Mitochondria and plastids in plant cells maintain their own genomes, which are remnants of their ancestral bacteria-endosymbiont genomes. Due to the multi-copy nature, organelle DNA can make up a substantial part of total cellular DNA. Our discovery of the Mg2+-dependent organelle exonuclease DEFECTIVE IN POLLEN ORGANELLE DNA DEGRADATION1 (DPD1) proves that organelle DNA degradation (ODD) proceeds during pollen maturation. To further our understanding of the molecular mechanism of ODD, we characterized a novel mutant (dpd2). Unlike dpd1, which retains both plastid and mitochondrial DNAs, dpd2 showed a specific retention of only plastid DNAs. In addition to pollen defect, various abnormalities were also detected in vegetative and reproductive tissues of dpd2. We found that DPD2 encodes the large subunit of ribonucleotide reductase (RNR), which is an enzyme responsible for the rate-limiting step of de novo nucleotide biosynthesis. The study of dpd2 demonstrated that defective RNR indirectly perturbs the activity of DPD1 nuclease in plastids. The relationship between DPD1 and DPD2 indicates a novel regulation of ODD in pollen. Our data indicates that DPD1 activity in plastids is associated with nucleotide levels. Using this study, the results reinforced our earlier conclusion that the DPD1 exonuclease plays a central role in ODD during pollen development. The ODD process mediated by DPD1 appears to function for nutrient salvage from DNA rather than maternal inheritance.