Desiccation and rehydration dynamics in the epiphytic resurrection fern Pleopeltis polypodioides

Abstract

The epiphytic resurrection—or desiccation-tolerant (DT)—fern Pleopeltis polypodioides can survive extreme desiccation and recover physiological activity within hours of rehydration. Yet, how epiphytic DT ferns coordinate between deterioration and recovery of their hydraulic and photosynthetic systems remains poorly understood. We examined the functional status of the leaf vascular system, chlorophyll fluorescence, and photosynthetic rate during desiccation and rehydration of P. polypodioides. Xylem tracheids in the stipe embolized within 3-4 hours during dehydration. When the leaf and rhizome received water, tracheids refilled after approximately 24 hours, which occurred along with dramatic structural changes in the stele. Photosynthetic rate and chlorophyll fluorescence recovered to pre-desiccation values within 12 hours of rehydration, regardless of whether fronds were connected to their rhizome. Our data show that the epiphytic DT fern P. polypodioides can utilize foliar water uptake to rehydrate the leaf mesophyll and recover photosynthesis despite a broken hydraulic connection to the rhizome.

A reduced role for water transport during the Cenozoic evolution of epiphytic Eupolypod ferns

“…A comparable mechanism may be occurring in the DT epiphytic fern, Pleopeltis polypodioides (Polypodiaceae), in which photosynthetic tissue is the first to rehydrate followed by xylem refilling (Prats & Brodersen, 2021). Lastly, rehydration via capillary action is expedited by more numerous, smaller vascular strands composed of narrow tracheids (Baer et al ., 2016; Holmlund et al ., 2019, 2020; Prats & Brodersen, 2021). By contrast, terrestrial Eupolypods, which are primarily in the Eu2 clade, appear to prioritize efficient water transport via larger vascular bundles containing wider conduits.…”

Changes in endogenous abscisic acid and stomata of the resurrection fern, Pleopeltis polypodioides, in response to de‐ and rehydration

“…The biosynthetic pathway of ABA in Pleopeltis is not known. However, the strong water uptake capacity of the fronds compared to rhizomes and roots and their ability to carry out photosynthetic and metabolic activities independent of the rhizome and roots (John and Hasenstein, 2018; Prats and Brodersen, 2021) indicates that ABA does not originate from roots but is synthesized in the fronds, similar to A. thaliana (Ikegami et al, 2009) and conifer leaves (McAdam and Brodribb, 2018). Furthermore, the response of ABA to de‐ and rehydration (Figure 2) strongly suggests that the ABA levels are sensitive to the changes in the water content.…”

“…The collapse of such cells has been documented in dehydrated P. polypodioides (Layton et al, 2010) and parallels embolisms in xylem tracheids (Zhang et al, 2016). Cavitation appears within 3 h and becomes prominent after 12 h of dehydration (Prats and Brodersen, 2021). The temporal coincidence between shape change, embolism, dehydration, and decreased ABA metabolism suggests a connection between these events.…”

“…Pleopeltis polypodioides (aka resurrection fern), a member of the Polypodiaceae, is an epiphytic and desiccation‐tolerant fern, which tolerates loss of ≥95% of the cellular water content and regains full metabolic activities within a few hours of rehydration (Pessin, 1924; Stuart, 1968; John and Hasenstein, 2017; Prats and Brodersen, 2021). Although there is growing information on the morphological and ecophysiological adaptation of Pleopeltis to desiccation (Pessin, 1924; Stuart, 1968; Helseth and Fischer, 2005; John and Hasenstein, 2017; Prats and Brodersen, 2021), biochemical and photosynthetic response to drought (Maslenkova and Homann, 2000; Georgieva and Maslenkova, 2001; Layton et al, 2010; John and Hasenstein, 2018) and to heat (John and Hasenstein, 2020), there is no information on the status of endogenous ABA levels and the response of stomata to dehydration.…”

Burning questions for a warming and changing world: 15 unknowns in plant abiotic stress

“…Indeed, new concepts are needed—there is no generally agreed definition for the time of death of an organ, tissue, or whole plant—and plants may be incredibly diverse in this death pattern ( Hammond and Adams, 2019 ). In many species, leaf cells are apparently damaged or killed by dehydration below the turgor loss point, but in resurrection plants, cells can recover completely ( Stuart, 1968 ; Alpert, 2000 ; Prats and Brodersen, 2021 ). In deciduous species, the leaves die first, and then the buds on the stem, but in some species, roots apparently die early on and spell the death of the plant ( Sack, 2004 ).…”