Identification and characterization of a class of MALAT1 -like genomic loci

Zhang, Bin; Mao, Yuntao S.; Diermeier, Sarah D.; Novikova, Irina V.; Nawrocki, Eric P.; Jones, Tom A.; Lazar, Zsolt; Tung, Chang -Shung; Luo, Weijun; Eddy, Sean R.; Sanbonmatsu, Karissa Y.; Spector, David L.

doi:10.1016/J.CELREP.2017.05.006

Identification and characterization of a class of MALAT1 -like genomic loci

Journal Article · Tue May 23 00:00:00 EDT 2017 · Cell Reports

DOI:https://doi.org/10.1016/J.CELREP.2017.05.006· OSTI ID:1364397

Zhang, Bin ^[1]; Mao, Yuntao S. ^[2]; Diermeier, Sarah D. ^[2]; Novikova, Irina V. ^[3]; Nawrocki, Eric P. ^[4]; Jones, Tom A. ^[5]; Lazar, Zsolt ^[2]; Tung, Chang -Shung ^[6]; Luo, Weijun ^[7]; Eddy, Sean R. ^[5]; Sanbonmatsu, Karissa Y. ^[6]; Spector, David L. ^[2]

Cold Spring Harbor Lab., Cold Spring Harbor, NY (United States); Univ. of Rochester, Rochester, NY (United States)
Cold Spring Harbor Lab., Cold Spring Harbor, NY (United States)
Pacific Northwest National Lab. (PNNL), Richland, WA (United States); Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
Howard Hughes Medical Institute, Ashburn, VA (United States); U.S. National Library of Medicine, Bethesda, MD (United States)
Harvard Univ., Cambridge, MA (United States)
Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
Univ. of North Carolina, Charlotte, NC (United States)

The MALAT1 (Metastasis-Associated Lung Adenocarcinoma Transcript 1) gene encodes a noncoding RNA that is processed into a long nuclear retained transcript (MALAT1) and a small cytoplasmic tRNA-like transcript (mascRNA). Using an RNA sequence- and structure-based covariance model, we identified more than 130 genomic loci in vertebrate genomes containing the MALAT1 3' end triple-helix structure and its immediate downstream tRNA-like structure, including 44 in the green lizard Anolis carolinensis. Structural and computational analyses revealed a co-occurrence of components of the 3' end module. MALAT1-like genes in Anolis carolinensis are highly expressed in adult testis, thus we named them testis-abundant long noncoding RNAs (tancRNAs). MALAT1-like loci also produce multiple small RNA species, including PIWI-interacting RNAs (piRNAs), from the antisense strand. The 3' ends of tancRNAs serve as potential targets for the PIWI-piRNA complex. Furthermore, we have identified an evolutionarily conserved class of long noncoding RNAs (lncRNAs) with similar structural constraints, post-transcriptional processing, and subcellular localization and a distinct function in spermatocytes.

View Accepted Manuscript (DOE)

Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC05-76RL01830

OSTI ID:: 1364397

Journal Information:: Cell Reports, Journal Name: Cell Reports Journal Issue: 8 Vol. 19; ISSN 2211-1247

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

References (63)

