands Tracy Mincer, John F. Heidelberg, Feixue Fu, John B. Jonathan A. Sherratt Waterbury, Tijana Glavina del Rio, Lynne Goodwin, Nikos C. Kyrpides, Miriam L. Land, Tanja Woyke, 4208 Route to thermalization in the α-Fermi–Pasta– David A. Hutchins, Wolfgang R. Hess, and Eric A. Webb Ulam system Miguel Onorato, Lara Vozella, Davide Proment, SUSTAINABILITY SCIENCE and Yuri V. Lvov 4257 Criticality of metals and metalloids T. E. Graedel, E. M. Harper, N. T. Nassar, Philip Nuss, and Barbara K. Reck ASTRONOMY 4214 Jupiter’s decisive role in the inner Solar System’s early evolution Konstantin Batygin and Greg Laughlin SOCIAL SCIENCES See Commentary on page 4189 ANTHROPOLOGY 4263 Late Pleistocene horse and camel hunting at the CHEMISTRY southern margin of the ice-free corridor: Reassessing 4218 Evidence for tunneling in base-catalyzed isomerization the age of Wally’s Beach, Canada of glyceraldehyde to dihydroxyacetone by hydride Michael R. , Thomas W. Stafford Jr., Brian Kooyman, shift under formose conditions and L. V. Hills Liang Cheng, Charles Doubleday, and Ronald Breslow 4268 Development of sedentary communities in the Maya 4221 Multiplexed metagenome mining using short DNA lowlands: Coexisting mobile groups and public sequence tags facilitates targeted discovery of ceremonies at Ceibal, Guatemala epoxyketone proteasome inhibitors Takeshi Inomata (猪俣 健), Jessica MacLellan, Daniela Jeremy G. Owen, Zachary Charlop-Powers, Triadan, Jessica Munson, Melissa Burham, Kazuo Alexandra G. Smith, Melinda A. Ternei, Paula Y. Aoyama (青山 和夫), Hiroo Nasu (那須 浩郎), Calle, Boojala Vijay B. Reddy, Daniel Montiel, Flory Pinzón, and Hitoshi Yonenobu (米延 仁志) and Sean F. Brady PSYCHOLOGICAL AND COGNITIVE SCIENCES 4227 Tunable molecular orientation and elevated 4274 Leader emergence through interpersonal thermal stability of vapor-deposited neural synchronization organic semiconductors Jing Jiang (蒋静), Chuansheng Chen (陈传升), Bohan Shakeel S. Dalal, Diane M. Walters, Ivan Lyubimov, Dai (代博涵), Guang Shi (时光), Guosheng Ding (丁国盛), Juan J. de Pablo, and M. D. Ediger Li Liu (刘丽), and Chunming Lu (卢春明) 4233 Engineering three-dimensional hybrid supercapacitors and microsupercapacitors for high-performance SUSTAINABILITY SCIENCE integrated energy storage 4375 Area burned in the western United States is unaffected Maher F. El-Kady, Melanie Ihns, Mengping Li, Jee Youn by recent mountain pine beetle outbreaks Hwang, Mir F. Mousavi, Lindsay Chaney, Andrew T. Lech, Sarah J. Hart, Tania Schoennagel, Thomas T. Veblen, and Richard B. Kaner and Teresa B.

