Alternative splicing of anciently exonized 5S rRNA regulates plant transcription factor TFIIIA

Yan Fu; Oliver Bannach; Hao Chen; Jan-Hendrik Teune; Axel Schmitz; Gerhard Steger; Liming Xiong; W. Brad Barbazuk

doi:10.1101/gr.086876.108

Alternative splicing of anciently exonized 5S rRNA regulates plant transcription factor TFIIIA

¹ Donald Danforth Plant Science Center, Saint Louis, Missouri 63132, USA;
² Institut für Physikalische Biologie, Heinrich-Heine-Universität Düsseldorf, 40225 Düsseldorf, Germany

↵3 These authors contributed equally to this work.

Abstract

Identifying conserved alternative splicing (AS) events among evolutionarily distant species can prioritize AS events for functional characterization and help uncover relevant cis- and trans-regulatory factors. A genome-wide search for conserved cassette exon AS events in higher plants revealed the exonization of 5S ribosomal RNA (5S rRNA) within the gene of its own transcription regulator, TFIIIA (transcription factor for polymerase III A). The 5S rRNA-derived exon in TFIIIA gene exists in all representative land plant species but not in green algae and nonplant species, suggesting it is specific to land plants. TFIIIA is essential for RNA polymerase III-based transcription of 5S rRNA in eukaryotes. Integrating comparative genomics and molecular biology revealed that the conserved cassette exon derived from 5S rRNA is coupled with nonsense-mediated mRNA decay. Utilizing multiple independent Arabidopsis overexpressing TFIIIA transgenic lines under osmotic and salt stress, strong accordance between phenotypic and molecular evidence reveals the biological relevance of AS of the exonized 5S rRNA in quantitative autoregulation of TFIIIA homeostasis. Most significantly, this study provides the first evidence of ancient exaptation of 5S rRNA in plants, suggesting a novel gene regulation model mediated by the AS of an anciently exonized noncoding element.

Footnotes

↵4 Present addresses: Department of Agronomy, Iowa State University, Ames, Iowa 50010, USA;
↵5 Department of Biology and Zoology and the Genetics Institute, University of Florida, Gainesville, Florida 32611, USA.
↵6 Corresponding author.

E-mail bbarbazuk{at}ufl.edu; fax (352) 273-8624.
[Supplemental material is available online at www.genome.org. The sequence data from this study have been submitted to GenBank (http://www.ncbi.nlm.nih.gov/Genbank/) under accession nos. DQ882178–DQ882180, EU574733–EU574735, EU924184, EU918200, EU919737.]
Article published online before print. Article and publication date are at http://www.genome.org/cgi/doi/10.1101/gr.086876.108.
- Received September 20, 2008.
- Accepted January 6, 2009.