Desiccation Mitigates Heat Stress in the Resurrection Fern, Pleopeltis polypodioides

Abstract

Although heat and desiccation stresses often coincide, the response to heat especially in desiccation tolerant plants is rarely studied. We subjected hydrated Pleopeltis polypodioides fronds to temperatures up to 50°C and dehydrated fronds up to 65°C for 24 h. The effect of heat stress was evaluated using morphological changes, photosystem (PS) II efficiency, and metabolic indicators. Pinnae of dried fronds exposed to more than 40°C curled tighter and became brittle compared to fronds dried at lower temperatures. Exposure to > 50°C leads to discolored fronds after rehydration. Hydrated fronds turned partially brown at > 35°C. Chlorophyll fluorescence (Ft) and quantum yield (Qy) increased following re-hydration but the recovery process after 40°C treatment lasted longer than at lower temperatures. Similarly, hydrated fronds showed reduced Qy when exposed to > 40°C. Dried and hydrated fronds remained metabolically active up to 40°C. Hydroperoxides and lipid hydroperoxides in dried samples remained high up to 50°C, but decreased in hydrated fronds at > 40°C. Catalase (CAT) and glutathione (GSH) oxidizing activities remained high up to 40°C in dehydrated fronds and up to 35°C in hydrated fronds. Major fatty acids detected in both dehydrated and hydrated fronds included palmitic (C16:0) and stearic (C18:0) acids, oleic (18:1), linoleic (C18:2); and linolenic (C18:3) acids. Linolenic acid was most abundant. In dried fronds, all fatty acids decreased at > 35°C. The combined data indicate that the thermotolerance of dry fronds is about 55°C but is at least 10°C lower for hydrated fronds.

Desiccation and rehydration dynamics in the epiphytic resurrection fern Pleopeltis polypodioides

“…Recovery of photosynthesis is tightly coupled to both relative water content (RWC) and relative humidity ( Stuart, 1968 ), and established modes of rehydration occur via either the rhizome or by foliar water uptake ( John and Hasenstein, 2017 ). Both pathways have their own temporal dynamics and biochemical and anatomical adaptations, yet rhizome recovery is slower (John and Hasenstein, 2017 , 2020 ).…”

Non‐chlorophyllous and crypto‐chlorophyllous fern spores differ in their mobilisation of fatty acids during priming

“…Additionally, the unsaturated fatty acids increase also protect the photosynthetic apparatus from damage (Gombos et al, 1994;John & Hasenstein, 2020). & Stetler, 1985;Gemmrich, 1977a;Raghavan, 1989;Seilheimer, 1978), but these changes are not clearly related to the biochemical changes occurring in the dark before germination, as in Daucus carota seeds during the imbibition (Zhao et al, 2021).…”

“…In the homoiochlorophylly found in desiccation‐tolerant plant species, chlorophyll is retained after tissues or cells dehydration and reconstituted during rehydration (Shivaraj et al, 2021 ; Tuba et al, 1994 ; Tuba et al, 1998 ), as occurs in the homoiochlorophyllous sporophyte of Pleopeltis polypodioides (L.) E.G. Andrews & Windham (John & Hasenstein, 2018 , 2020 ; López‐Pozo et al, 2019 ). This might also occur in crypto‐chlorophyllous and chlorophyllous spores; thus, chlorophyll reconstitution and repair of organelles might occur simultaneously during Phase II of imbibition of the priming treatments.…”

“…Other processes linked to hydration–dehydration–rehydration treatments (as in priming treatments) might also explain the increase in fatty acids content observed after dehydration at the end of the priming treatments in Alsophila firma and S. horrida . In the homoiochlorophyllous P. polypodioides , an increase in fatty acids content after dehydration has been considered as (1) an adaptation aimed to prevent lipid peroxidation caused by the increase of reactive oxygen species (ROS) in the components of the pre‐existing photosynthetic apparatus, or (2) an adaptation to desiccation stress where fatty acids play a role of stress‐responsive metabolites in cell membranes, depending on temperature (John & Hasenstein, 2018 , 2020 ). Additionally, the unsaturated fatty acids increase also protect the photosynthetic apparatus from damage (Gombos et al, 1994 ; John & Hasenstein, 2020 ).…”

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

“…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.…”