Epigenetic : related to modification of the chromatin or the DNA that affects the biology of the organism and is stable over rounds of cell division but does not involve changes in the underlying DNA sequence of the organism INTRODUCTION

Transposable elements are mobile genetic units that exhibit broad diversity in their structure and transposition mechanisms. Transposable elements occupy a large fraction of many eukaryotic genomes and their movement and accumulation represent a major force shaping the genes and genomes of almost all organisms. This review focuses on DNA-mediated or class 2 transposons and emphasizes how this class of elements is distinguished from other types of mobile elements in terms of their structure, amplification dynamics, and genomic effect. We provide an up-to-date outlook on the diversity and taxonomic distribution of all major types of DNA transposons in eukaryotes, including Helitrons and Mavericks. We discuss some of the evolutionary forces that influence their maintenance and diversification in various genomic environments. Finally, we highlight how the distinctive biological features of DNA transposons have contributed to shape genome architecture and led to the emergence of genetic innovations in different eukaryotic lineages. 331 A nn u. R ev . G en et . 2 00 7. 41 :3 31 -6 8. D ow nl oa de d fr om a rj ou rn al s. an nu al re vi ew s. or g by U ni ve rs ity o f T ex as A rl in gt on o n 05 /0 9/ 08 . F or p er so na l u se o nl y. ANRV329-GE41-15 ARI 12 October 2007 11:1 Epigenetic: related to modification of the chromatin or the DNA that affects the biology of the organism and is stable over rounds of cell division but does not involve changes in the underlying DNA sequence of the organism INTRODUCTION Dazzling advances in molecular biology, genetics, and genomics have allowed scientists to understand in great detail many aspects of transposable element (TE) biology. Significant discoveries at the interface of these fields have provided new insight into transposition mechanisms, allowed the identification of new TEs and the broadening of their taxonomic distribution, revealed relationships between TEs and viruses, and uncovered the means by which TE movement can be controlled epigenetically by their host. Coupled to these new discoveries is a greater understanding of the extent to which TEs influence the structure and dynamics of the genomes they inhabit. The focus of this review is on one specific class of TEs, the class 2 or DNA transposons. We begin by presenting key features of the structure and life cycle of these elements, with an emphasis on the factors that govern their maintenance and propagation within the genome and throughout the eukaryotic tree of life. We then shift our focus to the repercussions of DNA transposon movement and amplification on the genome, including large-scale structural changes and epigenetic modifications, and the contribution of elements of this type to the generation of allelic diversity, new genes, and biological innovations. EVOLUTIONARY DYNAMICS OF DNA TRANSPOSONS Classification and Distribution of DNA Transposons Class 2 transposable elements (TEs) or DNA transposons are mobile DNA that move utilizing a singleor double-stranded DNA intermediate (35). Eukaryotic DNA transposons can be divided into three major subclasses: (i ) those that excise as double-stranded DNA and reinsert elsewhere in the genome, i.e., the classic “cut-and-paste” transposons (35); (ii ) those that utilize a mechanism probably related to rolling-circle replication, Helitrons (91); and (iii ) Mavericks, whose mechanism of transposition is not yet well understood, but that likely replicate using a self-encoded DNA polymerase (94, 160). Both Helitrons and Mavericks most likely rely on distinct transposition mechanisms involving the displacement and replication of a single-stranded DNA intermediate, respectively. Thus these elements probably transpose through a replicative, copy-and-paste process. All cut-and-paste transposons are characterized by a transposase encoded by autonomous copies and, with few exceptions, by the presence of terminal inverted repeats (TIRs). Helitrons have no TIRs, but rather short conserved terminal motifs and autonomous copies encode a Rep/Helicase (91, 158). Mavericks, also known as Polintons, are very large transposons with long TIRs and coding capacity for multiple proteins, most of which are related to double-stranded DNA viruses, including a B-type DNA polymerase (52, 94, 160). To date, ten superfamilies of cut-and-paste DNA transposons are recognized (Table 1). Elements belong to the same superfamily when they can be linked to transposases that are significantly related in sequence. Typically, transposases from the same superfamily can be confidently aligned in their core catalytic region and a monophyletic ancestry can be inferred from phylogenetic analysis (22, 164). In some cases, such as Tc1/mariner, the superfamily can be further divided into monophyletic groups that deeply diverged in eukaryotic evolution (155, 164). Two superfamilies (CACTA and PIF/Harbinger) are characterized by the presence of a second transposon-encoded protein required for transposition (Table 1). The explosion of sequence data in the databases over the past decade has fueled the discovery of large numbers of elements in a wide range of organisms. These discoveries have yielded several new insights into the distribution and broad evolutionary history of eukaryotic DNA transposons. First, the taxonomic distribution of superfamilies initially 332 Feschotte · Pritham A nn u. R ev . G en et . 2 00 7. 41 :3 31 -6 8. D ow nl oa de d fr om a rj ou rn al s. an nu al re vi ew s. or g by U ni ve rs ity o f T ex as A rl in gt on o n 05 /0 9/ 08 . F or p er so na l u se o nl y. ANRV329-GE41-15 ARI 12 October 2007 11:1 T ab le 1 C la ss ifi ca ti on an d ch ar ac te ri st ic s of eu ka ry ot ic D N A tr an sp os on s Su pe rf am ily R el at ed IS T SD L en gt h 1 (k b) T IR s 1 (b p) T er m in al m ot if (5 ′ 3 ′ ) T P as e 1 (a a) C at al yt ic m ot if D N A -b in di ng m ot if A dd it io na l