EARTH, ATMOSPHERIC, AND PLANETARY SCIENCES BIOLOGICAL SCIENCES 4239 Continental erosion and the Cenozoic rise of marine diatoms Pedro Cermeño, Paul G. Falkowski, Oscar E. Romero, APPLIED BIOLOGICAL SCIENCES Morgan F. Schaller, and Sergio M. Vallina 4280 Sparse feature selection methods identify unexpected global cellular response to 4245 Evidence for indigenous nitrogen in sedimentary and strontium-containing materials aeolian deposits from the Curiosity rover investigations Hélène Autefage, Eileen Gentleman, Elena Littmann, at Gale crater, Mars Martin A. B. Hedegaard, Thomas Von Erlach, Matthew Jennifer C. Stern, Brad Sutter, Caroline Freissinet, O’Donnell, Frank R. Burden, David A. Winkler, Rafael Navarro-González, Christopher P. McKay, and Molly M. Stevens P. Douglas Archer Jr., Arnaud Buch, Anna E. Brunner, Patrice Coll, Jennifer L. Eigenbrode, Alberto G. Fairen, Heather B. , Daniel P. Glavin, Srishti Kashyap, BIOCHEMISTRY Amy C. McAdam, Douglas W. Ming, Andrew Steele, E1697 Motion of proximal histidine and structural allosteric Cyril Szopa, James J. Wray, F. Javier Martín-Torres, transition in soluble guanylate cyclase Maria-Paz Zorzano, Pamela G. Conrad, Paul R. Byung-Kuk Yoo, Isabelle Lamarre, Jean-Louis Martin, Mahaffy, and the MSL Science Team Fabrice Rappaport, and Michel Negrerie

iv u www.pnas.org Downloaded by guest on September 30, 2021 E1705 Altered cofactor regulation with disease-associated 4334 N-Glycosylation as determinant of epidermal growth p97/VCP mutations factor receptor conformation in membranes Xiaoyi Zhang, Lin Gui, Xiaoyan Zhang, Stacie L. Bulfer, Karol Kaszuba, Michał Grzybek, Adam Orłowski, Reinis Valentina Sanghez, Daniel E. Wong, YouJin Lee, Lynn Danne, Tomasz Róg, Kai Simons, Ünal Coskun, Lehmann, James Siho Lee, Pei-Yin Shih, Henry J. Lin, and Ilpo Vattulainen Michelina Iacovino, Conrad C. Weihl, Michelle R. Arkin, Yanzhuang Wang, and Tsui-Fen Chou CELL BIOLOGY 4218 Evidence for tunneling in base-catalyzed isomerization E1724 Oncogenesis driven by the Ras/Raf pathway requires of glyceraldehyde to dihydroxyacetone by hydride the SUMO E2 ligase Ubc9 shift under formose conditions Bing Yu, Stephen Swatkoski, Alesia Holly, Liam C. Lee, Liang Cheng, Charles Doubleday, and Ronald Breslow Valentin Giroux, Chih-Shia Lee, Dennis Hsu, Jordan L. 4286 Human RECQ1 helicase-driven DNA unwinding, Smith, Garmen Yuen, Junqiu Yue, David K. Ann, R. Mark annealing, and branch migration: Insights Simpson, Chad J. Creighton, William D. Figg, Marjan Gucek, from DNA complex structures and Ji Luo Ashley C. W. Pike, Shivasankari Gomathinayagam, 4340 KLHL3 regulates paracellular chloride transport in the Paolo Swuec, Matteo Berti, Ying Zhang, Christina kidney by ubiquitination of claudin-8 Schnecke, Francesca Marino, Frank von Delft, Yongfeng Gong, Jinzhi Wang, Jing Yang, Ernie Gonzales, Ludovic Renault, Alessandro Costa, Opher Gileadi, Ronaldo Perez, and Jianghui Hou and Alessandro Vindigni 4346 TRAPPII regulates exocytic Golgi exit by mediating 4292 Structural mechanisms of DNA binding and unwinding nucleotide exchange on the Ypt31 in bacterial RecQ helicases ortholog RabERAB11 Kelly A. Manthei, Morgan C. Hill, Jordan E. , Mario Pinar, Herbert N. Arst Jr., Areti Pantazopoulou, Samuel E. Butcher, and James L. Keck Víctor G. Tagua, Vivian de los Ríos, Javier Rodríguez-Salarichs, J. Fernando Díaz, 4298 Phosphorylation of ORF1p is required for and Miguel A. Peñalva L1 retrotransposition Pamela R. , Charles E. Jones, and Anthony V. Furano 4352 Expanded palette of Nano-lanterns for real-time multicolor luminescence imaging 4304 SWI/SNF chromatin-remodeling complexes function in Akira Takai, Masahiro Nakano, Kenta Saito, Remi Haruno, noncoding RNA-dependent assembly of nuclear bodies Tomonobu M. Watanabe, Tatsuya