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Sex of fern gametophytes

Sex of fern gametophytes


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The following image is from Campbell Biology, 12th edition

It says, "Each gametophyte develops sperm-producing organs called antheridia and egg-producing organs called archegonia". This seems to suggest gametophytes are either always hermaphrodites or most of the times hermaphrodites.

I have done a little bit of searching and now am convinced that they are not always hermaphrodites.

"Most ferns, on the other hand, are homosporous; they produce a single type of spore. After germination, each fern spore has the potential to develop into a male, female, or hermaphrodite gametophyte."

https://science.sciencemag.org/content/346/6208/423.summary#:~:text=Most%20ferns%2C%20on%20the%20other,%2C%20female%2C%20or%20hermaphrodite%20gametophyte.

Are they most of the time hermaphrodites? How common are unisexual gametophytes?


The effects of light on sex determination in gametophytes of the fern Ceratopteris richardii

The sexuality of homosporous fern gametophytes is usually determined by antheridiogen, a pheromone that promotes maleness. In this work the effect of photomorphogenically active light on antheridiogen-induced male development was examined for gametophytes of Ceratopteris richardii. Although blue light did not affect sensitivity to Ceratopteris antheridiogen (ACe) in wild-type gametophytes, it was found that the gametophytes of the her1 mutant, which are insensitive to ACe, developed into males when grown under blue light in the presence of ACe. Thus, we conclude that another ACe-signal transduction pathway activated by blue light exists latently in the gametophytes of C. richardii. Red light, on the other hand, suppressed male development. Because simultaneous red and blue light-irradiation did not promote male development in the her1 gametophytes, the action of red light seems to dominate that of blue light. The results of experiments with a photomorphogenic mutant also suggested that phytochrome may be involved in the action of red light.

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Biology and evolution of ferns and lycophytes

About once every decade for the last 80 years, a volume has been produced that reports comprehensively on recent developments in pteridology. Some have an emphasis on particular aspects, such as phylogeny, cytogenetics or gametophytes, while others have a broader coverage. Together with several substantial proceedings of conferences, these books have helped to maintain the momentum of interest in ferns and lycophytes. With the current changes in fashion in botanical curricula and the reduction in research support for pteridology, the stimulus of another major publication of this kind was needed. Ranker and Haufler have followed in the tradition of Verdoorn's multi-authored compendium Manual of Pteridology (1938) and assembled contributions that include a broad selection of topics across the range currently being investigated. They cover all the plant groups traditionally included in the ‘Pteridophytes’, but avoid the use of the name in the title in recognition of the current view that the groups do not share a common ancestor and therefore a collective noun is no longer valid (this has robbed us also of the term ‘pteridologist’, for which there is no convenient alternative.) The 16 chapters are grouped into four parts: ‘Development and Morphogenesis’ (103 pages), ‘Genetics and Reproduction’ (94 pages), ‘Ecology’ (102 pages) and ‘Systematics and Evolutionary Biology’ (167 pages). The list of 28 authors includes several of the elder statesmen of today's ‘pteridology’, along with some of the rising stars. Twenty authors are based in the USA, the remainder with addresses in Canada, Mexico, Japan, Sweden, Switzerland and the UK. This may reflect the fact that both editors are from the USA as much as it mirrors the geographical distribution of current pteridological activity, but it is true that in the UK at least there are now few active research pteridologists who can contribute to such a volume.

The intended readership is stated to be advanced undergraduates, graduates and academic researchers. This means that each chapter should provide sufficient background for those new to the field, a survey of recent developments to bring the reader up to date, and a synthesis of ideas to stimulate further investigation. This in turn means that those who have read earlier accounts might be disappointed to find that some of the content is familiar, particularly in the areas where research progress is slow. However, this is balanced by the fact that this volume provides a one-stop source for beginners.

In Chapter 1, M. Wada discusses ‘Photoresponses in fern gametophytes’. He describes the investigation of most of the growth responses and intracellular reactions (from chloroplast movement to nuclear division) to monochromatic or polarized light, and the current understanding of the photoreceptors (more than 10 already identified in Adiantum) and the mechanisms involved. This account would of course be useful to students new to the topic, but should also be read by fern ecologists interested in the gametophyte in the natural environment and by plant physiologists researching photoresponses in angiosperms.

In Chapter 2, ‘Alternation of generations’, E. Sheffield presents a brief review of the familiar and fundamental issue of the alternation of gametophyte and sporophyte generations. This is nowhere more conspicuous than in the ferns and lycophytes, the only organisms in which both phases are capable of independent, free-living existence. There is little that is new to report about the origin and adaptive success of this two-phase life cycle, but the availability of new techniques promises progress in our understanding of the controlling mechanisms. A review of the events and modifications of the homosporous life cycle is illustrated by some excellent SEM photographs heterosporous life cycles are not considered. The brevity of the treatment of obligate apomixis, despite its adaptive importance, is perhaps an indication that there have been few recent investigations of its mechanism or ecological success.

In Chapter 3, ‘Meristem organisation and organ diversity’, R. Imaichi presents a concise, clear and well-ordered review of apical development of stems and stem branches, leaves and roots. Also covered are the specialized rhizomes of the whisk ferns, the rhizophores unique to the Selaginellaceae, and the rhizomorphs found only in the Isoetaceae. Progress is slow in this field (only 10 of the 91 papers quoted were written in the last 10 years) and Imaichi covers the major developments of the last 40 years. Most pteridologists, whatever their specialism, would find this account interesting because the events at the meristems, and particularly the apical meristems, determine the conspicuous characteristics that define the ferns, lycophytes and their component groups.

Chapter 4, ‘Population genetics’ by T. Ranker and J. M. O. Geiger, provides a useful critical review of 40 years of investigation by a variety of techniques into population genetics and the reproductive biology fundamental to it. Most observations relate to homosporous ferns and increasingly in recent years depend on molecular techniques. On the basis of the small proportion of the world flora that has been studied, a coherent picture is emerging. Most diploid fern species form mainly unisexual gametophytes and are to a greater or lesser extent outcrossing, with levels of genetic diversity no lower than seed plants. However, some pioneer species that colonize new habitats, many polyploid species, and those with subterranean gametophytes are able to inbreed by intra-gametophytic selfing of bisexual gametophytes. Further clarification will require the use of a broader range of species and the wider application of molecular techniques.

J. J. Schneller, who has been a source of interesting observations on fern reproductive biology for 30 years, has contributed Chapter 5, ‘Antheridiogens’. This provides a useful summary of the history of investigations, mostly in the laboratory, into sex determination by antheridiogen pheromones in gametophytes of homosporous ferns. The account highlights the need for more research, especially into the role of antheridiogens in nature, the occurrence of antheridiogens in other (especially tropical) species, the interaction of antheridiogens with the phytochrome system, and the molecular aspects of genetic regulation of sex determination.