Evolution of the Long Non-coding RNAs MALAT1 and MENβ/ε Stadler, Peter F. Advances in Bioinformatics and Computational Biology https://doi.org/10.1007/978-3-642-15060-9_1	book	January 2010
MALAT1 — a paradigm for long noncoding RNA function in cancer Gutschner, Tony; Hämmerle, Monika; Diederichs, Sven Journal of Molecular Medicine, Vol. 91, Issue 7 https://doi.org/10.1007/s00109-013-1028-y	journal	March 2013
Functional Demarcation of Active and Silent Chromatin Domains in Human HOX Loci by Noncoding RNAs Rinn, John L.; Kertesz, Michael; Wang, Jordon K. Cell, Vol. 129, Issue 7 https://doi.org/10.1016/j.cell.2007.05.022	journal	June 2007
3′ End Processing of a Long Nuclear-Retained Noncoding RNA Yields a tRNA-like Cytoplasmic RNA Wilusz, Jeremy E.; Freier, Susan M.; Spector, David L. Cell, Vol. 135, Issue 5 https://doi.org/10.1016/j.cell.2008.10.012	journal	November 2008
Long Noncoding RNAs with Enhancer-like Function in Human Cells Ørom, Ulf Andersson; Derrien, Thomas; Beringer, Malte Cell, Vol. 143, Issue 1 https://doi.org/10.1016/j.cell.2010.09.001	journal	October 2010
ncRNA- and Pc2 Methylation-Dependent Gene Relocation between Nuclear Structures Mediates Gene Activation Programs Yang, Liuqing; Lin, Chunru; Liu, Wen Cell, Vol. 147, Issue 4 https://doi.org/10.1016/j.cell.2011.08.054	journal	November 2011
Conserved Function of lincRNAs in Vertebrate Embryonic Development despite Rapid Sequence Evolution Ulitsky, Igor; Shkumatava, Alena; Jan, Calvin H. Cell, Vol. 147, Issue 7 https://doi.org/10.1016/j.cell.2011.11.055	journal	December 2011
Long Noncoding RNAs: Cellular Address Codes in Development and Disease Batista, Pedro J.; Chang, Howard Y. Cell, Vol. 152, Issue 6 https://doi.org/10.1016/j.cell.2013.02.012	journal	March 2013
lincRNAs: Genomics, Evolution, and Mechanisms Ulitsky, Igor; Bartel, David P. Cell, Vol. 154, Issue 1 https://doi.org/10.1016/j.cell.2013.06.020	journal	July 2013
Regulation of the Mammalian Elongation Cycle by Subunit Rolling: A Eukaryotic-Specific Ribosome Rearrangement Budkevich, Tatyana V.; Giesebrecht, Jan; Behrmann, Elmar Cell, Vol. 158, Issue 1 https://doi.org/10.1016/j.cell.2014.04.044	journal	July 2014
RNA-RNA Interactions Enable Specific Targeting of Noncoding RNAs to Nascent Pre-mRNAs and Chromatin Sites Engreitz, Jesse M.; Sirokman, Klara; McDonel, Patrick Cell, Vol. 159, Issue 1 https://doi.org/10.1016/j.cell.2014.08.018	journal	September 2014
On-Enzyme Refolding Permits Small RNA and tRNA Surveillance by the CCA-Adding Enzyme Kuhn, Claus-D.; Wilusz, Jeremy E.; Zheng, Yuxuan Cell, Vol. 160, Issue 4 https://doi.org/10.1016/j.cell.2015.01.005	journal	February 2015
Noncoding RNA NORAD Regulates Genomic Stability by Sequestering PUMILIO Proteins Lee, Sungyul; Kopp, Florian; Chang, Tsung-Cheng Cell, Vol. 164, Issue 1-2 https://doi.org/10.1016/j.cell.2015.12.017	journal	January 2016
The lncRNA Malat1 Is Dispensable for Mouse Development but Its Transcription Plays a cis-Regulatory Role in the Adult Zhang, Bin; Arun, Gayatri; Mao, Yuntao S. Cell Reports, Vol. 2, Issue 1 https://doi.org/10.1016/j.celrep.2012.06.003	journal	July 2012
Myriad Triple-Helix-Forming Structures in the Transposable Element RNAs of Plants and Fungi Tycowski, Kazimierz T.; Shu, Mei-Di; Steitz, Joan A. Cell Reports, Vol. 15, Issue 6 https://doi.org/10.1016/j.celrep.2016.04.010	journal	May 2016
