Why Plants Harbor Complex Endophytic Fungal Communities: Insights From Perennial Bunchgrass Stipagrostis sabulicola in the Namib Sand Sea

Abstract

All perennial plants harbor diverse endophytic fungal communities, but why they tolerate these complex asymptomatic symbioses is unknown. Using a multi-pronged approach, we conclusively found that a dryland grass supports endophyte communities comprised predominantly of latent saprophytes that can enhance localized nutrient recycling after senescence. A perennial bunchgrass, Stipagrostis sabulicola, which persists along a gradient of extreme abiotic stress in the hyper-arid Namib Sand Sea, was the focal point of our study. Living tillers yielded 20 fungal endophyte taxa, 80% of which decomposed host litter during a 28-day laboratory decomposition assay. During a 6-month field experiment, tillers with endophytes decomposed twice as fast as sterilized tillers, consistent with the laboratory assay. Furthermore, profiling the community active during decomposition using next-generation sequencing revealed that 59–70% of the S. sabulicola endophyte community is comprised of latent saprophytes, and these dual-niche fungi still constitute a large proportion (58–62%) of the litter community more than a year after senescence. This study provides multiple lines of evidence that the fungal communities that initiate decomposition of standing litter develop in living plants, thus providing a plausible explanation for why plants harbor complex endophyte communities. Using frequent overnight non-rainfall moisture events (fog, dew, high humidity), these latent saprophytes can initiate decomposition of standing litter immediately after tiller senescence, thus maximizing the likelihood that plant-bound nutrients are recycled in situ and contribute to the nutrient island effect that is prevalent in drylands.