In Chapter 6, ‘Structure and evolution of fern plastid genomes’, P. G. Wolf and J. M. Roper describe the progress in mapping the chloroplast genome. It is nearly 20 years since restriction mapping revealed that lycophytes lack an inverted repeat (IR) present in all other extant vascular plants. This approach has been succeeded by complete genome mapping (first achieved for Adiantum capillus-veneris in 2003 by Wolf et al.) and PCR mapping of the gene order of the IR sequence. Recent results have shown that the rare changes in the structure of the evolutionarily conservative IR provide phylogenetic data. Wolf and Roper describe the methodological approach and present previously unpublished results. New molecular techniques promise significant developments in the near future. The implications of the results will interest all pteridologists, even if the methods can be fully appreciated only by other molecular phylogeneticists.

In a parallel chapter (Chapter 7), T. Nakazato, M. S. Barker, L. H. Rieseberg and G. J. Gastony consider the ‘Evolution of the nuclear genome of ferns and lycophytes’. Genomic studies in these seedless plants lag behind those in flowering plants the first linkage map of a fern was not published until 2006, more than 20 years after the first for angiosperms. The results from new molecular technologies, including linkage mapping and targeted gene silencing, are fine-tuning the long-established theory that homosporous fern and lycophyte genomes with large numbers of chromosomes are the consequence of repeated genome doubling events followed by gene silencing or even gene elimination. Full resolution of the issues relating to the unique features of genome evolution in ferns and lycophytes requires further research into various aspects, from meiotic pairing, C values, gene expression and gene mapping to whole-genome sequencing. Much of the recent work has focussed on Ceratopteris richardii, a model fern with a conveniently short life cycle in future it will be necessary to widen the range of plants analysed to include the heterosporous ferns and lycophytes as well as other homosporous species, both palaeopolyploids and neopolyploids, representative of all the main phylogenetic lineages.

Little has been written about tropical fern ecology over the last 100 years but in Chapter 8, ‘Phenology and habitat specificity of tropical ferns’, K. Mehltreter, one of those who has helped to stimulate interest in the last few years, has reviewed recent investigations of habitat preferences and periodicity in biological processes. The facts presented in this chapter reveal not how much but how little we know about tropical fern ecology. There is a need for more quantitative field data obtained over long periods and across a wide range of species and habitats, and in conjunction with the investigations of physiology, biochemistry, morphology and genetics, without which fern ecology is unlikely to be fully understood. This draws our attention to the fact that there is no chapter in this book on the physiology and biochemistry of ferns, reflecting the current lack of interest. The absence of any mention of the gametophytes' role in determining phenology or habitat specificity is no doubt in deference to the chapter that follows.

Chapter 9, ‘Gametophyte Ecology’ by D. R. Farrar, C. Dassler, J. E. Watkins, Jr. and C. Skelton, is one of the longest chapters in the book and goes some way towards reversing the past neglect in print of the gametophyte in natural habitats. No one is better qualified than Farrar to review this topic, although in one or two places this chapter appears to have been written in separate sections by different authors and then ‘bolted’ together. With a focus on leptosporangiate species, the account summarizes what little has been published and adds some new unpublished observations. Contrary to popular belief, the familiar short-lived cordiform prothallus is not the archetypical fern gametophyte it is an evolutionarily advanced form that is adapted to disturbed terrestrial microhabitats and is largely restricted to modern leptosporangiate species. Most older fern groups, and those species of the more recent Polypodiales that occupy the more stable epiphytic habitats, together present a diverse array of long-lived, elongate and proliferating gametophytes, some with vegetative propagules. The chapter finishes with some interesting original observations on differences between laboratory-raised and field-grown gametophytes, which in turn point towards some of the factors influencing development in the wild. Because of the central role of the gametophyte generation in establishment and reproduction, this chapter should be essential reading for everyone with an interest in fern ecology.

Chapter 10, ‘Conservation biology’ by N. N. Arcand and T. A. Ranker, presents a concise outline of the issues relating to the conservation of ferns and lycophytes, in particular endemic species of high conservation priority and species in identified diversity ‘hot-spots’. It covers the case for conservation, the range of threats to diversity and their causes, and the different practical approaches to in situ and ex situ conservation. Although habitat restoration is highlighted, there is no discussion of the contentious issues relating to re-introduction (planting at sites where a species once grew but has become extinct) and augmentation (planting in populations endangered because of their very small number of individuals) using ex situ-raised plants. The need for more evaluation of conservation requirements, and for more research into fern and lycophyte ecology and in situ development, is made clear. The comprehensive list of relevant literature, mostly from the last 10 years, will be useful.

In Chapter 11, ‘Ex situ conservation of ferns and lycophytes – approaches and techniques’, V. C. Pence enlarges on one aspect of practical conservation, touched upon in the previous chapter and likely to be of growing interest as the various available techniques are developed. In most cases, the various types of ex situ gene banks are derived from initial samples taken as spores from surviving wild plants or natural soil spore banks, but where spores are not available or not viable, techniques known as ‘in vitro collecting’ (IVC) are being developed for establishing tissue cultures from excised explants obtained from plants in the wild without harming them. It is unlikely that there is one method of ex situ conservation that is optimal for all species, so more research into the effectiveness of alternative techniques and the requirements of individual species, as well as the physiology of spores and plant tissues in storage, is needed in order to facilitate the establishment of more long-term conservation germplasm banks.

Chapter 12, ‘Species and speciation’ by C. H. Haufler, will be largely familiar to anyone who has read earlier reviews by this author, but it is convenient to have this well-written account along with all the other topics. There was a time when speciation in ferns and lycophytes was considered to be a less dynamic process than in angiosperms, but this is not so. Primary speciation (diploid divergence after geographic or ecological isolation despite the capacity for wide spore dispersal), secondary speciation (involving genetically isolated autopolyploids, ecological isolation in rare fertile hybrids, and allopolyploids derived from sterile hybrids), and tertiary speciation (divergence in polyploids, sometimes involving gene silencing and ‘diploidization’) have all been detected in one or other group of ferns and lycophytes. Haufler issues a plea for more research into the role of the gametophyte in defining habitat specificity because ecological specialization in peripheral populations can be an important step in speciation, particularly in tropical species. We must now view ferns not as a relatively few widely dispersed species but as many, more narrowly defined, often cryptic species.

In Chapter 13, ‘Phylogeny and evolution of ferns a paleontological perspective’, G. R. Rothwell and R. A. Stockey consider the early stages of that phylogeny. They state that their account is intended for the non-paleontologist, but the reader will benefit considerably from being familiar with the morphological and phylogenetic terminology as well as the (American) names of the geological periods and their dates. The authors' interpretation of the relationships among euphyllophytes (i.e. excluding lycophytes) is not the only one and the concentrated text is not an easy read, but it is a good reference source. Throughout, only the sporophyte is considered, implying that no gametophytes have been found in the fossil record. The chapter is illustrated by more than 70 photographs but much of their potential value is lost because they are so small, with up to 20, together with captions, on a single page. The authors finish with a plea for including fossil evidence in any phylogenetic analysis basing it entirely on studies of living representatives often leads to a different interpretation.

