Desiccation Tolerance in Ferns: From the Unicellular Spore to the Multi-tissular Sporophyte

López‐Pozo, Marina; Fernández‐Marín, Beatriz; Garcı́a-Plazaola, José Ignacio; Ballesteros, Daniel

doi:10.1007/978-3-319-75103-0_19

Cited by 12 publications

(11 citation statements)

References 139 publications

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“…Moreover, structures within cells either dismantle or fortify during development and maturation. Changes to cell structures include folded cell walls, condensed chromatin and dismantled thylakoids of chloroplasts (Webb and Arnott, 1982; Vertucci and Farrant, 1995; Hoekstra, 2005; Carranco et al, 2010; Nagel et al, 2015; Sano et al, 2016; Arif et al, 2017; Leprince et al, 2017; Pereira Lima et al, 2017; López-Pozo et al, 2018). DT cells tend to be undifferentiated, having relatively small if any vacuoles and considerable deposits of dry matter reserves (Farrant et al, 1997; Pérez et al, 2012; Walters, 2015).…”

Section: Acquisition Of Dt and Longevitymentioning

confidence: 99%

“…The ability to survive desiccation is a common trait among seeds, pollen and fern spores. An estimated 90% of angiosperm species produce DT seeds (Wyse and Dickie, 2017), DT appears to be widespread among pollen of most plant families studied (Hoekstra, 2002; Franchi et al, 2011; Nebot et al, 2018) and most fern spores are DT (López-Pozo et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

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Dry architecture: towards the understanding of the variation of longevity in desiccation-tolerant germplasm

Ballesteros

Pritchard

Walters³

2020

Seed Sci. Res.

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Desiccation-tolerant (DT) plant germplasm (i.e. seeds, pollen and spores) survive drying to low moisture contents, when cytoplasm solidifies, forming a glass, and chemical reactions are slowed. DT germplasm may survive for long periods in this state, though inter-specific and intra-specific variation occurs and is not currently explained. Such variability has consequences for agriculture, forestry and biodiversity conservation. Longevity was previously considered in the context of morphological features, cellular constituents or habitat characteristics. We suggest, however, that a biophysical perspective, which considers the molecular organization – or structure – within dried cytoplasm, can provide a more integrated understanding of the fundamental mechanisms that control ageing rates, hence the variation of longevity among species and cell types. Based on biochemical composition and physical–chemical properties of dried materials, we explore three types of the interplay between structural conformations of dried cytoplasm and ageing: (1) cells that lack chlorophyll and contain few storage lipids may exhibit long shelf life, with ageing probably occurring through slow autoxidative processes within the glassy matrix as it relaxes; (2) cells with active chlorophyll may die quickly, possibly because they are prone to oxidative stress promoted by the photosynthetic pigments in the absence of metabolic water and (3) cells that lack chloroplasts but contain high storage lipids may die quickly during storage at −20°C, possibly because lipids crystallize and destabilize the glassy matrix. Understanding the complex variation in structural conformation in space and time may help to design strategies that increase longevity in germplasm with generally poor shelf life.

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Section: Acquisition Of Dt and Longevitymentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Dry architecture: towards the understanding of the variation of longevity in desiccation-tolerant germplasm

Ballesteros

Pritchard

Walters³

2020

Seed Sci. Res.

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“…it is estimated that around 90–95% of seeds are DT; Hong et al , Gaff and Oliver ), but its occurrence among photosynthetic tissues has a much more restricted distribution, particularly among tracheophytes (Alpert , Fernández‐Marín et al , López‐Pozo et al ). DT in photosynthetic tissues is quite frequent among lichens and bryophytes, uncommon among pteridophytes, not reported in gymnosperms, and is very rare (135 species) among angiosperms, the latter referred to as ‘resurrection plants’ (Gaff , , Porembski , Gaff and Oliver , Fernández‐Marín et al , Farrant et al , López‐Pozo et al ). Only a few monocots among DT plants degrade chlorophyll and dismantle the photosynthetic apparatus in a reversible manner during dehydration, the so‐called poikilochlorophyllous species (Tuba and Lichtenthaler , Fernández‐Marín et al ).…”

Section: Introductionmentioning

confidence: 99%

A field portable method for the semi‐quantitative estimation of dehydration tolerance of photosynthetic tissues across distantly related land plants

