Specialized proteins that bind to Holliday junctions can catalyze a reaction known as branch migration (Figure 5–56), whereby DNA is spooled through the Holliday junction by continually breaking and re-forming base pairs (Figure 5–57). In this way, the Holliday junction proteins use ATP hydrolysis to expand the region of heteroduplex DNA initially created by the strand-exchange reaction. In meiosis, heteroduplex regions often “migrate” thousands of nucleotides from the original site of the double-strand break. As shown in Figure 5–54, Holliday junctions usually occur in pairs, known as double Holliday junctions.
As shown in Figure 5–54, there are two basic outcomes of homologous recombination during meiosis. In humans, approximately 90% of the double-strand breaks produced during meiosis are resolved as non-crossovers (see right side of Figure 5–54). Here, the two original DNA duplexes separate from each other in a form unaltered except for a region of heteroduplex that formed near the site of the original double-strand break. This set of reactions resembles that described above for the repair of double-strand breaks (see Figure 5–48).
The other outcome is more profound: a double Holliday junction is formed and is cleaved by specialized enzymes to create a crossover (see left side of Figure 5–54). The two original portions of each chromosome upstream and downstream
Figure 5–55 A Holliday junction. The initially formed structure (A) is usually drawn with two strands crossing, as in Figure 5–54.  An isomerization of the Holliday junction produces an open, symmetrical structure that is bound by specialized proteins.
These proteins “move” the Holliday junctions by a coordinated set of branch-migration reactions (see Figure 5–57 and Movie 5.8). (D) Structure of the Holliday junction in the open form depicted in (B). The Holliday junction is named for the scientist who first proposed its formation. (PDB code: 1DCW.) direction of branch migration
Figure 5–56 Simplified view of branch migration. In branch migration, base pairs are continually broken and formed as the branch point moves. Although branch migration can happen spontaneously on naked DNA molecules, the process is inefficient and the branch moves back and forth at random. In the cell, branch migration is carried out using specialized proteins and ATP hydrolysis to ensure that, as shown, the branch moves rapidly and in one direction. As shown in Figure 5–57, branch migrations often occur at Holliday junctions, where two branch-migration reactions are coupled.
Figure 5–57 Enzyme-catalyzed branch movement at a Holliday junction by branch migration. In E. coli, a tetramer of the RuvA protein (green) and two hexamers of the RuvB protein (yellow) bind to the open form of the junction. The RuvB protein, which resembles the hexameric helicases used in DNA replication (Figure 5–14), uses the energy of ATP hydrolysis to spool DNA rapidly through the Holliday junction, extending the heteroduplex region as shown. The RuvA protein coordinates this movement, threading the DNA strands to avoid tangling. (PDB codes: 1IXR, 1C7Y.) from the two Holliday junctions are thereby swapped, creating two chromosomes that have crossed over.