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

Anthony J Wenndt,Anne D Van Diepeningen,Sarah E Evans,Kathryn M Jacobson,J Robert Logan,Peter J Jacobson,Mary K Seely

doi:10.3389/fmicb.2021.691584

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.

Highlights

All perennial plants sampled to date harbor asymptomatic fungal endophytes in the apoplast of their stems, leaves and roots
Of the 20 identified taxa, the six most abundant species were found in both regions, collectively comprising 72% of all identified isolates: Aspergillus welwitschiae (15 isolates), Alternaria alternata (10), Chaetomium strumarium (9), Curvularia eragrostidis (7), Thielavia subthermophila (5), and Aspergillus amstelodami (3) (Figure 2A)
Our multi-pronged study yields strong evidence supporting the hypothesis that dryland plants tolerate complex endophyte communities in living tillers because these fungi initiate decomposition of standing tillers immediately post-senescence. Both nextgeneration sequencing (NGS)- and isolate-based sampling methods revealed that endophyte communities are abundant and species-rich in S. sabulicola stems throughout the Namib Sand Sea (NSS) (Tables 2, 3 and Figures 2A, 3)

Summary

Introduction

All perennial plants sampled to date harbor asymptomatic fungal endophytes in the apoplast of their stems, leaves and roots. Co-adaptive one-to-one relationships are wellknown between endophytes and their plant hosts: fungi play roles in ameliorating thermal, drought, soil disturbance and herbivory-related stresses (Porras-Alfaro and Bayman, 2011), offsetting the nutritional costs associated with supporting specific endosymbionts. Given the energetic costs associated with supporting endosymbionts in general, and the potential challenges of navigating relationships with multiple endophytic taxa, it is still unclear what benefits might accrue to plants from hosting diverse endophytic communities. While these dynamics have been relatively unexplored among endophytes, associations between mycorrhizal fungi and their plant hosts offer a useful parallel. We predicted that due to the moisture gradient, endophytic communities in the eastern region (∼65 mm/year) would be comparable to those in other drylands (Rosa et al, 2009; Sun et al, 2012; Massimo et al, 2015), but absent in the extreme environment of the western NSS (< 19mm/year) where plants appear to minimize their energetically costly interactions with microbial symbionts

Methods

Results

Conclusion