Physiological and ultrastructural characterisation of a desiccation‐tolerant filmy fern, Hymenophyllum caudiculatum: Influence of translational regulation and ABA on recovery

Abstract

The filmy fern Hymenophyllum caudiculatum can lose 60% of its relative water content, remain dry for some time and recover 88% of photochemical efficiency after 30 min of rehydration. Little is known about the protective strategies and regulation of the cellular rehydration process in this filmy fern species. The aim of this study was to characterise the filmy fern ultrastructure during a desiccation-rehydration cycle, and measure the physiological effects of transcription/translation inhibitors and ABA during desiccation recovery. Confocal and transmission electron microscopy were used to compare changes in structure during fast or slow desiccation. Transcription (actinomycin D) and translation (cycloheximide) inhibitors and ABA were used to compare photochemical efficiency during desiccation recovery. Cell structure was conserved during slow desiccation and rehydration, constitutive properties of the cell wall, allowing invagination and folding of the membranes and an important change in chloroplast size. The use of a translational inhibitor impeded recovery of photochemical efficiency during the first 80 min of rehydration, but the transcriptional inhibitor had no effect. Exogenous ABA delayed photochemical inactivation, and endogenous ABA levels decreased during desiccation and rehydration. Frond curling and chloroplast movements are possible strategies to avoid photodamage. Constitutive membrane plasticity and rapid cellular repair can be adaptations evolved to tolerate a rapid recovery during rehydration. Further research is required to explore the importance of existing mRNAs during the first minutes of recovery, and ABA function during desiccation of H. caudiculatum.

Changes in photosynthetic rate and stress volatile emissions through desiccation‐rehydration cycles in desiccation‐tolerant epiphytic filmy ferns (Hymenophyllaceae)

“…In the angiosperm X. humilis (Beckett et al, 2012), the enhanced hexanal emission under desiccation stress was hypothesized to be associated with thylakoid disassembly into membranous vesicles (Farrant, 2000), and this was likely responsible for delayed recovery of photosynthesis upon rehydration (Beckett et al, 2012;Tuba, Lichtenthaler, Csintalan, & Pocs, 1993;Tuba, Lichtenthaler, Maroti, et al, 1993;Tuba, Lichtenthaler, Csintalan, Nagy, & Szente, 1996). In Hymenophyllaceae, chloroplast movements toward the cell walls and chloroplast size reduction have been reported (Garcés et al, 2018), and both these changes can contribute to avoidance of overexcitation of thylakoids. However, modifications in chloroplast ultrastructure are much less pronounced in filmy ferns Garcés Cea et al, 2014).…”

“…Physiological changes are further accompanied by cell shrinkage and ultrastructural alterations in cell walls and chloroplasts as well as in chemical modifications in cell wall polysaccharides and associated proteins (Bravo et al, ). Once rewatered, physiological, ultrastructural, and chemical changes are rapidly, within tens of minutes to a few hours, reversed (Bravo et al, ; Garcés, Ulloa, Miranda, & Bravo, ), implying that the filmy ferns have a very high constitutive capacity to cope with recurrent desiccation–rewatering cycles, a strategy called homoiochlorophyllous (Bravo et al, ; Garcés Cea, Claverol, Alvear Castillo, Rabert Pinill, & Bravo Ramírez, ).…”

Multi‐Omics Insights into the Evolution of Angiosperm Resurrection Plants

“…Germination of A. thaliana seeds is prevented by cycloheximide treatment, an inhibitor of protein synthesis, but not by the transcriptional inhibitor a-amanitin (Rajjou et al, 2004). Similarly, though recovery of the poikilochlorophyllous resurrection plant X. humilis and the VDT fern Hymenophyllum caudiculatum requires translation, inhibition of transcription by actinomycin-D has no effect (Dace et al, 1998;Garcés et al, 2017). The homoichlorophyllous resurrection plant C. wilmsii, when dried slowly, can recover almost completely in the presence of both transcriptional and translational inhibitors, though protein synthesis is required for recovery from rapid desiccation (Cooper, 2002).…”

Canopy leaf area index at its higher end: dissection of structural controls from leaf to canopy scales in bryophytes

“…In addition, in pteridophytes, the gametophyte is often very thin and can be unistratose, especially at the margins (Yatskievych, 2003). Furthermore, in hymenophyllous ferns, the sporophyte is typically unistratose (Garc es et al, 2018). At the other extreme, leaves in several vascular plants, such as succulents or conifers, can be extremely thick from sub-millimeter to centimeter range (Niinemets, 1999), and there is a debate over how to measure LAI in such species (Chen & Black, 1992).…”