15. Rebagliati, M. R., Toyama, R., Haffter, P. & Dawid, I. B. cyclops encodes a nodal-related factor involved
in midline signaling. Proc. Natl Acad. Sci. USA 95, 9932±7 (1998).
16. Schier, A. F. & Shen, M. M. Nodal signalling in vertebrate development. Nature 403, 385±389 (2000).
17. Erter, C. E., Solnica-Krezel, L. & Wright, C. V. Zebra®sh nodal-related 2 encodes an early
mesendodermal inducer signaling from the extraembryonic yolk syncytial layer. Dev. Biol. 204, 361±
372 (1998).
18. Gritsman, K., Talbot, W. S. & Schier, A. F. Nodal signaling patterns the organizer. Development 127,
921±932 (2000).
19. Thisse, B., Wright, C. V. & Thisse, C. Activin- and Nodal-related factors control antero-posterior
patterning of the zebra®sh embryo. Nature 403, 425±428 (2000).
20. Jones, C. M., Kuehn, M. R., Hogan, B. L., Smith, J. C. & Wright, C. V. Nodal-related signals induce
axial mesoderm and dorsalize mesoderm during gastrulation. Development 121, 3651±3662 (1995).
21. Agius, E., Oelgeschlager, M., Wessely, O., Kemp, C. & De Robertis,E. M. Endodermal Nodal-related
signals and mesoderm induction in Xenopus. Development 127, 1173±1183 (2000).
22. Gritsman, K. et al. The EGF-CFC protein one-eyed pinhead is essential for nodal signaling. Cell 97,
121±132 (1999).
23. Vogel, A. M. & Gerster, T. Promoter activity of the zebra®sh bhikhari retroelement requires an intact
activin signaling pathway. Mech. Dev. 85, 133±146 (1999).
24. Ruppert, R., Hoffmann, E. & Sebald, W. Human bone morphogenetic protein 2 contains a heparin-
binding site which modi®es its biological activity. Eur. J. Biochem. 237, 295±302 (1996).
25. Pfeiffer, S., Alexandre, C., Calleja, M. & Vincent, J. P. The progeny of wingless-expressing cells deliver
the signal at a distance in Drosophila embryos. Curr. Biol. 10, 321±324 (2000).
26. Schier, A. F., Neuhauss, S. C., Helde, K, A., Talbot, W. S. & Driever, W. The one-eyed pinhead gene
functions in mesoderm and endoderm formation in zebra®sh and interacts with no tail. Development
124, 327±342 (1997).
27. Zhang, J., Talbot, W. S. & Schier, A. F. Positional cloning identi®es zebra®sh one-eyed pinhead asa
permissive EGF-related ligand required during gastrulation. Cell 92, 241±251 (1998).
28. Stra Èhle, U. et al. one-eyed pinhead is required for development of the ventral midline of the zebra®sh
(Danio rerio) neural tube. Genes Funct. 1, 131±148 (1997).
Supplementary information is available on Nature's World-Wide Web site
(http://www.nature.com) or as paper copy from the London editorial of®ce of Nature.
Acknowledgements
We thank members of the Schier and Yelon laboratories for discussions; R. Burdine,
A. Carmany-Rampey, K. Joubin, R. Lehmann, G. Struhl, W. Talbot and D. Yelon for
comments on the manuscript; S. Zimmerman, R. Feeney and T. Bruno for ®sh care. Y.C. is
the Rebecca Ridley Kry Fellow of the Cancer Research Fund of the Damon Runyon±Walter
Winchell Foundation. A.F.S. is a Scholar of the McKnight Endowment Fund for
Neuroscience and the Irma T. Hirschl Trust, and is supported by grants from the NIH.
Correspondence and requests for materials should be addressed to A.F.S.
(e-mail: schier@saturn.med.nyu.edu).
letters to nature
610 NATURE | VOL 411 | 31 MAY 2001 | www.nature.com
.................................................................
