Myosin XI-i Links the Nuclear Membrane to the Cytoskeleton to Control Nuclear Movement and Shape in Arabidopsis

Abstract

The cell nucleus communicates with the cytoplasm through a nucleocytoplasmic linker that maintains the shape of the nucleus and mediates its migration. In contrast to animal nuclei, which are moved by motor proteins (kinesins and dyneins) along the microtubule cytoskeleton, plant nuclei move rapidly and farther along an actin filament cytoskeleton. This implies that plants use a distinct nucleocytoplasmic linker for nuclear dynamics, although its molecular identity is unknown. Here, we describe a new type of nucleocytoplasmic linker consisting of a myosin motor and nuclear membrane proteins. In the Arabidopsis thaliana mutant kaku1, nuclear movement was impaired and the nuclear envelope was abnormally invaginated. The responsible gene was identified as myosin XI-i, which encodes a plant-specific myosin. Myosin XI-i is specifically localized on the nuclear membrane, where it physically interacts with the outer-nuclear-membrane proteins WIT1 and WIT2. Both WIT proteins are required for anchoring myosin XI-i to the nuclear membrane and for nuclear movement. A striking feature of plant cells is dark-induced nuclear positioning in mesophyll cells. A deficiency of either myosin XI-i or WIT proteins diminished dark-induced nuclear positioning. The unique nucleocytoplasmic linkage in plants might enable rapid nuclear positioning in response to environmental stimuli.

Myosin-driven transport network in plants

“…Fittingly, this outer nuclear membrane protein has been identified previously as a linker between the nucleus and myosin XI-I, an interaction required for slow nuclear relocation (11). This result further supports the specificity and functional relevance of our Y2H screens.…”

“…However, these two myosins share highly similar network connectivity patterns and could perform analogous functions in distinct cell types. Finally, myosin XI-I is the most narrow specialist, in accord with its distinct position in the phylogenetic tree (21) and unusual functional and enzymatic properties (11,39). Fittingly, the most specialized myosin interactor, WIT2, exclusively interacts with myosin XI-I.…”

“…Despite the accumulating supportive evidence, the existence of the F-actin-myosin complexes in the nucleus remains controversial (42,43). Although the presence of actins in the plant nucleus (44), as well as the contributions of F-actin and myosin XI-I to nucleus relocation and shape, has been described (11,45), to our knowledge, myosin-driven transport through the nucleus has not. Although the molecular architecture of the linear arrays associated with myosin XI-K:mCherry (Fig.…”

“…Among the 13 paralogous myosins XI encoded in the Arabidopsis thaliana genome, the highly expressed myosins XI-K, XI-1, and XI-2 have been shown to provide the most pronounced, functionally redundant contributions to each of these processes. In contrast, another highly expressed paralog, myosin XI-I, plays only limited roles in cell and plant growth but has a specialized function in nuclear repositioning through binding nuclear envelope protein WIT2 (11).…”

Nuclear migration events throughout development

“…The role of LINC complexes in moving nuclei is conserved across eukaryotes. For example, LINC complexes mediate nuclear migration in Arabidopsis thaliana and/or Physcomitrella patens root hairs, trichomes and pollen tubes (Folkers et al, 1997;Mathur et al, 1999;Miki et al, 2015;Tamura et al, 2013;Zhou et al, 2012Zhou et al, , 2015Zhou and Meier, 2014).…”