Desiccation tolerance of Hymenophyllacea filmy ferns is mediated by constitutive and non-inducible cellular mechanisms

Garcés, Marcelo; Claverol, S.; Castillo, Carla Alvear; Pinilla, Claudia Rabert; Ramírez, León Bravo

doi:10.1016/j.crvi.2014.02.002

Cited by 29 publications

(11 citation statements)

References 25 publications

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“…However, unlike Hennequin et al (2008) we suggest that these habitats may have been conducive to epiphytic growth by or shortly after the middle-Triassic origin of the Hymenophyllaceae reported here. We believe that these ferns could have attained epiphytic growth earlier than previously hypothesized for three reasons: 1) recent work has provided evidence for the existence of complex forest ecosystems much earlier than previously thought (Cúneo et al, 2003, Stein et al, 2012; 2) many filmy fern species have been reported to be desiccation tolerant, especially among the primarily epiphytic Hymenophyllum clade (Shreve, 1911, Proctor, 2003, 2012, Cea et al, 2014; and 3) desiccation tolerance is an ancient (rather than highly derived) trait with deep homology that facilitated other major growth habit transitions in the plant kingdom, including the appearance of the first land plants (Oliver et al, 2000, 2005, Rensing et al, 2008.…”

Section: Divergence Time Estimatesmentioning

confidence: 75%

A 4000-species dataset provides new insight into the evolution of ferns

Testo

Sundue

2016

Molecular Phylogenetics and Evolution

228

278

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Ferns are the second-most diverse lineage of vascular plants on Earth, yet the best-sampled time-calibrated phylogeny of the group to date includes fewer than 5% of global diversity and was published seven years ago. We present a time-calibrated phylogeny that includes nearly half of extant fern diversity. Our results are evaluated in the context of previous studies and the fossil record, and we develop new hypotheses about the radiation of leptosporangiate ferns. We used sequence data from six chloroplast regions for nearly 4000 species of ferns to generate the most comprehensive phylogeny of the group ever published. We calibrate the phylogeny with twenty-six fossils and use an array of phylogenetic methods to resolve phylogenetic relationships, estimate divergence times, and infer speciation, extinction, and net diversification rates. We infer a mid-late Silurian origin for ferns (including horsetails) and an early Carboniferous origin for leptosporangiate ferns. Most derived fern families appeared in the Cretaceous and persisted for millions of years before rapidly diversifying in the Cenozoic. We find no evidence of differential rates of diversification among terrestrial and epiphytic species. Our findings challenge previous hypotheses on the evolutionary history of ferns and present a new paradigm for their Cenozoic radiation. We estimate earlier divergences for most fern lineages than were reported in previous studies and provide evidence of extended persistence of major fern lineages prior to rapid diversification in the last fifty million years.

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Section: Divergence Time Estimatesmentioning

confidence: 75%

A 4000-species dataset provides new insight into the evolution of ferns

Testo

Sundue

2016

Molecular Phylogenetics and Evolution

228

278

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“…2.45 kPa) vs. -86 MPa (c. 1.25 kPa) when the ambient VPD is typically < c. 0.10 kPa and only rarely exceeds > 0.50 kPa. The recent finding of a constitutive mechanism for DT in filmy ferns (Cea et al 2014) supports the need for a relatively wide "safety margin," and similar (or even more extreme) levels of constitutive DT are well known in bryophytes (Oliver et al 1993). The conservative behavior of fern stomata, which lack a response to the plant stress hormone ABA, is well documented (Brodribb and McAdam 2011;Brodribb 2012, 2013).…”

Section: Filmy Fern Sporophytes Have a Wide Range Of Dtmentioning

confidence: 86%

“…Vegetative DT was a key innovation linked to the rise of early land plants, but is largely limited to non-vascular groups such as bryophytes and algae among extant plants. Filmy ferns have received considerable attention for their remarkable reversion to vegetative DT in the sporophyte phase (e.g., Cea et al 2014;Ostria-Gallardo et al 2020a;Proctor 2003;Shreve 1911). Yet, no previous study to our knowledge has evaluated parallel physiology of sporophytes and gametophytes of filmy ferns in relation to DT.…”

