Symbiosis: Enforced Surrender?

An international team of research scientists from INRA and Lorraine University in France, Oak Ridge National Laboratory in the USA and the Hawkesbury Institute for the Environment at the University of Western Sydney in Australia have discovered that beneficial symbiotic fungi, which improve the health and vigor of host plants, do so by nefarious means. During this mutually beneficial interaction, the fungus takes control of its host plant by injecting a small protein that neutralizes its immune defenses thereby allowing the fungus to colonise the plant. This finding is a major advance in our understanding of the evolution and functioning of symbiotic interactions between fungi and plants - relationships that play a significant role in supporting the health and sustainability of our natural ecosystems. Details of these results are published in the advance online edition of Proceedings of the National Academy of Sciences USA in May 2014.

In the complex world of the rhizosphere - the soil surrounding plant roots - thousands of species of bacteria and fungi compete for sugars released into the soil by the plant. Some fungi, such as truffles, have evolved the ability to live symbiotically within plant roots thereby by-passing their competitors to obtain sugars from the plant directly.  In return for this sugar source, symbiotic fungi promote the absorption of mineral nutrients by plant roots.  The increased nutrition for the plant improves its health, vigor and productivity. Mycorrhizal fungi are one class of symbiotic fungi that make their way to plant roots where they negotiate with the plant for real estate within the root and the all-you-can-eat sugar buffet provided there-in. But how does this negotiation play out?  Is the host plant able to distinguish between beneficial and parasitic fungi? How does the fungus avoid the plant immune defenses during the interaction? As it turns out, it's all about biochemical dialogue. Part of the molecular language used by mycorrhizal fungi has been partially decrypted through a global collaboration between INRA, Lorraine University, Oak Ridge National Laboratory and the University of Western Sydney.

The roots of plants are constantly releasing a diverse set of molecules into the soil environment surrounding the root system.  These molecules act as food for some organisms inhabiting the soil and also act to attract beneficial microbes that help the plant survive. In forest soils, one of these beneficial microbes is the ectomycorrhizal fungus Laccaria bicolor.  Once Laccaria perceives these plant molecules in the soil, it directs fungal growth toward the plant root.  The presence of a plant root also triggers the release of small proteins by the fungus. Generically termed 'efectors,' these small fungal proteins are bioactive molecular signals that prepare plant tissues for a symbiotic relationship. How these molecular signals prepare the plant host for symbiosis with an ectomycorrhizal fungus has remained clouded in mystery – until now.  MiSSP7, a molecular signal from Laccaria, was found by this research consortia to bind a plant molecular switch that controls plant immunity induced by the hormone jasmonic acid.  Normally, when a plant is confronted by a disease-causing microbe, jasmonic acid is one of the main hormones that immediately triggers a battery of defense reactions to kill off the invading organism. MiSSP7 neutralizes this defensive response by directly targeting the jasmonic acid-associated control switch of plant immunity.  By impeding the plants ability to raise an immune response, MiSSP7 buys time for the fungus to develop within plant tissue and establish a free trade market whereby mineral nutrients are traded in return for plant sugars.  These findings mean that beneficial microbes, rather than playing nice, are forcing themselves upon the plant and enacting a symbiotic relationship with the plant nefariously. Research is underway to identify if the other effector's of mycorrhizal fungi act similarly to control plant host function and force symbiosis.

Reference: 

The Effector MiSSP7 of the Mutualistic Fungus Laccaria bicolor Stabilizes the Populus JAZ6 Protein and Represses JA-responsive Genes. Proc Ntl Acad Sci – online Early Edition 00 mai 2014

Jonathan M. Plett, Yohann Daguerre, Sebastian Wittulsky, Alice Vayssieres, Aurelie Deveau, Sarah J. Melton, Annegret Kohler, Jennifer Morrell-Falvey, Annick Brun, Claire Veneault-Fourrey, Francis Martin

More information:
Dr Jonathan Plett - j.plett@uws.edu.au
Media: Mr David Thompson - d.thompson@uws.edu.au - +61 2 4570 1623

Related article: phys.org/news/2014-05-symbiosis-surrender.html

Provided by University of Western Sydney - Hawkesbury Institute for the Environment