Abstract
Mycorrhizal fungi form mutualistic associations with the roots of most land plants and provide them with mineral nutrients from the soil in exchange for fixed carbon derived from photosynthesis. The common symbiosis pathway (CSP) is a conserved molecular signaling pathway in all plants capable of associating with arbuscular mycorrhizal fungi. It is required not only for arbuscular mycorrhizal symbiosis but also for rhizobia-legume and actinorhizal symbioses. Given its role in such diverse symbiotic associations, we hypothesized that the CSP also plays a role in ectomycorrhizal associations. We showed that the ectomycorrhizal fungus Laccaria bicolor produces an array of lipochitooligosaccharides (LCOs) that can trigger both root hair branching in legumes and, most importantly, calcium spiking in the host plant Populus in a CASTOR/POLLUX-dependent manner. Nonsulfated LCOs enhanced lateral root development in Populus in a calcium/calmodulin-dependent protein kinase (CCaMK)-dependent manner, and sulfated LCOs enhanced the colonization of Populus by L. bicolor. Compared with the wildtype Populus, the colonization of CASTOR/POLLUX and CCaMK RNA interference lines by L. bicolor was reduced. Our work demonstrates that similar to other root symbioses, L. bicolor uses the CSP for the full establishment of its mutualistic association with Populus.
| Original language | English |
|---|---|
| Pages (from-to) | 2386-2410 |
| Number of pages | 25 |
| Journal | Plant Cell |
| Volume | 31 |
| Issue number | 10 |
| DOIs | |
| State | Published - 2019 |
Funding
We thank Sarah Swanson for training and support with confocal microscopy techniques, Francis Martin for providing L. bicolor strain S238N, Giles Oldroyd for providing the binary vector pEC11579 carrying G-GECO, Fabienne Maillet for providing purified sLCOs and nsLCOs, and Hugues Driguez for providing synthetic LCO standards for mass spectrometry. Financial support for this project was primarily provided by the USDA (grant WIS01695) and National Science Foundation (NSF; grant DGE-1256259). Additional financial support was provided by the U.S. Department of Energy (DOE; grant DE-SC0018247) and NSF (grants 1546742 and 1331098) for partial analysis of Ca2+ spiking; the French Agence Nationale de la Recherche (contract ANR-14-CE18-0008-01) and the Laboratoire d’Excellence entitled TULIP (grant ANR-10-LABX-41) for the mass spectrometry analyses with additional support from the ICT-Mass Spectrometry and MetaToul facilities, and from the MetaboHUB-ANR-11-INBS-0010 network; the Tree Genomics and Biosafety Cooperative at Oregon State University and the NSF Center for Advanced Forestry Systems (grant 1238305) for partial support of RNAi line development; the Plant–Microbe Interfaces Scientific Focus Area in the Genomic Science Program, the Office of Biological and Environmental Research in the DOE Office of Science (Oak Ridge National Laboratory is managed by UT-Battelle, LLC, the DOE (contract DE-AC05-00OR22725) for the AM colonization assays; and from the USDA (grant 2017-67014-26530 to H.B.).