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Symbiotic signal perception and arbuscular mycorrhiza in non-legumes.
The arbuscular mycorrhizal (AM) symbiosis. Most plants including cereals form an endosymbiosis with AM fungi belonging to the group of Glomeromycota. AM fungi are beneficial for plants because of their ability to colonize both soil and roots and collect nutrients from a much higher soil volume than plant roots. AM fungi penetrate root cortical cells and exchange nutrients through structures called arbuscules. AM fungi provide soil nutrients (phosphorus, nitrogen and other nutrients) to plants and benefit from fixed carbon (photosynthates) from the plants through carbohydrate and lipid tranfers. AM fungi can also protect plants from biotic and abiotic stress. This interaction is described as a mutualistic symbiosis, however antagonistic effects on plant host growth can sometimes be observed.
A tomato root colonized by a strain of the AM fungus Rhizophagus irregularis. The fungus is stained by ink (blue). Arrows show arbuscules. Arrowheads show extraradical hyphae.
Our research: We are interested in understanding plant molecular mechanisms which influence 1/ host colonization by AM fungi and 2/ mycorrhizal growth response (which can positive or negative).
Plant models: In 2012, I initiated studies on model and crop plants including dicots: Nicotiana benthamiana and Solanum lycopersicum (tomato) and monocots: Brachypodium distachyon and Triticum aestivum (wheat).
A B. distachyon plant grown for 9 weeks in a growth chamber.
Note that Arabidopsis thaliana, a widely used plant model is one of the few plants unable to form the AM symbiosis.
Objective 1: To determine the role of signal molecules produced by AM fungi in the establishment of the symbiosis. Lipo-chitooligosaccharidic (LCO) and short chitooligosaccharidic (CO) produced by AM fungi are able to activate a host signalling pathway required for host colonization by AM fungi and thus LCOs and COs are likely involved in mechanisms of host colonization. Our strategy consists of the identification and characterization of plant LCO and CO receptors. Candidates belong to the family of Receptor-Like Kinases (RLKs) containing LysM domains. We are characterizing LCO or CO binding properties of LysM-RLKs using radiolabelled molecules or Microscale Thermophoresis. We are also determining the biological roles of these receptors by reverse genetic approaches. We also aim to purify LCO or CO binding proteins from membrane fractions and to identify them by mass spectrometry.
Objective 2: To identity the genetic determinants and the molecular mechanisms that control plant benefit from AM fungi. To address this objective, we are investigating the natural genetic variability of B. distachyon. This includes analysis of growth and transcriptional responses of plants to various AM fungal strains in various environments. The aim is to identify molecular mechanisms that are critical for mycorrhizal growth responses using quantitative genetic approaches. For this, we use the new Toulouse plant phenotyping platform to measure growth kinetics of various B. distachyon genotypes in the presence or the absence of AM fungi.
Objective 3: Characterize functional interactions between AM fungi and soil bacteria and measure effect of agricultural practices on AM fungal and associated bacterial communities. We have initiated a research program to explore the interactions between bacterial and AM fungal communities associated with wheat roots in fields, and their effects on plant benefit from AM fungi. To do this, we characterize the communities by metagenomic approaches and isolate bacterial and AM fungal strains associated with wheat roots. The growth of various wheat cultivars will be measured in the presence or the absence of combinations of isolated bacteria and AM fungi.
