Recurrent rewiring and emergence of RNA regulatory networks.
Alterations in regulatory networks contribute to evolutionary change. Transcriptional networks are reconfigured by changes in the binding specificity of transcription factors and their cognate sites. The evolution of RNA-protein regulatory networks is far less understood. The PUF (Pumilio and FBF) family of RNA regulatory proteins controls the translation, stability, and movements of hundreds of mRNAs in a single species. We probe the evolution of PUF-RNA networks by direct identification of the mRNAs bound to PUF proteins in budding and filamentous fungi and by computational analyses of orthologous RNAs from 62 fungal species. Our findings reveal that PUF proteins gain and lose mRNAs with related and emergent biological functions during evolution. We demonstrate at least two independent rewiring events for PUF3 orthologs, independent but convergent evolution of PUF4/5 binding specificity and the rewiring of the PUF4/5 regulons in different fungal lineages. These findings demonstrate plasticity in RNA regulatory networks and suggest ways in which their rewiring occurs.
Department of Biochemistry, University of Wisconsin-Madison, Madison, WI 53706.
Daniel
D
Wilinski
Department of Biochemistry, University of Wisconsin-Madison, Madison, WI 53706.
Natascha
N
Buter
Institute of Molecular Biology, University of Oregon, Eugene, OR 97403.
Andrew D
AD
Klocko
Department of Biochemistry, University of Wisconsin-Madison, Madison, WI 53706.
Christopher P
CP
Lapointe
Institute of Molecular Biology, University of Oregon, Eugene, OR 97403.
Eric U
EU
Selker
Laboratory of Genetics, University of Wisconsin-Madison, Madison, WI 53706.
Audrey P
AP
Gasch
Department of Biochemistry, University of Wisconsin-Madison, Madison, WI 53706; wickens@biochem.wisc.edu.
Marvin
M
Wickens
D020413:3' Untranslated Regions; D001233:Aspergillus nidulans / Q000235:genetics; D001665:Binding Sites; D019143:Evolution, Molecular; D005656:Fungal Proteins / Q000235:genetics* / Q000378:metabolism; D015966:Gene Expression Regulation, Fungal; D053263:Gene Regulatory Networks; D009492:Neurospora crassa / Q000235:genetics; D010802:Phylogeny; D012333:RNA, Messenger / Q000235:genetics*; D016601:RNA-Binding Proteins / Q000235:genetics* / Q000378:metabolism; D029701:Saccharomyces cerevisiae Proteins / Q000235:genetics / Q000378:metabolism
D020413:3' Untranslated Regions; D005656:Fungal Proteins; C510155:PUF3 protein, S cerevisiae; D012333:RNA, Messenger; D016601:RNA-Binding Proteins; D029701:Saccharomyces cerevisiae Proteins
3′UTR elements; PUF proteins; RNA regulation; evolution