Simple Combinations of Lineage-Determining Transcription Factors Prime cis-Regulatory Elements Required for Macrophage and B Cell Identities Heinz, Sven; Benner, Christopher; Spann, Nathanael Molecular Cell, Vol. 38, Issue 4 https://doi.org/10.1016/j.molcel.2010.05.004	journal	May 2010
The Nuclear-Retained Noncoding RNA MALAT1 Regulates Alternative Splicing by Modulating SR Splicing Factor Phosphorylation Tripathi, Vidisha; Ellis, Jonathan D.; Shen, Zhen Molecular Cell, Vol. 39, Issue 6 https://doi.org/10.1016/j.molcel.2010.08.011	journal	September 2010
The Long Noncoding RNAs NEAT1 and MALAT1 Bind Active Chromatin Sites West, Jason A.; Davis, Christopher P.; Sunwoo, Hongjae Molecular Cell, Vol. 55, Issue 5 https://doi.org/10.1016/j.molcel.2014.07.012	journal	September 2014
Cell-Type-Based Analysis of MicroRNA Profiles in the Mouse Brain He, Miao; Liu, Yu; Wang, Xiaowo Neuron, Vol. 73, Issue 1 https://doi.org/10.1016/j.neuron.2011.11.010	journal	January 2012
Role of tRNA-like structures in controlling plant virus replication Dreher, Theo W. Virus Research, Vol. 139, Issue 2 https://doi.org/10.1016/j.virusres.2008.06.010	journal	February 2009
piRNA biogenesis during adult spermatogenesis in mice is independent of the ping-pong mechanism Beyret, Ergin; Liu, Na; Lin, Haifan Cell Research, Vol. 22, Issue 10 https://doi.org/10.1038/cr.2012.120	journal	August 2012
A long nuclear-retained non-coding RNA regulates synaptogenesis by modulating gene expression Bernard, Delphine; Prasanth, Kannanganattu V.; Tripathi, Vidisha The EMBO Journal, Vol. 29, Issue 18 https://doi.org/10.1038/emboj.2010.199	journal	August 2010
Analysis of the mouse transcriptome based on functional annotation of 60,770 full-length cDNAs No authors listed Nature, Vol. 420, Issue 6915, p. 563-573 https://doi.org/10.1038/nature01266	journal	December 2002
A novel class of small RNAs bind to MILI protein in mouse testes Aravin, Alexei; Gaidatzis, Dimos; Pfeffer, Sébastien Nature, Vol. 442, Issue 7099 https://doi.org/10.1038/nature04916	journal	June 2006
A germline-specific class of small RNAs binds mammalian Piwi proteins Girard, Angélique; Sachidanandam, Ravi; Hannon, Gregory J. Nature, Vol. 442, Issue 7099 https://doi.org/10.1038/nature04917	journal	June 2006
Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals Guttman, Mitchell; Amit, Ido; Garber, Manuel Nature, Vol. 458, Issue 7235 https://doi.org/10.1038/nature07672	journal	February 2009
Landscape of transcription in human cells Djebali, Sarah; Davis, Carrie A.; Merkel, Angelika Nature, Vol. 489, Issue 7414 https://doi.org/10.1038/nature11233	journal	September 2012
Direct visualization of the co-transcriptional assembly of a nuclear body by noncoding RNAs Mao, Yuntao S.; Sunwoo, Hongjae; Zhang, Bin Nature Cell Biology, Vol. 13, Issue 1 https://doi.org/10.1038/ncb2140	journal	December 2010
Nucleation of nuclear bodies by RNA Shevtsov, Sergey P.; Dundr, Miroslav Nature Cell Biology, Vol. 13, Issue 2 https://doi.org/10.1038/ncb2157	journal	January 2011
Digital transcriptome profiling using selective hexamer priming for cDNA synthesis Armour, Christopher D.; Castle, John C.; Chen, Ronghua Nature Methods, Vol. 6, Issue 9 https://doi.org/10.1038/nmeth.1360	journal	August 2009
Genome-wide transcription and the implications for genomic organization Kapranov, Philipp; Willingham, Aarron T.; Gingeras, Thomas R. Nature Reviews Genetics, Vol. 8, Issue 6 https://doi.org/10.1038/nrg2083	journal	May 2007
All-atom homology model of the Escherichia coli 30S ribosomal subunit Tung, Chang-Shung; Joseph, Simpson; Sanbonmatsu, Kevin Y. Nature Structural Biology, Vol. 9, Issue 10 https://doi.org/10.1038/nsb841	journal	September 2002
