Intron Evolution in Saccharomycetaceae

被引:31
作者
Hooks, Katarzyna B. [1 ,2 ]
Delneri, Daniela [1 ]
Griffiths-Jones, Sam [1 ]
机构
[1] Univ Manchester, Fac Life Sci, Manchester M13 9PL, Lancs, England
[2] Univ Bordeaux, INSERM U1053, Bordeaux, France
基金
英国惠康基金;
关键词
intron loss; yeast; fungi; SPLICEOSOMAL INTRONS; COMPARATIVE GENOMICS; PROTEIN GENES; YEAST; DUPLICATION; POSITIONS; REVEALS; ORIGIN; GAIN; DNA;
D O I
10.1093/gbe/evu196
中图分类号
Q [生物科学];
学科分类号
07 ; 0710 ; 09 ;
摘要
Introns in protein-coding genes are very rare in hemiascomycetous yeast genomes. It has been suggested that these species have experienced extensive intron loss during their evolution from the postulated intron-rich fungal ancestor. However, no intron-devoid yeast species have been identified and some of the introns remaining within the genomes of intron-poor species, such as Saccharomyces cerevisiae, appear to be beneficial during growth under stress conditions. In order to reveal the pattern of intron retention within intron-poor yeast species and better understand the mechanisms of intron evolution, we generated a comprehensive set of 250 orthologous introns in the 20 species that comprise the Saccharomycetaceae, by analyzing RNA deep-sequencing data and alignments of intron-containing genes. Analysis of these intron sets shows that intron loss is at least two orders of magnitude more frequent than intron gain. Fine mapping of intron positions shows that intron sliding is rare, and that introns are almost always removed without changing the primary sequence of the encoded protein. The latter finding is consistent with the prevailing view that homologous recombination between reverse-transcribed mature mRNAs and the corresponding genomic locus is the primary mechanism of intron loss. However, we also find evidence that loss of a small number of introns is mediated by micro-homology, and that the number of intron losses is diminished in yeast species that have lost the microhomology end joining and nonhomologous end joining machinery.
引用
收藏
页码:2543 / 2556
页数:14
相关论文
共 49 条
[1]   U12 type introns were lost at multiple occasions during evolution [J].
Bartschat, Sebastian ;
Samuelsson, Tore .
BMC GENOMICS, 2010, 11
[2]  
Bolotin-Fukuhara M, 2006, TOP CURR GENET, V15, P165, DOI 10.1007/b136677
[3]   Molecular evolution of eukaryotic genomes:: hemiascomycetous yeast spliceosomal introns [J].
Bon, E ;
Casaregola, S ;
Blandin, G ;
Llorente, B ;
Neuvéglise, C ;
Munsterkotter, M ;
Guldener, U ;
Mewes, HW ;
Van Helden, J ;
Dujon, B ;
Gaillardin, C .
NUCLEIC ACIDS RESEARCH, 2003, 31 (04) :1121-1135
[4]   LAGAN and Multi-LAGAN: Efficient tools for large-scale multiple alignment of genomic DNA [J].
Brudno, M ;
Do, CB ;
Cooper, GM ;
Kim, MF ;
Davydov, E ;
Green, ED ;
Sidow, A ;
Batzoglou, S .
GENOME RESEARCH, 2003, 13 (04) :721-731
[5]   The Yeast Gene Order Browser: Combining curated homology and syntenic context reveals gene fate in polyploid species [J].
Byrne, KP ;
Wolfe, KH .
GENOME RESEARCH, 2005, 15 (10) :1456-1461
[6]   The Third Exon of the Budding Yeast Meiotic Recombination Gene HOP2 Is Required for Calcium-dependent and Recombinase Dmc1-specific Stimulation of Homologous Strand Assimilation [J].
Chan, Yuen-Ling ;
Brown, M. Scott ;
Qin, Daoming ;
Handa, Naofumi ;
Bishop, Douglas K. .
JOURNAL OF BIOLOGICAL CHEMISTRY, 2014, 289 (26) :18076-18086
[7]   Computational identification of functional introns: high positional conservation of introns that harbor RNA genes [J].
Chorev, Michal ;
Carmel, Liran .
NUCLEIC ACIDS RESEARCH, 2013, 41 (11) :5604-5613
[8]   Surveying Saccharomyces genomes to identify functional elements by comparative DNA sequence analysis [J].
Cliften, PF ;
Hillier, LW ;
Fulton, L ;
Graves, T ;
Miner, T ;
Gish, WR ;
Waterston, RH ;
Johnston, M .
GENOME RESEARCH, 2001, 11 (07) :1175-1186
[9]   Origins of recently gained introns in Caenorhabditis [J].
Coghlan, A ;
Wolfe, KH .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2004, 101 (31) :11362-11367
[10]   GENES IN PIECES - WERE THEY EVER TOGETHER [J].
DOOLITTLE, WF .
NATURE, 1978, 272 (5654) :581-582