Remarkable Interkingdom Conservation of Intron Positions and Massive, Lineage-Specific Intron Loss and Gain in Eukaryotic Evolution
Open accessAbstract
Sequencing of eukaryotic genomes allows one to address major evolutionary problems, such as the evolution of gene structure. We compared the intron positions in 684 orthologous gene sets from 8 complete genomes of animals, plants, fungi, and protists and constructed parsimonious scenarios of evolution of the exon-intron structure for the respective genes. Approximately one-third of the introns in the malaria parasite Plasmodium falciparum are shared with at least one crown group eukaryote; this number indicates that these introns have been conserved through >1.5 billion years of evolution that separate Plasmodium from the crown group. Paradoxically, humans share many more introns with the plant Arabidopsis thaliana than with the fly or nematode. The inferred evolutionary scenario holds that the common ancestor of Plasmodium and the crown group and, especially, the common ancestor of animals, plants, and fungi had numerous introns. Most of these ancestral introns, which are retained in the genomes of vertebrates and plants, have been lost in fungi, nematodes, arthropods, and probably Plasmodium. In addition, numerous introns have been inserted into vertebrate and plant genes, whereas, in other lineages, intron gain was much less prominent.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The clustering of scaffolds and chromosome segments defines 15 large PALs, each with descendants of more than one hundred ancestral eumetazoan genes.
“This clustering of scaffolds and chromosome segments defines 15 large PALs, each with descendants of more than one hundred ancestral eumetazoan genes.”
From Sea Anemone Genome Reveals Ancestral Eumetazoan Gene Repertoire and Genomic Organization (2007) · cites this paper as [41]
Cites
The COG database: an updated version includes eukaryotes
Tatusov, R. L., Fedorova, N. D., Jackson, J. D., Jacobs, A. R., Kiryutin, B., Koonin, E. V., Krylov, D. M., Mazumder, R., Mekhedov, S., Nikolskaya, A. N., et al. (2003) · BMC Bioinformatics · doi:10.1186/1471-2105-4-41 · Cited by 4,410 · see citing works
Self-citationGenome sequence of the human malaria parasite Plasmodium falciparum
Gardner, M. J., Hall, N., Fung, E., White, O., Berriman, M., Hyman, R. W., Carlton, J. M., Pain, A., Nelson, K. E., Bowman, S., et al. (2002) · Nature · doi:10.1038/nature01097 · Cited by 4,407 · see citing works
A genomic perspective on protein families.
Tatusov, R., Koonin, E., & Lipman, D. (1997) · Science · doi:10.1126/science.278.5338.631 · Cited by 3,777 · see citing works
Self-citationEvidence for a clade of nematodes, arthropods and other moulting animals
Aguinaldo, A. M. A., Turbeville, J. M., Linford, L. S., Rivera, M. C., Garey, J. R., Raff, R. A., & Lake, J. A. (1997) · Nature · doi:10.1038/387489a0 · Cited by 1,609 · see citing works
A kingdom-level phylogeny of eukaryotes based on combined protein data.