After more than 170 years of publication on the subject, the literature on biogeography of ferns and lycophytes is now overwhelming, so in Chapter 14, ‘Diversity, biogeography and floristics’, R. Moran has limited himself to three interrelated topics: diversity, long-distance dispersal, and vicariance, and to 214 references. Diversity increases from the temperate latitudes to the equator and is greatest in the middle altitudes of mountains. The whole of Britain and Ireland has just over 70 native species whereas a single tree in Costa Rica can contain 50 species. While mountains can form barriers to migration of species, there is considerable circumstantial evidence for long-distance dispersal. Molecular phylogeny also indicates a role for continental drift and climate change in explaining some instances of disjunct distribution. Moran finishes by highlighting the need for more plant collecting and publication of floras and more research into, for example, speciation rates and the influence of ploidy, morphology and life cycle characteristics on ecological and geographical distribution. Progress will be accelerated by greater dissemination of information via the web and by the questions raised by new phylogenetic trees derived from improved DNA sequencing.

In Chapter 15, ‘Fern phylogeny’, E. Scheuttpelz and K. M. Pryer present a series of diagrams of the fern ‘tree of life’ with accompanying commentary and supporting references. This clearly summarizes the current hypotheses concerning fern relationships based on molecular phylogenetic analysis in a way that those not routinely immersed in the intricacies can easily refer to and follow. The account starts with the early vascular plant divergences that explain the abandonment of the concept of ‘pteridophytes’ (a term previously used to include all the spore-bearing and ‘seed-free’ plants) and that justify the inclusion of horsetails and whisk ferns within a broadly defined group of ‘ferns’. It then progresses through the early separation of leptosporangiates from other ferns and the divergence of the monophyletic older families like Osmundaceae and Hymenophyllaceae from the remainder, to the relationships between the leptosporangiate families, including the ‘tree ferns’ (not all have trunks), heterosporous water ferns, and the ‘Polypods’, a group united by having sporangia with a vertical annulus interrupted by the stalk, and which contains the majority of fern species. Within these groupings, relationships between genera and selected species are suggested. At this level there are many uncertainties, as well as inconsistencies between conclusions based on molecular analyses and those based on morphology. However, this framework derived from DNA sequence analysis provides a focus for further resolution of evolutionary patterns.

The final Chapter 16, ‘Fern classification’, is essentially an update of the 2006 paper (in Taxon) by the same authors: A. R. Smith, K. M. Pryer, E. Schuettpelz, P. Korall, H. Schneider and P. Wolf. The classification is based on the consensus relationships that are presented in Chapter 15 by two of these authors the common authorship results in close compatability, but also a little repetition, between the two chapters. Ferns are described as a monophyletic group of about 9000 species (compare with the estimate of over 12 000 given in Chapter 14) with several shared characteristics. Accounts are presented of 37 fern families in 11 orders within four classes: Psilotopsida, Equisetopsida, Marattiopsida and Polypodiopsida. For each family there is a description of characters, the numbers and names of genera, chromosome numbers, synonyms, references and outstanding classification problems. Although recent molecular analyses have produced some surprises, and despite the need to resolve some circumscriptions, many of the families and monotypic genera that had been recognized in past major classifications, mostly morphologically based, still have strong support, with evidence of monophyly. The chapter finishes with appendices listing familial and generic names, both those accepted by the authors and others. The family summaries and genus placements, although no doubt already familiar to those who work in the field of fern classification, provide a useful reference source for those who do not.

Throughout the volume, which finishes with a comprehensive index, the editors' beneficial influence is apparent in the consistent approach of many of the chapters (introduction and plan, historical survey, review of important recent advances, future directions, and a comprehensive list of relevant references, more than 200 in some chapters) and in the commendable rarity of typographical errors. I found only three that were potentially misleading. First, on page 368, line 2, ‘13 600’ should be ‘1 360’ second, ‘Smith et al, 2006a’ in Table 16·1, page 418, should be ‘Smith et al, 2006b’ third, the editors will not be happy that ‘homoeologous’ was changed to ‘homologous’ in several places on pages 112, 178, and 179 after they handed over the final draft.

This book will be indispensable for complementing any fern biology or systematics courses still taught at university. It will provide essential background information for those beginning research in any of the areas covered. Botanists working in similar areas of seed-plant biology will benefit from reading about the parallel processes in a different vascular plant group. However, for all but the most dedicated of amateur fern enthusiasts, many chapters will probably appear to be too detailed and technical, despite the fact that contained within them are statements that might well interest them.


Gametophyte Generation in Non-vascular Plants

The gametophyte phase is the primary phase in non-vascular plants, such as mosses and liverworts. Most plants are heteromorphic, meaning that they produce two different types of gametophytes. One gametophyte produces eggs, while the other produces sperm. Mosses and liverworts are also heterosporous, meaning that they produce two different types of spores. These spores develop into two distinct types of gametophytes one type produces sperm and the other produces eggs. The male gametophyte develops reproductive organs called antheridia (produce sperm) and the female gametophyte develops archegonia (produce eggs).

Non-vascular plants must live in moist habitats and rely on water to bring the male and female gametes together. Upon fertilization, the resulting zygote matures and develops into a sporophyte, which remains attached to the gametophyte. The sporophyte structure is dependent upon the gametophyte of nourishment because only the gametophyte is capable of photosynthesis. The gametophyte generation in these organisms consists of the green, leafy or moss-like vegetation located at the base of the plant. The sporophyte generation is represented by the elongated stalks with spore-containing structures at the tip.


About Ferns

Ferns are one of the oldest groups of plants on Earth, with a fossil record dating back to the middle Devonian (383-393 million years ago) (Taylor, Taylor, and Krings, 2009). Recent divergence time estimates suggest they may be even older, possibly having first evolved as far back as 430 mya (Testo and Sundue, 2016). However, despite the venerable age of the group as a whole, most of the earliest ferns have since gone extinct. Groups like the Rhacophytales, which were possibly some of the earliest progenitors of ferns, the ancient tree ferns Pseudosporochnales and Tempskya, and the small, bush-like Stauropterids have all long ago disappeared. The diversity of ferns we see today evolved relatively recently in geologic time, many of them in only the last 70 million years.

Today, ferns are the second-most diverse group of vascular plants on Earth, outnumbered only by flowering plants. With around 10,500 living species (PPG 1), ferns outnumber the remaining non-flowering vascular plants (the lycophytes and gymnosperms) by a factor of 4 to 1. How did ferns become so diverse, and what are the secrets to their success? What traits do they share in common, and how are they different from other groups of plants? What follows is a short primer on the biology of ferns, starting at the beginning, with how ferns first originated and evolved into the plants we see in the present, making special note of some of the groups that went extinct along the way. There are separate sections that cover topics ranging from fern morphology, phylogenetic relationships, and the fern lifecycle, along with the important role gametophytes play in the biology of ferns.

