Cooperativity between the β‐tubulin carboxy tail and the body of the molecule is required for microtubule function

Using Drosophila spermatogenesis as a model, we show that function of the β‐tubulin C‐terminal tail (CTT) is not independent of the body of the molecule. For optimal microtubule function, the β‐tubulin CTT and body must match. β2 is the only β‐tubulin used in meiosis and spermatid differentiation. β1‐tubulin is used in basal bodies, but β1 cannot replace β2. However, when β1 is co‐expressed with β2, both β‐tubulins are equally incorporated into all microtubules, and males exhibit near wild type fertility. In contrast, co‐expression of β2β1C and β1β2C, two reciprocal chimeric molecules with bodies and tails swapped, results in defects in meiosis, cytoskeletal microtubules, and axonemes; males produce few functional sperm and few or no progeny. In these experiments, all the same β‐tubulin parts are present, but unlike the co‐assembled native β‐tubulins, the “trans” configuration of the co‐assembled chimeras is poorly functional. Our data thus reveal essential intra‐molecular interactions between the CTT and other parts of the β‐tubulin molecule, even though the CTT is a flexible surface feature of tubulin heterodimers and microtubules. In addition, we show that Drosophila sperm tail length depends on the total tubulin pool available for axoneme assembly and spermatid elongation. D. melanogaster and other Drosophila species have extraordinarily long sperm tails, the length of which is remarkably constant in wild type flies. We show that in males of experimental genotypes that express wild type tubulins but have half the amount of the normal tubulin pool size, sperm tails are substantially shorter than wild type. Cell Motil. Cytoskeleton 2008. © 2008 Wiley‐Liss, Inc.