Baldauf, S., Roger, A., Wenk-Siefert, I., & Doolittle, W. (2000) · Science · doi:10.1126/science.290.5493.972 · Cited by 1,243 · see citing works
The origin and evolution of model organisms
Hedges, S. B. (2002) · Nature Reviews Genetics · doi:10.1038/nrg929 · Cited by 806 · see citing works
The Exon Theory of GenesPreprint
Gilbert, W. (1987) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.1987.052.01.098 · Cited by 393 · see citing works
The recent origins of spliceosomal introns revisited
Logsdon, J. M., Jr. (1998) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(98)80031-2 · Cited by 205 · see citing works
Selfish DNA and the origin of introns
Cavalier‐Smith, T. (1985) · Nature · doi:10.1038/315283b0 · Cited by 203 · see citing works
The triosephosphate isomerase gene from maize introns antedate the plant-animal divergence
Marchionni, M. A., & Gilbert, W. (1986) · Cell · doi:10.1016/0092-8674(86)90867-6 · Cited by 189 · see citing works
Large-scale comparison of intron positions among animal, plant, and fungal genes
Fedorov, A. N., Merican, A. F., & Gilbert, W. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.242624899 · Cited by 189 · see citing works
SOUZA, S. J. D., Long, M., Klein, R. J., Roy, S. W., Lin, S., & Gilbert, W. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.9.5094 · Cited by 183 · see citing works
The evolution of spliceosomal introns
Lynch, M. (2002) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(02)00360-x · Cited by 157 · see citing works
Intron “sliding” and the diversity of intron positions
Stoltzfus, A., Logsdon, J. M., Jr., Palmer, J. D., & Doolittle, W. F. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.20.10739 · Cited by 156 · see citing works
A spliceosomal intron in Giardia lamblia
Nixon, J. E. J., Wang, A., Morrison, H. G., McArthur, A. G., Sogin, M. L., Loftus, B., & Samuelson, J. C. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.042700299 · Cited by 151 · see citing works
On the ancient nature of introns
Gilbert, W., & Glynias, M. J. (1993) · Gene · doi:10.1016/0378-1119(93)90058-b · Cited by 143 · see citing works
Evolutionary relationships of eukaryotic kingdoms
Kumar, S., & Rzhetsky, A. (1996) · Journal of Molecular Evolution · doi:10.1007/bf02198844 · Cited by 142 · see citing works
Boudet, N., Aubourg, S., Toffano‐Nioche, C., Kreis, M. E., & Lecharny, A. (2001) · Genome Research · doi:10.1101/gr.200801 · Cited by 142 · see citing works
Logsdon, J. M., Jr., Tyshenko, M. G., Dixon, C. K., D-Jafari, J., Walker, V. K., & Palmer, J. D. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.18.8507 · Cited by 132 · see citing works
Intron sliding in conserved gene families
Rogozin, I. B., Lyons‐Weiler, J., & Koonin, E. V. (2000) · Trends in Genetics · doi:10.1016/s0168-9525(00)02096-5 · Cited by 118 · see citing works
Self-citationMolecular evolution: Recent cases of spliceosomal intron gain?
Logsdon, J. M., Stoltzfus, A., & Doolittle, W. F. (1998) · Current Biology · doi:10.1016/s0960-9822(07)00361-2 · Cited by 112 · see citing works
Exon/intron structure of aldehyde dehydrogenase genes supports the “ introns-late ” theory
Rzhetsky, A., Ayala, F. J., Hsu, L. C., Chang, C., & Yoshida, A. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.13.6820 · Cited by 72 · see citing works
Early origin of canonical introns
Simpson, A. G. B., MacQuarrie, E. K., & Roger, A. J. (2002) · Nature · doi:10.1038/419270a · Cited by 60 · see citing works
The Chaperonin Genes of Jakobid and Jakobid-Like Flagellates: Implications for Eukaryotic Evolution