Section: Discussionmentioning

confidence: 99%

“…They found that species occurring at greater heights in the trees tended to have greater DT, higher photosynthetic capacity (A max ), and lower rates of evapotranspiration. A study using two species of Hymenophyllum demonstrated that DT in filmy ferns likely operates via a homoiochlorophyllous, constitutive mechanism, which is more similar to that of bryophytes than other drought-tolerant vascular plants, thus allowing filmy ferns to adjust to dry conditions extremely rapidly (Cea et al 2014). This was further supported by evidence that induced biomechanical mechanisms likely do not play a role in DT of filmy ferns (Fallard et al 2018; but see Mkhize et al 2020).…”

Section: Introductionmentioning

confidence: 94%

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Ecophysiological differentiation between life stages in filmy ferns (Hymenophyllaceae)

Nitta

Watkins

Holbrook

et al. 2021

Preprint

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Desiccation tolerance was a key trait that allowed plants to colonize land. However, little is known about the transition from desiccation tolerant non-vascular plants to desiccation sensitive vascular ones. Filmy ferns (Hymenophyllaceae) represent a useful system to investigate how water-stress strategies differ between non-vascular and vascular stages within a single organism because they have vascularized sporophytes and nonvascular gametophytes that are each capable of varying degrees of desiccation tolerance. To explore this, we surveyed sporophytes and gametophytes of 19 species (22 taxa including varieties) of filmy ferns on Moorea (French Polynesia) and used chlorophyll fluorescence to measure desiccation tolerance and light responses. We conducted phylogenetically informed analyses to identify differences in physiology between life stages and growth habits. Gametophytes had similar or less desiccation tolerance (ability to recover from 2 d desiccation at -86 MPa) and lower photosynthetic optima (maximum electron transport rate of photosystem II and light level at 95% of that rate) than sporophytes. Epiphytes were more tolerant of desiccation than terrestrial species in both generations. Despite their lack of greater physiological tolerances, gametophytes of several species occurred over a wider elevational range than conspecific sporophytes. Our results demonstrate that filmy fern gametophytes and sporophytes differ in their physiology and niche requirements, and point to the importance of microhabitat in shaping the evolution of water-use strategies in vascular plants.

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“…The proteomic approach seems to be the most suitable way to reveal the direct physiological processes involved in plant development [18]. The mechanisms involved in fern development and stress responses have been studied with proteomics approaches [19–21]. Previous studies on Blechnum spicant have found that female and male gametophytes have enrichment differences in proteins related to stress or defense, protein biosynthesis, and photosynthesis [22].…”

Section: Introductionmentioning

confidence: 99%

Proteomic analysis of gametophytic sex expression in the fern Ceratopteris thalictroides

Chen

Huang

et al. 2019

PLoS ONE

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Ceratopteris thalictroides , a model fern, has two kinds of gametophytes with different sex expression: male and hermaphrodite. Hermaphroditic gametophytes have one or several archegonia beneath the growing point and a few antheridia at the base or margin. Male gametophytes show a spoon-like shape with much longer than the width and produce many antheridia at the margin and surface. The results of chlorophyll fluorescence detection showed that the photochemical efficiency of hermaphrodites was higher than that of males. By using two-dimensional electrophoresis and mass spectrometry, the differentially abundant proteins in hermaphroditic and male gametophytes were identified. A total of 1136 ± 55 protein spots were detected in Coomassie-stained gels of proteins from hermaphroditic gametophytes, and 1130 ± 65 spots were detected in gels of proteins from male gametophytes. After annotation, 33 spots representing differentially abundant proteins were identified. Among these, proteins involved in photosynthesis and chaperone proteins were over-represented in hermaphrodites, whereas several proteins involved in metabolism were increased in male gametophytes in order to maintain their development under relatively nutritionally deficient conditions. Furthermore, the differentially abundant cytoskeletal proteins detected in this study, such as centrin and actin, may be involved in the formation of sexual organs and are directly related to sex expression. These differentially abundant proteins are important for maintaining the development of gametophytes of different sexes in C . thalictroides .

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Desiccation tolerance of Hymenophyllacea filmy ferns is mediated by constitutive and non-inducible cellular mechanisms

Cited by 29 publications

References 25 publications

A 4000-species dataset provides new insight into the evolution of ferns

A 4000-species dataset provides new insight into the evolution of ferns

Ecophysiological differentiation between life stages in filmy ferns (Hymenophyllaceae)

Proteomic analysis of gametophytic sex expression in the fern Ceratopteris thalictroides

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