An Integrative Study of Endophyte Symbioses: Environmental Change, Evolutionary Dynamics, and Leaf Colonization

Abstract

Fungi have evolved to encompass a diversity of strategies that collectively allow them to occupy the majority of earth’s ecosystems. Among these, endophytism is one of the most widespread and yet least well understood. Endophytes are fungi that live in plants without causing disease. These fungal symbionts are highly diverse and have been found in plants from tropical forests to hot deserts and arctic tundra. Even though endophytes are globally distributed as a whole, it is clear that environmental factors, interactions with potential hosts, and a variety of evolutionary processes together determine the content of endophyte communities at various geographic scales. Fragmentary sampling provides useful but limited information to our understanding of endophyte diversity, such that large-scale surveys that take into account major environmental factors are needed. Such work is urgent for documenting biodiversity in the context of climate change and other environmental shifts. At the same time, examining endophyte communities in the context of such shifts helps clarify how environmental factors shape endophyte assemblages, and how fungal lineages that contain endophytes arise and diversify relative to environment-driven selection. These broader dynamics of endophyte ecology and evolution reflect the foundational process of leaf colonization by fungi –– yet colonization has not been studied extensively nor visualized carefully in the most diverse and abundant plant lineages. In this dissertation, I used the dynamic history of wildfire in the southwestern USA to understand how endophyte communities differ as a function of time since pervasive environmental change. I then conducted a case study using exhaustive collections of endophytes to discover the biogeography and environmental factors relevant to endophyte community structure. To place these studies in an evolutionary context, I reconstructed ancestral states to understand the evolution of ecological modes in a focal class of fungi in which evolutionary processes of diversification appear to be particularly dynamic and endophytes are phylogenetically diverse. Finally, I used microscopy and inoculation experiments to observe the process of leaf colonization by endophytes, with a special focus on a model woody plant and members of three classes of Ascomycota. Together these studies reveal that pervasive environmental changes have significant and lasting effects on the diversity and community structure of endophytes; that endophyte community structure at a regional scale tracks the biogeographic structure of plant communities; that endophytes in a focal class have multiple origins from different ancestral states, consistent with their tremendous biodiversity and diversity of function; and that focal endophytes that sporulate prodigiously appear to colonize leaves and persist at low biomass by opportunistically entering leaf tissue and growing intercellularly. This integrative study extends our understanding of endophytes in terms of plant biology, forest ecology, community ecology, and evolution, and provides a perspective on one of the most widespread and important symbioses between plants and fungi.