Defective Processing of Cytoplasmic and Chloroplast Ribosomal RNA in the Absence of Arabidopsis DXO1

Decapping 5′-3′ exoribonucleases from the DXO/Rai1 family are highly conserved among eukaryotes and exhibit diverse enzymatic activities depending on the organism. The biochemical and structural properties of the plant DXO1 differ from the yeast and animal counterparts, which is reflected in the in vivo functions of this enzyme. Here we show that Arabidopsis DXO1 contributes to the efficient processing of rRNA precursors in both nucleolar/cytosolic and chloroplast maturation pathways. However, the processing defects in DXO1-deficient plants do not depend on the catalytic activity of the enzyme but rely on its plant-specific N-terminal extension, which is responsible for the interaction with the mRNA cap methyltransferase RNMT1. Our RNA sequencing analyses show that the dxo1 mutation deregulates the expression of many ribosomal protein genes, most likely leading to inefficient or delayed pre-rRNA maturation. These phenotypes are partially suppressed by RNMT1 overexpression, suggesting that defective cap synthesis may be responsible, at least to some extent, for the observed effects.