XMAP215, CLASP, and Crescerin use arrayed tubulin-binding tumor overexpressed 
gene (TOG) domains to modulate microtubule dynamics. We hypothesized that TOGs 
have distinct architectures and tubulin-binding properties that underlie each 
family's ability to promote microtubule polymerization or pause. As a model, we 
investigated the pentameric TOG array of a Drosophila melanogaster XMAP215 
member, Msps. We found that Msps TOGs have distinct architectures that bind 
either free or polymerized tubulin, and that a polarized array drives 
microtubule polymerization. An engineered TOG1-2-5 array fully supported 
Msps-dependent microtubule polymerase activity. Requisite for this activity was 
a TOG5-specific N-terminal HEAT repeat that engaged microtubule 
lattice-incorporated tubulin. TOG5-microtubule binding maintained mitotic 
spindle formation as deleting or mutating TOG5 compromised spindle architecture 
and increased the mitotic index. Mad2 knockdown released the spindle assembly 
checkpoint triggered when TOG5-microtubule binding was compromised, indicating 
that TOG5 is essential for spindle function. Our results reveal a TOG5-specific 
role in mitotic fidelity and support our hypothesis that architecturally 
distinct TOGs arranged in a sequence-specific order underlie TOG array 
microtubule regulator activity.