Pheromonal Interactions among Gametophytes of<i>Osmundastrum cinnamomeum</i>and the Origins of Antheridiogen Systems in Leptosporangiate Ferns

Hollingsworth, Stephanie N.; Andres, Eric A.; Greery, Gary K.

doi:10.1086/664717

Cited by 9 publications

(10 citation statements)

References 28 publications

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“…Our results in combination with Hornych et al (2021) suggest that C. multiflora possesses an antheridiogen system, similar to the putative system in Osmundastrum cinnamomeum found by Hollingsworth et al (2012). In species with this system, sex among initially germinating gametophytes is determined primarily by growth conditions, or possibly a genetic polymorphism (Hollingsworth et al, 2012).…”

Section: Discussionsupporting

confidence: 91%

Antheridiogen controls spatial dynamics of sex expression in naturally occurring gametophytes of the tree fern Cyathea multiflora

Harrington

Blake‐Mahmud

Watkins

2022

American J of Botany

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Premise: Antheridiogen systems are a set of pheromonal mechanisms that control sex expression in fern gametophytes. However, antheridiogen has rarely been studied outside of the laboratory, and little is known about its function in natural settings. Combining predictions based on field and laboratory study, we tested whether the sexual structure of gametophytic colonies of a tree fern were attributable to antheridiogen. Methods: Gametophytic colonies of the antheridiogen-producing tree fern Cyathea multiflora were collected at La Selva Biological Station in Costa Rica in January 2019. The sex of each gametophyte was determined, mapped, and spatial statistic approaches were used to examine the distribution of sex in each colony.Results: In all gametophytic colonies, males were most common, representing 62-68% of individuals. No hermaphroditic gametophytes were identified in any colony. A quadrat-based method showed female gametophytes were not clustered in each colony, while male gametophytes were clustered. In two of the colonies, the K(r) test statistic for males was greater than expected compared to random simulations of sex expression, indicating male sex expression was spatially associated with females. Conclusions: This study provides the first documentation of spatial sex expression in natural settings of gametophytes of an antheridiogen-producing tree fern species. The profound impact of antheridiogen on gametophytic sex expression in field settings suggests this system is intimately tied to mating system, fitness, and genetic diversity in Cyathea multiflora.

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Section: Discussionsupporting

confidence: 91%

Antheridiogen controls spatial dynamics of sex expression in naturally occurring gametophytes of the tree fern Cyathea multiflora

Harrington

Blake‐Mahmud

Watkins

2022

American J of Botany

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“…All pairings involving Equisetum indicate that it has no AG system, suggesting that AGs evolved within the ferns after the divergence of Equisetum . No other eusporangiate ferns have yet been tested, but studies of sexual expression in Osmundaceae, which are sister to all other leptosporangiate ferns, indicate a potential pheromonal control different from AG (Hollingsworth et al ., 2012). Phylogenetically, the three types of AG system we recognize could represent three separate origins.…”

Section: Discussionmentioning

confidence: 99%

Insights into the evolutionary history and widespread occurrence of antheridiogen systems in ferns

Hornych¹,

Testo

Sessa

et al. 2020

New Phytologist

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Sex expression of homosporous ferns is controlled by multiple factors, one being the antheridiogen system. Antheridiogens are pheromones released by sexually mature female fern gametophytes, turning nearby asexual gametophytes precociously male. Nevertheless, not all species respond. It is still unknown how many fern species use antheridiogens, how the antheridiogen system evolved, and whether it is affected by polyploidy and/or apomixis. We tested the response of 68 fern species to antheridiogens in cultivation. These results were combined with a comprehensive review of literature to form the largest dataset of antheridiogen interactions to date. Analyzed species also were coded as apomictic or sexual and diploid or polyploid. Our final dataset contains a total of 498 interactions involving 208 species (c. 2% of all ferns). About 65% of studied species respond to antheridiogen. Multiple antheridiogen types were delimited and their evolution is discussed. Antheridiogen responsiveness was not significantly affected by apomixis or polyploidy. Antheridiogens are widely used by ferns to direct sex expression. The antheridiogen system likely evolved multiple times and provides homosporous ferns with the benefits often associated with heterospory, such as increased rates of outcrossing. Despite expectations, antheridiogens may be beneficial to polyploids and apomicts.

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“…Despite this view, a growing body of literature suggests that several factors play an important role in mediating reproductive success. A large proportion of fern species produce sex-determining antheridiogens (D€ opp, 1950;N€ af et al, 1975;Haufler & Gastony, 1978;Schneller et al, 1990;Chiou & Farrar, 1997;Schneller, 2008;Hollingsworth et al, 2012). In nature, antheridiogen systems generate gametophyte populations comprising large female gametophytes and small male gametophytes, resulting in a disproportionate number of gametophytes that may act only as male parents relative to those in non-antheridiogen-induced populations (Tryon & Vitale, 1977;Haufler & Soltis, 1984;Schneller et al, 1990;Hamilton & Lloyd, 1991).…”

Section: Introductionmentioning

confidence: 99%

Dynamics of asymmetrical hybridization in North American wood ferns: reconciling patterns of inheritance with gametophyte reproductive biology

2014

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SummaryHybridization is an important evolutionary force in plants, but the mechanisms underlying it have not been well studied for many groups. In particular, the drivers of non-random patterns of interspecific gene flow (asymmetrical hybridization) remain poorly understood, especially in the seed-free vascular plants. Here, we examine patterns of asymmetrical hybridization in two widespread fern hybrids from eastern North America and study the role of gametophyte ecology in the determination of hybridization bias.We characterized the maternal parentage of > 140 hybrid sporophytes by sequencing a c. 350-bp region of chloroplast DNA (cpDNA). To identify factors contributing to patterns of asymmetrical hybridization, we cultured gametophytes of the parental species and evaluated critical aspects of their reproductive biology.We found that asymmetrical hybridization was prevalent across the populations of both hybrids. Reproductive traits varied across species and suggest that selfing potential, antheridiogen responsiveness, sperm dispersal capacity and gamete size all contribute to the mediation of the direction of hybridization in this group.Our findings suggest that asymmetrical hybridization in ferns is driven by an array of reproductive traits. This study helps to sharpen and define a mechanistic understanding of patterns of hybridization in this group and demonstrates the importance of considering gametophyte biology when studying evolutionary processes in ferns.

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Pheromonal Interactions among Gametophytes ofOsmundastrum cinnamomeumand the Origins of Antheridiogen Systems in Leptosporangiate Ferns

Cited by 9 publications

References 28 publications

Antheridiogen controls spatial dynamics of sex expression in naturally occurring gametophytes of the tree fern Cyathea multiflora

Antheridiogen controls spatial dynamics of sex expression in naturally occurring gametophytes of the tree fern Cyathea multiflora

Insights into the evolutionary history and widespread occurrence of antheridiogen systems in ferns

Dynamics of asymmetrical hybridization in North American wood ferns: reconciling patterns of inheritance with gametophyte reproductive biology

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