López‐Pozo

Flexas

Gulías

et al. 2019

Physiologia Plantarum

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Desiccation tolerant (DT) plants withstand complete cellular dehydration, reaching relative water contents (RWC) below 30% in their photosynthetic tissues. Desiccation sensitive (DS) plants exhibit different degrees of dehydration tolerance (DHT), never surviving water loss >70%. To date, no procedure for the quantitative evaluation of DHT extent exists that is able to discriminate DS species with differing degrees of DHT from truly DT plants. We developed a simple, feasible and portable protocol to differentiate between DT and different degrees of DHT in the photosynthetic tissues of seed plants and between fast desiccation (< 24 h) tolerant (FDT) and sensitive (FDS) bryophytes. The protocol is based on (1) controlled desiccation inside Falcon tubes equilibrated at three different relative humidities that, consequently, induce three different speeds and extents of dehydration and (2) an evaluation of the average percentage of maximal photochemical efficiency of PSII (F v /fm) recovery after rehydration. Applying the method to 10 bryophytes and 28 tracheophytes from various locations, we found that (1) imbibition of absorbent material with concentrated salt-solutions inside the tubes provides stable relative humidity and avoids direct contact with samples; (2) for 50 ml capacity tubes, the optimal plant amount is 50-200 mg fresh weight; (3) the method is useful in remote locations due to minimal instrumental requirements; and (4) a threshold of 30% recovery of the initial F v /fm upon reaching RWC ≤ 30% correctly categorises DT species, with three exceptions: two poikilochlorophyllous species and one gymnosperm. The protocol provides a semi-quantitative expression of DHT that facilitates comparisons of species with different morpho-physiological traits and/or ecological attributes.

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“…Fern spores are generally DT, but their lifespan in the dry state may vary among species, probably due to different extents of DT (Ballesteros et al, 2017). Notwithstanding the above, most of them are non-CS (López-Pozo et al, 2018). Spores are the main dispersal structure in ferns.…”

Section: Introductionmentioning

confidence: 99%

“…The unicellular structure of CS makes them a good unicellular model to investigate DT and longevity in the dry state. The knowledge generated can be used to understand what happens in more complex systems, such as seeds and photosynthetic vegetative tissues, in which the presence of multiple cells and tissues can confound the interpretation of the results obtained (Ballesteros et al, 2017; López-Pozo et al, 2018; Ballesteros et al, 2019; López-Pozo et al, 2019). In addition, the intermediate position of ferns in the plant phylogeny (between the bryophytes and the seeded plants) can be useful to understand the evolution of DT across different plant lineages (López-Pozo et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

Desiccation Tolerance in Chlorophyllous Fern Spores: Are Ecophysiological Features Related to Environmental Conditions?

et al. 2019

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Fern spores of most species are desiccation tolerant (DT) and, in some cases, are photosynthetic at maturation, the so-called chlorophyllous spores (CS). The lifespan of CS in the dry state is very variable among species. The physiological, biochemical, and biophysical mechanisms underpinning this variability remain understudied and their interpretation from an ecophysiological approach virtually unexplored. In this study, we aimed at fulfilling this gap by assessing photochemical, hydric, and biophysical properties of CS from three temperate species with contrasting biological strategies and longevity in the dry state: Equisetum telmateia (spore maturation and release in spring, ultrashort lifespan), Osmunda regalis (spore maturation and release in summer, medium lifespan), Matteuccia struthiopteris (spore maturation and release in winter, medium-long lifespan). After subjection of CS to controlled drying treatments, results showed that the three species displayed different extents of DT. CS of E. telmateia rapidly lost viability after desiccation, while the other two withstood several dehydration–rehydration cycles without compromising viability. The extent of DT was in concordance with water availability in the sporulation season of each species. CS of O. regalis and M. struthiopteris carried out the characteristic quenching of chlorophyll fluorescence, widely displayed by other DT cryptogams during drying, and had higher tocopherol and proline contents. The turgor loss point of CS is also related to the extent of DT and to the sporulation season: lowest values were found in CS of M. struthiopteris and O. regalis. The hydrophobicity of spores in these two species was higher and probably related to the prevention of water absorption under unfavorable conditions. Molecular mobility, estimated by dynamic mechanical thermal analysis, confirmed an unstable glassy state in the spores of E. telmateia, directly related to the low DT, while the DT species entered in a stable glassy state when dried. Overall, our data revealed a DT syndrome related to the season of sporulation that was characterized by higher photoprotective potential, specific hydric properties, and lower molecular mobility in the dry state. Being unicellular haploid structures, CS represent not only a challenge for germplasm preservation (e.g., as these spores are prone to photooxidation) but also an excellent opportunity for studying mechanisms of DT in photosynthetic cells.

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Desiccation Tolerance in Ferns: From the Unicellular Spore to the Multi-tissular Sporophyte

Cited by 12 publications

References 139 publications

Dry architecture: towards the understanding of the variation of longevity in desiccation-tolerant germplasm

Dry architecture: towards the understanding of the variation of longevity in desiccation-tolerant germplasm

A field portable method for the semi‐quantitative estimation of dehydration tolerance of photosynthetic tissues across distantly related land plants

Desiccation Tolerance in Chlorophyllous Fern Spores: Are Ecophysiological Features Related to Environmental Conditions?

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