Archibald, J. M., O’Kelly, C. J., & Doolittle, W. F. (2002) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a004097 · Cited by 59 · see citing works
Long, M., & Rosenberg, C. (2000) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a026279 · Cited by 49 · see citing works
Proto-splice site model of intron origin
Dibb, N. J. (1991) · Journal of Theoretical Biology · doi:10.1016/s0022-5193(05)80388-1 · Cited by 42 · see citing works
Feiber, A. L., Rangarajan, J. R., & Vaughn, J. C. (2002) · Journal of Molecular Evolution · doi:10.1007/s00239-002-2336-y · Cited by 31 · see citing works
Lamond, A. I. (1999) · Nature · doi:10.1038/17697 · Cited by 21 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Sea Anemone Genome Reveals Ancestral Eumetazoan Gene Repertoire and Genomic Organization
Putnam, N. H., Srivastava, M., Hellsten, U., Dirks, B., Chapman, J., Salamov, A., Terry, A., Shapiro, H., Lindquist, E., Kapitonov, V. V., et al. (2007) · Science · doi:10.1126/science.1139158 · Cited by 1,555 · see citing works
The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans
King, N., Westbrook, M. J., Young, S. L., Kuo, A., Abedin, M., Chapman, J., Fairclough, S., Hellsten, U., Isogai, Y., Letunic, I., et al. (2008) · Nature · doi:10.1038/nature06617 · Cited by 1,139 · see citing works
Alternative splicing and evolution: diversification, exon definition and function
Keren, H., Lev-Maor, G., & Ast, G. (2010) · Nature Reviews Genetics · doi:10.1038/nrg2776 · Cited by 1,082 · see citing works
Carretero‐Paulet, L., Galstyan, A., Roig‐Villanova, I., Martínez‐García, J. F., Bilbao-Castro, J. R., & Robertson, D. L. (2010) · PLANT PHYSIOLOGY · doi:10.1104/pp.110.153593 · Cited by 681 · see citing works
The evolution of spliceosomal introns: patterns, puzzles and progress
Roy, S. W., & Gilbert, W. (2006) · Nature Reviews Genetics · doi:10.1038/nrg1807 · Cited by 642 · see citing works
Endosymbiotic theories for eukaryote origin
Martin, W. F., Garg, S., & Zimorski, V. (2015) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2014.0330 · Cited by 583 · see citing works
Introns and the origin of nucleus–cytosol compartmentalization
Martin, W. F., & Koonin, E. V. (2006) · Nature · doi:10.1038/nature04531 · Cited by 497 · see citing works
Self-citationDeep intronic mutations and human disease
Vaz‐Drago, R., Custódio, N., & Carmo‐Fonseca, M. (2017) · Human Genetics · doi:10.1007/s00439-017-1809-4 · Cited by 448 · see citing works
Origin and evolution of spliceosomal introns
Rogozin, I. B., Carmel, L., Csürös, M., & Koonin, E. V. (2012) · Biology Direct · doi:10.1186/1745-6150-7-11 · Cited by 419 · see citing works
Self-citationThe Origins of Eukaryotic Gene Structure
Lynch, M. (2005) · Molecular Biology and Evolution · doi:10.1093/molbev/msj050 · Cited by 391 · see citing works
Caenorhabditis phylogeny predicts convergence of hermaphroditism and extensive intron loss
Kiontke, K. C., Gavin, N. P., Raynes, Y., Roehrig, C., Piano, F., & Fitch, D. H. A. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0403094101 · Cited by 367 · see citing works
Chorev, M., & Carmel, L. (2012) · Frontiers in Genetics · doi:10.3389/fgene.2012.00055 · Cited by 367 · see citing works
Introns: The Functional Benefits of Introns in Genomes
Jo, B.-S., & Choi, S. S. (2015) · Genomics & Informatics · doi:10.5808/gi.2015.13.4.112 · Cited by 357 · see citing works
Intron retention is a major phenomenon in alternative splicing in Arabidopsis
Ner‐Gaon, H., Halachmi, R., Savaldi‐Goldstein, S., Rubin, E., Ophir, R., & Fluhr, R. (2004) · The Plant Journal · doi:10.1111/j.1365-313x.2004.02172.x · Cited by 356 · see citing works
