A simple model to explain evolutionary trends of eukaryotic gene architecture and expression

Catania, Francesco; Lynch, Michael

doi:10.1002/bies.201200127

Cited by 13 publications

(13 citation statements)

References 101 publications

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…If so, then weakly counter-selected intronic polyA sites would preferentially occur downstream of strong (rather than weak) donor splice sites, which facilitate the recruitment of U1. This scenario is consistent with previously proposed models that invoke competing splice and cleavage and polyadenylation reactions ( Catania and Lynch 2008 , 2013 ; Martinson 2011 ).…”

Section: Discussionsupporting

confidence: 92%

“…The reasons why (silenced) cryptic PAS should be favored at the gene 5′ end are still unclear. Drawing from our previous theoretical work ( Catania and Lynch 2013 ), we speculate that exonic AATAAAs may act as splicing enhancer. In particular, exonic AATAAAs might serve to reroute and advantageously sequester cleavage/polyadenylation factors that could otherwise access and perturb the splicing of the neighboring intron.…”

Section: Discussionmentioning

confidence: 75%

“…It is well established that these molecular interactions are instrumental for the accurate processing of nascent transcripts ( Maniatis and Reed 2002 ; Bentley 2014 ). What is less clear is whether these interactions affect the structure of eukaryotic genes, as has been previously proposed ( Catania and Lynch 2008 ; Catania and Lynch 2013 ). A number of experimental studies provide clues as to how mRNA-associated processes might influence gene architecture.…”

mentioning

confidence: 87%

See 2 more Smart Citations

mRNA-Associated Processes and Their Influence on Exon-Intron Structure in Drosophila melanogaster

Lepennetier

Catania

2016

G3 Genes|Genomes|Genetics

Self Cite

View full text Add to dashboard Cite

mRNA-associated processes and gene structure in eukaryotes are typically treated as separate research subjects. Here, we bridge this separation and leverage the extensive multidisciplinary work on Drosophila melanogaster to examine the roles that capping, splicing, cleavage/polyadenylation, and telescripting (i.e., the protection of nascent transcripts from premature cleavage/polyadenylation by the splicing factor U1) might play in shaping exon-intron architecture in protein-coding genes. Our findings suggest that the distance between subsequent internal 5′ splice sites (5′ss) in Drosophila genes is constrained such that telescripting effects are maximized, in theory, and thus nascent transcripts are less vulnerable to premature termination. Exceptionally weak 5′ss and constraints on intron-exon size at the gene 5′ end also indicate that capping might enhance the recruitment of U1 and, in turn, promote telescripting at this location. Finally, a positive correlation between last exon length and last 5′ss strength suggests that optimal donor splice sites in the proximity of the pre-mRNA tail may inhibit the processing of downstream polyadenylation signals more than weak donor splice sites do. These findings corroborate and build upon previous experimental and computational studies on Drosophila genes. They support the possibility, hitherto scantly explored, that mRNA-associated processes impose significant constraints on the evolution of eukaryotic gene structure.

show abstract

Section: Discussionsupporting

confidence: 92%

Section: Discussionmentioning

confidence: 75%

mentioning

confidence: 87%

See 1 more Smart Citation

mRNA-Associated Processes and Their Influence on Exon-Intron Structure in Drosophila melanogaster

Lepennetier

Catania

2016

G3 Genes|Genomes|Genetics

Self Cite

View full text Add to dashboard Cite

show abstract

“…It is becoming increasingly clear that there can be important connections between splicing and polyadenylation during processing of pre-mRNAs (21)(22)(23). In addition to read-through of (pA)p, access to the VP1 AUG and hence the capsid gene open reading frame requires splicing of the proximal 3D⁄3A intron (Fig.…”

Section: Resultsmentioning

confidence: 99%

NP1 Protein of the Bocaparvovirus Minute Virus of Canines Controls Access to the Viral Capsid Genes via Its Role in RNA Processing