Benoit Lefebvre, researcher (DR2 INRA)
Yi Ding, PhD student (Chinese scholarship)
Margot Trinquier, PhD student (fellowship from Toulouse University - Région Occitanie), co-supervised by Christophe Roux (LRSV, Toulouse)
Tongming Wang, post-doc (fellowship from Southwest university, Chongqing, China)
Mégane Gaston, assistant IE (WHEATSYM grant)
Virginie Gasciolli, Technician
Marie Cumener, assistant IE (2012-2014)
Ariane Girardin, PhD student (2014-2017)
Tongming Wang, PhD student (2014-2018)
Claudia Bartoli, post-doc (2016-2018)
Luis Buendia, PhD student (2015-2018, co-supervision with S. Bensmihen)
Camille Ribeyre, assistant AI (2018-2019)
Project WHEATSYM (ANR, 2017-2021), coordinator: B. Lefebvre
Projet Stress'n'Sym (Institut Carnot Plant2Pro, 2017-2020), coordinator: B. Lefebvre
Project DIBAM (SPE INRA, 2018-2019), coordinator: B. Lefebvre
Projet RHIZOWHEAT (IDEX ATS, 2016-2017), coordinator: C. Masson (LIPM)
Projet SPE (INRA, 2014-2015), coordinator: J. Cullimore (LIPM)
Projet LCOinNONLEGUMES (ANR young scientist, 2011-2014), coordinator: B. Lefebvre
PICS (CNRS, 2011-2012), coordinator: B. Lefebvre
Recent Publications (2013-2018)
Lefebvre B. 2020. An opportunity to breed rice for improved benefits from the arbuscular mycorrhizal symbiosis? New Phytol, 225:1404-1406
Girardin A, Wang T, Ding Y, Keller J, Buendia L, Gaston M, Ribeyre C, Gasciolli V, Auriac MC, Vernié T, Bendahmane A, Ried MK, Parniske M, Vandenbussche M, Schorderet M, Reinhardt D, Delaux PM, Bono JJ and Lefebvre B. 2019. LCO receptors involved in arbuscular mycorrhiza are functional for rhizobia perception in legumes. Current Biol, 29: 4249-4259
Buendia L, Ribeyre C, Bensmihen S, Lefebvre B. 2019. Brachypodium distachyon tar2lhypo mutant shows reduced root developmental response to symbiotic signal but increased arbuscular mycorrhiza. Plant Signal Behav 14: e1651608.
Buendia L., Maillet F., O’Connor D., van de-Kerkhove Q., Danoun S., Gough C., Lefebvre B. and Bensmihen S. 2019. LCOs promote lateral root formation and modify auxin homeostasis in Brachypodium distachyon. New Phytol, 221: 2190-2202
Buendia L., Girardin A., Wang T., Cottret L. and Lefebvre B. 2018 LysM Receptor-Like Kinase and LysM Receptor-Like Protein Families: An Update on Phylogeny and Functional Characterization. Front. Plant Sci. 9:1531
Gough C., Cottret L., Lefebvre B. and Bono JJ. 2018. Evolutionary History of Plant LysM Receptor Proteins Related to Root Endosymbiosis. Front Plant Sci. 9:923
Lefebvre B. 2017. Arbuscular mycorrhiza: A new role for N-acetylglucosamine. Nature Plants 3, 17085
Vernié T., Camut S., Camps C., Rembliere C., de Carvalho-Niebel F., Mbengue M., Timmers T., Gasciolli V., Thompson R., Le Signor C., Lefebvre B., Cullimore J. and Hervé C. 2016. PUB1 interacts with the receptor kinase DMI2 and negatively regulates rhizobial and arbuscular mycorrhizal symbioses through its ubiquitination activity in Medicago truncatula. Plant Physiol 170: 2312-2324
Buendia L., Wang T., Girardin A. and Lefebvre B. 2016. The LysM receptor-like kinase SlLYK10 regulates the arbuscular mycorrhizal symbiosis in tomato. New Phytol 210, 184-195
Fliegmann J., Canova S., Lachaud C., Uhlenbroich S., Gasciolli V., Pichereaux C., Rossignol M., Rosenberg C., Cumener M., Pitorre D., Lefebvre B., Gough C., Samain E., Fort S., Driguez H., Vauzeilles B., Beau J.M., Nurisso A., Imberty A., Cullimore J. and Bono J.J. 2013. Lipo-chitooligosaccharidic symbiotic signals are recognized by the LysM receptor like kinase LYR3 in the legume Medicago truncatula. ACS Chemical Biology 8: 1900-1906
Pietraszewska-Bogiel A., Lefebvre B., Koini M.A., Klaus-Heisen D., Takken F.L.W., Geurts R., Cullimore J.V and Gadella T.W.J. 2013. Interaction of Medicago truncatula Lysin motif receptor-like kinases, NFP and LYK3, produced in Nicotiana benthamianaleaf induces a defence-like response. PlosOne 8(6):e65055
Park C.J., Sharma R., Lefebvre B., Canlas P.E, and Ronald P.C. 2013. Endoplasmic reticulum-quality control component SDF2 is essential for XA21-mediated immunity in rice. Plant Science 210:53-60