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

Abstract

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.

Gametophytic phase of the Indonesian ferns Amblovenatum immersum (Blume) Mazumdar and Christella subpubescens (Blume) Holttum (Thelypteridaceae)

“…The antheridiogen suppresses the early developmental functions of gametophytes, which is why they are small, asymmetrical in appearance, or in some cases lack meristem (Banks 1999), promoting the rapid differentiation of gametophyte cells into antheridia. The function attributed to the antheridiogen is to promote crossing in pteridophytes, through the ontogenetic control of the formation of gametangia in gametophyte populations (Schneller et al 1990;Yatskievych 1993;Hornych et al 2020). The observations carried out on male gametophytes are consistent with those reported by other studies, and supports the idea of the presence of antheridiogens in the species A. immersum and C. subpubescens.…”

“…These are pheromones released into the environment by sexually mature female or bisexual gametophytes (Banks 1999) and promote maleness on the nearby presexual gametophytes. Although not all species can produce or respond to antheridiogens, the family Thelypteridaceae is one of the families that respond and produce antheridiogens (Raghavan 1989;Hornych et al 2020) along with others such as Blechnaceae, Dryopteridaceae or Polypodiaceae (Yatskievych 1993;Hornych et al 2020). The antheridiogen suppresses the early developmental functions of gametophytes, which is why they are small, asymmetrical in appearance, or in some cases lack meristem (Banks 1999), promoting the rapid differentiation of gametophyte cells into antheridia.…”

The biology of C. richardii as a tool to understand plant evolution

“…These gibberellin-related chemicals are released by early-germinating archegoniate gametophytes to promote antheridiate gametophyte development in immature gametophytes. This pheromone system confers some of the benefits of heterospory to homosporous plants, namely outcrossing ( Bateman and DiMichele, 1994 ; Hornych et al, 2021 ). In the case of Ceratopteris , however, solitary gametophytes can also become bisexual and self-fertilize; therefore, theoretically, only one spore can colonize new habitats ( Schedlbauer and Klekowski, 1972 ).…”

Efecto de la luz, la temperatura y la competencia en la fase gametofítica de dos helechos nemorales: Athyrium filix-femina y Dryopteris affinis subsp. affinis.

“…En cuanto a la expresión sexual, que afecta a los modos de reproducción (Willson 1981;Korpelainen 1998;Hornych et al 2021), en las muestras control solo se observaron gametófitos presexuales y masculinos, aunque alcanzaron un tamaño significativamente mayor que a las menores intensidades de luz estudiadas. Muchos de los gametófitos presexuales eran merísticos, con posibilidad de secretar anteridiógeno y favorecer la presencia de masculinos en ambas especies (Schneller 2008).…”

“…La formación de anteridios en gametófitos apomícticos quizá sea una respuesta al anteridiógeno y, aunque la presencia de un sistema hormonal controlando la expresión sexual en una especie apógama parezca superflua, juega un papel importante en las interacciones entre estas especies y otras congenéricas sexuales (Haufler & Gastony 1978;Schneller 1981;Hornych et al 2021). En concreto, se pueden producir híbridos entre especies apomícticas, que en su mayoría no producen arquegonios (Whittier 1968;Bell 1990;Yatskievych 1993), con especies sexuales relacionadas, que a su vez se reproducirán por apogamia (Ekrt et al 2009;Hornych et al 2021).…”