SHARED, DERIVED TRAITS

Figure 1. Stele structure of seed plants and ferns, with extinct relatives, adapted from Kenrick and Crane, 1997. The position of the protoxylem is denoted by circles and lines within the stele. Open circles denote protoxylem lacunae.

Figure 2. Selected anatomical traits of ferns. Species represented is Polypodium remotum Desv., illustrated in Garden Ferns (1862) by William Hooker.

Figure 3. Sporangia grouped into a sorus. Courtesy of Rogelio Moreno.

Partly because of their considerable age, ferns contain a high amount of diversity, with some groups that look nothing like the more common representatives we usually associate with ferns. There is consequently only one anatomical feature that unites them, an inconspicuous trait that requires observing the development of vascular tissue in the stem. According to Kenrick and Crane (1997), the mesarch (derived in the middle) protoxylem (protoxylem = the water-conducting cells that are the first to grow in a developing stem, the result of primary growth) in ferns is confined to lobes of the xylem strand (Fig. 1). This is opposed to the condition in seed plants in which the protoxylem also develops through the midpoints and center of the xylem strand in any given vascular bundle. Fortunately, further sub-divided groups within ferns have shared traits that are easier to observe.

Most ferns have rhizomes, underground stems from which the leaves are produced (Figure 2). Many ferns have long, creeping rhizomes that form intricate networks underground, and while the leaves may senesce and drop off due to age or cold weather, these rhizomes can persist indefinitely, sending up new leaves year after year. An entire leaf is called a frond, while further subdivisions are referred to as pinnae (first division), which grow along the main stem (called a rachis in ferns), and pinnules (subsequent divisions). The portion of the rachis without pinnae is referred to as the stipe (petiole), which attaches directly to the rhizome. Most fern fronds also have circinate vernation, in which the new growth is tightly coiled in a fractal spiral, which gradually unfurls as the leaf develops, protecting the meristem. This curling forms the familiar fiddlehead at the tip of new fronds. Ferns reproduce by spores, which are generally produced on the bottom (abaxial side) of leaves by specialized structures called sporangia. Sporangia can develop in clusters called sori, which can be circular (Figure 3), in distinct rows, or may even cover the entire underside of a leaf (acrostichoid sori) and are sometimes protected by an overhanging structure called an indusium. Other species have a sterile/fertile frond dimorphy, in which spores are produced on only certain leaves and not on others.

RELATIONSHIPS

Figure 4. Individual sporangium with selective labeling. Courtesy of Rogelio Moreno.

Figure 5. Currently accepted phylogeny of ferns, according to the Pteridophyte Phylogeny Group (PPG 1).

Broadly speaking, ferns can be divided into two groups, the eusporangiates and leptosporangiates, with most of the diversity occurring in the latter. These terms refer to how sporangia develop and mature. In eusporangiates, a given sporangium develops from multiple initial cells on the surface of stems or leaves and consists of several cell layers in the early stages of development. Each sporangium can go on to produce several hundred spores. In contrast, leptosporangia arise from just one initial cell, which produces a stalked capsule that is just one cell layer in thickness. These sporangia also have a row of hollow cells arranged along two-thirds of the upper surface that fill with water (Figure 4). The thin, membranous cells are highly permeable, easily allowing water to evaporate. This causes tension to build within the water column inside, forcing the remaining water to contract, which causes the annulus to slowly pull open the thin-walled sporangium, exposing the spores within. But at some point, the tension in the column becomes stronger than the adhesion properties of water, and the column snaps, which jettisons the spores at high speeds into the surrounding environment.

The eusporangiates are comprised of the horsetails (Equisetales), whisk ferns (Psilotales), moonworts (Ophioglossales), and marattioid ferns, which altogether number about 255 species (PPG 1) (Figure 5). The exact relationships of the first three groups were for a long time unknown it was unclear whether they represented true ferns or were actually the last vestiges of ancient plant groups that were entirely separate from ferns. For this reason, these groups were often referred to as the fern allies. Recent molecular work, however, has demonstrated that the whisk ferns (Psilotales) and moonworts (Ophioglossales) are unequivocally ferns and that the horsetails are sister to all other species within the fern clade (Knie et al., 2014 Rothfels et al. 2015). Many researchers now use the term ‘monilophyte’ to encompass all of these groups, including all eusporangiate and leptosporangiate clades.

The leptosporangiates contain the bulk of fern diversity, comprised of some 10,323 species, grouped into 44 families (PPG 1). Most leptosporangiate ferns, as well as all eusporangiates, are homosporous, meaning that each species produces spores of only one size. The aquatic ferns in the order Salviniales are the only exception to this rule, having heterosporous spores. In this condition, a single plant produces both small microspores, which develop male gametophytes, and a few much larger megaspores, which develop into endosporic female gametophytes. Whereas the gametophytes of most species will break open the spore casing upon germination, becoming independent and photosynthetic, the female gametophytes of heterosporous species are retained within the megaspore and are dependent on stored lipids and carbohydrates for nutrition. It’s likely that the retention of the female gametophyte in a heterosporous lineage of plants led to the evolution of the first seeds.

EVOLUTIONARY HISTORY

Table 1. List of ferns and extinct relatives with their associated fossil record dates. Those groups that still exist are marked as ‘present’ (from Taylor, Taylor, and Kring, 2009).

The Devonian was a period of major change for the planet. The ancestors of green algae had migrated from their marine and freshwater environments onto land earlier in the Paleozoic era and began to evolve stems and roots to enable their survival in the harsh conditions they faced in Earth’s prehistoric terrestrial environments. These first plants, however, lacked true leaves for millions of years, instead possessing chloroplasts in their stems to enable photosynthesis. In the middle and late Devonian, however, as plants began to spread throughout the world’s ecosystems, they locked up a significant amount of CO2 through burial and the weathering of bare rock, causing the planet to cool (Mora, Driese, and Calarusso, 1996). This meant that plants could evolve bigger structures to intercept more light without overheating, and it is during this time that the first leaves begin to appear (Beerling, Osborne, and Chaloner, 2001). While leaves likely evolved multiple times in land plants, the earliest ancestors of ferns were some of the first to possess them.

Some extant species of ferns have either extremely small and specialized leaves (horsetails) or even no leaves at all (whisk ferns), but there is evidence to suggest that this wasn’t always the case for these groups. Some of the ancestors of modern horsetails, the Calamites, grew to the size of trees and had leaves with prominent vascular bundles (Taylor, Taylor, and Krings, 2009).

