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Spatial Control Of Cell Division
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Keywords : Arabidopsis thaliana - cytoskeleton - development - mutant - microtubule - preprophase band

Doctoral school affiliation : ED145 "Sciences du Végétal" Université Paris 11-Orsay

Contacts :

Institut Jean-Pierre Bourgin, UMR1318 INRA-AgroParisTech
Bâtiment 7
INRA Centre de Versailles-Grignon
Route de St-Cyr (RD10)
78026 Versailles Cedex France

tél : +33 (0)1 30 83 30 00 - fax : +33 (0)1 30 83 33 19


Group leader
David Bouchez

Senior scientist

Magalie Uyttewaal
Research scientist


Marie-Ludivine de Tauzia-Moreau
Technician


Martine Pastuglia

Research scientist

Katia Belcram
Assistant Engineer

Summary :

 

Colonization of land by plants 500 million years ago was a major evolutionary transition in the history of life on earth. Adaptations linked to this colonization include cellular features that are specific to this group of organisms. Plant cells are notably encaged in a stiff pecto-cellulosic cell wall, allowing them to resist to the high turgor pressure generated by large water-filled vacuoles, and preventing any relative movement of cells within tissues. The balance between turgor pressure on the one hand and resistance of the wall on the other hand is the main driving force for oriented cell expansion in plants. The cell wall and the vacuoles also impose a specific mode of cell division, where separation of the daughter cytoplasms is achieved by de novo construction of a new cell plate, rather than by membrane infurrowing and fusion as seen in other eukaryotes.
These peculiar modes of cell elongation and division rely on distinctive cytoskeletal arrays that are specific to land plants: in an interphase cell, the cortical microtubule array, located at the cell's periphery (or cortex), drives the oriented deposition of cellulose for cell growth. Upon division, two arrays are mobilized to achieve cytokinesis. First, the preprophase band (PPB) is a transient structure forming before mitotic entry and precisely predicting the final plane of division (Figure 1). At the end of mitosis, a second specific array, the phragmoplast, drives the synthesis of the new cell plate separating the two daughter cells.

Precise positioning of the division plane is of special importance in plants, since in the absence of any cell migration, it is the major mechanism driving 3D organization of plant tissues, together with oriented cell elongation. Our research group is interested in understanding these elongation and division mechanisms specific to land plants. We aim at determining the regulation pathways and interaction networks involved in organizing the microtubule cytoskeleton, their links with the cell cycle machinery, and their significance for the evolution of development in plants.


Main Results :


In recent years, we have isolated and characterized an intriguing class of Arabidopsis mutants called ton1 and fass, which display severe developmental alterations and, at the cellular level, strong defects in cell division and elongation. Cortical microtubule networks are perturbed, in interphase as well as in mitosis. The PPB is totally absent, resulting in incorrect positioning of division planes and abnormal polarized cell expansion.

The multidisciplinary study of the TON1 and FASS genes and proteins and of their partners allowed us to discover and characterize a protein complex named TTP (Figure 2). This complex plays a key role in the spatial control of cell division and in the organization of cortical microtubules. It is composed of a core of five proteins (Figure 2): a trimeric PP2A phosphatase comprising FASS as the regulatory subunit, TON1, and a member of the TRM family, the latter being responsible for anchoring the complex to the microtubule cytoskeleton. The TRM family is specific of land plants and has several members in Arabidopsis. It potentially confers to the TTP complex a diversity of composition and function during the cell cycle.
We have shown that the TTP complex plays a major role in PPB formation. Mutants in members of the complex are unable to form a PPB (Figure 4) and have severe defects in division plane positioning (Figure 3).
In an evo-devo perspective, we have studied the consequence of a TON1 loss of function mutation in the moss Physcomitrella patens. These study has shown that the function of this protein in division plane setup has been conserved during 500 million years of land plant evolution.


Interestingly, all TTP partners exhibit various levels of sequence similarity with animal centrosomal proteins, despite the fact that higher plants are totally devoid of such central microtubule organizer, which has been lost during the evolution of land plants. Our results are a first indication of a functional and evolutionary link between the cortical cytoskeleton of plants and animal centrosomes, apart from microtubule nucleation aspects. This conserved molecular network could stem back to the origin of eukaryotes, and its ancestral function in spatial coordination of the microtubule cytoskeleton would have diverged between plants and animals in accordance with their respective cellular organization. 

 


Selected Publications :

Tisne, S., Serrand, Y., Bach, L., Gilbault, E., Ben Ameur, R., Balasse, H., Voisin, R., Bouchez, D., Durand-Tardif, M., Guerche, P., Chareyron, G., Da Rugna, J., Camilleri, C., and Loudet, O. (2013). Phenoscope: an automated large-scale phenotyping platform offering high spatial homogeneity. Plant Journal 74, 534-544. (pubmed)

Spinner, L., Gadeyne, A., Belcram, K., Goussot, M., Moison, M., Duroc, Y., Eeckhout, D., De Winne, N., Schaefer, E., Van De Slijke, E., Persiau, G., Witters, E., Gevaert, K., De Jaeger, G., Bouchez, D., Van Damme, D., and Pastuglia, M. (2013). A protein phosphatase 2A complex spatially controls plant cell division. Nature Communications 4, 1863. (pubmed)