Koonin, E. V. (2006) · Biology Direct · doi:10.1186/1745-6150-1-22 · Cited by 281 · see citing works
Self-citationAnalysis of evolution of exon-intron structure of eukaryotic genes
Rogozin, I. B. (2005) · Briefings in Bioinformatics · doi:10.1093/bib/6.2.118 · Cited by 268 · see citing works
Self-citationVertebrate-Type Intron-Rich Genes in the Marine Annelid <i>Platynereis dumerilii</i>
Raible, F., Tessmar-Raible, K., Osoegawa, K., Wincker, P., Jubin, C., Balavoine, G., Ferrier, D., Benes, V., de Jong, P., Weissenbach, J., et al. (2005) · Science · doi:10.1126/science.1119089 · Cited by 257 · see citing works
Darwinian evolution in the light of genomics
Koonin, E. V. (2008) · Nucleic Acids Research · doi:10.1093/nar/gkp089 · Cited by 254 · see citing works
Self-citationThe biology of intron gain and loss
Jeffares, D. C., Mourier, T., & Penny, D. (2006) · Trends in Genetics · doi:10.1016/j.tig.2005.10.006 · Cited by 296 · see citing works
Rewitz, K., O’Connor, M. B., & Gilbert, L. I. (2007) · Insect Biochemistry and Molecular Biology · doi:10.1016/j.ibmb.2007.02.012 · Cited by 234 · see citing works
Kertész, S., Kerényi, Z., Mérai, Z., Bartos, I., Pálfy, T. B., Barta, E., & Silhavy, D. (2006) · Nucleic Acids Research · doi:10.1093/nar/gkl737 · Cited by 231 · see citing works
Roy, S. W., & Penny, D. (2006) · Molecular Biology and Evolution · doi:10.1093/molbev/msl159 · Cited by 225 · see citing works
The Cancer Spliceome: Reprograming of Alternative Splicing in Cancer
Marabti, E. E., & Younis, I. (2018) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2018.00080 · Cited by 217 · see citing works
Evolution of genome architecture
Koonin, E. V. (2008) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2008.09.015 · Cited by 215 · see citing works
Self-citationRates of intron loss and gain: Implications for early eukaryotic evolution
Roy, S. W., & Gilbert, W. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0500383102 · Cited by 214 · see citing works
Evolutionary History of Chemosensory-Related Gene Families across the Arthropoda
Eyun, S., Soh, H. Y., Posavi, M., Munro, J. B., Hughes, D., Murali, S. C., Qu, J., Dugan, S., Lee, S. L., Chao, H., et al. (2017) · Molecular Biology and Evolution · doi:10.1093/molbev/msx147 · Cited by 205 · see citing works
Origins and Evolution of Spliceosomal Introns
Rodrı́guez-Trelles, F., Tarrı́o, R., & Ayala, F. J. (2006) · Annual Review of Genetics · doi:10.1146/annurev.genet.40.110405.090625 · Cited by 198 · see citing works
Intron gain and loss in segmentally duplicated genes in rice
Lin, H., Zhu, W., da Silva, J. C. F., Gu, X., & Buell, C. R. (2006) · Genome biology · doi:10.1186/gb-2006-7-5-r41 · Cited by 191 · see citing works
Evolutionary Diversity of Vertebrate Small Heat Shock Proteins
Franck, E., Madsen, O., van Rheede, T., Ricard, G., Huynen, M. A., & JONG, W. W. D. (2004) · Journal of Molecular Evolution · doi:10.1007/s00239-004-0013-z · Cited by 189 · see citing works
YANG, C., Zhang, J., Li, F., Ma, H., ZHANG, Q., Priya, T. A. J., ZHANG, X., & Xiang, J. (2008) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2007.12.012 · Cited by 188 · see citing works
Jiang, C., Gu, X., & Peterson, T. (2004) · Genome biology · doi:10.1186/gb-2004-5-7-r46 · Cited by 188 · see citing works
Schwartz, S., Silva, J., Burstein, D., Pupko, T., Eyras, E., & Ast, G. (2007) · Genome Research · doi:10.1101/gr.6818908 · Cited by 186 · see citing works
Intron Size, Abundance, and Distribution within Untranslated Regions of Genes
