Axoneme-specific beta-tubulin specialization: a conserved C-terminal motif specifies the central pair.
Axonemes are ancient organelles that mediate motility of cilia and flagella in animals, plants, and protists. The long evolutionary conservation of axoneme architecture, a cylinder of nine doublet microtubules surrounding a central pair of singlet microtubules, suggests all motile axonemes may share common assembly mechanisms. Consistent with this, alpha- and beta-tubulins utilized in motile axonemes fall among the most conserved tubulin sequences [1, 2], and the beta-tubulins contain a sequence motif at the same position in the carboxyl terminus [3]. Axoneme doublet microtubules are initiated from the corresponding triplet microtubules of the basal body [4], but the large macromolecular "central apparatus" that includes the central pair microtubules and associated structures [5] is a specialization unique to motile axonemes. In Drosophila spermatogenesis, basal bodies and axonemes utilize the same alpha-tubulin but different beta-tubulins [6--13]. beta 1 is utilized for the centriole/basal body, and beta 2 is utilized for the motile sperm tail axoneme. beta 2 contains the motile axoneme-specific sequence motif, but beta 1 does not [3]. Here, we show that the "axoneme motif" specifies the central pair. beta 1 can provide partial function for axoneme assembly but cannot make the central microtubules [14]. Introducing the axoneme motif into the beta 1 carboxyl terminus, a two amino acid change, conferred upon beta 1 the ability to assemble 9 + 2 axonemes. This finding explains the conservation of the axoneme-specific sequence motif through 1.5 billion years of evolution.
Nielsen
M G
MG
Indiana Molecular Biology Institute and Department of Biology, Indiana University, Bloomington, IN 47405, USA.
Turner
F R
FR
Hutchens
J A
JA
Raff
E C
EC
D000818:Animals; D002678:Chimera; D004331:Drosophila melanogaster / Q000166:cytology / Q000235:genetics; D019476:Insect Proteins / Q000737:chemistry / Q000235:genetics / Q000378:metabolism*; D008297:Male; D008571:Men; D008870:Microtubules / Q000235:genetics / Q000378:metabolism* / Q000648:ultrastructure; D009024:Morphogenesis; D016296:Mutagenesis; D015388:Organelles / Q000235:genetics*; D013081:Sperm Motility; D013082:Sperm Tail / Q000737:chemistry / Q000378:metabolism* / Q000648:ultrastructure; D014404:Tubulin / Q000235:genetics / Q000378:metabolism*
D019476:Insect Proteins; D014404:Tubulin