While ferns first evolved in the Devonian, they became one of the most dominant groups of plants on the planet during the Carboniferous (299-369 mya). Growing alongside the giant tree lycophytes (e.g., Lepidodendron) in vast swamps, ferns thrived and diversified for several million years. Leptosporangiate ferns evolved during this time and underwent the first of three major radiations, giving rise to several families (Rothwell and Stokey, 2008).

When these plants died, they sank into the anoxic swamps, where the lack of oxygen prevented bacteria from degrading dead tissue. The rampant growth in these swamps, and their subsequent burial, created most of the coal and natural gas deposits we have today. Every time you drive your car, you’re using fossilized ferns to reach your destination.

As the Carboniferous came to a close, most of the first leptosporangiate families to have evolved gradually went extinct. At least one lineage survived, however, to give rise to the second major radiation of leptosporangiate ferns, which began in the late Permian (

250 mya) (Rothwell and Stokey, 2008). Some of the oldest fossils from this diversification are of the Osumundales, which include species such as the cinnamon fern (Osmundastrum cinnamomeum) and royal fern (Osmunda regalis) (see table 1 for a list of families and their ages). Most of the groups that evolved during this time have survived to the present, and while they contain a modest amount of diversity, the third and final radiation gave rise to the greatest bulk of fern species by far.

About 135 mya, during the Cretaceous, a small group of plants evolved that would quickly and drastically change the planet’s ecosystems. Originating in the tropics, flowering plants (angiosperms) rapidly diversified and spread to all major portions of the globe, driving several groups of plants to extinction and severely reducing the diversity in others. Leptosporangiate ferns appear to be the only group of vascular plants that thrived alongside angiosperms, rather than being marginalized (Schuettpelz and Pryer, 2009). The advent of towering, angiosperm-dominated rainforests in the tropics opened up new environments that ferns were able to successfully exploit and diversify in, which led to the third radiation of leptosporangiate ferns. Consequently, most species of ferns today grow in the tropics. Costa Rica, for example, is smaller than the state of West Virginia and yet has nearly 3X as many fern species as the entire continental United States and Canada combined.

LIFECYCLE

Figure 6. Lifecycle of ferns, depicting the various modes of reproduction that can take place, excluding asexual reproduction, such as apomixis (from Sessa, Testo, and Watkins, 2016).

Figure 7. Various morphologies of fern gametophytes (from Pinson et al., 2017 and Paul K).

Across the land plant phylogeny, there is a pattern of increasing sporophyte complexity along with an associated decrease in the independence of the gametophyte portion of the lifecycle. Bryophytes, which were the first plants to colonize land, grow as independent gametophytes that produce nutritionally-dependent sporophytes. Conversely, on the opposite end of the land plant phylogeny, the seed plants have dominant sporophytes with dependent gametophytes that have been reduced to just a few cells. Ferns and lycophytes, which span the evolutionary gap between these lineages, are the only groups of plants in which both the sporophyte and gametophyte are completely independent of each other.

In ferns, a mature sporophyte will develop haploid spores via the process of meiosis. Once these spores mature, they are dispersed into the surrounding environment and will eventually germinate into gametophytes. In eusporangiate ferns, the gametophytes are subterranean (with the exception of Marattioid ferns) and non-photosynthetic, obtaining carbohydrates from a symbiotic relationship with a fungus. In homosporous leptosporangiate ferns, the gametophytes grow above ground and are photosynthetic. Gametophytes may either go on to produce both male (antheridia) and female (archegonia) sex organs, or they may produce them separately. Sperm in all ferns are motile, possessing several flagella that allow them to travel short distances. Many leptosporangiate ferns have small, heart-shaped (cordate) gametophytes that must therefore grow close enough together to allow for sperm to swim between them in order for outcrossing to occur (although some ferns are capable of self-fertilization). Once the sperm has united with the egg, a new diploid sporophyte grows directly from the gametophytic tissue, after which the gametophyte senesces and/or is subsumed within the new growth (Figure 6).

The heart-shaped gametophytes of most leptosporangiate ferns are often found in recently disturbed areas, as spores buried in the soil are then exposed and capable of germinating with little surrounding competition. The gametophytes then grow quickly in order to establish new sporophtyes before the next disturbance (Watkins, Mack, and Mulkey, 2007). A large percentage of ferns (

10%), however, are epiphytic, from having diversified in the canopies of angiosperm-dominated forests in the Cretaceous (Schuettpelz and Pryer, 2009). Life in tropical canopies imposes entirely different constraints on the growth of both sporophytes and gametophytes, requiring that each stage of the lifecycle adapt in order to survive. Tropical canopies support dense vegetation, which makes it hard for new plants to become established and compete for the limited available resources. Dense mats of bryophytes also hinder the growth of the gametophyte mats needed for outcrossing. The gametophytes of many epiphytic ferns consequently have a much more branched and dissected morphology than their terrestrial counterparts (either ribbon-shaped, filamentous, or strap-shaped), which is capable of continued meristematic growth (Figure 7) (Dassler and Farrar, 2001). This not only allows them to compete in a dense network of bryophyte growth, but if two spores land a significant distance from each other on the same tree, rather than having to undergo self-fertilization, these gametophytes can grow until they are close enough for sperm to swim between them.

The ability to grow continuously, and often asexually, in these gametophytes means that they can live indefinitely. Because of their small size, they can also exploit small, protected microhabitats in areas where conditions are otherwise unfavorable for their growth. Because the sporophytes are much larger, this means that gametophytes can often grow in places where the sporophyte can’t, which has led to a spatial separation of the two generations (Pinson et al., 2017). Gametophytes of some species have also been shown to tolerate a wider range of environmental conditions than their sporophyte counterparts (Watkins and Cardelús, 2009 Sato and Sakei, 1981). Around thirty known species of ferns have distributions in which the gametophyte occupies a wider geographic range than its sporophyte, and at least three fern species have no known sporophyte anywhere on Earth.

Literature cited

Beerling, D. J., Osborne, C. P., & Chaloner, W. G. (2001). Evolution of leaf-form in land plants linked to atmospheric CO2 decline in the Late Palaeozoic era. Nature. 410: 352-354.

Dassler, C. L., & Farrar, D. R. (2001). Significance of gametophyte form in long-distance colonization by tropical, epiphytic ferns. Brittonia. 53: 352-369.

Kenrick, P., & Crane, P. R. (1997). The origin and early diversification of land plants a cladistic study. Washington, DC: Smithsonian Institution Press.

Knie, N., Fischer, S., Grewe, F., Polsakiewicz, M., & Knoop, V. (2015). Horsetails are the sister group to all other monilophytes and Marattiales are sister to leptosporangiate ferns. Molecular phylogenetics and evolution. 90: 140-149.

Mora, C. I., Driese, S. G., & Colarusso, L. A. (1996). Middle to late Paleozoic atmospheric CO2 levels from soil carbonate and organic matter. Science. 271: 1105.

