Microbial Ecology

, Volume 70, Issue 1, pp 61–76 | Cite as

Fungal Endophytes in Aboveground Tissues of Desert Plants: Infrequent in Culture, but Highly Diverse and Distinctive Symbionts

  • Nicholas C. Massimo
  • M. M. Nandi Devan
  • Kayla R. Arendt
  • Margaret H. Wilch
  • Jakob M. Riddle
  • Susan H. Furr
  • Cole Steen
  • Jana M. U’Ren
  • Dustin C. Sandberg
  • A. Elizabeth Arnold
Fungal Microbiology
First Online:
Received:
Accepted:

Abstract

In hot deserts, plants cope with aridity, high temperatures, and nutrient-poor soils with morphological and biochemical adaptations that encompass intimate microbial symbioses. Whereas the root microbiomes of arid-land plants have received increasing attention, factors influencing assemblages of symbionts in aboveground tissues have not been evaluated for many woody plants that flourish in desert environments. We evaluated the diversity, host affiliations, and distributions of endophytic fungi associated with photosynthetic tissues of desert trees and shrubs, focusing on nonsucculent woody plants in the species-rich Sonoran Desert. To inform our strength of inference, we evaluated the effects of two different nutrient media, incubation temperatures, and collection seasons on the apparent structure of endophyte assemblages. Analysis of >22,000 tissue segments revealed that endophytes were isolated four times more frequently from photosynthetic stems than leaves. Isolation frequency was lower than expected given the latitude of the study region and varied among species a function of sampling site and abiotic factors. However, endophytes were very species-rich and phylogenetically diverse, consistent with less arid sites of a similar latitudinal position. Community composition differed among host species, but not as a function of tissue type, sampling site, sampling month, or exposure. Estimates of abundance, diversity, and composition were not influenced by isolation medium or incubation temperature. Phylogenetic analyses of the most commonly isolated genus (Preussia) revealed multiple evolutionary origins of desert-plant endophytism and little phylogenetic structure with regard to seasonality, tissue preference, or optimal temperatures and nutrients for growth in vitro. Together, these results provide insight into endophytic symbioses in desert-plant communities and can be used to optimize strategies for capturing endophyte biodiversity at regional scales.

Keywords

Arid lands Ascomycota Diversity Dothideomycetes Fungi Larrea Phylogeny Parkinsonia Preussia Simmondsia Symbiosis 
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Notes

Acknowledgments

We thank the Western National Parks Association (MMND, SHF, NCM, AEA), the National Geographic Society (MMND, SHF, NCM, AEA), the National Institutes of Health (R01-CA90265, AEA), the National Science Foundation (DEB-1045766, AEA), Science Foundation Arizona (MHW), and the College of Agriculture and Life Sciences at the University of Arizona for supporting this research. For logistical support, we thank the staff of Saguaro National Park, especially Don Swann, Anna Iwaki, and Natasha Kline. We are particularly grateful to >400 citizen scientists who interacted with our research group at the National Geographic BioBlitz in Saguaro National Park, during which the first sampling was conducted (October 2011), and to ca. 120 students at Tucson High Magnet School, who contributed greatly to all aspects of the February 2012 sampling. For their help in working with students from Tucson High and contributing to our group’s BioBlitz outreach and research activities, we thank Brett Baxter, Lauren Dominick, Chan Jung, Adrian Ramirez, and Robert (Ethan) Posey. Support for our outreach and research activities with students and citizen scientists is gratefully acknowledged: the College of Agriculture and Life Sciences at the University of Arizona, the Robert L. Gilbertson Mycological Herbarium, and Tucson High Magnet School.

Supplementary material

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Supplementary Table 1 (XLS 68 kb)
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Supplementary Table 2 (XLS 37.0 kb)
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Supplementary Table 3 (XLS 225 kb)
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Supplementary Table 4 (XLSX 41 kb)

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Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Nicholas C. Massimo
    • 1
  • M. M. Nandi Devan
    • 2
  • Kayla R. Arendt
    • 1
  • Margaret H. Wilch
    • 3
  • Jakob M. Riddle
    • 1
  • Susan H. Furr
    • 1
  • Cole Steen
    • 1
  • Jana M. U’Ren
    • 1
  • Dustin C. Sandberg
    • 1
  • A. Elizabeth Arnold
    • 1
    • 2
  1. 1.School of Plant SciencesThe University of ArizonaTucsonUSA
  2. 2.Department of Ecology and Evolutionary BiologyThe University of ArizonaTucsonUSA
  3. 3.Tucson High Magnet SchoolTucsonUSA

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