Ohyanagi, Takashi Jin, Tetsuya Kawaguchi, Akie Tanigawa, Takao Naganuma, Yasushi Okada, and Takeharu Nagai Yasuyuki Ohkawa, Sylvie Souquere, Gerard Pierron, and Tetsuro Hirose 4357 The frequency natural antisense transcript first promotes, then represses, frequency gene expression 4310 A functional role of Rv1738 in Mycobacterium via facultative heterochromatin tuberculosis persistence suggested by racemic Na Li, Tammy M. Joska, Catherine E. Ruesch, Samuel J. protein crystallography Coster, and William J. Belden Richard D. Bunker, Kalyaneswar Mandal, Ghader Bashiri, Jessica J. Chaston, Bradley L. Pentelute, J. Shaun Lott, Stephen B. H. Kent, and Edward N. Baker DEVELOPMENTAL BIOLOGY 4316 Biochemical characterization of a Naegleria TET-like E1734 Emergence of hematopoietic stem and progenitor cells oxygenase and its application in single molecule involves a Chd1-dependent increase in total sequencing of 5-methylcytosine nascent transcription June E. Pais, Nan Dai, Esta Tamanaha, Romualdas Fong Ming Koh, Carlos O. Lizama, Priscilla Wong, John S. Vaisvila, Alexey I. Fomenkov, Jurate Bitinaite, Zhiyi Sun, Hawkins, Ann C. Zovein, and Miguel Ramalho-Santos Shengxi Guan, Ivan R. Corrêa Jr., Christopher J. Noren, 4363 Plexin D1 determines body fat distribution by regulating Xiaodong Cheng, Richard J. Roberts, Yu Zheng, the type V collagen microenvironment in visceral and Lana Saleh adipose tissue James E. N. Minchin, Ingrid Dahlman, Christopher J. Harvey, BIOPHYSICS AND COMPUTATIONAL BIOLOGY Niklas Mejhert, Manvendra K. Singh, Jonathan A. Epstein, Peter Arner, Jesús Torres-Vázquez, and John F. Rawls E1715 Single-molecule analysis of RAG-mediated V(D)J DNA cleavage 4369 RNA transcribed from a distal enhancer is required for Geoffrey A. Lovely, Robert C. Brewster, David G. Schatz, activating the chromatin at the promoter of the David Baltimore, and Rob Phillips gonadotropin α-subunit gene Lilach Pnueli, Sergei Rudnizky, Yahav Yosefzon, 4322 Immunoglobulin transcript sequence and somatic and Philippa Melamed hypermutation computation from unselected RNA-seq reads in chronic lymphocytic leukemia James S. Blachly, Amy S. Ruppert, Weiqiang Zhao, ECOLOGY Susan Long, Joseph Flynn, Ian Flinn, Jeffrey Jones, 4202 Using wavelength and slope to infer the historical Kami Maddocks, Leslie Andritsos, Emanuela M. Ghia, origin of semiarid vegetation bands Laura Z. Rassenti, Thomas J. Kipps, Albert de la Chapelle, Jonathan A. Sherratt and John C. Byrd 4375 Area burned in the western United States is unaffected

4328 The entropic contributions in vitamin B12 enzymes still by recent mountain pine beetle outbreaks reflect the electrostatic paradigm Sarah J. Hart, Tania Schoennagel, Thomas T. Veblen, Patrick Schopf, Matthew J. L. Mills, and Arieh Warshel and Teresa B. Chapman

PNAS u April 7, 2015 u vol. 112 u no. 14 u v Downloaded by guest on September 30, 2021 4381 Phosphorus sequestration in the form of polyphosphate 4429 Regulatory vs. inflammatory cytokine T-cell responses to by microbial symbionts in marine sponges mutated insulin peptides in healthy and type 1 Fan Zhang, Leah C. Blasiak, Jan O. Karolin, Ryan J. Powell, diabetic subjects Chris D. Geddes, and Russell T. Hill Maki Nakayama, Kristen McDaniel, Lisa -Miller, See Commentary on page 4191 Carol Kiekhaefer, Janet K. Snell-Bergeon, Howard W. Davidson, Marian Rewers, Liping Yu, Peter Gottlieb, John W. 4387 Non-native plants add to the British flora without Kappler, and Aaron Michels negative consequences for native diversity Chris D. Thomas and G. Palmer MEDICAL SCIENCES E1754 TCR contact residue hydrophobicity is a hallmark of EVOLUTION immunogenic CD8+ T cell epitopes 4239 Continental erosion and the Cenozoic rise of Diego Chowell, Sri Krishna, Pablo D. Becker, Clément Cocita, marine diatoms Jack