An evolutionarily conserved NIMA-related kinase directs rhizoid tip growth in the basal land plant <i>Marchantia polymorpha</i>

Otani, Kento; Ishizaki, Kimitsune; Nishihama, Ryuichi; Takatani, Shogo; Kohchi, Takayuki; Takahashi, Taku; Motose, Hiroyasu

doi:10.1242/dev.154617

Cited by 29 publications

(40 citation statements)

References 62 publications

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“…2a), the promoter:mCitrine sequences were amplified from the genomic constructs described above, and inserted at a HindIII site of pMpGWB301 using the In-Fusion HD Cloning System. pENTR MpTUB2 52,53 was kindly provided from Dr. R. Nishihama and introduced into pMpGWB301 pro MpSYP2:mCitrine-GW ( Supplementary Fig. 2a) using the Gateway LR Clonase™ II Enzyme Mix.…”

Section: Methodsmentioning

confidence: 99%

The liverwort oil body is formed by redirection of the secretory pathway

et al. 2020

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Eukaryotic cells acquired novel organelles during evolution through mechanisms that remain largely obscure. The existence of the unique oil body compartment is a synapomorphy of liverworts that represents lineage-specific acquisition of this organelle during evolution, although its origin, biogenesis, and physiological function are yet unknown. We find that two paralogous syntaxin-1 homologs in the liverwort Marchantia polymorpha are distinctly targeted to forming cell plates and the oil body, suggesting that these structures share some developmental similarity. Oil body formation is regulated by an ERF/AP2-type transcription factor and loss of the oil body increases M. polymorpha herbivory. These findings highlight a common strategy for the acquisition of organelles with distinct functions in plants, via periodical redirection of the secretory pathway depending on cellular phase transition.

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Section: Methodsmentioning

confidence: 99%

The liverwort oil body is formed by redirection of the secretory pathway

et al. 2020

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“…pMpGWB304-proMpAN and pMpGWB315-proMpAN were transformed to Tak-1 and Tak-2. Additionally, the pMpGWB307-proMpAN:MpAN vector and the pMpGWB202-TagRFP-MpTUB2 vector for the CaMV35Spro:TagRFP-MpTUB2 construct (Otani et al, 2018) were co-transfomed to Mpan-1 ko (male). Transformants were selected on half-strength B5 agar medium containing 1% (w/v) agar, 0.5 µM chlorsulfuron and 100 mg l −1 cefotaxime (Claforan; Sanofi-Aventis).…”

Section: Agrobacterium-mediated Transformationmentioning

confidence: 99%

ANGUSTIFOLIA contributes to the regulation of three-dimensional morphogenesis in the liverwort Marchantia polymorpha

et al. 2018

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mutants deficient in ANGUSTIFOLIA (AN) exhibit several phenotypes at the sporophyte stage, such as narrow and thicker leaves, trichomes with two branches, and twisted fruits. It is thought that these phenotypes are caused by abnormal arrangement of cortical microtubules (MTs). AN homologs are present in the genomes of diverse land plants, including the basal land plant , and their molecular functions have been shown to be evolutionarily conserved in terms of the ability to complement the mutation. However, the roles of ANs in bryophytes, the life cycle of which includes a dominant haploid gametophyte generation, remain unknown. Here, we have examined the roles of AN homologs in the model bryophyte (MpAN). Mp knockout mutants showed abnormal twisted thalli and suppressed thallus growth along the growth axis. Under weak blue light conditions, elongated thallus growth was observed in wild-type plants, whereas it was suppressed in the mutants. Moreover, disordered cortical MT orientations were observed. Our findings suggest that MpAN contributes to three-dimensional morphogenesis by regulating cortical MT arrangement in the gametophytes of bryophytes.