Pinson, J. B., Chambers, S. M., Nitta, J. H., Kuo, L. Y., & Sessa, E. B. (2017). The Separation of Generations: Biology and Biogeography of Long-Lived Sporophyteless Fern Gametophytes. International Journal of Plant Sciences. 178: 1-18.

PPG 1: The Pteridophyte Phylogeny Group*. (2016) A community-derived classification for extant lycophytes and ferns. Journal of Systematics and Evolution. 54: 563-603. *This project was organized by E Schuettpelz, H Schneider, AR Smith, P Hovenkamp, J Prado, G Rouhan, A Salino, M Sundue, TE Almeida, B Parris, EB Sessa, AR Field, AL de Gasper, CJ Rothfels, MD Windham, M Lehnert, B Dauphin, A Ebihara, S Lehtonen, PB Schwartsburd, J Metzgar, L-B Zhang, L-Y Kuo, PJ Brownsey, M Kato, and MD Arana, with 68 additional contributors.

Rothfels, C. J., Li, F. W., Sigel, E. M., Huiet, L., Larsson, A., Burge, D. O., . & Shaw, S. W. (2015). The evolutionary history of ferns inferred from 25 low-copy nuclear genes. American Journal of Botany. 102: 1089-1107.

Rothwell, G., & Stokey, R. (2008). Phylogeny and evolution of ferns: a paleontological perspective. In T. Ranker & C. Haufler (Eds.), Biology and Evolution of Ferns (pp. 332-366). Cambridge: Cambridge University Press.

Sato, T., & Sakai, A. (1981). Cold tolerance of gametophytes and sporophytes of some cool temperate ferns native to Hokkaido. Canadian Journal of Botany. 59: 604-608.

Schuettpelz, E., & Pryer, K. M. (2009). Evidence for a Cenozoic radiation of ferns in an angiosperm-dominated canopy. Proceedings of the National Academy of Sciences, 106: 11200-11205.

Sessa, E. B., Testo, W. L., & Watkins, J. E. (2016). On the widespread capacity for, and functional significance of, extreme inbreeding in ferns. New Phytologist. 211: 1108-1119.

Taylor, E. L., Taylor, T. N., & Krings, M. (2009). Paleobotany: the biology and evolution of fossil plants. London: Academic.

Testo, W., & Sundue, M. (2016). A 4000-species dataset provides new insight into the evolution of ferns. Molecular phylogenetics and evolution. 105: 200-211.

Watkins Jr, J. E., & Cardelús, C. (2009). Habitat differentiation of ferns in a lowland tropical rain forest. American Fern Journal. 99: 162-175.

Watkins, J. E., Mack, M. K., & Mulkey, S. S. (2007). Gametophyte ecology and demography of epiphytic and terrestrial tropical ferns. American Journal of Botany. 94:701-708.


Discussion

The soil environment in which plants interact is complex (Torsvik et al. 1996 Torsvik and Øvreås 2002). Bacterial diversity is likely to be high (Torsvik et al. 1990) and bacteria are known to participate in communication with plant roots (Bais et al. 2004). Less studied are potential interactions between soil bacteria and free-living gametophytes, such as those found in the fern lineage.

The soil bacterium used in our research is a pseudomonad best identified as P. nitroreducens using both 16S rRNA analysis and biochemical testing. The addition of this bacterium to cultures of C. richardii had profound effects on gametophyte development. The pseudomonad reduced the percentage of male gametophytes across a range of C. richardii densities and increased rhizoid and thalli growth, while decreasing rhizoid number in both hermaphrodite and male gametophytes.

Sex determination

In C. richardii, the presence of hermaphrodite-produced antheridiogen (ACE) can induce male development through a process known as induction. The pseudomonad used in these experiments reduced induction rates in C. richardii, resulting in a higher proportion of hermaphrodite gametophytes even when density was taken into account. The effects of ACE and other antheridiogens produced by other species are dosage dependent (Stevens and Werth 1999 Quintanilla et al. 2007 Ganger and Sturey 2012). Thus, a reduction in the concentration of ACE by the pseudomonad could explain the reduced percentages of hermaphrodites observed, for example, if the bacteria were using ACE as a carbon source. Other strains of P. nitroreducens have been shown to utilize complex molecules, such as estrogen, as a carbon source (Huang et al. 2014). ACE is thought to be a gibberellin (Warne and Hickok 1989 Yamane 1998), and there is a great deal of similarity between the basic structure of gibberellins and estrogen, though gibberellins are inherently more similar to androgens (Chailakhyan and Khrianin 1987). Additionally, members of the genus Pseudomonas have been shown to degrade complex hydrocarbons (Nie et al. 2010 Palleroni et al. 2010).

Alternatively, the pseudomonad may affect sex determination by altering nutrient availability and quality. Some have argued a link between environmental quality and the likelihood of undifferentiated gametophytes developing as males. Where environmental quality, specifically nutrient availability, is low, more males would be expected to develop given the increased resource demands of being a hermaphrodite (Haig and Westoby 1988). Versions of this hypothesis have been previously tested for C. richardii by Ayrapetov and Ganger (2009) and Goodnoe et al. (2016). In both cases, no effect of nutrient concentration on induction rates was found for the concentrations and stoichiometry of nutrients that were used however, there is some empirical support of a nutrient effect in another fern, Woodwardia radicans (DeSoto et al. 2008).

If the pseudomonad participates in nutrient cycling and frees up nutrients that would normally be unavailable to C. richardii, then these additional resources could affect induction rates. We do not consider this likely given that C-Fern media is widely used to culture C. richardii gametophytes and likely represents a high-quality resource environment. Alternatively, the bacterium may be yielding novel nutrients as the bacteria conduct metabolism or as bacteria decompose.

Gametophytes experiencing higher resource environments would likely be affected in other ways besides decreased induction rates. Growth rates of the gametophyte thallus and germination rates would be expected to increase as well. Hermaphrodite thalli were significantly larger in the presence of the pseudomonad than similarly aged thalli in the control. However, cumulative germination rates did not differ between C. richardii spores grown in the presence or absence of the pseudomonad for days 4𠄸 post sowing.

It is also possible that the bacterium identified as P. nitroreducens directly affects induction by releasing a molecule or molecules that function to communicate with C. richardii gametophytes. The pseudomonad could be producing abscisic acid (ABA). Soil bacteria, including members of the genus Pseudomonas (Naz and Bano 2010), have been shown to produce ABA (Karadeniz et al. 2006). Abscisic acid in culture increases the percentage of hermaphrodites (Warne and Hickok 1991) by acting in opposition to ACE, which is presumed to be a gibberellin (Warne and Hickok 1989 Yamane 1998).

Rhizoid development

The length and number of rhizoids increased between 9 and 19 days post sowing for both hermaphrodite and male gametophytes. However, the rates of increase and the effects of the pseudomonad and gametophyte area on hermaphrodite and male development were different, and thus the two types of gametophytes are considered separately.

