Antheridiogen determines sex in ferns via a spatiotemporally split gibberellin synthesis pathway

Tanaka, Junmu; Yano, Kenji; Aya, Koichiro; Hirano, Ken; Takehara, Shoichiro; Koketsu, Eriko; Ordonio, Reynante Lacsamana; Park, Seung-Hyun; Nakajima, Miki; Ueguchi-Tanaka, Miyako; Matsuoka, Makoto

doi:10.1126/science.1259923

Cited by 70 publications

(59 citation statements)

References 25 publications

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“…In multispore cultures of antheridiogen-sensitive species, the earliest-maturing gametophytes (those with defined meristems) typically become archegoniate (female) and secrete antheridiogen into the substrate, inducing adjacent, less developed gametophytes to become exclusively antheridial (male). As reviewed by Schneller and colleagues (1990), there are obvious breeding system implications associated with the ability of an individual sporophyte to control the sex ratio of the gametophytes formed from its spores in a given population (Schneller 2008, Tanaka et al 2014. Unfortunately, owing to the challenge of studying gametophytes in nature, there have been few attempts to demonstrate the operation of antheridiogen in situ (but see Tryon and Vitale 1977).…”

Section: Alternation Of Generationsmentioning

confidence: 99%

Sex and the Single Gametophyte: Revising the Homosporous Vascular Plant Life Cycle in Light of Contemporary Research

Haufler

Pryer²,

Schuettpelz³

et al. 2016

BioScience

123

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Homosporous vascular plants are typically depicted as extreme inbreeders, with bisexual gametophytes that produce strictly homozygous sporophytes. This view is promulgated in textbook life cycles despite ample evidence that natural populations of most species regularly outcross. We review research on a variety of mechanisms, including genetic load, asynchronous production of eggs and sperm, and pheromonal control of gamete production, that actively promote heterozygosity in ferns and lycophytes. Evolution of the land plants cannot be reconstructed without accurate depictions of the unique life cycle that has helped make ferns the second most diverse lineage of vascular plants on Earth. With revised illustrations and definitions, we provide scientists, educators, and students with a contemporary understanding of fern and lycophyte reproduction, revealing them as evolutionarily dynamic and exploiting a wide range of mating systems.

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Section: Alternation Of Generationsmentioning

confidence: 99%

Sex and the Single Gametophyte: Revising the Homosporous Vascular Plant Life Cycle in Light of Contemporary Research

Haufler

Pryer²,

Schuettpelz³

et al. 2016

BioScience

123

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“…It is known that ABA and SnRK2s are both present in early land plants, yet the only function clearly associated with ABA action in ferns involves sex determination of the free-living, haploid gametophyte generation of C. richardii (14). In many fern species, antheridiogen [a modified form of GA that is converted to bioactive GA 4 once imported into fern cells (15)] is secreted by hermaphroditic gametophytes, causing their immature neighbors to develop as males (14,15). Experiments with C. richardii demonstrate that exogenous ABA completely blocks the sex-determining effect of antheridiogen, such that no male gametophytes develop when grown in the presence of ABA and the antheridiogen of C. richardii (A CE ) (16).…”

mentioning

confidence: 99%

Abscisic acid controlled sex before transpiration in vascular plants

McAdam

Brodribb

Banks

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Sexual reproduction in animals and plants shares common elements, including sperm and egg production, but unlike animals, little is known about the regulatory pathways that determine the sex of plants. Here we use mutants and gene silencing in a fern species to identify a core regulatory mechanism in plant sexual differentiation. A key player in fern sex differentiation is the phytohormone abscisic acid (ABA), which regulates the sex ratio of male to hermaphrodite tissues during the reproductive cycle. Our analysis shows that in the fern Ceratopteris richardii, a gene homologous to core ABA transduction genes in flowering plants [SNF1-related kinase2s (SnRK2s)] is primarily responsible for the hormonal control of sex determination. Furthermore, we provide evidence that this ABA-SnRK2 signaling pathway has transitioned from determining the sex of ferns to controlling seed dormancy in the earliest seed plants before being co-opted to control transpiration and CO 2 exchange in derived seed plants. By tracing the evolutionary history of this ABA signaling pathway from plant reproduction through to its role in the global regulation of plant-atmosphere gas exchange during the last 450 million years, we highlight the extraordinary effect of the ABA-SnRK2 signaling pathway in plant evolution and vegetation function.OST1 | fern | stomata | evolution | sex determination

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“…Bioactive GA is necessary for stamen development in early flowers (Hu et al, 2008) and also promotes sex reversion of female flowers (Peterson and Anhder, 1960;Galun, 1961;Shifriss and George, 1964). Translocation of the GA precursor instead of the hormone has recently been proposed for regulating sex expression of fern (Tanaka et al, 2014). In a similar manner, translocation of GA as a biologically inactive precursor might help to maintain ovary identity, while stamen development is suppressed, realising sitespecific GA-regulated sepal/petal development in female flowers.…”

Section: Results and Discussion Cucumber Female Flower Developmentmentioning

confidence: 94%

Ovary-derived precursor gibberellin A9 is essential for female flower development in cucumber

Lange

2016

Development

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Gibberellins (GAs) are hormones that control many aspects of plant development, including flowering. It is well known that stamen is the source of GAs that regulate male and bisexual flower development. However, little is known about the role of GAs in female flower development. In cucumber, high levels of GA precursors are present in ovaries and high levels of bioactive GA 4 are identified in sepals/ petals, reflecting the expression of GA 20-oxidase and 3-oxidase in these organs, respectively. Here, we show that the biologically inactive precursor GA 9 moves from ovaries to sepal/petal tissues where it is converted to the bioactive GA 4 necessary for female flower development. Transient expression of a catabolic GA 2-oxidase from pumpkin in cucumber ovaries decreases GA 9 and GA 4 levels and arrests the development of female flowers, and this can be restored by application of GA 9 to petals thus confirming its function. Given that bioactive GAs can promote sex reversion of female flowers, movement of biologically inactive precursors, instead of the hormone itself, might help to maintain floral organ identity, ensuring fruit and seed production.

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Antheridiogen determines sex in ferns via a spatiotemporally split gibberellin synthesis pathway

Cited by 70 publications

References 25 publications

Sex and the Single Gametophyte: Revising the Homosporous Vascular Plant Life Cycle in Light of Contemporary Research

Sex and the Single Gametophyte: Revising the Homosporous Vascular Plant Life Cycle in Light of Contemporary Research

Abscisic acid controlled sex before transpiration in vascular plants

Ovary-derived precursor gibberellin A9 is essential for female flower development in cucumber

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