The productivity of modern land plants is coupled to the structure and function of the plant vascular system. Specifically, it is the xylem tissue that determines the efficiency of water transport in higher plants. A great deal is known about the structure-function trade-offs that limit water transport in woody taxa, and yet very little work has examined the vascular performance of their relatives, the ferns. Like conifer wood, fern xylem is primarily comprised of single-celled, hollow conduits, but it is distinguished by the absence of wood and other key anatomical features that promote transport efficiency in conifers. What are the hydraulic and photosynthetic limitations imposed by this primitive type of primary xylem, and how can it inform our understanding of the evolution of vascular tissue? The goal of this project is to examine the structure and function of fern xylem using hydraulic, chemical and anatomical methods, across the fern evolutionary tree. These data will provide us with a deeper understanding of the evolution of plant vascular function, and will be used to model water transport in Archaeopteris, a Devonian conifer-fern hybrid representing the first modern tree. A second, long-term effort will monitor the morphology and physiology of local fern species in the redwood forest understory along a precipitation gradient spanning northern to central California. Fern frond size is directly related to water availability, and can serve as a convenient indicator of understory vegetation response in response to changes in precipitation. This field-based project aims to increase the participation of under-represented undergraduates in the natural sciences, inform students about climate change and build a long-term database of understory community structure in coastal California.
Intellectual Merit: In plants, efficient water transport is synonymous with higher rates of photosynthesis, growth and reproduction. Throughout the plant body, water moves through xylem tissue, a network of dead, hollow, tube-like cells (Figure 1). Much is known about the structure and function of xylem in woody plants but few studies have examined water transport in seed-free vascular plants such as ferns and lycopods. Ancestral to conifers and angiosperms, seed-free vascular plants make their first appearance in the Early Devonian and manage to persist for over 400 million years through periods of climate change and the appearance of seed plants. Yet despite their impressive history and their high species estimates, ferns and lycopods have been perceived as less adaptive and less successful than trees and flowering plants. However, one could just as well argue that these ancient lineages are incredibly resilient and that much remains to be learned about their physiology, specifically their ability to transport water and resist drought. That is indeed the goal of this research. Project Description: Earlier studies of fern physiology report low rates of water transport coupled with a low tolerance to drought, two attributes that presumably preclude seed-free plants from effectively competing with conifers and angiosperms for space, light and nutrients. However, the picture changes dramatically when temperate species such as bracken fern and chain fern are examined. By measuring water flow through frond petioles, our data show that these and other taxa exhibit high rates of water transport that are consistent with their large size and high demand for water. In several ferns, transport efficiencies are greater than the average rates of of conifers and angiosperms. Modern seed-free plants have no wood so how could so-called primitive plants possibly outperform more derived taxa? The answer lies in three attributes of the xylem tissue: 1) conduit size, 2) conduit arrangement and 3) the lateral permeability of conduit walls to water. Many temperate ferns have xylem conduits that are both wide (some over 100 microns) and long (up to several centimeters; Figure 1). Exceptional species such as bracken fern have vessels, the wide and long conduits that are found in angiosperm xylem. Since transport efficiency scales with conduit size, larger conduits are able to support higher flow rates. Secondly, these large, conductive cells are arranged in close proximity, which means that very little of the xylem volume is consumed by non-conductive cells. Lastly, our data indicate that the lateral permeability of fern conduits to water is surprisingly high, allowing water to move from one xylem conduit to another with little friction. Taken together, natural selection acted on fern and lycopod xylem tissue to increase transport efficiency in an otherwise ancestral, developmentally constrained vascular system. This may have allowed ferns and lycopods to retain a foothold in a world dominated by seed-plants. Seed-free vascular plants may have efficient xylem but they would not be able to persist without some degree of drought resistance. Water deficit can compromise water transport by allowing air to enter previously water-filled, functional xylem conduits. Once air-filled, embolized conduits are unable to transport water. Our research showed several fern species to be as resilient to embolism as woody plants, although the reasons behind this are complex. A significant finding was that the smaller the xylem conduit, the lower the likelihood that air will enter it. This implies that species with smaller conduits should be more resistant to embolism, and on the whole more tolerant of drought than species with large conduits. Furthermore, data from a companion study suggested that the arrangement of the xylem tissue within a frond may also influence patterns and rates of air spread. Altogether, our research indicates that seed-free vascular plants have highly functional xylem with respect to transport efficiency and resistance to water deficit. We hope our findings will inspire plant breeders looking for alternative approaches to generating hydraulic efficiency and drought tolerance in economically important plants. Broader Impacts: This project supported one post-doctoral scientist, one graduate student, five undergraduates, and produced seven publications. We also developed an annual outreach and data-collection activity in partnership with the non-profit conservation agency Save the Redwoods League (San Francisco, CA), in which local high school students collected spring-time data on the size and population density of redwood forest understory ferns for the League's Citizen Science initiative. The students had an opportunity to work with scientific instruments, take a guided tour of the campus redwood forests, learn about forests and climate change and also learn about the ecology of our Monterey Bay kelp 'forests' by touring the marine labs. This activity has recently been expanded to include two classroom modules that demonstrate the functional and anatomical aspects of plant water transport.
