The physiological resilience of fern sporophytes and gametophytes: advances in water relations offer new insights into an old lineage

Abstract

Ferns are some of the oldest vascular plants in existence and they are the second most diverse lineage of tracheophytes next to angiosperms. Recent efforts to understand fern success have focused on the physiological capacity and stress tolerance of both the sporophyte and the gametophyte generations. In this review, we examine these insights through the lens of plant water relations, focusing primarily on the form and function of xylem tissue in the sporophyte, as well as the tolerance to and recovery from drought and desiccation stress in both stages of the fern life cycle. The absence of secondary xylem in ferns is compensated by selection for efficient primary xylem composed of large, closely arranged tracheids with permeable pit membranes. Protection from drought-induced hydraulic failure appears to arise from a combination of pit membrane traits and the arrangement of vascular bundles. Features such as tracheid-based xylem and variously sized megaphylls are shared between ferns and more derived lineages, and offer an opportunity to compare convergent and divergent hydraulic strategies critical to the success of xylem-bearing plants. Fern gametophytes show a high degree of desiccation tolerance but new evidence shows that morphological attributes in the gametophytes may facilitate water retention, though little work has addressed the ecological significance of this variation. We conclude with an emergent hypothesis that selection acted on the physiology of both the sporophyte and gametophyte generations in a synchronous manner that is consistent with selection for drought tolerance in the epiphytic niche, and the increasingly diverse habitats of the mid to late Cenozoic.

Xylem embolism refilling and resilience against drought‐induced mortality in woody plants: processes and trade‐offs

“…Plant hydraulic failure (catastrophic loss of hydraulic conductivity) is one of the major and widespread mechanistic causes of drought-induced mortality (Anderegg et al 2012;Nardini et al 2014). Much research has investigated how plants avoid hydraulic failure by preventing formation and spread of catastrophic xylem embolism (Brodribb and Cochard 2009;Pittermann et al 2013). However, recent research suggests the existence of a spectrum of strategies ranging from 'resistance' to 'recovery', with some plants coming remarkably close to hydraulic failure, but recovering once xylem tension is partially or fully relaxed (Ogasa et al 2013;Martorell et al 2014).…”

Cavitation Resistance in Seedless Vascular Plants: The Structure and Function of Interconduit Pit Membranes

“…When xylem sap tension exceeds the air-seeding threshold, air can be aspirated from an air-filled conduit into a functional water-filled conduit through perhaps a large, preexisting pore or one that is created by tension-induced membrane stress (Rockwell et al, 2014). Air seeding leads to cavitation and embolism formation, with emboli potentially propagating throughout the xylem network (Tyree and Sperry, 1988;Brodersen et al, 2013). So, on the one hand, pit membranes are critical to controlling the spread of air throughout the vascular network, while on the other hand, they must facilitate the efficient flow of water between conduits (Choat et al, 2008;Domec et al, 2008;Pittermann et al, 2010;Schulte, 2012).…”

“…Transport in seedless vascular plants presents an interesting conundrum because, with the exception of a handful of species, their primary xylem is composed of tracheids, the walls of which are occupied by homogenous pit membranes (Gibson et al, 1985;Carlquist andSchneider, 2001, 2007; but see Morrow and Dute, 1998, for torus-margo membranes in Botrychium spp.). At first pass, this combination of traits appears hydraulically maladaptive, but several studies have shown that ferns can exhibit transport capacities that are on par with more recently evolved plants Watkins et al, 2010;Pittermann et al, 2011Pittermann et al, , 2013Brodersen et al, 2012). Certainly, several taxa possess large-diameter, highly overlapping conduits, some even have vessels such as Pteridium aquilinum and many species have high conduit density, all of which could contribute to increased hydraulic efficiency Pittermann et al, 2011Pittermann et al, , 2013.…”

Orthodox Seeds and Resurrection Plants: Two of a Kind?

“…Resisting drought allowed these plants to invest more time and energy into growth and reproduction, overcoming the slow growth associated with DT. Less than 1% of the sporophytes of modern pteridophytes are desiccation tolerant (Pittermann et al, 2013). On the other hand, DT is widespread in the gametophytes of pteridophytes.…”