Hong, X., Scofield, D. G., & Lynch, M. (2006) · Molecular Biology and Evolution · doi:10.1093/molbev/msl111 · Cited by 184 · see citing works
Wang, Y., Wang, Q., Zhao, Y., Han, G., & Zhu, S. (2015) · Gene · doi:10.1016/j.gene.2015.04.041 · Cited by 182 · see citing works
Three distinct modes of intron dynamics in the evolution of eukaryotesPreprint
Carmel, L., Wolf, Y. I., Rogozin, I. B., & Koonin, E. V. (2007) · Genome Research · doi:10.1101/gr.6438607 · Cited by 178 · see citing works
Self-citationThe phylogenetic relationships of Caenorhabditis and other rhabditids
Kiontke, K. C. (2005) · WormBook · doi:10.1895/wormbook.1.11.1 · Cited by 170 · see citing works
Kondrashov, F. A., Koonin, E. V., Morgunov, I. G., Finogenova, T. V., & Kondrashova, M. N. (2006) · Biology Direct · doi:10.1186/1745-6150-1-31 · Cited by 165 · see citing works
Self-citationConstraints and plasticity in genome and molecular-phenome evolution
Koonin, E. V., & Wolf, Y. I. (2010) · Nature Reviews Genetics · doi:10.1038/nrg2810 · Cited by 163 · see citing works
Self-citationCsürös, M., Rogozin, I. B., & Koonin, E. V. (2011) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1002150 · Cited by 163 · see citing works
Self-citationPrevalence of intron gain over intron loss in the evolution of paralogous gene families
Babenko, V. N. (2004) · Nucleic Acids Research · doi:10.1093/nar/gkh686 · Cited by 156 · see citing works
Genome-enabled development of DNA markers for ecology, evolution and conservation
Thomson, R. C., Wang, I., & Johnson, J. R. (2010) · Molecular Ecology · doi:10.1111/j.1365-294x.2010.04650.x · Cited by 148 · see citing works
Origin of Spliceosomal Introns and Alternative SplicingPreprint
Irimia, M., & Roy, S. W. (2014) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a016071 · Cited by 148 · see citing works
Characterization of intron loss events in mammalsPreprint
Coulombe-Huntington, J., & Majewski, J. (2006) · Genome Research · doi:10.1101/gr.5703406 · Cited by 148 · see citing works
Roy, S. W., & Gilbert, W. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0408355101 · Cited by 144 · see citing works
Energetics and genetics across the prokaryote-eukaryote divide
Lane, N. J. (2011) · Biology Direct · doi:10.1186/1745-6150-6-35 · Cited by 142 · see citing works
Integrated analysis of cytochrome P450 gene superfamily in the red flour beetle, Tribolium castaneum
Zhu, F., Moural, T. W., Shah, K., & Palli, S. R. (2013) · BMC Genomics · doi:10.1186/1471-2164-14-174 · Cited by 137 · see citing works
Comparative genomic analysis of fungal genomes reveals intron-rich ancestors
Stajich, J., Dietrich, F. S., & Roy, S. W. (2007) · Genome biology · doi:10.1186/gb-2007-8-10-r223 · Cited by 133 · see citing works
Patterns of Intron Gain and Loss in Fungi
Nielsen, C. B., Friedman, B. A., Birren, B. W., Burge, C. B., & Galagan, J. E. (2004) · PLoS Biology · doi:10.1371/journal.pbio.0020422 · Cited by 128 · see citing works
Origins of recently gained introns in Caenorhabditis
Coghlan, A., & Wolfe, K. H. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0308192101 · Cited by 128 · see citing works
Evolution of secretin family GPCR members in the metazoa
Cardoso, J. C. R., Pinto, V., Vieira, F. A., Clark, M. S., & Power, D. M. (2006) · BMC Evolutionary Biology · doi:10.1186/1471-2148-6-108 · Cited by 123 · see citing works
Extensive, Recent Intron Gains in Daphnia Populations
Li, W., Tucker, A. E., Sung, W., Thomas, W. K., & Lynch, M. (2009) · Science · doi:10.1126/science.1179302 · Cited by 122 · see citing works
