Relaxed Transcription in Arabidopsis Mitochondria Is Counterbalanced by RNA Stability Control Mediated by Polyadenylation and Polynucleotide Phosphorylase

Abstract

Plant mitochondrial genomes are extraordinarily large and complex compared to their animal counterparts, due to the presence of large noncoding regions. Multiple promoters are common for plant mitochondrial genes, and transcription exhibits little or no modulation. Mature functional RNAs are produced through various posttranscriptional processes, and control of RNA stability has a major impact on RNA abundance. This control involves polyadenylation which targets RNA for degradation by polynucleotide phosphorylase (PNPase). Here, we have analyzed polyadenylated RNA fragments from Arabidopsis plants down-regulated for PNPase (PNP⁻ plants). Because of their polyadenylated status and the accumulation of the corresponding RNA in PNP⁻ versus wild-type plants, these sequences represent mitochondrial RNA degradation tags. Analysis of these tags revealed that PNPase is involved in degrading rRNA and tRNA maturation by-products but also RNA transcribed from regions that are in some cases highly expressed although lacking known functional genes. Some of these transcripts, such as RNA containing chimeric open reading frames created by recombination or antisense RNA transcribed on the opposite strand of a known gene, may present potential detrimental effects to mitochondrial function. Taken together, our data show that the relaxed transcription in Arabidopsis mitochondria is counterbalanced by RNA stability control mediated by polyadenylation and PNPase.

Supplemental material for this article may be found at http://mcb.asm.org/.

This work was supported by the Centre National de la Recherche Scientifique (France), an EMBO long-term fellowship to H.L., an ACI JC grant from the French Ministry of Research to D.G., Deutsche Forschungsgemeinschaft grant SFB 429 to T.B., and the Berliner Programm zur Förderung der Chancengleichheit für Frauen in Forschung und Lehre (K.K.).

We thank Philippe Giegé for critical reading of the manuscript and Théophile Ofodo for technical assistance.