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Branching control in plants
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Keywords : Pisum sativum - Physcomitrella patens -  mutant - branching - meristem – long distance signaling - hormones - strigolactones – synthetic analogs – structure-activity relationship studies

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
Catherine Rameau

Senior scientist

Jean-Paul Pillot
Technician

 

Sandrine Bonhomme
Research Scientist

Beate Hoffmann
Assistant Engineer

Alexandre de Saint-Germain
Post-Doc

Alexandre.De-Saint-Germain@inra.fr

 

Summary :

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Figure 1: Strigolactone chemical structure

Strigolactones (SLs) are the most recent discovered plant hormones (Gomez-Roldan et al., 2008 ) for their role in the control of shoot branching. SL-deficient mutants or not responding to SLs are highly branched (Figure 2). SLs, not only repress axillary bud outgrowth located at most leaf axils, but also stimulate secondary growth of stem, plant height and control root architecture. These molecules were already known for their roles in the rhizosphere. SLs are mainly produced by plant roots and exuded in the rhizosphere where they are involved in the establishment of the arbuscular mycorrhizal symbiosis between soil fungi and more than 80% of land plants (– see http://www.lrsv.ups-tlse.fr/?-Themes-de-recherche,80-&lang=en ). They also stimulate seed germination of the root parasitic plants, Striga and Orobanche and signal the presence of the host root – see http://www.sciences-techniques.univ-nantes.fr/91385/0/fiche___laboratoire/ . Their important role in the arbuscular mycorrhizal symbiosis suggests that SLs are very ancient molecules that may have played a crucial role in plant ecological adaptation to terrestrial environment more than 400 MY ago. We have shown that these molecules are also synthesized by the non-vascular plant, the moss Physcomitrella patens where they play a role in the communication between individuals and in the control of plant extension (Figure 3).
One objective of the laboratory is to have a better understanding of how the same group of molecules has been recruited during plant evolution for both chemical interactions between organisms and the control of plant architecture. Our work is based on 2 model plants, garden pea (Pisum sativum) and the moss Physcomitrella patens and the use of SL-biosynthesis and response mutants in both species (Figures 2 and 3). We use several approaches in the group where various expertises are represented (physiologists, geneticists, molecular biologists and organic chemists). We have a special partnership with the Institut de Chimie des Substances Naturelles (ICSN-CNRS Gif sur Yvette) (http://www.icsn.cnrs-gif.fr/ ) for chemistry, and with URGV d’Evry (http://www.versailles.inra.fr/urgv/ ) for TILLING in pea, and for transcriptomics.

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Figure 2 : Wild type pea (Pisum sativum) (left) and SL-deficient mutant (right)

Figure 3 : Wild type moss (Physcomitrella patens) (left) and SL-deficient mutant (right)

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Main Results :

 

Recent main results

SLs repress or stimulate growth according meristems (de Saint Germain et al., 2013b)

Another strong phenotype of SL-mutants together with their high branching is their reduced stature (Figure 2). After demonstrating that this dwarfism was not due to the high branching of the mutants, the objective of this work was to gain a better understanding of the effect of SLs on internode elongation in pea. Our results suggest that SLs stimulate internode elongation by controlling cell division, whereas other hormones controlling plant height (auxin, gibberellins, brassinosteroids) mainly affect cell elongation. Different approaches have been used to show that SLs act independently from gibberellins to stimulate internode elongation. Consequently it seems that SLs repress cell division of axillary meristems located at the axils of leaves while they stimulate cell division in both apical meristem and cambium.

Which part of the molecule is essential for SL bioactivity in the control of shoot branching? (Boyer et al., 2012)

We are interested by SL mode of action, their binding to the receptor and by the identification of more specific SL analogs. By a structure-activity relationship study, we have established the important structural motifs for hormonal activity (Figure 4). SL analogs with strong activity for the control of branching but with very low activity for seed germination of parasitic plants (Striga, Phelipanche, Orobanche) have been discovered (3 patents).

 

What is the function of SLs in a non-vascular plant? (Proust et al., 2011)

The moss Physcomitrella patens is a new model in plant biology due to the possibility of gene targeting by homologous recombination (http://moss.nibb.ac.jp/). This non-vascular plant belongs to Bryophytes which are considered as the extant lineage of the first land plants. The haploid gametophytic generation is predominant. With the identification and characterization of Physcomitrella patens mutants in homologues of SL-biosynthesis and response genes, we hope to bring major insights in both the evolution of function of this novel plant hormone and the origine of vascular plant shoot branching.
The identification and characterization of a SL-deficient mutant in moss showed that SLs control plant extension according their density on the media mainly by repressing cell division of caulonema, the filaments involved in radial extension of individuals.   