Shu, Xuefang Tan, Philip D. Greenberg, Linda S. Pedro Cermeño, Paul G. Falkowski, Oscar E. Romero, Klavinskis, Joseph N. Blattman, and Karen S. Anderson Morgan F. Schaller, and Sergio M. Vallina 4435 Infection by Toxoplasma gondii, a severe parasite in 4251 Trichodesmium genome maintains abundant, neonates and AIDS patients, causes impaired anion widespread noncoding DNA in situ, despite secretion in airway epithelia oligotrophic lifestyle Hong-Mei Guo, Jiang-Mei Gao, Yu-Li Luo, Yan-Zi Wen, Nathan Walworth, Ulrike Pfreundt, William C. Nelson, Yi-Lin Zhang, Geoff Hide, Wen-Liang Zhou, Francisco J. Tracy Mincer, John F. Heidelberg, Feixue Fu, John B. Ayala, and Zhao-Rong Lun Waterbury, Tijana Glavina del Rio, Lynne Goodwin, 4441 Hypoxic induction of AKAP12 variant 2 shifts Nikos C. Kyrpides, Miriam L. Land, Tanja Woyke, PKA-mediated protein phosphorylation to enhance David A. Hutchins, Wolfgang R. Hess, and Eric A. Webb migration and metastasis of melanoma cells 4393 Sexual selection drives evolution and rapid turnover of Elizabeth C. Finger, Laura Castellini, Erinn B. Rankin, Marta male gene expression Vilalta, Adam J. Krieg, Dadi Jiang, Alice Banh, Wayne Peter W. Harrison, Alison E. Wright, Fabian Zimmer, Zundel, Marianne Broome Powell, and Amato J. Giaccia Rebecca Dean, Stephen H. Montgomery, Marie A. Pointer, 4447 Myocardin is required for maintenance of vascular and Judith E. Mank and visceral smooth muscle homeostasis during postnatal development 4399 Constraints, independence, and evolution of thermal Jianhe Huang, Tao Wang, Alexander C. Wright, Jifu plasticity: Probing genetic architecture of long- and Yang, Su Zhou, Li Li, Jisheng Yang, Aeron Small, short-term thermal acclimation and Michael S. Parmacek Alison R. Gerken, Olivia C. Eller, Daniel A. Hahn, and Theodore J. Morgan MICROBIOLOGY E1763 An adenosine triphosphate-independent proteasome GENETICS activator contributes to the virulence of 4405 Molecular coevolution of a sex pheromone and its Mycobacterium tuberculosis receptor triggers reproductive isolation in Jordan B. Jastrab, Tong Wang, J. Patrick Murphy, Lin Bai, Schizosaccharomyces pombe Kuan Hu, Remco Merkx, Jessica Huang, Champak Taisuke Seike, Taro Nakamura, and Chikashi Shimoda Chatterjee, Huib Ovaa, Steven P. Gygi, Huilin Li, and K. Heran 4411 Enhanced expression of DNA polymerase eta contributes to cisplatin resistance of ovarian cancer E1773 cGAS-mediated stabilization of IFI16 promotes stem cells innate signaling during herpes simplex Amit Kumar Srivastava, Chunhua Han, Ran Zhao, virus infection Tiantian Cui, Yuntao Dai, Charlene Mao, Weiqiang Megan H. Orzalli, Nicole M. Broekema, Benjamin A. Diner, Zhao, Xiaoli Zhang, Jianhua Yu, and Qi-En Wang Dustin C. Hancks, Nels C. Elde, Ileana M. Cristea, and David M. Knipe 4417 Unilateral incompatibility gene ui1.1 encodes an S-locus F-box protein expressed in pollen of E1782 RNA virus replication depends on enrichment of Solanum species phosphatidylethanolamine at replication sites in Wentao Li and Roger T. Chetelat subcellular membranes Kai Xu and Peter D. Nagy E1792 Structure of the paramyxovirus parainfluenza virus 5 IMMUNOLOGY AND INFLAMMATION nucleoprotein–RNA complex E1744 T-cell receptor α enhancer is inactivated in αβ Maher Alayyoubi, George P. Leser, Christopher A. Kors, T lymphocytes and Robert A. Lamb Beatriz del Blanco, Úrsula Angulo, Michael S. Krangel, and Cristina Hernández-Munain 4221 Multiplexed metagenome mining using short DNA sequence tags facilitates targeted discovery of 4423 Dynamin 2-dependent endocytosis sustains T-cell epoxyketone proteasome inhibitors receptor signaling and drives metabolic reprogramming Jeremy G. Owen, Zachary Charlop-Powers, in T lymphocytes Alexandra G. Smith, Melinda A. Ternei, Paula Y. Tim Willinger, Matthew Staron, Shawn M. Ferguson, Pietro Calle, Boojala Vijay B. Reddy, Daniel Montiel, De Camilli, and Richard A. Flavell and Sean F. Brady

