New Phytologist Research Structure–function constraints of tracheid-based xylem: a comparison of conifers and ferns Jarmila Pittermann1, Emily Limm2, Christopher Rico1 and Mairgareth A. Christman3 1Department of Ecology and Evolutionary Biology, University of California, Santa Cruz, CA 95064, USA; 2Save the Redwoods League, 114 Sansome St Suite 1200, San Francisco, CA 94104, USA; 3Institute for Ecohydrology Research, 1111 Kennedy Place Suite 4, Davis, CA 95616, USA Summary Author for correspondence: • The ferns comprise one of the most ancient tracheophytic plant lineages, and Jarmila Pittermann occupy habitats ranging from tundra to deserts and the equatorial tropics. Like Tel: +1 831 459 1782 their nearest relatives the conifers, modern ferns possess tracheid-based xylem but Email: [email protected] the structure–function relationships of fern xylem are poorly understood. Received: 20 April 2011 • Here, we sampled the fronds (megaphylls) of 16 species across the fern phylo- Accepted: 6 June 2011 geny, and examined the relationships among hydraulic transport, drought-induced cavitation resistance, the xylem anatomy of the stipe, and the gas-exchange New Phytologist (2011) 192: 449–461 response of the pinnae. For comparison, the results are presented alongside a doi: 10.1111/j.1469-8137.2011.03817.x similar suite of conifer data. • Fern xylem is as resistant to cavitation as conifer xylem, but exhibits none of the hydraulic or structural trade-offs associated with resistance to cavitation. On a Key words: cavitation, gas exchange, hydraulic conductivity, primary xylem, conduit diameter basis, fern xylem can exhibit greater hydraulic efficiency than sporophytes, xylem evolution. conifer and angiosperm xylem. • In ferns, wide and long tracheids compensate in part for the lack of secondary xylem and allow ferns to exhibit transport rates on a par with those of conifers. We suspect that it is the arrangement of the primary xylem, in addition to the intrinsic traits of the conduits themselves, that may help explain the broad range of cavita- tion resistance in ferns. peaked with the appearance of the torus-margo pit mem- Introduction brane found in conifers, Gingko and some angiosperms The evolution of tracheid-based xylem in the Lower (Niklas, 1985; Sperry, 2003; Pittermann, 2010; Pittermann Devonian led to profound shifts in plant size and structure, et al., 2005; Jansen et al., 2004). The subsequent specializa- and marked the first appearance of tracheophytes, the tion of tracheids into fibers and vessels that characterized so-called true vascular plants (Pittermann, 2010; Kenrick the evolution of angiosperm wood allowed for a division of & Crane, 1997; Niklas, 1992; Bateman et al., 1998; Sperry, labor whereby short, narrow fibers provide mechanical sup- 2003). Tracheids preceded the widespread appearance of port while multicellular vessels function solely for water vessels by an estimated 150 million yr and served as the fun- transport (Bailey & Tupper, 1918; Carlquist, 1988). damental water transport tissue for some of the earliest land Although vessels may confer water transport efficiencies that plants, including Rhynia and Psilophyton, horsetails, ferns are well over three orders of magnitude greater than those of and the extinct arborescent lineages of the Late Devonian conifers (Tyree & Zimmermann, 2002; McCulloh et al., such as the lycopod Lepidodendron and pro-gymnosperms 2010), it is remarkable that tracheid-based xylem continues such as Archaeopteris (Cichan, 1985; Stewart & Rothwell, to serve as the primary transport tissue for two abundant and 1993; Taylor et al., 2009). Generally, the evolution of trac- diverse plant lineages, the conifers and the ferns. We know heids is characterized by increasing length and diameter that, on a xylem area basis, conifers and angiosperms can exhi- (particularly during the Devonian), greater deposition of bit similar hydraulic efficiencies (Pittermann et al., 2005), secondary cell wall material and progressive specialization in but how does the performance of the tracheid-based xylem of the inter-tracheid pit membranes, the complexity of which ferns compare with the more derived xylem of conifers? Ó 2011 The Authors New Phytologist (2011) 192: 449–461 449 New Phytologist Ó 2011 New Phytologist Trust www.newphytologist.com New 450 Research Phytologist Despite the extraordinary diversity and world-wide abun- tree ferns, produced secondary xylem from a polystelic dance of terrestrial and epiphytic ferns (Moran, 2008; arrangement of several bifacial vascular cambia (Cichan, Schuettpelz & Pryer, 2009), our understanding of the vas- 1986; Wilson et al., 2008; Taylor et al., 2009). Interestingly, cular performance of these primitive plants is just gaining a recent examination