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“…By contrast, ARMADILLO-REPEAT KINESIN1 (ARK1) destabilizes microtubules by promoting the transition of microtubules from the polymerizing to the depolymerizing state, and root hairs are wavy in the ark1 loss of function mutant [ 15 ]. In the liverwort Marchantia polymorpha , the microtubule destabilizing MAP NIMA-RELATED PROTEIN (MpNEK) is required to maintain a stable position of the growing region in rhizoids [ 16 ]. However, no microtubule stabilizing MAP has been reported to function in stabilizing tip-growth in the liverwort model to date.…”

Section: Introductionmentioning

confidence: 99%

“…To identify microtubule stabilizing MAPs that stabilize tip-growth in liverworts, we screened T-DNA- and UV-mutagenized Marchantia polymorpha populations for mutants with wavy rhizoids that are morphologically similar to oryzalin-treated or Taxol-treated rhizoids. We isolated two nek mutants, demonstrating that mutants with defective microtubule organization were identified in the screen [ 16 ]. Moreover, we identified four mutant lines with T-DNA insertions in the gene encoding the MAP, WAVE DAMPENED2 LIKE ( WDL ).…”

Section: Introductionmentioning

confidence: 99%

Microtubule associated protein WAVE DAMPENED2-LIKE (WDL) controls microtubule bundling and the stability of the site of tip-growth in Marchantia polymorpha rhizoids

et al. 2021

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Tip-growth is a mode of polarized cell expansion where incorporation of new membrane and wall is stably restricted to a single, small domain of the cell surface resulting in the formation of a tubular projection that extends away from the body of the cell. The organization of the microtubule cytoskeleton is conserved among tip-growing cells of land plants: bundles of microtubules run longitudinally along the non-growing shank and a network of fine microtubules grow into the apical dome where growth occurs. Together, these microtubule networks control the stable positioning of the growth site at the cell surface. This conserved dynamic organization is required for the spatial stability of tip-growth, as demonstrated by the formation of sinuous tip-growing cells upon treatment with microtubule-stabilizing or microtubule-destabilizing drugs. Microtubule associated proteins (MAPs) that either stabilize or destabilize microtubule networks are required for the maintenance of stable tip-growth in root hairs of flowering plants. NIMA RELATED KINASE (NEK) is a MAP that destabilizes microtubule growing ends in the apical dome of tip-growing rhizoid cells in the liverwort Marchantia polymorpha. We hypothesized that both microtubule stabilizing and destabilizing MAPs are required for the maintenance of the stable tip-growth in liverworts. To identify genes encoding microtubule-stabilizing and microtubule-destabilizing activities we generated 120,000 UV-B mutagenized and 336,000 T-DNA transformed Marchantia polymorpha plants and screened for defective rhizoid phenotypes. We identified 119 mutants and retained 30 mutants in which the sinuous rhizoid phenotype was inherited. The 30 mutants were classified into at least 4 linkage groups. Characterisation of two of the linkage groups showed that MAP genes–WAVE DAMPENED2-LIKE (WDL) and NIMA-RELATED KINASE (NEK)–are required to stabilize the site of tip growth in elongating rhizoids. Furthermore, we show that MpWDL is required for the formation of a bundled array of parallel and longitudinally orientated microtubules in the non-growing shank of rhizoids where MpWDL-YFP localizes to microtubule bundles. We propose a model where the opposite functions of MpWDL and MpNEK on microtubule bundling are spatially separated and promote tip-growth spatial stability.

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An evolutionarily conserved NIMA-related kinase directs rhizoid tip growth in the basal land plant Marchantia polymorpha

Cited by 29 publications

References 62 publications

The liverwort oil body is formed by redirection of the secretory pathway

The liverwort oil body is formed by redirection of the secretory pathway

ANGUSTIFOLIA contributes to the regulation of three-dimensional morphogenesis in the liverwort Marchantia polymorpha

Microtubule associated protein WAVE DAMPENED2-LIKE (WDL) controls microtubule bundling and the stability of the site of tip-growth in Marchantia polymorpha rhizoids

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