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The Ecophysiology and Evolution of Mycoheterotrophic Plants in the Tribe Pyroleae (Ericaceae)

  • Author(s): Hynson, Nicole
  • Advisor(s): Bruns, Thomas D
  • et al.
Abstract

The original inspiration for this dissertation was to resolve the over two hundred year-old debate regarding the trophic nature of the leafless and non-photosynthetic species of Pyrola, Pyrola aphylla Sm. (Ericaceae). To do this, I integrated the use of molecular methods and the analysis of stable isotopes to examine the role of mycorrhizal fungi in the carbon acquisition strategies of P. aphylla as well as its closely related and leafy-green sister taxa P. picta Sm. and Chimaphila umbellata (L.) W. Bartram. My goals were to: 1) determine if P. aphylla was fully mycoheterotrophic and therefore dependent on mycorrhizal fungi to meet all of its carbon and nutrient demands (Chapter 1); 2) identify the mycorrhizal fungi associated with P. aphylla and P. picta (Chapter 2); 3) determine if P. picta and C. umbellata were partially mycoheterotrophic meeting their carbon demands both through photosynthesis and mycorrhizal fungi (Chapters 2 and 3) and; 4) examine the role of increased shade on the degree of mycoheterotrophy in P. picta and C. umbellata (Chapter 3).

The novel findings of this work include a new example of full mycoheterotrophy in Ericaceae based on the similarity of the carbon and nitrogen stable isotope values of P. aphylla to other full mycoheterotrophs that associate with ectomycorrhizal fungi. Surprisingly, unlike all other fully mycoheterotrophic plants within Ericaceae based on the DNA sequence analysis of the fungi associated with P. aphylla, this species has not specialized on a particular lineage of ectomycorrhizal fungi. Rather, P. aphylla associates with a phylogenetically broad suite ectomycorrhizal fungi and there is little to no overlap in fungal symbionts of this species across its geographic range. Pyrola picta was also found to associate with a diversity of ectomycorrhizal fungi indicating that fungal specificity is not necessarily a precursor to the loss of photosynthesis among mycoheterotrophic plants. Furthermore, both P. picta and C. umbellata have nitrogen stable isotope values that are indistinguishable from fully mycoheterotrophic species in Ericaceae, while their bulk leaf carbon stable isotope values are most similar to autotrophic plants in the forest understory. These findings led to the final experiment of this dissertation where leaf soluble sugars of P. picta and C. umbellata were extracted and analyzed for their carbon stable isotope values. This experiment was conducted on populations of P. picta and C. umbellata in the foothills of the Sierra Nevada Mountains in California. In the field, light availability and access to mycorrhizal networks were manipulated to determine if the degree of dependency on fungal carbon gains in the two test species increased under decreased light availability. This study revealed that P. picta and C. umbellata have disparate ecophysiologies that are potentially related to their C-acquisition strategies. Based on the out-put of an isotope mixing model C. umbellata showed no indications of mycoheterotrophy while P. picta is partially mycoheterotrophic, but a decrease in light availability did not significantly increase the fungal-C sink strength of this species.

Based on the outcomes of this dissertation, future work on mycoheterotrophic plants should include: examining within an coevolutionary framework the significance of fungal specificity for mycoheterotrophy, determining what factors-environmental or physiological, lead to the nitrogen stable isotope values of these plants, and gaining a better understanding of the biochemical pathways and transformations of carbon and nutrients in this symbiosis. The tribe Pyroleae provides a useful group with which to explore these lines of research, as it is the only group of eudicots found thus far that contains species across the spectrum from autotrophy to full mycoheterotrophy.

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