Abstract
In animals and fungi, cytoplasmic dynein is a processive minus-end-directed motor that plays dominant roles in various intracellular processes. In contrast, land plants lack cytoplasmic dynein but contain many minus-end-directed kinesin-14s. No plant kinesin-14 is known to produce processive motility as a homodimer. OsKCH2 is a plant-specific kinesin-14 with an N-terminal actin-binding domain and a central motor domain flanked by two predicted coiled-coils (CC1 and CC2). Here, we show that OsKCH2 specifically decorates preprophase band microtubules in vivo and transports actin filaments along microtubules in vitro. Importantly, OsKCH2 exhibits processive minus-end-directed motility on single microtubules as individual homodimers. We find that CC1, but not CC2, forms the coiled-coil to enable OsKCH2 dimerization. Instead, our results reveal that removing CC2 renders OsKCH2 a nonprocessive motor. Collectively, these results show that land plants have evolved unconventional kinesin-14 homodimers with inherent minus-end-directed processivity that may function to compensate for the loss of cytoplasmic dynein.
Highlights
In animals and fungi, cytoplasmic dynein is a processive minus-end-directed motor that plays dominant roles in various intracellular processes
To summarize, we have revealed an unexpected finding that OsKCH2(289–767), a motor-neck construct of the kinesin-14 OsKCH2 from the rice plant O. sativa, is a novel processive minus-end-directed microtubule motor
This study shows that some land plants, if not all, have evolved unconventional kinesin-14s with intrinsic minusend-directed processive motility, which could potentially function to compensate for the lack of cytoplasmic dynein20, 33
Summary
Cytoplasmic dynein is a processive minus-end-directed motor that plays dominant roles in various intracellular processes. OsKCH2 exhibits processive minus-end-directed motility on single microtubules as individual homodimers. Our results reveal that removing CC2 renders OsKCH2 a nonprocessive motor These results show that land plants have evolved unconventional kinesin homodimers with inherent minus-end-directed processivity that may function to compensate for the loss of cytoplasmic dynein. While it has long been speculated that land plants might have evolved unconventional kinesin14s with intrinsic minus-end-directed processivity to compensate for the loss of cytoplasmic dynein , no plant kinesin-14 has yet been found that exhibits processive minusend-directed motility on single microtubules as individual homodimers . Our single-molecule TIRF microscopy experiments reveal that unlike all other kinesin-14s that have been studied to date, OsKCH2 is a novel kinesin-14 motor that is capable of producing processive minus-end-directed motility on single microtubules as a homodimer. Our results show that land plants have evolved unconventional kinesin-14 motors with intrinsic minus-end-directed processivity, and markedly advance current knowledge of the design principles of kinesin-14s
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