The phylogenomics of desiccation tolerance in the land plants (Visiting Scholar)
Life originated in water: our aquatic legacy is reflected in the fact that all living things require water for their survival. A few remarkable groups of organisms, however, have evolved the ability to survive near complete drying of their tissues. This rare trait, referred to as desiccation tolerance, is broadly distributed throughout the tree of life, and is generally restricted to very tiny organisms or life stages (resting cysts or spores, for example). In the plants, desiccation tolerance is fairly common the bryophytes (mosses, liverworts and hornworts), which are the modern-day descendants of the first plants that evolved on land. Through the course of land plant evolution, desiccation tolerance was lost in the increasingly large and complex vegetative bodies of plants, but was retained in their spores, pollen, and seeds. Remarkably, in the flowering plants, desiccation tolerance of the vegetative tissues has re-evolved at least 8 times. These plants, often called resurrection plants, represent the earths largest desiccation tolerant organisms, and they have captured the interest of the plant biotechnology industry due to the potential applications of desiccation tolerance for improving agriculturally important plants. My project at NESCent was motivated by the idea that evolution generally must act on existing genes and pathways, which means that novel traits are often cobbled together from genetic raw materials that originally played a different functional role. With this in mind, I focused on the resurrection plants and asked the question: if the complex trait of vegetative desiccation tolerance evolved independently in so many different flowering plant groups, was there a common function that the genes involved in desiccation tolerance were borrowed or co-opted from to produce this trait? To answer this question, I investigated the evolutionary relationships within several key gene families thought to be involved in desiccation tolerance, and used various estimation methods to trace their functional evolution throughout the history of the land plants. Two functions, seed maturation and stress tolerance, emerged as potential alternative sources for genes co-opted for desiccation tolerance. My analyses supported the idea that the independent evolution of desiccation tolerance in the resurrection plants had occurred through the co-option of genes involved in seed and pollen development, highlighting the regulation of seed development as an area of focus for future research aimed at producing desiccation tolerance in the vegetative tissues of sensitive crop plants.