Roy, S. W., & Gilbert, W. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0408274102 · Cited by 121 · see citing works
Cao, Y., Han, Y., Meng, D., Li, D., Jin, Q., Lin, Y., & Cai, Y. (2016) · Frontiers in Plant Science · doi:10.3389/fpls.2016.01874 · Cited by 120 · see citing works
Li, W., Liu, B., Yu, L., Feng, D., Wang, H., & Wang, J. (2009) · BMC Evolutionary Biology · doi:10.1186/1471-2148-9-90 · Cited by 120 · see citing works
Evolution of the Caenorhabditis elegans Genome
Cutter, A. D., Dey, A., & Murray, R. L. (2009) · Molecular Biology and Evolution · doi:10.1093/molbev/msp048 · Cited by 120 · see citing works
Leterrier, M., Holappa, L. D., Broglie, K. E., & Beckles, D. M. (2008) · BMC Plant Biology · doi:10.1186/1471-2229-8-98 · Cited by 118 · see citing works
Coevolution of genomic intron number and splice sites
Irimia, M., Penny, D., & Roy, S. W. (2007) · Trends in Genetics · doi:10.1016/j.tig.2007.04.001 · Cited by 108 · see citing works
Genome-wide analysis of cytochrome P450 monooxygenase genes in the silkworm, Bombyx mori
Ai, J., Zhu, Y., Duan, J., Yu, Q., Zhang, G., Fei, W., & Xiang, Z. (2011) · Gene · doi:10.1016/j.gene.2011.03.002 · Cited by 107 · see citing works
Evolutionary convergence of alternative splicing in ion channels
Copley, R. R. (2004) · Trends in Genetics · doi:10.1016/j.tig.2004.02.001 · Cited by 106 · see citing works
Spliceosomal introns as tools for genomic and evolutionary analysis
Irimia, M., & Roy, S. W. (2008) · Nucleic Acids Research · doi:10.1093/nar/gkn012 · Cited by 102 · see citing works
Conservation versus parallel gains in intron evolution
Sverdlov, A. V. (2005) · Nucleic Acids Research · doi:10.1093/nar/gki316 · Cited by 101 · see citing works
Roy, S. W., & Penny, D. (2007) · Molecular Biology and Evolution · doi:10.1093/molbev/msm048 · Cited by 101 · see citing works
Do transposable elements really contribute to proteomes?
Gotea, V., & Makałowski, W. (2006) · Trends in Genetics · doi:10.1016/j.tig.2006.03.006 · Cited by 97 · see citing works
The C. elegans Rab Family: Identification, Classification and Toolkit Construction
Gallegos, M. E., Balakrishnan, S., Chandramouli, P., Arora, S., Azameera, A., Babushekar, A., Bargoma, E., Bokhari, A. A., Chava, S. K., Das, P., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0049387 · Cited by 90 · see citing works
Spliceosomal introns in the deep-branching eukaryote Trichomonas vaginalis
Vaňáčová, Š., Yan, W., Carlton, J. M., & Johnson, P. J. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0407500102 · Cited by 90 · see citing works
Wagner and Dollo: A Stochastic Duet by Composing Two Parsimonious Solos
Alekseyenko, A. V., Lee, C. J., & Suchard, M. A. (2008) · Systematic Biology · doi:10.1080/10635150802434394 · Cited by 89 · see citing works
Rogozin, I. B., Basu, M. K., Csürös, M., & Koonin, E. V. (2009) · Genome Biology and Evolution · doi:10.1093/gbe/evp011 · Cited by 88 · see citing works
Self-citationEvolutionarily conserved genes preferentially accumulate intronsPreprint
Carmel, L., Rogozin, I. B., Wolf, Y. I., & Koonin, E. V. (2007) · Genome Research · doi:10.1101/gr.5978207 · Cited by 87 · see citing works
Self-citationIdentifying the mechanisms of intron gain: progress and trends
Yenerall, P. M., & Zhou, L. (2012) · Biology Direct · doi:10.1186/1745-6150-7-29 · Cited by 86 · see citing works
Genome-wide functional analysis of human 5' untranslated region introns
Cenik, C., Derti, A., Mellor, J. C., Berriz, G. F., & Roth, F. P. (2010) · Genome biology · doi:10.1186/gb-2010-11-3-r29 · Cited by 84 · see citing works
New Maximum Likelihood Estimators for Eukaryotic Intron Evolution