Structure of the SAM-II riboswitch bound to S-adenosylmethionine Gilbert, Sunny D.; Rambo, Robert P.; Van Tyne, Daria Nature Structural & Molecular Biology, Vol. 15, Issue 2 https://doi.org/10.1038/nsmb.1371	journal	January 2008
Triple-helix structure in telomerase RNA contributes to catalysis Qiao, Feng; Cech, Thomas R. Nature Structural & Molecular Biology, Vol. 15, Issue 6 https://doi.org/10.1038/nsmb.1420	journal	May 2008
Promiscuous RNA binding by Polycomb repressive complex 2 Davidovich, Chen; Zheng, Leon; Goodrich, Karen J. Nature Structural & Molecular Biology, Vol. 20, Issue 11 https://doi.org/10.1038/nsmb.2679	journal	September 2013
Structural insights into the stabilization of MALAT1 noncoding RNA by a bipartite triple helix Brown, Jessica A.; Bulkley, David; Wang, Jimin Nature Structural & Molecular Biology, Vol. 21, Issue 7 https://doi.org/10.1038/nsmb.2844	journal	June 2014
MALAT-1, a novel noncoding RNA, and thymosin β4 predict metastasis and survival in early-stage non-small cell lung cancer Ji, Ping; Diederichs, Sven; Wang, Wenbing Oncogene, Vol. 22, Issue 39 https://doi.org/10.1038/sj.onc.1206928	journal	September 2003
Formation of triple-helical structures by the 3'-end sequences of MALAT1 and MEN noncoding RNAs Brown, J. A.; Valenstein, M. L.; Yario, T. A. Proceedings of the National Academy of Sciences, Vol. 109, Issue 47 https://doi.org/10.1073/pnas.1217338109	journal	November 2012
Structural determinants for ligand capture by a class II preQ ₁ riboswitch Kang, Mijeong; Eichhorn, Catherine D.; Feigon, Juli Proceedings of the National Academy of Sciences, Vol. 111, Issue 6 https://doi.org/10.1073/pnas.1400126111	journal	January 2014
Methyltransferase-like protein 16 binds the 3′-terminal triple helix of MALAT1 long noncoding RNA Brown, Jessica A.; Kinzig, Charles G.; DeGregorio, Suzanne J. Proceedings of the National Academy of Sciences, Vol. 113, Issue 49 https://doi.org/10.1073/pnas.1614759113	journal	November 2016
The 3'-terminal end (NCCA) of tRNA determines the structure and stability of the aminoacyl acceptor stem. Limmer, S.; Hofmann, H. P.; Ott, G. Proceedings of the National Academy of Sciences, Vol. 90, Issue 13 https://doi.org/10.1073/pnas.90.13.6199	journal	July 1993
STAR: ultrafast universal RNA-seq aligner Dobin, Alexander; Davis, Carrie A.; Schlesinger, Felix Bioinformatics, Vol. 29, Issue 1 https://doi.org/10.1093/bioinformatics/bts635	journal	October 2012
Infernal 1.1: 100-fold faster RNA homology searches Nawrocki, E. P.; Eddy, S. R. Bioinformatics, Vol. 29, Issue 22 https://doi.org/10.1093/bioinformatics/btt509	journal	September 2013
A novel class of small RNAs in mouse spermatogenic cells Grivna, Shane T.; Beyret, Ergin; Wang, Zhong Genes & Development, Vol. 20, Issue 13 https://doi.org/10.1101/gad.1434406	journal	June 2006
A triple helix stabilizes the 3' ends of long noncoding RNAs that lack poly(A) tails Wilusz, J. E.; JnBaptiste, C. K.; Lu, L. Y. Genes & Development, Vol. 26, Issue 21 https://doi.org/10.1101/gad.204438.112	journal	October 2012
Differentiation of mammary tumors and reduction in metastasis upon Malat1 lncRNA loss Arun, Gayatri; Diermeier, Sarah; Akerman, Martin Genes & Development, Vol. 30, Issue 1 https://doi.org/10.1101/gad.270959.115	journal	December 2015
The GENCODE v7 catalog of human long noncoding RNAs: Analysis of their gene structure, evolution, and expression Derrien, T.; Johnson, R.; Bussotti, G. Genome Research, Vol. 22, Issue 9 https://doi.org/10.1101/gr.132159.111	journal	September 2012
