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Transcription factors and architecture
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Keywords : Morphogenesis - Shoot apical meristem - Leaf - Boundary domain – miRNA- Evo-devo.

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

Contacts :

Institut Jean-Pierre Bourgin, UMR1318 INRA-AgroParisTech
Bâtiment 2
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
Patrick Laufs

Senior scientist

Catherine Perrot-Rechenmann
Senior scientist CNRS



Bernard Adroher
Technician

 Magali Goussot
Assitant Engineer

 Léo Serra
PhD student



Associate Group leader
Véronique Pautot

Senior scientist


Nicolas Arnaud
research scientitst 

 

Pierre Libeau
Assitant ingénieur CNRS

 

Manon Boudin
PhD student

 


 

Summary :


Plants present a wide variability of architecture that results from the activity of groups of pluripotent cells that constitute meristems. The shoot apical meristem, produces the entire aerial part of the plant, first leaves, then later upon floral transition, flowers. Meristems function is regulated by intricate networks in which in which transcription factors (TFs) play a central role.

We are interested in the morphogenetic processes that take place in the meristems or during the early phases of leaf development. We focus on two major meristematic families of transcription factors: the class-I KNOTTED like (KNOX I) class of “Three amino acid loop extension” (TALE) homeodomain proteins and the NAM/CUC proteins. These factors work in concert to promote meristem formation and establish boundaries. Boundaries are smalls groups of cells, which not only separate different units but also appear to have a prominent role as organisers of the surrounding domains. Our aim is to understand the contribution of these two families of transcription factors in the control of plant development. We are also interested in the evolution of these genes, and whether they could contribute to the diversification of plant architecture. Finally, we are investigating how these genes are integrated in larger regulatory networks.

 




Main Results :
 

Roles of the CUC genes during Arabidopsis leaf development.

We showed previously that a balance between the CUC2 gene and its regulatory miRNA, miR164 (encoded by MIR164a) controls the level of leaf serration in Arabidopsis (Nikovics et al., 2006), thus revealing a new role for the CUC genes outside the meristem. We further analysed the role of the two other CUC genes, CUC1 and CUC3 (Hasson, 2011). In particular, we showed that CUC1 does not contribute to Arabidopsis leaf development, that CUC3 contributes to a later stage of leaf serration, whereas CUC2 acts during initiation of leaf serration. We also retraced and discussed the evolutionary history of CUC genes in Arabidopsis, showing that following duplication of an ancestral gene, CUC1 and CUC2 have evolved differently and acquired specific functions.

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Roles of the CUC genes in Angiosperm leaves.

To extend our work in Arabidopsis, we analysed the role of the CUC genes during compound leaf development in a large selection of Eudicots (Blein et al., 2008). We showed that the CUC genes have a conserved expression in the boundaries between leaflet primordia, and that they are not only required for leaflet separation but also for leaflet formation. These observations extend and generalize those described for Arabidopsis. They show that the CUC genes are "universal dissectors" acting whatever the level of dissection of the leaf margin.

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Role of the KNAT6/2 genes in inflorescence patterning.

To investigate the role of KNAT6 and KNAT2 in the inflorescence, we examined their genetic interactions with BREVIPEDICELLUS/KNAT1 (BP/KNAT1) and PENNYWISE (PNY) two regulators of inflorescence patterning. BP/KNAT1 plays a primary role in inflorescence growth, and PNY is required to maintain the proper phyllotaxy. Both BP and PNY proteins interact to regulate inflorescence patterning. The defects in internode patterning typical of mutations in BP, were partially suppressed in the bp knat6 double mutant. Similarly, the pny phyllotaxy defects were suppressed in the pny knat6 double mutant, and were mainly attributable to the misexpression of KNAT6 and to a lesser extent of KNAT2 in the inflorescence. Our data showed antagonistic interactions of KNAT6 and KNAT2 with BP and PNY in the inflorescence (Ragni 2008).


Role of the KNAT6/2 genes in organ abscission.

Floral organ abscission involves several steps, including differentiation of the abscission zone, cell separation and differentiation of a protective layer following organ abscission. This process involves enzymes associated with modification of the cell wall, such as PGs, EGases, pectin methylesterases, pectate lyases,and expansins. In collaboration with Melinka Butenko (University of Oslo, Norway, http://www.mn.uio.no/ibv/english/people/aca/melinka/), we discovered that the knat6 knat2 double mutant shows a delay in floral organ abscission when plants are under high light intensity conditions. We found that BP/KNAT1 is important in regulating the timing of floral abscission by controlling abscission zone cell size and by regulating negatively KNAT2 and KNAT6 (Shi 2011). This work confirms the antagonism between BP/KNAT1 and KNAT2/6, and the positive link between KNAT6/2 and enzyme activity associated with cell wall modifications.

Role of the KNAT6/2 genes in flower formation.

Current research focuses on the interaction of KNAT6/2 with Arabidopsis thaliana homeodomain1, ATH1, a TALE member, and BLADE-ON-PETIOLE1 (BOP1) and BOP2,two BTB-ankryin transcriptional coregulators, and their role in flower formation. This is  in collaboration with the group of Shelley Hepworth (University of British Columbia, Vancouver, Canada) and Marcel Proveniers (University of Utrecht, Netherlands)


Construction of new tools.

In order to allow inducible gene expression in specific domains, we have developed a collection of inducible lines expressing GFP in different meristem subdomains (Deveaux et al., 2003). This is based on the ethanol switch that we used previously to dissect the functions of UFO during flower development or to analyse miR164 function (Laufs et al., 2003, 2004). The system of inducible reporter expression under the control of specific
promoters, combined with the observation of living meristems (Grandjean et al., 2004), allow us to follow in vivo cell differentiation in the meristem.