MOR1 is essential for organizing
cortical microtubules in plants
Angela T. Whittington, Oliver Vugrek, Ke Jun Wei, Nortrud G. Hasenbein,
Keiko Sugimoto*, Madeleine C. Rashbrooke & Geoffrey O. Wasteneys
Plant Cell Biology Group, Research School of Biological Sciences, The Australian
National University, GPO Box 475, Canberra, ACT 2601, Australia
..............................................................................................................................................
Microtubules orchestrate cell division and morphogenesis, but
how they disassemble and reappear at different subcellular loca-
tions is unknown. Microtubule organizing centres are thought to
have an important role, but in higher plants microtubules assem-
ble in ordered con®gurations even though microtubule organiz-
ing centres are inconspicuous or absent. Plant cells generate
highly organized microtubule arrays that coordinate mitosis,
cytokinesis and expansion. Inhibiting microtubule assembly pre-
vents chromosome separation
1
, blocks cell division
2
and impairs
growth polarity
3
. Microtubules are essential for the formation of
cell walls, through an array of plasma-membrane-associated
cortical microtubules whose control mechanisms are unknown.
Using a genetic strategy to identify microtubule organizing
factors in Arabidopsis thaliana, we isolated temperature-sensitive
*Present address: John Innes Centre, Department of Cell and Developmental Biology, Norwich
NR4 7UH, UK.
mutant alleles of the MICROTUBULE ORGANIZATION 1
(MOR1) gene. Here we show that MOR1 is the plant version of
an ancient family of microtubule-associated proteins
4
. Point
mutations that substitute single amino-acid residues in an
amino-terminal HEAT repeat impart reversible temperature-
dependent cortical microtubule disruption, showing that MOR1
is essential for cortical microtubule organization.
In most plant cells that display diffuse rather than tip growth,
microtubules localize to the cortical cytoplasm perpendicular to the
major axis of expansion. Microtubules and cellulose micro®brils
often have similar orientation patterns in elongating cells
5
and it is
generally accepted, but not proven, that cortical microtubules
control the alignment of cellulose micro®brils
6
. Identifying the
factors that organize microtubule arrays at the periphery of plant
cells is a necessary step towards understanding the mechanisms that
underlie wall deposition and, hence, plant morphogenesis.
To identify factors regulating cortical microtubule organization
in plant cells, we used immuno¯uorescence microscopy to screen
chemically mutagenized seedlings of A. thaliana for aberrant
microtubule patterns. One mutant locus, mor1, causes tempera-
ture-sensitive cortical microtubule shortening and disorganization
(Fig. 1) and consequent morphological defects. We used ecotype-
speci®c markers to identify MOR1 as a gene of around 14 kilobases
(kb) that encodes a protein with a predicted relative molecular mass
of 217,000 (M
r
217K) (Fig. 2a) that has signi®cant deduced amino-
acid sequence similarity to human TOGp
7
, Xenopus MAP215
Figure 1 Mutations in the MOR1 gene cause temperature-dependent microtubule
disruption. We used anti-tubulin immuno¯uorescence to label cortical microtubules in
epidermal cells of the ®rst true leaf of 21-day-old seedlings after incubating seedlings at
29 8C for 2 h before ®xation. a, Wild type. b, mor1-1 homozygote. Scale bar, 25 mm.
a
HR1 23 4 5 67 8 910
1,979
amino
acids
b
E195K L174F
mor1-1 mor1-2
Figure 2 MOR1 protein structure. a, Schematic representation with shaded boxes
indicating conserved domains between MOR1, TOGp, XMAP215, MSPS and DdCP224.
The shorter ZYG-9 and yeast proteins share the ®rst ®ve and ®rst four regions of
homology, respectively. Black stripes show putative HEAT repeats (HR) in relation to these
conserved domains. b, Deduced amino-acid sequence comparison of MOR1's HEAT
repeat-1 with equivalent repeats in homologues. Black-shaded residues indicate identity,
grey-shaded residues indicate similarity (40% threshold), outlined box indicates HEAT
repeat. Mutations altering MOR1 amino-acid residues are indicated by arrowheads.
© 2001 Macmillan Magazines Ltd