Systematic identification of long noncoding RNAs expressed during zebrafish embryogenesis Pauli, A.; Valen, E.; Lin, M. F. Genome Research, Vol. 22, Issue 3 https://doi.org/10.1101/gr.133009.111	journal	November 2011
GENCODE: The reference human genome annotation for The ENCODE Project Harrow, J.; Frankish, A.; Gonzalez, J. M. Genome Research, Vol. 22, Issue 9 https://doi.org/10.1101/gr.135350.111	journal	September 2012
Small RNA Silencing Pathways in Germ and Stem Cells Aravin, A. A.; Hannon, G. J. Cold Spring Harbor Symposia on Quantitative Biology, Vol. 73, Issue 0 https://doi.org/10.1101/sqb.2008.73.058	journal	January 2008
Crystal Structure of Argonaute and Its Implications for RISC Slicer Activity Song, J. -J. Science, Vol. 305, Issue 5689 https://doi.org/10.1126/science.1102514	journal	September 2004
Global Identification of Human Transcribed Sequences with Genome Tiling Arrays Bertone, P. Science, Vol. 306, Issue 5705 https://doi.org/10.1126/science.1103388	journal	December 2004
Characterization of the piRNA Complex from Rat Testes Lau, N. C. Science, Vol. 313, Issue 5785 https://doi.org/10.1126/science.1130164	journal	July 2006
Poly(A) Tail Recognition by a Viral RNA Element Through Assembly of a Triple Helix Mitton-Fry, R. M.; DeGregorio, S. J.; Wang, J. Science, Vol. 330, Issue 6008 https://doi.org/10.1126/science.1195858	journal	November 2010
Role for piRNAs and Noncoding RNA in de Novo DNA Methylation of the Imprinted Mouse Rasgrf1 Locus Watanabe, T.; Tomizawa, S. -i.; Mitsuya, K. Science, Vol. 332, Issue 6031 https://doi.org/10.1126/science.1203919	journal	May 2011
tRNAs Marked with CCACCA Are Targeted for Degradation Wilusz, J. E.; Whipple, J. M.; Phizicky, E. M. Science, Vol. 334, Issue 6057 https://doi.org/10.1126/science.1213671	journal	November 2011
Genome Regulation by Long Noncoding RNAs Rinn, John L.; Chang, Howard Y. Annual Review of Biochemistry, Vol. 81, Issue 1 https://doi.org/10.1146/annurev-biochem-051410-092902	journal	July 2012
The Noncoding RNA MALAT1 Is a Critical Regulator of the Metastasis Phenotype of Lung Cancer Cells Gutschner, Tony; Hämmerle, Monika; Eißmann, Moritz Cancer Research, Vol. 73, Issue 3 https://doi.org/10.1158/0008-5472.CAN-12-2850	journal	December 2012
A screen for nuclear transcripts identifies two linked noncoding RNAs associated with SC35 splicing domains Hutchinson, John N.; Ensminger, Alexander W.; Clemson, Christine M. BMC Genomics, Vol. 8, Issue 1 https://doi.org/10.1186/1471-2164-8-39	journal	February 2007
Ultrafast and memory-efficient alignment of short DNA sequences to the human genome Langmead, Ben; Trapnell, Cole; Pop, Mihai Genome Biology, Vol. 10, Issue 3 https://doi.org/10.1186/gb-2009-10-3-r25	journal	January 2009
Long noncoding RNA genes: conservation of sequence and brain expression among diverse amniotes Chodroff, Rebecca A.; Goodstadt, Leo; Sirey, Tamara M. Genome Biology, Vol. 11, Issue 7 https://doi.org/10.1186/gb-2010-11-7-r72	journal	January 2010
Malat1 is not an essential component of nuclear speckles in mice Nakagawa, S.; Ip, J. Y.; Shioi, G. RNA, Vol. 18, Issue 8 https://doi.org/10.1261/rna.033217.112	journal	June 2012
Loss of the abundant nuclear non-coding RNA MALAT1 is compatible with life and development Eißmann, Moritz; Gutschner, Tony; Hämmerle, Monika RNA Biology, Vol. 9, Issue 8 https://doi.org/10.4161/rna.21089	journal	August 2012

