Moss antheridia are desiccation tolerant: Rehydration dynamics influence sperm release in <i>Bryum argenteum</i>

Stark, Lloyd R.; McLetchie, D. Nicholas; Greenwood, Joshua L.; Eppley, Sarah M.

doi:10.3732/ajb.1600026

Cited by 14 publications

(8 citation statements)

References 54 publications

(64 reference statements)

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“…The procedure to observe bryophyte sperms described in literature is to submerge the antheridia in water, wait for the release of white sperm masses, collect these with a micropipette, and observe them in a microscope counting chamber [23, 24, 26]. Attempting to use these methods with P. patens , we failed to observe the release of white sperm masses under a dissecting microscope (shown e.g.…”

Section: Resultsmentioning

confidence: 99%

“…Attempting to use these methods with P. patens , we failed to observe the release of white sperm masses under a dissecting microscope (shown e.g. in [24]) or motile spermatozoids. Paolillo [21] describes observing the release of sperms of Funaria hygrometrica (like P. patens a Funariaceae species) as “delicate and tedious” in comparison to e.g.…”

Section: Resultsmentioning

confidence: 99%

“…While the light-microscopic analysis of the sperms is documented in many moss species, e.g. [19–24], and has become a recent focus in the liverwort Marchantia polymorpha [25, 26], the methodology is not established for P. patens . We assume the lack of detailed protocols is the major obstacle preventing research on P. patens sperms and discuss possible reasons so far hindering the establishment of suitable protocols.…”

Section: Introductionmentioning

confidence: 99%

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Microscopy of Physcomitrella patens sperm cells

Horst

Reski

2017

Plant Methods

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BackgroundArchegoniates (bryophytes, ferns and gymnosperms), such as the moss Physcomitrella patens, possess freely motile sperm cells (spermatozoids) which reach the egg cell via surface water. Although these motile flagellated sperm cells are a traditional botanical subject, they have not been thoroughly analysed in the flagship non-seed plant model species P. patens. Protocols are required to determine the behaviour of wild type sperms as a prerequisite for future research such as the characterization of mutants or factors that influence sperm number, morphology, viability and motility.ResultsHere, we present protocols for the observation of fixed, as well as live sperms utilizing a standard microscope at intermediate magnifications. Fixed samples can be used for the fast assessment of sperm number and morphology. To determine functionality, the observation of live sperms is required. Protocols for determining both sperm motility and viability are provided, allowing both parameters to be distinguished.ConclusionsThese step-by-step protocols are particularly useful for researchers so far not familiar with the analysis of motile gametes and are meant to aid the establishment and improvement of these analyses in order to stimulate research on spermatogenesis in the moss model species P. patens.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Microscopy of Physcomitrella patens sperm cells

Horst

Reski

2017

Plant Methods

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“…The sheer quantities of sperm produced and their release over several months ensure that at least one flooding event will result in sporophyte production. Highly effective spermatozoid transport both within individual plants and between them, plus recent demonstrations of sperm and antheridial desiccation tolerance (Abel, ; Shortlidge et al, ; Stark et al, ; Döbbeler, ) must also make further contributions to the very high success rate of fertilization. The internalized external water‐conducting system in Marchantia , comprising pegged rhizoids inside the ventral scales and carpocephala grooves, with flow rates of several cm/h (Duckett et al, ) is in fact far more effective at maintaining water balance than hydroids in polytrichalean mosses (Duckett & Ligrone, ).…”

Section: Discussionmentioning

confidence: 99%

Do motile spermatozoids limit the effectiveness of sexual reproduction in bryophytes? Not in the liverwort Marchantia polymorpha

Pressel

Duckett

2019

J of Sytematics Evolution

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To test the premise that fertilization distances in bryophytes are limited by spermatozoid motility, we measured the distances between over 80 000 male and female thalli of Marchantia polymorpha on heathland over 2 successive years after a major fire and recorded the incidence of sporophytes. The first comparative data on spermatozoid numbers per antheridium across bryophytes and pteridophytes were calculated from antheridial sizes and spermatid diameters and cross‐checked with the likely numbers produced by successive antheridial mitoses. Individual antheridia of Marchantia produce over 200 000 spermatozoids. Extrapolating from individual antheridia to the numbers of mature antheridia per antheridiophore and then to individual male plants, we calculated that a single flooding event on a male thallus with 10–12 antheridiophores will result in the release of over 50 million spermatozoids. Assuming radial dispersal in surface water films by lipids released from the dehiscing antheridia, spermatozoids can reach distances exceeding 20 m from the parent plants, in line with our finding of 100% fertilization in female plants of Marchantia up to 19 m from the nearest males, far beyond published fertilization distances in dioicous bryophytes. We attribute this to (i) much greater spermatozoid production and numbers in Marchantia than in other bryophytes and (ii) highly effective sperm transport both within the antheridiophores and archegoniophores via their overlapping scales and grooves in the stalks and between male and female thalli via surface water films. These features, coupled with the massive production of small spores, explain the success of Marchantia as the primary colonist of open habitats.

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“…Schofield (1971) discussed how low levels of free water along with the generally isolated patches of mostly dioicous (>60%) species (which may form single sex colonies) may limit sexual reproduction in the Arctic. Recent studies have shown, however, that sexual reproduction can occur in environments with only short-term availability of free water, as sperm cells and antheridia can withstand dehydration (Shortlidge et al 2012;Stark et al 2016). Monoicous acrocarpous taxa tend to reproduce sexually regularly (Schofield 1971;Longton 1988), but phenological data are lacking or incomplete for most taxa.…”

Section: Long-distance Dispersalmentioning

confidence: 99%

Future directions and priorities for Arctic bryophyte research

et al. 2017

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The development of evidence-based international strategies for the conservation and management of Arctic ecosystems in the face of climate change is hindered by critical knowledge gaps in Arctic floristic diversity and evolution. Particularly poorly studied are the bryophytes, which dominate the vegetation across vast areas of the Arctic and consequently play an important role in global biogeochemical cycles. Currently, much of what is known about Arctic floristic evolution is based on studies of vascular plants. Bryophytes, however, possess a number of features, such as poikilohydry, totipotency, several reproductive strategies, and the ability to disperse through microscopic diaspores, that may cause their responses to Arctic environments to differ from those of the vascular plants. Here we discuss several priority areas identified in the Arctic Council's "Arctic Biodiversity Assessment" that are necessary to illuminate patterns of Arctic bryophyte evolution and diversity, including dispersal, glacial refugia, local adaptation, and ecological interactions with bryophyte-associated microbiomes. A survey of digitally available herbarium data archived in the largest online aggregate, GBIF, across the Arctic to boreal zones indicates that sampling coverage of mosses is heterogeneous and relatively sparse in the Arctic sensu stricto. A coordinated international effort across the Arctic will be necessary to address knowledge gaps in Arctic bryophyte diversity and evolution in the context of ongoing climate change.Key words: biodiversity, dispersal, local adaptation, microbiome, phylogeography.

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Moss antheridia are desiccation tolerant: Rehydration dynamics influence sperm release in Bryum argenteum

Abstract: For the first time, moss antheridia are shown to be fully desiccation tolerant at a functional level, capable of releasing fully functional sperm following a slow drying event provided the antheridia are allowed to rehydrate at least 3 h before immersion in water.

Cited by 14 publications

References 54 publications

Microscopy of Physcomitrella patens sperm cells

Microscopy of Physcomitrella patens sperm cells

Do motile spermatozoids limit the effectiveness of sexual reproduction in bryophytes? Not in the liverwort Marchantia polymorpha

Future directions and priorities for Arctic bryophyte research

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