of two Botrychium species excluded momentum (Calkin et al., 1985; Veres, 1990; Brodribb the possibility that these ferns exhibit true cambial-derived et al., 2005; Watkins et al., 2010). Early work on water secondary growth, although the developmental pattern of transport in several fern species showed that the main axis their rhizomes is regarded as a departure from standard of the frond exhibits progressively lower hydraulic conduc- definitions of primary and secondary growth (Rothwell & tivities along its length as a result of a decrease in conduit Karrfalt, 2008). abundance and conduit size, especially from the start of the Tracheid-based xylem is common to both conifers and leafy rachis to the tip of the frond (Gibson et al., 1985; ferns, but key differences in xylem architecture have a pro- Schulte et al., 1987). These seemingly low rates of water found effect on the overall structure of these plants, as well transport were again reported in a broad sampling of tropi- as the physical principles that guide the shape and size of cal pteridophytes, a finding that was mirrored in the the xylem conduits. Most importantly, the evolution of a concurrently low rates of gas exchange (Brodribb & bifacial vascular cambium and the resultant secondary Holbrook, 2004, Brodribb et al., 2007, Watkins et al., xylem in conifers and woody angiosperms marked a radical 2010). Low transpiration rates are consistent with the pref- departure in the evolution of xylem function as well as over- erence of these tropical ferns for the low-light habitats all plant structure because it allowed plants to have the characteristic of forest understories and dense canopies: architectural flexibility to vary the height and horizontal dis- because understory plants may only experience brief photo- play of their foliage, an otherwise impossible endeavor in synthetic peaks during sunflecks, selection places a lower plants limited by a unifacial cambium or simple strands of premium on the evolution of high vascular and gas- primary xylem (Rowe & Speck, 2005; Spicer & Groover, exchange capacity in favor of a smaller sized, nonwoody, 2010). In conifers and pro-gymnosperms, the xylem slow-growing life form with reduced metabolic costs. There acquired the capacity not only to transport water to the leaf are, however, some exceptions to these generalizations, most canopy, but also to structurally support it (Meyer-Berthaud notably in the form of tree ferns, desert-dwelling ferns and et al., 1999; Tyree & Zimmermann, 2002; Pittermann the many temperate species that appear to thrive in a broad et al., 2006a,b; Sperry et al., 2006; Pittermann, 2010). variety of temperate high-light habitats, such as Pteridium Recent work has shown that, in north-temperate conifers, aquilinum and Blechnum chilense (Page, 2002; Saldana the combined requirements for canopy support along et al., 2007). Considering that several species of ferns, such with reinforced, implosion-resistant tracheids constrain the Lygodium microphyllum and P. aquilinum, can be highly maximum hydraulic efficiency of conifer xylem because of invasive (Robinson et al., 2010), it is not unreasonable to the necessity to build a strong, secondary cell wall coupled hypothesize that ferns are capable of high rates of water with a narrower lumen diameter (Pittermann et al., 2006a; transport and photosynthesis. Sperry et al., 2006). Both the cell size and the volume of The vascular system in both fern fronds and rhizomes the conduit wall are limited by the metabolic output of the consists of tracheids that tend to be longer and wider than developing xylem cell over the growing season, so it is those of conifers, with scalariform pitting extending along impossible for conifer tracheids to be long and wide and the entirety of at least one side of the tracheid wall (Gibson also sufficiently fortified to offer structural support et al., 1985; Veres, 1990; Carlquist & Schneider, 2001). (Pittermann et al., 2006a; Sperry et al., 2006). By contrast, Cryptic vessels have been reported in the rhizomes of several fern xylem is released from the structural support require- species on the basis of what appeared to be scalariform per- ment by virtue of the hypodermal sterome, a ring of foration plates in the terminal ends of vessel elements, but schlerenchyma fibers that surrounds the main axis of the their frequency in the ferns is now presumed to be much frond as well as the thicker secondary axes in some species lower than originally thought (Carlquist & Schneider, (Rowe & Speck, 2004; Rowe et al., 2004). This tissue 2001, 2007). Because water transport in ferns occurs exclu- supports the frond and provides it with a high degree of sively through primary vascular tissue, the xylem and flexural stiffness (Niklas, 1992;