Figure 4 : SL structural motifs important for hormonal activity in the control of shoot branching in pea

   

 


Selected Publications :

Lopez-Obando M, Conn C, Hoffmann B, Bythell-Douglas R, David C. Nelson DC, Rameau C, Bonhomme S (2016)Structural modelling and transcriptional responses highlight a clade of PpKAI2-LIKE genes as candidate receptors for strigolactones in Physcomitrella patens. Planta  243:1441-53. (Pubmed)

de Saint Germain A, Clavé G, Badet-Denisot M-A, Pillot J-P, Cornu D, Le Caer J-P, Burger M, Pelissier F, Retailleau P, Turnbull C, Bonhomme S, Chory J, Rameau C and Boyer F-D (2016) An histidine covalent receptor and butenolide complex mediates strigolactone perception. Nature Chem Biol 12:787-94. doi: 10.1038/nchembio.2147. Epub 2016 Aug 1. (PubMed) communiqué de presse INRA

Lopez-Obando M, Hoffmann B, Géry C, Guyon-Debast A, Téoulé E, Rameau C, Bonhomme S, Nogué F. (2016) Simple and Efficient Targeting of Multiple Genes Through CRISPR-Cas9 in Physcomitrella patens. G3 (Bethesda). 2016 Sep 9. pii: g3.116.033266. doi: 10.1534/g3.116.033266. [Epub ahead of print] (Pubmed)

Kameoka H, Dun EA, Lopez-Obando M, Brewer PB, de Saint Germain A, Rameau C, Beveridge CA, Kyozuka J. (2016) Phloem transport of the receptor, DWARF14 protein, is required for full function of strigolactones.Plant Physiol. Sep 26. pii: pp.01212.2016. [Epub ahead of print] (PubMed)

Catherine Rameau, Jessica Bertheloot, Nathalie Leduc, Bruno Andrieu, Fabrice Foucher3 and Soulaiman Sakr (2015) Multiple pathways regulate shoot branching. Front Plant Sci. 2015 Jan 13;5:741. doi: 10.3389/fpls.2014.00741. eCollection 2014. (PubMed)

Lopez-Obando M, Ligerot Y, Bonhomme S, Boyer FD, Rameau C. (2015) Strigolactone biosynthesis and signaling in plant development. Development. Nov 1;142(21):3615-9. doi: 10.1242/dev.120006. (PubMed)

Boyer FD, de Saint Germain A, Pouvreau JB, Clavé G, Pillot JP, Roux A, Rasmussen A, Depuydt S, Lauressergues D, Frei Dit Frey N, Heugebaert TS, Stevens CV, Geelen D, Goormachtig S, Rameau C (2014) New strigolactone analogs as plant hormones with low activities in the rhizosphere. Mol Plant 7: 675-90 (PubMed)

Hoffmann B, Proust H, Belcram K, Labrune C, Boyer FD, Rameau C, Bonhomme S (2014) Strigolactones Inhibit Caulonema Elongation and Cell Division in the Moss Physcomitrella patens. PLoS One:9(6):e99206. doi: 10.1371(pdf)

de Saint Germain A, Bonhomme S, Boyer FD, Rameau C (2013a) Novel insights into strigolactone distribution and signalling. Curr Opin Plant Biol 16: 583-589 (pdf)

de Saint Germain A, Ligerot Y, Dun EA, Pillot JP, Ross JJ, Beveridge CA, Rameau C (2013b) Strigolactones stimulate internode elongation independently of gibberellins. Plant Physiol 163: 1012-25 (pubMed)

Bonhomme S, Nogue F, Rameau C, Schaefer DG (2013) Usefulness of Physcomitrella patens for studying plant organogenesis. Methods Mol Biol 959: 21-43 (pdf)

Chen VX, Boyer FD, Rameau C, Pillot JP, Vors JP, Beau JM (2013) New synthesis of A-ring aromatic strigolactone analogues and their evaluation as plant hormones in pea (Pisum sativum). Chemistry 19: 4849-4857 (pdf)

Boyer FD, de Saint Germain A, Pillot JP, Pouvreau JB, Chen VX, Ramos S, Stevenin A, Simier P, Delavault P, Beau JM, Rameau C (2012) Structure-activity relationship studies of strigolactone-related molecules for branching inhibition in garden pea: molecule design for shoot branching. Plant Physiol 159: 1524-1544 (pdf)

Braun N, de Saint Germain A, Pillot JP, Boutet-Mercey S, Dalmais M, Antoniadi I, Li X, Maia-Grondard A, Le Signor C, Bouteiller N, Luo D, Bendahmane A, Turnbull C, Rameau C (2012) The pea TCP transcription factor PsBRC1 acts downstream of strigolactones to control shoot branching. Pl Physiol 158:225–238 (pdf)

Proust H, Hoffmann B, Xie X, Yoneyama K, Schaefer DG, Nogue F, Rameau C (2011) Strigolactones regulate protonema branching and act as a quorum sensing-like signal in the moss Physcomitrella patens. Development 138: 1531-1539 (pdf)

Chen X, Boyer FD, Rameau C, Retailleau P, Vors JP, and Beau JM (2010). Stereochemistry, total synthesis, and biological evaluation of the new plant hormone solanacol. Chemistry 16, 13941-13945 (pdf)

Beveridge CA, Dun EA, and Rameau C (2009). Pea has its tendrils in branching discoveries spanning a century from auxin to strigolactones. Plant Physiol 151: 985-990 (pdf)

Gomez-Roldan, V., Fermas, S., Brewer, P.B., Puech-Pages, V., Dun, E.A., Pillot, J.P., Letisse, F., Matusova, R., Danoun, S., Portais, J.C., Bouwmeester, H., Becard, G., Beveridge, C.A., Rameau, C., and Rochange, S.F. (2008). Strigolactone inhibition of shoot branching. Nature 455: 189-194 (pdf)

Johnson, X., Brcich, T., Dun, E.A., Goussot, M., Haurogne, K., Beveridge, C.A., and Rameau, C. (2006). Branching genes are conserved across species. Genes controlling a novel signal in pea are coregulated by other long-distance signals. Plant Physiol 142: 1014-1026 (pdf)

 

Detailed list of Publications

 


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