Editors' ChoiceDevelopment

Algae Present a New Cell Cycle Paradigm

Science Signaling  03 Jun 2008:
Vol. 1, Issue 22, pp. ec209
DOI: 10.1126/scisignal.122ec209

Classical embryologists long ago demonstrated that sperm entry initiates Ca2+ waves that trigger important early developmental events such as the cortical reaction, meiotic release (egg activation), establishment of polarity, and passage through the G1/S checkpoint. Zygotic polarity in the brown alga Fucus serratus is established by changes in intracellular Ca2+ concentration ([Ca2+]int) that occur over a period of several hours and induce growth at the basal pole, ultimately resulting in an asymmetric first mitosis. In yeast, G1/S progression and bud growth are initiated at the same time, but passage through the G2/M transition requires actin localization at the bud collar. Bothwell et al. report that polarization and the G1/S transition in Fucus are coordinately triggered by a Ca2+ wave but, unlike yeast, there is no morphogenesis checkpoint at the G2/M transition. Using two-photon microscopy to measure the ratio of fluorescent Ca2+-sensitive and Ca2+-insensitive dyes, they determined that both cytosolic and nuclear [Ca2+] ([Ca2+]cyt and [Ca2+]nuc) increased steadily upon fertilization and peaked after about 30 minutes, the same time at which the sperm pronucleus began migrating toward the egg pronucleus. Both [Ca2+]cyt and [Ca2+]nuc decreased during the migration, but [Ca2+]nuc increased again just as the zygote entered S phase about 2.5 hours after fertilization. When zygotes were treated with the high-affinity Ca2+ chelator BAPTA before S phase, there was no effect on pronuclear migration, but both S phase and asymmetric growth were prevented. BAPTA treatment after S phase had no effect on asymmetric growth, which indicates that polarization was established before S phase. BAPTA also prevented the first mitosis in about half of treated zygotes, regardless of whether it was added before or after S phase. In contrast, only very high concentrations of the lower-affinity Ca2+ chelator Br2BAPTA affected mitosis, but it had no effect on polarization regardless of when it was administered. Treating zygotes with the actin depolymerizing drug lantrunculin B inhibited polarization but did not have any effect on mitosis. These results are consistent with a model in which the [Ca2+] wave initiates both polarization and cell cycle progression, but the two processes occur independently. This stands in direct contrast to budding yeast, where polarized growth of the bud is absolutely required for the G2/M transition. In Fucus the two events are coordinately regulated, but there is no such morphogenesis checkpoint.

J. H. F. Bothwell, J. Kisielewska, M. J. Genner, M. R. McAinsh, C. Brownlee, Ca2+ signals coordinate zygotic polarization and cell cycle progression in the brown alga Fucus serratus. Development 135, 2173-2181 (2008). [Abstract] [Full Text]