In hermaphrodite gametophytes the pseudomonad increased rhizoid lengths when compared to control hermaphrodites. The effect was such that hermaphrodite rhizoids in the presence of the pseudomonad were 2.95× longer on average across all thalli sizes than control rhizoids. New rhizoids were produced at a slower rate in hermaphrodites grown with the pseudomonad such that control hermaphrodites had 1.23× more rhizoids across all thalli areas. The pseudomonad appears to have caused a change in resource allocation within hermaphrodites from a larger number of shorter rhizoids to a smaller number of longer rhizoids.

In male gametophytes the effect of the pseudomonad is more complex. As with hermaphroditic gametophytes the pseudomonad increased rhizoid length in male gametophytes by 2.72× when compared to the control, a number that is similar to the increase for hermaphrodite gametophytes. The addition of new rhizoids in male gametophytes grown in the presence of the pseudomonad was slower than for control male gametophytes. This overall effect of new rhizoid suppression was not consistent across all male gametophyte sizes, but was rather stronger in larger male gametophytes. Perhaps flexibility in new rhizoid development is not possible in males to the same extent as in hermaphrodites. This may be in part due to the smaller overall resource budget of males given their much smaller overall size.

Roots have been shown to engage in optimal foraging and are known to elongate in nutrient poor habitats and proliferate in nutrient rich habitats (Hodge 2004 Kembel and Cahill 2005 de Kroon and Mommer 2006). If rhizoids, the analogous structures in gametophytes (Jones and Dolan 2012), were to follow the same model, then the lengthening observed in C. richardii rhizoids might be due to lower overall nutrient quality. It is possible that the pseudomonad, through nitrate reduction, is lowering the levels of nitrate available to the gametophytes. However, if lower levels of nutrients are affecting rhizoid growth, then we might expect germination rates and thalli sizes to be affected as well. As discussed above, no differences in the germination rates of spores in the presence or absence of the bacteria were found. Additionally, though thalli sizes on all days were larger in the presence of the bacteria, this is counter to what would be predicted if the pseudomonad were lowering nitrogen availability.

In fact, the Pseudomonas genus is one of a number of genera described as plant growth promoting (PGP Lugtenberg and Kamilova 2009 Mitter et al. 2013). Members of the genus have been shown to increase root hair length in Arabidopsis thaliana (Contesto et al. 2008), increase overall biomass in Maize (Shaharoona et al. 2006) and Oryza sativa (Mirza et al. 2006), and increase root and shoot biomass in mung bean (Sharma and Johri 2003). The mechanisms behind such effects on sporophyte growth and development are not fully understood (Dey et al. 2004). However, one well-studied mechanism involves the bacterial production of phytohormones (Danger and Basu 1987 Patten and Glick 2002 Dobbelaere et al. 2003 Dey et al. 2004).

Many species of bacteria are known to communicate with plant roots hormonally. A large number of soil bacteria produce auxin (Patten and Glick 1996), including a strain of P. nitroreducens (Halda-Alija 2003) and many other species of the Pseudomonas genus (Glickmann et al. 1998 Patten and Glick 2002 Ahmad et al. 2005 Picard and Bosco 2005). The addition of auxin to sporophytes is known to stimulate root production, both adventitious and non-adventitious, and has been shown to increase the number of marginal rhizoids in C. richardii gametophytes at 2,4-dichlorophenoxyacetic acid (2,4-D) and α-napthaleneacetic acid (NAA) concentrations above 1 × 10 𢄦 (Hickok and Kiriluk 1984). Auxin has also been shown to increase the length of rhizoids in Physcomitrella (Sakakibara et al. 2003), a non-vascular plant. Synthetic and natural auxins have been shown to increase both cell size and division in gametophytes (Miller 1968). Interestingly, auxin has also been shown to affect sexual development in C. richardii by working to reduce the percentage of hermaphrodites in culture (Hickok and Kiriluk 1984). This is in contrast to the increased percentage of hermaphrodites in the presence of the pseudomonad observed in our experiments. The increased percentage of hermaphrodites in the presence of the pseudomonad does not negate the potential for auxin to influence rhizoid development in C. richardii, since different concentrations and forms of auxin may have contradictory results, or perhaps auxin release and either nutrient effects or ACE degradation are acting in concert. If separate mechanisms are at work on rhizoid development and sexual development, then it is likely that other soil bacteria may produce molecules that employ one but not the other mechanism, in which case it may be possible to decouple the effects on rhizoid development changes from effects on sex determination.

In addition to auxin, soil bacteria are known to produce cytokinins (Dey et al. 2004), ABA (Danger and Basu 1987 Dobbelaere et al. 2003), gibberellic acid (GA Sivasakthi et al. 2013) and jasmonic acid (JA Forchetti et al. 2007) and reduce ethylene production in plant roots (Li et al. 2000 Penrose and Glick 2001). Cytokinins have been shown to induce the formation of rhizoid initials in C. richardii gametophytes grown in the dark (Spiro et al. 2004). This effect is opposite to that seen here by gametophytes in the presence of the pseudomonad. Abscisic acid has been shown to increase rhizoid number in C. richardii at molarities between 1 × 10 𢄧 and 1 × 10 𢄥 M and inhibit their development at higher concentrations (Hickok 1983). Gibberellic acid has a relatively minor effect on gametophytic growth, while it has a major effect on sex determination (Miller 1968). Promotion of rhizoid elongation and cell division has been reported in the presence of GA, but only for low light environments (Miller 1968). Jasmonic acid has been studied in the fern Platycerium bifurcatum and promoted early gametophyte development by causing increased length and number of rhizoids and increased number of cells per gametophyte (Camloh et al. 1996).

Working with gametophytes directly in the environment is challenging due to difficulty in finding and identifying gametophytes to species (Schneider and Schuettpelz 2006). In the few studies that have explored sex determination of fern gametophytes in nature, higher percentages of hermaphrodites tend to occur (Schneller 1979 Ranker and Houston 2002). Working with fern gametophytes is made much easier by utilizing sterile culture in the laboratory. Doing so has facilitated the understanding of sex determination and rhizoid development. However, the interactions between gametophytes and bacteria in the soil paint a much more complex image of gametophyte sexual development and rhizoid development.


Published by William Salter

William (Tam) Salter is a Postdoctoral Research Fellow in the School of Life and Environmental Sciences and Sydney Institute of Agriculture at the University of Sydney. He has a bachelor degree in Ecological Science (Hons) from the University of Edinburgh and a PhD in plant ecophysiology from the University of Sydney. Tam is interested in the identification and elucidation of plant traits that could be useful for ecosystem resilience and future food security under global environmental change. He is also very interested in effective scientific communication.View all posts by William Salter

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Proteomic analysis of gametophytic sex expression in the fern Ceratopteris thalictroides

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.

Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1. The sex expression of C…

Fig 1. The sex expression of C . thalictroides gametophytes.

(A) Cultures grown on Knop's medium…

Fig 2. Morphological features of C .…

Fig 2. Morphological features of C . thalictroides gametophytes.

(A) Male gametophytes, (B, C) with antheridium…

Fig 3. Photosynthetic efficiency of C .…

Fig 3. Photosynthetic efficiency of C . thalictroides gametophytes.

(A) The activity of the chlorophyll fluorescence…

Fig 4. Representative 2-DE images of proteins…

Fig 4. Representative 2-DE images of proteins from C . thalictroides gametophytes.


Contents

Environmental sex determination is similar to certain forms [ vague ] of sexual selection in that there are oftentimes different and opposing selective pressures on males and females because of the costs of reproduction. Sexual selection is common throughout the tree of life (most known in birds) often resulting in sexual dimorphism, or size and appearance differences between sexes in the same species. [3] In environmental sex determination, selective pressures over evolutionary time have selected for flexibility in sex determination to optimize fitness in a heterogenous environment because of the different costs of sex in males and females. [4] Certain environmental conditions differentially affect each sex such that it would be beneficial to become one sex and not the other. [5] This is especially pertinent for sessile organisms that cannot move to a different environment. In plants, for example, female sexual function is often more energetically expensive because once fertilized they must use significant stored energy to produce fruits, seeds, or sporophytes whereas males must only produce sperm (and sperm-containing structure antheridium in seedless plants, and pollen in seed plants).

Lacking genetic information coding for separate sexes such as sex chromosomes, individuals that exhibit environmental sex determination contain genetic information coding for both sexes on autosomes. [6] In general, once exposed to certain environmental cues, epigenetic changes cause developing individuals to become either male or female. Environmental cues that often trigger the development of males or females include temperature, nutrient (or food in the case of animals) and water availability, photoperiod, competitive stress, and pheromones from conspecific individuals. [7] [8] Specific mechanisms and cues vary between species.

Crustaceans Edit

The amphipod crustacean Gammarus duebeni produces males early in the mating season, and females later, in response to the length of daylight, the photoperiod. Because male fitness improves more than female fitness with increased size, environmental sex determination is adaptive in this system by permitting males to experience a longer growing season than females. [9]

The branchiopod crustacean Daphnia magna parthenogenetically produces male progeny in response to a combination of three environmental factors, namely a reduced photoperiod in autumn, shortage of food and raised population density. [10]

Annelids Edit

Bonellia viridis, a marine worm, has location-dependent sex determination sex depends on where the larvae land. [11]

Vertebrates Edit

The sex of most amniote vertebrates, such as mammals and birds, is determined genetically. [12] However, some reptiles have temperature-dependent sex determination, where sex is permanently determined by thermal conditions experienced during the middle third of embryonic development. [13] [14] The sex of crocodilians and sphenodontians is exclusively determined by temperature. In contrast, squamates (lizards and snakes) and turtles exhibit both genotypic sex determination and temperature-dependent sex determination, although temperature dependence is much more common in turtles than in squamates. [15]

Ferns Edit

Most fern species (with a few exceptions, namely the Salvineales) are homosporous and lack sex chromosomes. Lacking genetic information coding for separate sexes, every fern spore has the capacity to become a male, female, or hermaphroditic gametophyte depending on the environment. [16] [17] In many fern species, including Ceratopteris richardii, environmental sex determination is linked to breeding systems. [18] Fern gametophytes exhibit a wide variety of breed systems which can be divided into outcrossing and inbreeding. To promote outcrossing, female gametophytes release a chemical pheromone known as Antheridiogen which controls the sex of nearby developing gametophytes. [19] Antheridiogen secreted by females promotes the development of nearby asexual gametophytes into males. This is adaptive because inducing maleness increases the probability of outcrossing as males provide sperm for the females rather than the females becoming hermaphroditic (or bisexual) and self-fertilizing. However, if no fertilization occurs, the female gametophyte can still become hermaphroditic and self-fertilize if the conditions are conducive to growth, ultimately resulting in inbreeding depression.

Additionally, similar to crocodilians, homosporous fern gametophyte sex is determined by the abiotic environment in accordance with the size-advantage model. In stressful environments (crowding or nutrient stress), gametophytes are smaller and develop into males. While in more favorable growing conditions, gametophytes are larger and develop into females. [20] [21]

Moss Edit

Moss gametophytes can be either asexual, female, male, or hermaphroditic like ferns. Unlike homosporous ferns, moss gametophytes can be either monoicous or dioicous (similar to monoecious and dioecious in vascular plants), with most studied dioicous species exhibiting genetic sex determination via the UV sex chromosome sex determination system. Some monoicous moss species such as Splachnum ampullaceum exhibit environmental sex determination during early development, with low light, low pH, and low nutrient availability all promoting male development. [22] In the presence of auxin, a widespread plant hormone, or gibberellins, compounds similar to Antheridiogen in ferns, both female and male individuals invest more in sexual structures (antheridia and archegonia). [23] Environmental sex determination in moss is fundamentally different from the spatial segregation of sexes, the occurrence of environmentally mediated sex ratios in moss patches, observed in sexually static moss species. Spatial segregation of the sexes in mosses is caused by differential survival rates between sexes as a result of the competitive advantage of female moss. [24] [25] This leads to female dominated populations maintained by asexual reproduction and minimal sexual reproduction. In contrast, environmental sex determination is the dynamic development of females or males in different environmental conditions.

Angiosperms Edit

Many angiosperms exhibit sequential hermaphroditism, meaning that they can switch sexes continually throughout their life based on the current conditions and resource availability to optimize fitness each flowering season. [26] But sequential hermaphroditism and environmental sex determination are not mutually exclusive. For example, Catasetum viridiflavum, an epiphyte (plant that grows on another plant) in the Orchidaceae family exhibits sequential hermaphroditism where the younger, smaller individuals have male inflorescences and the older, larger individuals have female inflorescences, but sex expression is also strongly influenced by light intensity. Individuals in high light are more often female and individuals in the low light are more often male, regardless of size. [27] [28] In higher light, individuals produce more ethylene, a common plant hormone, which promotes the formation of female flowers.


References & further reading:

Campbell Biology, Chapter 29: How Plants Colonized Land. In particular, study the diagram of the life cycle of a fern (fig. 29.11, 10th edition).

Sex and the single fern. Tai-ping Sun, 2014, Science Vol. 346 no. 6208 pp. 423-424. Fern gametophytes can be male, female, or both, but their sex isn't genetically determined. Older gametophytes secrete pheromones that can determine the sex of newly developing gametophytes that haven't determined their sex yet. This brief, accesible Perspective article is based on the research article Antheridiogen determines sex in ferns via a spatiotemporally split gibberellin synthesis pathway. For an even briefer news article, see Ferns communicate to decide their sexes in Nature.



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