Open Mitosis: Nuclear Envelope Dynamics 221
Electron microscopy studies revealed that in the charophyte algaSpirogyra,
nuclear envelope disruption starts around the spindle equator in metaphase,
suggesting a connection between spindle formation and nuclear membrane
disassembly early in the plant lineage (Ueda et al. 1986).
The orientation of the spindle and position of the division plane in a plant
cell is determined by the preprophase band (PPB), a ring of microtubules con-
centrated below the plasma membrane. Disintegration of the PPB is closely
linked with mitotic breakdown of the nuclear envelope, suggestive of a co-
regulation of these two events. Evidence for this mechanism stems from dual
labeling experiments with tubulin and the Golgi/nuclear envelope-marker
Nag. When fused to green and red fluorescent proteins, respectively, these
markers showed that nuclear envelope breakdown in tobacco cells preceded
the disappearance of the PPB microtubules by roughly 2 min. Both processes
appeared to stimulate each other as nuclear envelope breakdown was accom-
panied by a ruffling of the nuclear envelope in an area adjacent to the PPB,
whereas the PPB was disassembled most rapidly in a region closest to the
disrupted nuclear envelope (Dixit and Cyr 2002).
Since higher plants lack dyneins, an intriguing candidate for a plant-
specific microtubule motor functioning during mitosis is the kinesin-like
calmodulin-binding protein (KCBP). KCBP has been found only in the green
algae and plants (Abdel-Ghany et al. 2005) and has been implicated in mi-
totic functions inChlamydomonasand higher plant cells (Dymek et al. 2006;
Preuss et al. 2003). Constitutive activation of KCBP via antibodies directed
against the calmodulin-binding region during late prophase has been shown
to induce nuclear envelope breakdown within minutes of injection (Vos et al.
2000). This suggests a role for Ca2+/calmodulin-mediated activation of KCBP
in the control of nuclear envelope breakdown in plants. Interestingly, the
plant nuclear envelope markers mentioned above included LCA1, a Ca2+
pump in tomato (Downie et al. 1998). It is tempting to speculate that Ca2+is
stored in the nuclear envelope lumen and could be readily available as a signal
in KCBP-mediated nuclear envelope breakdown in plants. Alternatively, the
ER–PPB, a membrane structure underlying the microtubular PPB, has been
proposed as a possible storage site for Ca2+asasignalattheonsetofmitosis
(Zachariadis et al. 2001).
An alternative to the mechanical force model for nuclear envelope break-
down has been proposed, based on observations of nuclear pores in starfish
oocytes (Terasaki et al. 2001). Nuclear envelope breakdown in animal cells
consists of two distinct phases of permeabilization. Using dextran entry as
a marker for “leaky” nuclear envelopes, it has been shown that permeabiliza-
tion occurs prior to visible disruption of the nuclear membranes. This first
permeabilization step coincides with the partial disassembly of nuclear pore
complexes and is followed by a second wave of rapidly spreading fenestra-
tion of the nuclear envelope (Lenart et al. 2003; Teresaki et al. 2001). Partially
disassembled nuclear pores have also been observed inDrosophila(Kiseleva