 

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Selected Publications :

 

Biot E, Cortizo M, Burguet J, Kiss A, Oughou M, Maugarny-Cales A, Goncalves B, Adroher B, Andrey P, Boudaoud A, Laufs P (2016) Multiscale quantification of morphodynamics: MorphoLeaf, software for 2-D shape analysis. Development (PubMed) communiqué de presse INRA

Maugarny-Cales A, Goncalves B, Jouannic S, Melkonian M, Wong GK, Laufs P (2016) Apparition of the NAC transcription factors predates the emergence of land plants. Molecular Plant 9(9):1345-8 (PubMed)

Michalko J, Glanc M, Perrot-Rechenmann C, Friml J (2016) Strong morphological defects in conditional Arabidopsis abp1 knock-down mutants generated in absence of functional ABP1 protein. F1000Research 5: 86 (PubMed)

Maugarny A, Goncalves B, Arnaud N, Laufs P (2015) CUC Transcription Factors: To the Meristem and Beyond. In DH Gonzalez, ed, Plant Transcription factors. Academic Press (Link)

Hepworth SR, Pautot VA (2015) Beyond the Divide: Boundaries for Patterning and Stem Cell Regulation in Plants. Frontiers in plant science 6: 1052 (PubMed)

Goncalves B, Hasson A, Belcram K, Cortizo M, Morin H, Nikovics K, Vialette-Guiraud A, Takeda S, Aida M, Laufs P, Arnaud N (2015) A conserved role for CUP-SHAPED COTYLEDON genes during ovule development. Plant J 83: 732-742 (PubMed)

Khan M, Ragni L, Tabb P, Salasini BC, Chatfield S, Datla R, Lock J, Kuai X, Despres C, Proveniers M, Yongguo C, Xiang D, Morin H, Rulliere JP, Citerne S, Hepworth SR, Pautot V (2015) Repression of Lateral Organ Boundary Genes by PENNYWISE and POUND-FOOLISH Is Essential for Meristem Maintenance and Flowering in Arabidopsis. Plant Physiology 169: 2166-2186 (PubMed)

Arnaud N, Pautot V (2014) Ring the BELL and tie the KNOX: roles for TALEs in gynoecium development. Frontiers in plant science 5: 93 (PubMed)

Blein T, Pautot V, Laufs P (2013) Combinations of mutations sufficient to alter Arabidopsis leaf dissection. Plants 2: 230-247 (PubMed)

Goncalves B, Nougue O, Jabbour F, Ridel C, Morin H, Laufs P, Manicacci D, Damerval C (2013) An APETALA3 homolog controls both petal identity and floral meristem patterning in Nigella damascena L. (Ranunculaceae). Plant J doi: 10.1111/tpj.12284.(PubMed)

Bilsborough GD, Runions A, Barkoulas M, Jenkins HW, Hasson A, Galinha C, Laufs P, Hay A, Prusinkiewicz P, Tsiantis M (2011) Model for the regulation of Arabidopsis thaliana leaf margin development. Proc Natl Acad Sci U S A 108: 3424-3429 (PubMed)

Hasson A, Plessis A, Blein T, Adroher B, Grigg S, Tsiantis M, Boudaoud A, Damerval C, Laufs P (2011) Evolution and Diverse Roles of the CUP-SHAPED COTYLEDON Genes in Arabidopsis Leaf Development. Plant Cell 23: 54-68 (PubMed)

Shi CL, Stenvik GE, Vie AK, Bones AM, Pautot V, Proveniers M, Aalen RB, Butenko MA (2011) Arabidopsis Class I KNOTTED-Like Homeobox Proteins Act Downstream in the IDA-HAE/HSL2 Floral Abscission Signaling Pathway. Plant Cell 23: 2553:2567 (PubMed)

Blein T, Hasson A, Laufs P (2010) Leaf development: what it needs to be complex. Curr Opin Plant Biol 13: 75-82 (PubMed)

Hasson A, Blein T, Laufs P (2010) Leaving the meristem behind: the genetic and molecular control of leaf patterning and morphogenesis. C R Biol 333: 350-360 (PubMed)

Hamant O, Pautot V (2010) Plant development: a TALE story. C R Biol 333: 371-381 (PubMed)

Pulido A, Laufs P (2010) Co-ordination of developmental processes by small RNAs during leaf development. J Exp Bot 61: 1277-1291 (PubMed)

Blein T, Pulido A, Vialette-Guiraud A, Nikovics K, Morin H, Hay A, Johansen IE, Tsiantis M, Laufs P (2008) A conserved molecular framework for compound leaf development. Science 322: 1835-1839 (PubMed /-/ "News" in Nature)

Ragni L, Belles-Boix E, Gunl M, Pautot V (2008) Interaction of KNAT6 and KNAT2 with BREVIPEDICELLUS and PENNYWISE in Arabidopsis inflorescences. Plant Cell 20: 888-900 (PubMed)

Nikovics K, Blein T, Peaucelle A, Ishida T, Morin H, Aida M, and Laufs P. (2006) The balance between the MIR164A and CUC2 genes controls leaf margin serration in Arabidopsis Plant Cell, 18, 2929-45 (PubMed)

Belles-Boix, E., Hamant, O., Witiak, S. M., Morin, H., Traas, J. and Pautot, V. (2006). KNAT6: An Arabidopsis Homeobox Gene Involved in Meristem Activity and Organ Separation. Plant Cell, 18, 1900-1907 (PubMed)


Other publications

The inductible system ethanol and the lines promoters


 


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