An autonomous Cy transposable element of Zea mays inserted at the a1 locus (a1-m5216: MuDR) was isolated genetically and molecularly cloned. Restriction mapping and sequencing results indicate that Cy (designated MuDR:Cy1) is another isolate of the autonomous element of the Mutator family, MuDR. Six defective derivative alleles of a1-m5216:MuDR were isolated genetically and molecularly cloned. Five of these a1-r alleles (a1-r5835, a1-r5431, a1-r182, a1-r5938 and a1-r5306) behave like non-autonomous elements in that their transposition can only be activated by active MuDR elements in trans. Three of these a1-r alleles have deletions that disrupt transcript mudrA. One allele has a deletion that disrupts transcript mudrB. The lesion associated with the remaining a1-r allele could disrupt either mudrA or mudrB, or both. Analysis of the a1-r alleles results suggests that both transcripts encoded by active MuDR elements, mudrA and mudrB, are necessary for autonomous transposition. The sixth allele, a1-nr5940, which does not respond to the activation of active MuDR elements, has a deletion involving transcript mudrA, the 5' terminal inverted repeat of MuDR and a1 coding sequence. The origin of the a1-r and a1-nr alleles can be explained by the gap-repair model. Another MuDR:Cy element (designated MuDR:Cy2 and which maps 10 cM distal of the pr1 locus on chromosome 5) was shown to transpose at a rate of 3.3% of gametes per generation and increase its copy numbers at rates from 0 to 28.6% of MuDR-containing gametes. Genetic and molecular tests in inactive Mutator lines demonstrated that an active MuDR:Cy2 element can restore the Mu1 hypomethylation and reactivate the high forward mutation rate associated with active Mutator lines. The subsequent loss of MuDR:Cy2 via meitotic segregation resulted in increased levels of Mu1 methylation. Analysis of a novel change of state of a Mu element insertion mutation at the bz1 locus (bz1-rcy4333y) revealed that developmental regulation of MuDR activity is not responsible for the unique insertion and excision patterns associated with Mu elements. Instead, a model involving developmentally regulated gap-repair is proposed.