Jean Dénarié on Molecular Signaling between Plants & Fungal Symbionts

Fast Breaking Papers Commentary, December 2011

Jean Dénarié
See group photo below.

Article: Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza

Authors: Maillet, F;Poinsot, V;Andre, O;Puech-Pages, V;Haouy, A;Gueunier, M;Cromer, L;Giraudet, D;Formey, D;Niebel, A;Martinez, EA;Driguez, H;Becard, G;Denarie, J
Journal: NATURE, Volume: 469, Issue: 7328, Page: 58-U1501, Year: JAN 6 2011
* CNRS, INRA 2594, UMR 441, Lab Interact Plantes Microorganismes, BP 52627, F-31326 Castanet Tolosan, France.
(Addresses have been truncated)

Jean Dénarié talks with and answers a few questions about this month's Fast Breaking Paper paper in the field of Plant & Animal Science.

SW: Why do you think your paper is highly cited?

Arbuscular mycorrhiza (AM) is a root endosymbiosis between plants and a specific group of soil fungi, the glomeromycetes. It is the most widespread plant symbiosis, improving plant uptake of water and mineral nutrients. During the last decade several reports indicated that the fungal partner is producing diffusible compound(s) which elicit plant symbiotic responses. The plant scientific community was waiting for the identification of these signals.

This paper describes the purification and characterization of such signals produced by the AM fungus Glomus intraradices. This finding is an important step in our understanding of early steps of mycorrhiza formation.

SW: Does it describe a new discovery, methodology, or synthesis of knowledge?

This paper describes a new discovery, concerning the molecular signaling between plants and their major fungal symbiont.

SW: Would you summarize the significance of your paper in layman's terms?

Most plants establish mycorrhizal symbiosis with a specific group of soil fungi which are able to penetrate into their roots and form arbuscules, symbiotic structures which allow an efficient metabolic exchange between the two partners. The host plant provides housing and energy to the microsymbiont and the fungus provides to its host water and mineral nutrients scavenged by the extended network of mycelium in the soil.

Jean Dénarié Jean Dénarié Jean Dénarié
The three photos above represent germinating spores of the AM fungus Glomus intraradices, developing an hyphen network around the host root. During this pre-infection step, molecular signals are exchanged between the two partners. Photo credit: Alexandra Haouy.

In this paper we describe the structure and biological activity of compounds, produced by a mycorrhizal fungus, which act as symbiotic signals on their host plants. These molecules stimulate root development and mycorrhiza formation. This opens the way to exploring the use of these very active natural molecules in agriculture.

SW: How did you become involved in this research, and how would you describe the particular challenges, setbacks, and successes that you've encountered along the way?

Twenty years ago we discovered symbiotic signals produced by rhizobia, nitrogen fixing soil bacteria, which elicit the formation of nodules on the roots of leguminous plants. These signals, called Nod factors (Nod for nodulation) were found to be lipo-chitooligosaccharides (LCOs). Trying to determine the chemical nature of symbiotic signals of a fungal root endosymbiotic organism was a very attractive challenge. After 4 years of hard work we discovered that these fungal signals are also LCOs.

The major difficulty of the project was the very low concentration of these signals in both mycorrhized root exudates (we used 300 liters of them) and germinating spore exudates. Fortunately, we had access to mass spectrometry apparatus of the last generation which are extremely sensitive and allowed the detection of tiny amounts of specific molecules in a complex mixture. Once analytical chemists had determined the chemical structure of candidate molecules, synthetic chemist colleagues in Grenoble managed to rapidly (two months) synthesize large amounts of these molecules, allowing the biologists of the project to test their biological activity on diverse bioassays.

Jean Dénarié
Left to right: Verena Poinsot (the mass spectrometry expert), Guillaume Becard (the mycorrhiza expert), and Jean Dénarié.

This project was clearly interdisciplinary and the success was due to the very close interactions between scientists of different and complementary expertise.

SW: Where do you see your research leading in the future?

The discovery of the chemical nature of a first type of Myc factors, fungal LCO metabolites, opens the way to dissecting the corresponding signaling pathway functioning in host plants. Molecular and cellular approaches will identify mechanisms involved in the perception and transduction of these fungal signals, leading to activation of the plant mycorrhizal program. Future research will try to identify other fungal symbiotic signals involved in early steps of AM formation.

The AM symbiosis is extremely ancient and appeared more than 400 million years ago. In contrast the root endosymbiosis associating rhizobial bacteria and legumes is more recent and estimated to have appeared about 60 million years ago. Interestingly, rhizobia produce symbiotic signals, the Nod factors, which belong to the same chemical family, LCOs. The finding that both fungal and bacterial symbiotic signals are LCOs support the hypothesis that the symbiotic signaling mechanisms involved in the rhizobium-legume associations derived in the course of evolution from pre-existing mycorrhizal signaling components. Future research will analyze by different approaches the evolution of symbiotic signaling.

SW: Do you foresee any social or political implications for your research?

Arbuscular mycorrhiza (AM) is the most widespread terrestrial plant symbiosis, formed by most crops, improving the uptake of water and mineral nutrients. In this paper we have shown that growing seedlings of species of various plant families in the presence of fungal LCOs can stimulate root development and/or formation of mycorrhiza. These results were obtained in laboratory conditions.

We are now addressing the question of the effects of Myc-LCOs on plant development and yield in agricultural conditions. In cooperation with an industrial partner, we are studying the effect of treating seeds of important crops such as cereals with Myc-LCOs. The objective is to stimulate the efficiency of mycorrhizal symbiosis to permit better plant nutrition and drought tolerance and contribute to the development of sustainable agricultural systems.End

Jean Dénarié
Emeritus research director
Laboratoire des Interactions Plantes-Microorganismes
Castanet-Tolosan, France



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