Drought‐induced lacuna formation in the stem causes hydraulic conductance to decline before xylem embolism in Selaginella

Abstract

Summary Lycophytes are the earliest diverging extant lineage of vascular plants, sister to all other vascular plants. Given that most species are adapted to ever‐wet environments, it has been hypothesized that lycophytes, and by extension the common ancestor of all vascular plants, have few adaptations to drought. We investigated the responses to drought of key fitness‐related traits such as stomatal regulation, shoot hydraulic conductance (Kshoot) and stem xylem embolism resistance in Selaginella haematodes and S. pulcherrima, both native to tropical understory. During drought stomata in both species were found to close before declines in Kshoot, with a 50% loss of Kshoot occurring at −1.7 and −2.5 MPa in S. haematodes and S. pulcherrima, respectively. Direct observational methods revealed that the xylem of both species was resistant to embolism formation, with 50% of embolized xylem area occurring at −3.0 and −4.6 MPa in S. haematodes and S. pulcherrima, respectively. X‐ray microcomputed tomography images of stems revealed that the decline in Kshoot occurred with the formation of an air‐filled lacuna, disconnecting the central vascular cylinder from the cortex. We propose that embolism‐resistant xylem and large capacitance, provided by collapsing inner cortical cells, is essential for Selaginella survival during water deficit.

Desiccation and rehydration dynamics in the epiphytic resurrection fern Pleopeltis polypodioides

“…The extent of the lacunae remained unchanged for 12 h of dehydration (42.9% ±19.9 sd ), and increased to 55.6% (±7.1 sd ) after 24 h of dehydration, that is, over half of the stele separated from the surrounding cortex as the stipes dehydrated. Unlike in Selaginella ( Cardoso et al, 2020 ), we did not observe any trabeculae, endodermal cells that connect the cortex with the pericycle and the vasculature. Lacunae quickly disappeared as the pericycle and endodermis swelled to meet the cortex cells during the rehydration ( Figures 3 and 4 ).…”

Primary tissues may affect estimates of cavitation resistance in ferns

“…Recent studies have shown that the vascular strand pulls away from the surrounding parenchyma during later stages of dehydration, such that lacunae surround the phloem tissue (Holmlund et al ., 2019; Cardoso et al ., 2020), while the xylem remains functional (Cardoso et al ., 2020). It is conceivable that the phloem functions in a protective role to maintain hydraulic continuity in the xylem, which may otherwise be vulnerable to air‐seeding.…”

Abscisic Acid Biosynthesis and Signaling in Plants: Key Targets to Improve Water Use Efficiency and Drought Tolerance

“…Although increasing levels of foliar ABA has long been associated with stomatal closure and increases in WUE in angiosperm species during drought [1,38,67,70,71], it has recently been discovered that the stomata of ferns and lycophytes do not close in response to both endogenous and exogenous ABA [72][73][74]. Instead, in these early-diverging species, changes in leaf water status regulate stomatal aperture by an ABA-independent, hydropassive mechanism [72,75,76].…”