Nguyen, H. D., Yoshihama, M., & Kenmochi, N. (2005) · PLoS Computational Biology · doi:10.1371/journal.pcbi.0010079 · Cited by 82 · see citing works
Plant Spliceosomal Introns: Not Only Cut and Paste
Morello, L., & Breviario, D. (2008) · Current Genomics · doi:10.2174/138920208784533629 · Cited by 81 · see citing works
Intron Loss and Gain in Drosophila
Coulombe‐Huntington, J., & Majewski, J. (2007) · Molecular Biology and Evolution · doi:10.1093/molbev/msm235 · Cited by 81 · see citing works
Hultquist, J. F., & Dorweiler, J. E. (2008) · Planta · doi:10.1007/s00425-008-0813-2 · Cited by 80 · see citing works
Intron-Dominated Genomes of Early Ancestors of Eukaryotes
Koonin, E. V. (2009) · Journal of Heredity · doi:10.1093/jhered/esp056 · Cited by 80 · see citing works
Self-citationPatterns of intron gain and conservation in eukaryotic genes
Carmel, L., Rogozin, I. B., Wolf, Y. I., & Koonin, E. V. (2007) · BMC Evolutionary Biology · doi:10.1186/1471-2148-7-192 · Cited by 80 · see citing works
Self-citationRel homology domain-containing transcription factors in the cnidarian Nematostella vectensis
Sullivan, J. C., Kalaitzidis, D., Gilmore, T. D., & Finnerty, J. R. (2006) · Development Genes and Evolution · doi:10.1007/s00427-006-0111-6 · Cited by 79 · see citing works
Identification of mammalian orthologs using local synteny
Jun, J., Mandoiu, I. I., & Nelson, C. E. (2009) · BMC Genomics · doi:10.1186/1471-2164-10-630 · Cited by 78 · see citing works
Evolution of the Metazoan-Specific Importin α Gene Family
Mason, D. A., Stage, D. E., & Goldfarb, D. S. (2009) · Journal of Molecular Evolution · doi:10.1007/s00239-009-9215-8 · Cited by 77 · see citing works
Mitochondria, the Cell Cycle, and the Origin of Sex via a Syncytial Eukaryote Common Ancestor
Garg, S. G., & Martin, W. F. (2016) · Genome Biology and Evolution · doi:10.1093/gbe/evw136 · Cited by 76 · see citing works
Sverdlov, A. V., Babenko, V. N., Rogozin, I. B., & Koonin, E. V. (2004) · Gene · doi:10.1016/j.gene.2004.05.027 · Cited by 76 · see citing works
Self-citationGenomewide identification, classification and analysis of NAC type gene family in maize
Peng, X., Zhao, Y., Li, X., WU, M., CHAI, W., SHENG, L., Wang, Y., Dong, Q., Jiang, H., & Cheng, B. (2015) · Journal of Genetics · doi:10.1007/s12041-015-0526-9 · Cited by 76 · see citing works
Square, T. A., Romášek, M., Jandzík, D., Cattell, M. V., Klymkowsky, M. W., & Medeiros, D. M. (2015) · Development · doi:10.1242/dev.125609 · Cited by 74 · see citing works
Nan, Q., Qian, D., Niu, Y., He, Y., Tong, S., Niu, Z., Ma, J., Yang, Y., An, L., Wan, D., et al. (2017) · The Plant Cell · doi:10.1105/tpc.16.00690 · Cited by 74 · see citing works
The Peculiarities of Large Intron Splicing in Animals
Shepard, S. S., McCreary, M., & Fedorov, A. N. (2009) · PLoS ONE · doi:10.1371/journal.pone.0007853 · Cited by 73 · see citing works
Chernikova, D., Motamedi, S., Csürös, M., Koonin, E. V., & Rogozin, I. B. (2011) · Biology Direct · doi:10.1186/1745-6150-6-26 · Cited by 72 · see citing works
Self-citationAwan, A. R., Manfredo, A., & Pleiss, J. A. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1218353110 · Cited by 72 · see citing works
Zheng, J., Rogozin, I. B., Koonin, E. V., & Przytycka, T. M. (2007) · Molecular Biology and Evolution · doi:10.1093/molbev/msm207 · Cited by 70 · see citing works
Self-citationThe landscape of human mutually exclusive splicing
Hatje, K., Rahman, R., Vidal, R. O., Simm, D., Hammesfahr, B., Bansal, V., Rajput, A., Mickael, M., Sun, T., Bonn, S., et al. (2017) · Molecular Systems Biology · doi:10.15252/msb.20177728 · Cited by 70 · see citing works
