Tryptophan synthase (TRPS) is a complex enzyme responsible for tryptophan biosynthesis. It occurs in bacteria, plants, and fungi as an αββα heterotetramer. Although encoded by independent genes in bacteria and plants, in fungi, TRPS is generated by a single gene that concurrently expresses the α and β entities, which are linked by an elongated peculiar segment. We conducted 1 µs all-atom molecular dynamics simulations on Hemileia vastatrix TRPS to address two questions: (i) the role of the linker segment and (ii) the comparative mode of action. Since there is not an experimental structure, we started our simulations with homology modeling. Based on the results, it seems that TRPS makes use of an already-existing tunnel that can spontaneously move the indole moiety from the α catalytic pocket to the β one. Such behavior was completely disrupted in the simulation without the linker. In light of these results and the αβ dimer's low stability, the full-working TRPS single genes might be the result of a particular evolution. Considering the significant losses that Hemileia vastatrix causes to coffee plantations, our next course of action will be to use the TRPS to look for substances that can block tryptophan production and therefore control the disease.