Plant-specific armadillo repeat kinesin directs organelle transport and microtubule convergence to promote tip growth

Abstract

Tip growth is a highly polarized growth process essential for plant growth and reproduction. However, its molecular mechanism and evolutional significance remain elusive. Here, we show that plant-specific armadillo-repeat containing kinesin, MpARK1, drives long-range organelle transport and microtubule convergence in tip growing rhizoids in a basal land plant Marchantia polymorpha. MpARK1 is required for anterograde transport of the nucleus and plastids to maintain their position during persistent tip growth. Furthermore, MpARK1 participates in microtubule focusing on the apex to stabilize growth direction. MpARK1-dependent rhizoid growth is essential for plant anchorage and soil holding capacity. Thus, ARK might be co-opted to serve as a long-range transporter and intracellular organizer in the primitive rooting structure (rhizoid) for the adaptation to terrestrial environments. Our findings suggest that ARK was comparable to animal anterograde kinesin, challenging the traditional view that actomyosin-based cytoplasmic streaming is a dominant transport mode in plant kingdom.

Overexpression of NIMA-related kinase suppresses cell proliferation and tip growth in a liverwortMarchantia polymorpha

“…Furthermore, it would be helpful to visualize protein transport toward the rhizoid apex and shank region because we observed MpNEK1 particles moved to the acropetal and basipetal direction (Video S3-S5). The velocity of MpNEK1 particles is quite similar to that of armadillo-repeat kinesin, about half of velocity of growing microtubule plus ends (Kanda et al 2022), suggesting this motility is not due to plus-end tracking but rather to the kinesin-dependent transport along microtubules. Anyway, MpNEK1 overexpression has the potent growth effect than that of Arabidopsis NEK6, whose overexpression caused slight reduction of root growth (Takatani, et al 2017).…”

“…Over-accumulated MpNEK1 may destabilize microtubule foci at the apex and/or longitudinal microtubules at the shank region. Because the longitudinal microtubules promote rhizoid elongation through organelle transport (Kanda, et al 2022), it is plausible that MpNEK1 dispersed along rhizoids depolymerizes longitudinal microtubules to suppress rhizoid growth.…”

“…Thanks to these advantages, MpNEK1 has been shown to direct tip growth of rhizoids through microtubule depolymerization in the apical region (Otani, et al 2018). Rhizoids are filamentous rooting cells, mainly elongating from the ventral epidermis and are thought to be required for plant anchorage to the soil and water/nutrient uptake (Jones and Dolan 2012; Shimamura, 2016; Kohchi, et al 2021; Kanda, et al 2022). Mp nek1 mutant rhizoids frequently change their growth direction, resulting in the zigzag morphology (Otani, et al 2018) and the defect of invasive growth to enter the hard substratum (Mase, et al 2022).…”

Armadillo repeat-containing kinesin represents the versatile plus-end-directed transporter in Physcomitrella

“…Four highly homologous genes are present in the ARK family of P. patens 35,36 . Previously, we examined the RNAi knockdown mutant of ARK and identified a specific defect in protonemal apical cells, namely, nuclear mispositioning 30 .…”

“…ARK genes are conserved in land plants, but are absent in algae or animals 35 . However, the overall ARK structure is typical for kinesin superfamily proteins, where the motor domain and coiled-coil are followed by a cargo-recognising tail.…”