Uyttewaal M, Burian A, Alim K, Landrein B, Borowska-Wykret D, Dedieu A, Peaucelle A, Ludynia M, Traas J, Boudaoud A, Kwiatkowska D and Hamant O (2012). Mechanical stress acts via katanin to amplify differences in growth rate between adjacent cells in Arabidopsis. Cell 149: 439-451. (pubmed)

Drevensek S, Goussot M, Duroc Y, Christodoulidou A, Steyaert S, Schaefer E, Duvernois E, Grandjean O, Vantard M, Bouchez D and Pastuglia M (2012). The Arabidopsis TRM1-TON1 interaction reveals a recruitment network common to plant cortical microtubule arrays and eukaryotic centrosomes. Plant Cell 24: 178-191 (pubmed)

Duroc, Y., Bouchez, D., and Pastuglia, M. (2011). The preprophase band and division site determination in land plants. In The Plant Cytoskeleton, B. Liu, ed (New York: Springer USA), pp. 145-186.

Spinner, L., Pastuglia, M., Belcram, K., Pegoraro, M., Goussot, M., Bouchez, D., and Schaefer, D.G. (2010). The function of TONNEAU1 in moss reveals ancient mechanisms of division plane specification and cell elongation in land plants. Development 137, 2733-2742. (pubmed)

Johannes, F., Porcher, E., Teixeira, F.K., Saliba-Colombani, V., Simon, M., Agier, N., Bulski, A., Albuisson, J., Heredia, F., Audigier, P., Bouchez, D., Dillmann, C., Guerche, P., Hospital, F., and Colot, V. (2009). Assessing the impact of transgenerational epigenetic variation on complex traits. PLoS Genet 5, e1000530. (pubmed)

Azimzadeh J, Nacry P, Christodoulidou A, Drevensek S, Camilleri C, Amiour N, Parcy F, Pastuglia M and Bouchez D (2008). Arabidopsis TONNEAU1 proteins are essential for preprophase band formation, share similarity with human centrosomal proteins and interact with centrin. Plant Cell, 20: 2146–2159 (pubmed)

Granier F, Bouchez D. (2007) Mutant Libraries: a High-throughput Arabidopsis Reverse Genetics System. Morot-Gaudry J.F, Lea P, Briat J.F. Title: Functional Plant Genomics. Science Publishers 143-164.

Johnson X, Bouchez D. (2007) The model species, Arabidopsis thaliana. Morot-Gaudry J.F, Lea P, Briat J.F. Functional Plant Genomics. Science Publishers 385-396.

Pastuglia M, Bouchez D (2007). Molecular encounters at microtubule ends in the plant cell cortex. Curr Op Plant Biol 10:1-7 (pubmed)

Pierre M, Traverso JA, Boisson B, Domenichini S, Bouchez D, Giglione C, Meinnel T (2007). N-myristoylation regulates the SnRK1 pathway in Arabidopsis. Plant Cell 19 :2804-2812 (pubmed)

Pastuglia M, Azimzadeh J, Goussot M, Camilleri C, Belcram K, Evrard JL, Schmit AC, Guerche P and Bouchez D (2006). Gamma-tubulin is essential for microtubule organization and development in Arabidopsis. Plant Cell 18 : 1412-1425 (pubmed)

Ostrowski MF, David J, Santoni S, McKhann H, Reboud X, Le Corre V, Camilleri C, Brunel D, Bouchez D, Faure B, Bataillon T (2006) Evidence for a large-scale population structure among accessions of Arabidopsis thaliana: possible causes and consequences for the distribution of linkage disequilibrium. Mol Ecol 15 :1507-1517 (pubmed)

Camilleri C, Azimzadeh J, Pastuglia M, Bellini C, Grandjean O and Bouchez D (2002). The Arabidopsis TONNEAU2 gene encodes a putative novel PP2A regulatory subunit essential for the control of cortical cytoskeleton. Plant Cell, 14 : 833-845. (pubmed)

Azimzadeh J, Traas J, Pastuglia M. (2001) Molecular aspects of microtubule dynamics in plants. Curr Opin Plant Biol. 4, 513-519. (pubmed)

Nacry P, Camilleri C, Courtial B, Caboche M, Bouchez D (1998) Major chromosomal rearrangements induced by T-DNA transformation in Arabidopsis. Genetics 149 : 641-650. (pubmed)

Thion L, Mazars C, Nacry P, Bouchez D, Moreau M, Ranjeva R, Thuleau P (1998). Plasma membrane depolarization-activated calcium channels, stimulated by microtubule-depolymerizing drugs in wild-type Arabidopsis thaliana protoplasts, display constitutively large activities and a longer half-life in ton2 mutant cells affected in the organizationof cortical microtubules. Plant Journal 13 : 603-610. (pubmed)

Traas J, Bellini C, Nacry P, Kronenberger J, Bouchez D, Caboche M (1995). Normal differentiation patterns in plants lacking microtubular preprophase bands. Nature 375 : 676-677.

 

 

 
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