Mystery of intron gain: new data and new models
Roy, S. W., & Irimia, M. (2008) · Trends in Genetics · doi:10.1016/j.tig.2008.11.004 · Cited by 69 · see citing works
High Rate of Recent Intron Gain and Loss in Simultaneously Duplicated Arabidopsis Genes
Knowles, D. G., & McLysaght, A. (2006) · Molecular Biology and Evolution · doi:10.1093/molbev/msl017 · Cited by 68 · see citing works
Ecdysozoan Clade Rejected by Genome-Wide Analysis of Rare Amino Acid Replacements
Rogozin, I. B., Wolf, Y. I., Carmel, L., & Koonin, E. V. (2007) · Molecular Biology and Evolution · doi:10.1093/molbev/msm029 · Cited by 68 · see citing works
Self-citationPIECE: a database for plant gene structure comparison and evolution
Wang, Y., You, F. M., Lazo, G. R., Luo, M., Thilmony, R. L., Gordon, S., Kianian, S. F., & Gu, Y. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks1109 · Cited by 67 · see citing works
Very little intron loss/gain in Plasmodium: Intron loss/gain mutation rates and intron numberPreprint
Roy, S. W., & Hartl, D. L. (2006) · Genome Research · doi:10.1101/gr.4845406 · Cited by 67 · see citing works
Lin, X., Zhang, Y., Kuang, H., & Chen, J. (2013) · BMC Genomics · doi:10.1186/1471-2164-14-335 · Cited by 66 · see citing works
Xie, Z., Li, X., Glover, B. J., Bai, S., Rao, G., Luo, J., & Yang, J. (2008) · Molecular Biology and Evolution · doi:10.1093/molbev/msn105 · Cited by 66 · see citing works
Genome-wide analyses supported by RNA-Seq reveal non-canonical splice sites in plant genomes
Pucker, B., & Brockington, S. F. (2018) · BMC Genomics · doi:10.1186/s12864-018-5360-z · Cited by 65 · see citing works
Aleem, M., Riaz, A., Raza, Q. S., Aleem, M., Aslam, M., Kong, K., Atif, R. M., Kashif, M., Bhat, J. A., & Zhao, T. (2021) · Genomics · doi:10.1016/j.ygeno.2021.11.016 · Cited by 65 · see citing works
Widespread Evolutionary Conservation of Alternatively Spliced Exons in Caenorhabditis
Irimia, M., Rukov, J. L., Penny, D., García‐Fernàndez, J., Vinther, J., & Roy, S. W. (2007) · Molecular Biology and Evolution · doi:10.1093/molbev/msm262 · Cited by 65 · see citing works
Comparative Analysis of Bacterial-Origin Genes for Plant Mitochondrial Ribosomal Proteins
Bonen, L., & Calixte, S. (2005) · Molecular Biology and Evolution · doi:10.1093/molbev/msj080 · Cited by 65 · see citing works
- Authors
- Rogozin, I. B., Wolf, Y. I., Sorokin, A. V., Mirkin, B. G., & Koonin, E. V.
- Affiliations
- National Institutes of Health (US)
- Birkbeck, University of London (GB)
- Corresponding author
- Koonin, Eugene V.
- Venue
- Current Biology
- Publisher
- Elsevier BV
- Published
- 2003-09
- Volume
- 13
- Issue
- 17
- Pages
- 1512-1517
- ISSN
- 0960-9822 (ISSN-L)
- OpenAlex
- W1968733465
- Cited by
- 445
- References
- 28
- Citations by year
- 2026: 7 · 2025: 19 · 2024: 11 · 2023: 15 · 2022: 25 · 2021: 22 · 2020: 10 · 2019: 13 · 2018: 9 · 2017: 16 · 2016: 14 · 2015: 18 · 2014: 15 · 2013: 17 · 2012: 14
- FWCI
- 33.53
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Current Biology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Chromosomal and Genetic Variations
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
- Keywords
- intron positions, intron loss, intron gain, orthologs, Plasmodium falciparum, Arabidopsis thaliana, eukaryotic evolution
- MeSH terms
- Amino Acid Sequence, Animals, Fungi, Humans, Introns, Invertebrates, Molecular Sequence Data, Phylogeny, Plants, Conserved Sequence, Evolution, Molecular
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review