Fasina

Dong

Pintel

2016

J Virol

View full text Add to dashboard Cite

Minute virus of canines (MVC) is an autonomous parvovirus in the genusBocaparvovirus. It has a single promoter that generates a single pre-mRNA processed via alternative splicing and alternative polyadenylation to produce at least 8 mRNA transcripts. MVC contains two polyadenylation sites, one at the right-hand end of the genome, (pA)d, and another complex site, (pA)p, within the capsid-coding region. During viral infection, the mRNAs must extend through (pA)p and undergo additional splicing of the immediately upstream 3D⁄3A intron to access the capsid gene. MVC NP1 is a 22-kDa nuclear phosphoprotein unique to the genus Bocaparvovirus of the Parvovirinae which we have shown governs suppression of (pA)p independently of viral genome replication. We show here that in addition to suppression of (pA)p, NP1 is also required for the excision of the MVC 3D⁄3A intron, independently of its effect on alternative polyadenylation. Mutations of the arginine⁄serine (SR) di-repeats within the intrinsically disordered amino terminus of NP1 are required for splicing of the capsid transcript but not suppression of polyadenylation at (pA)p. 3=-end processing of MVC mRNAs at (pA)p is critical for viral genome replication and the optimal expression of NP1 and NS1. Thus, a finely tuned balance between (pA)p suppression and usage is necessary for efficient virus replication. NP1 is the first parvovirus protein implicated in RNA processing. Its characterization reveals another way that parvoviruses govern access to their capsid protein genes, namely, at the RNA level, by regulating the essential splicing of an intron and the suppression of an internal polyadenylation site. IMPORTANCEThe Parvovirinae are small nonenveloped icosahedral viruses that are important pathogens in many animal species, including humans. Although parvoviruses have only subtle early-to-late expression shifts, they all regulate access to their capsid genes. Minute virus of canines (MVC) is an autonomous parvovirus in the genusBocaparvovirus. It has a single promoter generating a single pre-mRNA which is processed via alternative splicing and alternative polyadenylation to generate at least 8 mRNA transcripts. MVC contains two polyadenylation sites, one at the right-hand end of the genome, (pA)d, and another, (pA)p, within the capsid-coding region. It had not been clear how the potent internal polyadenylation motif is suppressed to allow processing, export, and accumulation of the spliced capsid protein-encoding mRNAs. We show here that MVC NP1, the first parvovirus protein to be implicated in RNA processing, governs access to the MVC capsid gene by facilitating splicing and suppressing internal polyadenylation of MVC pre-mRNAs. M inute virus of canines (MVC) is an autonomous parvovirus in the genusBocaparvovirus. Infection in young dogs can result in neonatal mortality (1) and respiratory and gastrointestinal distress (2) and can cause infertility and stillbirths in adult pregnant female dogs (3). The parvovirus genus Bocaparvovirus has 12 currently known...

show abstract

“…А. Виноградов [12] показал, что интроны короче в конститутивных генах, чем в тканеспецифичных, или генах, отвечающих за развитие организма. Исследована зависимость между длиной интрона и уровнем экспрессии генов [13]. Показано, что соотношение между длиной интронов и GC-содержанием у различных видов может быть связано с изохорной структурой геномов [14].…”

Section: закономерности связанные с распределением длин интроновunclassified

Regularities Related to Introns Lengths Distribution

Astakhova¹,

Ройтберг²,

Цитович³

et al. 2014

Math.Biol.Bioinf.

View full text Add to dashboard Cite

Аннотация. Изучены закономерности распределения длин интронов в геномах 17 организмов, принадлежащих к различным таксонам (насекомые, рыбы, земноводные, пресмыкающиеся, птицы, млекопитающие). Показано, что доля интронов, имеющих фазу 1, растет с ростом длины интрона. Кроме того, показано, что короткие и длинные интроны имеют тенденцию образовывать серии, например, доля коротких (длинных) интронов среди тех интронов, которые следуют за коротким (длинным) интроном, существенно выше, чем доля коротких (длинных) интронов в геноме. Эти закономерности показаны для всех рассмотренных геномов. Ключевые слова: интрон, экзон, фаза интрона, длина интрона. ВВЕДЕНИЕПроблема функционирования и эволюции генов эукариот, включая экзон-интронную структуру генов -одна из важнейших задач современной молекулярной биологии. С ростом объемов доступных данных возрастает роль биоинформатических подходов при изучении этой проблемы.Изучение генов эукариот ведется, начиная с 80-х годов XX века. В это время большинство исследований были связаны с распознаванием белок-кодирующих участков ДНК. Обзор результатов первого периода исследований содержится в работах [1,2]. К основным результатам этого периода можно отнести построение моделей сайтов сплайсинга в виде позиционных весовых матриц (ПВМ, англ. термин -PWSM), введение понятия кодирующего потенциала участка и постановку задачи распознавания белок-кодирующих участков как задачи выделения «оптимальных» путей в графах. В это же время был разработан ряд программных систем (GRAIL, GeneMark др.), которые обеспечивали точность распознавания на уровне около 70%. В последующие годы (конец девяностых -начало двухтысячных) в распознавании генов был достигнут существенный прогресс, и с практической точки зрения задачу распознавания белок-кодирующих областей можно считать решенной. Основными причинами такого прогресса являются использование сведений об экзон-интронной структуре уже известных генов, использование методов машинного обучения и построение скрытых марковских моделей для различных участков генов.Изучение экзон-интронной структуры генов в качестве самостоятельного направления исследований, не связанного непосредственно с распознаванием генов,

show abstract

A simple model to explain evolutionary trends of eukaryotic gene architecture and expression

Cited by 13 publications

References 101 publications

mRNA-Associated Processes and Their Influence on Exon-Intron Structure in Drosophila melanogaster

mRNA-Associated Processes and Their Influence on Exon-Intron Structure in Drosophila melanogaster

NP1 Protein of the Bocaparvovirus Minute Virus of Canines Controls Access to the Viral Capsid Genes via Its Role in RNA Processing

Regularities Related to Introns Lengths Distribution

Contact Info

Product

Resources

About