vi u www.pnas.org Downloaded by guest on September 30, 2021 4453 Auranofin exerts broad-spectrum bactericidal activities PHYSIOLOGY by targeting thiol-redox homeostasis 4495 Src-family protein tyrosine kinase phosphorylates WNK4 Michael B. Harbut, Catherine Vilchèze, Xiaozhou Luo, and modulates its inhibitory effect on KCNJ1 (ROMK) Mary E. Hensler, Hui Guo, Baiyuan Yang, Arnab K. Dao-Hong Lin, Peng Yue, Orlando Yarborough III, Ute I. Chatterjee, Victor Nizet, William R. Jacobs Jr., Peter G. Scholl, Gerhard Giebisch, Richard P. Lifton, Jesse Rinehart, Schultz, and Feng Wang and Wen-Hui Wang 4459 Insight into the evolution and origin of leprosy bacilli from the genome sequence of SYSTEMS BIOLOGY Mycobacterium lepromatosis 4501 Systematic identification of signal integration by protein Pushpendra Singh, Andrej Benjak, Verena J. kinase A Schuenemann, Alexander Herbig, Charlotte Avanzi, Marie Filteau, Guillaume Diss, Francisco Torres-Quiroz, Philippe Busso, Kay Nieselt, Johannes Krause, Lucio Alexandre K. Dubé, Andrea Schraffl, Verena A. Vera-Cabrera, and Stewart T. Cole Bachmann, Isabelle Gagnon-Arsenault, Andrée-Ève 4465 Carbon monoxide as a metabolic energy source for Chrétien, Anne-Lise Steunou, Ugo Dionne, Jacques Côté, extremely halophilic microbes: Implications for Nicolas Bisson, Eduard Stefan, and Christian R. Landry microbial activity in Mars regolith Gary M. King 4471 A viral regulator of glycoprotein complexes CORRECTIONS (ONLINE ONLY) contributes to human cytomegalovirus cell tropism PSYCHOLOGICAL AND COGNITIVE SCIENCES Gang Li, Christopher C. Nguyen, Brent J. Ryckman, E1810 Coincidence avoidance principle in surface William J. Britt, and Jeremy P. Kamil haptic interpretation Steven G. Manuel, Roberta L. Klatzky, Michael A. NEUROSCIENCE Peshkin, and James Edward Colgate 4195 Candidate ionotropic taste receptors in the NEUROSCIENCE Drosophila larva Shannon Stewart, Tong-Wey Koh, Arpan C. Ghosh, E1811 Nitric oxide regulates synaptic transmission between and John R. Carlson spiny projection neurons Yotam Sagi, Myriam Heiman, Jayms D. Peterson, Sergei 4477 A multistage mathematical approach to automated Musatov, Michael G. Kaplitt, J. Surmeier, clustering of high-dimensional noisy data Nathaniel Heintz, and Paul Greengard Alexander Friedman, Michael D. Keselman, Leif G. Gibb, and Ann M. Graybiel SYSTEMS BIOLOGY β – 4483 -Arrestin biased signaling mediates E1812 Cardiac ferroportin regulates cellular iron homeostasis memory reconsolidation and is important for cardiac function Xing Liu, Li Ma, Hao Hong Li, Bing Huang, You Xing Li, Samira Lakhal-Littleton, Magda Wolna, Carolyn A. Carr, Ye Zheng Tao, and Lan Ma Jack J. J. Miller, Helen C. Christian, Vicky Ball, Ana 4489 Structural and kinetic analysis of protein-aggregate Santos, Rebeca Diaz, Daniel Biggs, Richard Stillion, strains in vivo using binary epitope mapping Philip Holdship, Fiona Larner, Damian J. Tyler, Kieran Johan Bergh, Per Zetterström, Peter M. Andersen, Clarke, Benjamin Davies, and Peter A. Robbins Thomas Brännström, Karin S. Graffmo, P. Andreas Jonsson, Lisa Lang, Jens Danielsson, Mikael Oliveberg, and Stefan L. Marklund RETRACTION (ONLINE ONLY)

PHARMACOLOGY MEDICAL SCIENCES E1800 Cross-talk between PKA-Cβ and p65 mediates E1813 Gastrin-releasing peptide blockade as a broad-spectrum synergistic induction of PDE4B by roflumilast anti-inflammatory therapy for asthma and NTHi Shutang Zhou, Erin N. Potts, Frank Cuttitta, W. Michael Seiko Susuki-Miyata, Masanori Miyata, Byung-Cheol , and Mary E. Sunday Lee, Haidong Xu, Hirofumi Kai, Chen Yan, and Jian-Dong Li ix Subscription Form

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