Pleoardoris graminearum, gen. et sp. nov., a new member of Pleosporales from North American Plains, its biogeography and effects on a foundation grass species

ABSTRACT

Diverse fungi colonize plant roots worldwide and include species from many orders of the phylum Ascomycota. These fungi include taxa with dark septate hyphae that colonize grass roots and may modulate plant responses to stress. We describe a novel group of fungal isolates and evaluate their effects on the grass Bouteloua gracilis in vitro. We isolated fungi from roots of six native grasses from 24 sites spanning replicated latitudinal gradients in the south-central US grasslands and characterized isolates phylogenetically using a genome analysis. We analyzed 14 isolates representing a novel clade within the family Montagnulaceae (order Pleosporales), here typified as Pleoardoris graminearum, closely related to the genera Didymocrea and Bimuria. This novel species produces asexual, light brown pycnidium-like conidioma, hyaline hyphae, and chlamydospores when cultured on quinoa and kiwicha agar. To evaluate its effects on B. gracilis, seeds were inoculated with one of three isolates (DS304, DS334, and DS1613) and incubated at 25 C for 20 d. We also tested the effect of volatile organic compounds (VOCs) produced by the same isolates on B. gracilis root and stem lengths. Isolates had variable effects on plant growth. One isolate increased B. gracilis root length up to 34% compared with uninoculated controls. VOCs produced by two isolates increased root and stem lengths (P < 0.05) compared with controls. Internal transcribed spacer ITS2 metabarcode data revealed that P. graminearum is distributed across a wide range of sites in North America (22 of 24 sites sampled), and its relative abundance is influenced by host species identity and latitude. Host species identity and site were the most important factors determining P. graminearum relative abundance in drought experiments at the Extreme Drought in the Grasslands Experiment (EDGE) sites. Variable responses of B. gracilis to inoculation highlight the potential importance of nonmycorrhizal root-associated fungi on plant survival in arid ecosystems.

KEYWORDS:

• Dark septate endophytes
• drought
• heat stress
• latitudinal gradient
• novel genus
• Pleosporales
• root-associated fungi
• 2 new taxa

ACKNOWLEDGMENTS

Isolation of Pleoardoris cultures was possible due to sampling efforts and processing by Anny Chung, Terri Billingsley Tobias, Terry Torres-Cruz, Cedric Ndinga-Muniania, Paris Salazar-Hamm, Shane Mason, and Adeyemi Olanrewaju. The authors would like to thank Aaron Jon Robinson for his support in the genome analysis as well as past and current members of the Fungal Ecology Laboratory at Western Illinois University for the help provided to process the samples.

DISCLOSURE STATEMENT

No potential conflict of interest was reported by the author(s).

SUPPLEMENTARY MATERIAL

Supplemental data for this article can be accessed online at https://doi.org/10.1080/00275514.2023.2258269.

Additional information

Funding

The research presented in this paper was supported by NSF-DEB no. 1457309 to Dr. Jumpponen, no. 1619935 to Dr. Herrera, no. 1457002 to Dr. Porras-Alfaro, and no. 1456955 to Dr. Rudgers, and by the U.S. Department of Energy (DOE) Biological and Environmental Research Division through Science Focus Area grants to Dr. Dunbar [F255LANL2018] and Dr. Cheryl Kuske [F260LANL2013]. This material is based upon work supported by the National Science Foundation (A.P.-A.). Any opinion, findings, and conclusions or recommendations expressed in this material are those of the author(s) and do not necessarily reflect the views of the National Science Foundation.