Cited By (12)

Molecular anatomy of the architectural NEAT1 noncoding RNA: The domains, interactors, and biogenesis pathway required to build phase‐separated nuclear paraspeckles Hirose, Tetsuro; Yamazaki, Tomohiro; Nakagawa, Shinichi Wiley Interdisciplinary Reviews: RNA, Vol. 10, Issue 6 https://doi.org/10.1002/wrna.1545	journal	May 2019
Zinc-finger protein CNBP alters the 3-D structure of lncRNA Braveheart in solution Kim, Doo Nam; Thiel, Bernhard C.; Mrozowich, Tyler Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-019-13942-4	journal	January 2020
Ribosomes guide pachytene piRNA formation on long intergenic piRNA precursors Sun, Yu H.; Zhu, Jiang; Xie, Li Huitong Nature Cell Biology, Vol. 22, Issue 2 https://doi.org/10.1038/s41556-019-0457-4	journal	February 2020
Shark genomes provide insights into elasmobranch evolution and the origin of vertebrates Hara, Yuichiro; Yamaguchi, Kazuaki; Onimaru, Koh Nature Ecology & Evolution, Vol. 2, Issue 11 https://doi.org/10.1038/s41559-018-0673-5	journal	October 2018
A stable tRNA-like molecule is generated from the long noncoding RNA GUT15 in Arabidopsis Plewka, Patrycja; Thompson, Agnieszka; Szymanski, Maciej RNA Biology https://doi.org/10.1080/15476286.2018.1445404	journal	March 2018
GraphClust2: Annotation and discovery of structured RNAs with scalable and accessible integrative clustering Miladi, Milad; Sokhoyan, Eteri; Houwaart, Torsten GigaScience, Vol. 8, Issue 12 https://doi.org/10.1093/gigascience/giz150	journal	December 2019
Challenges and perspectives for structural biology of lncRNAs—the example of the Xist lncRNA A-repeats Jones, Alisha N.; Sattler, Michael Journal of Molecular Cell Biology, Vol. 11, Issue 10 https://doi.org/10.1093/jmcb/mjz086	journal	July 2019
Empowering the annotation and discovery of structured RNAs with scalable and accessible integrative clustering Miladi, Milad; Sokhoyan, Eteri; Houwaart, Torsten https://doi.org/10.1101/550335	posted_content	October 2019
Conservation of gene architecture and domains amidst sequence divergence in the hsrω lncRNA gene across the Drosophila genus: An in silico analysis Sahu, Ranjan Kumar; Mutt, Eshita; Lakhotia, Subhash Chandra https://doi.org/10.1101/695486	posted_content	April 2019
Long Non-coding RNAs as Communicators and Mediators Between the Tumor Microenvironment and Cancer Cells Chen, Di; Lu, Tong; Tan, Junying Frontiers in Oncology, Vol. 9 https://doi.org/10.3389/fonc.2019.00739	journal	August 2019
Identifying Structural Domains and Conserved Regions in the Long Non-Coding RNA lncTCF7 Owens, Michael C.; Clark, Sean C.; Yankey, Allison International Journal of Molecular Sciences, Vol. 20, Issue 19 https://doi.org/10.3390/ijms20194770	journal	September 2019
Secondary Structural Model of Human MALAT1 Reveals Multiple Structure–Function Relationships McCown, Phillip J.; Wang, Matthew C.; Jaeger, Luc International Journal of Molecular Sciences, Vol. 20, Issue 22 https://doi.org/10.3390/ijms20225610	journal	November 2019

Similar Records

Detection of PIWI and piRNAs in the mitochondria of mammalian cancer cells

Journal Article · Fri Mar 28 00:00:00 EDT 2014 · Biochemical and Biophysical Research Communications · OSTI ID:22416339

Functional importance of cardiac enhancer-associated noncoding RNAs in heart development and disease

Journal Article · Mon Aug 18 20:00:00 EDT 2014 · Journal of Molecular and Cellular Cardiology · OSTI ID:1257346

The nascent RNA binding complex SFiNX licenses piRNA-guided heterochromatin formation

Journal Article · Sun Aug 04 20:00:00 EDT 2019 · Nature Structural & Molecular Biology · OSTI ID:1561310

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
60 APPLIED LIFE SCIENCES
Anolis carolinesis
MALAT1
PIWI
evolution
lizard
long noncoding RNA
piRNA
tRNA-like
testis
triple helix

Identification and characterization of a class of MALAT1 -like genomic loci

Citation Formats

References (63)

Cited By (12)

Similar Records

Related Subjects