Gynodioecy is a reproductive system of interest for evolutionary biologists, as it poses the question of how females can be maintained while competing with hermaphrodites that possess both male and female functions. One necessary condition for the maintenance of this polymorphism is the occurrence of a female advantage, i.e. a better seed production or quality by females compared with hermaphrodites. Theoretically, its magnitude can be low when sterility mutations are cytoplasmic, while a 2-fold advantage is needed in the case of nuclear sterility. Such a difference is often thought to be due to reduced inbreeding depression in obligatory outcrossed females. Finally, variation in sex ratio and female advantage occur among populations of some gynodioecious species, though the prevalence of such variation is unknown.
By reviewing and analysing the data published on 48 gynodioecious species, we examined three important issues about female advantage. (1) Are reduced selfing and inbreeding depression likely to be the major cause of female advantage? (2) What is the magnitude of female advantage and does it fit theoretical predictions? (3) Does the occurrence or the magnitude of female advantage vary among populations within species and why?
It was found that a female advantage occurred in 40 species, with a magnitude comprised between 1 and 2 in the majority of cases. In many species, reduced selfing may not be a necessary cause of this advantage. Finally, female advantage varied among populations in some species, but both positive and negative correlations were found with female frequency. The role of reduced selfing in females for the evolution of gynodioecy, as well as the various processes that affect sex ratios and female advantage in populations are discussed.
Female advantage; female compensation; male sterility; gynodioecy; inbreeding depression; mating system; resource allocation; sex ratio; self-incompatibility
Baker's Law states that colonization by self-compatible organisms is more likely to be successful than colonization by self-incompatible organisms because of the ability for self-compatible organisms to produce offspring without pollination agents. This simple model has proved very successful in plant ecology and has been applied to various contexts, including colonizing or ruderal species, islands colonizers, invasive species or mating system variation across distribution ranges. Moreover, it is one of the only models in population biology linking two traits of major importance in ecology, namely dispersal and mating system. Although Baker's Law has stimulated a large number of empirical studies reporting the association of self-fertilization and colonizing ability in various contexts, the data have not established a general pattern for the association of traits.
In this paper, a critical position is adopted to discuss and clarify Baker's Law. From the literature referring to Baker's Law, an analysis made regarding how mating success is considered in such studies and discrepancies with population genetics theory of mating systems are highlighted. The data reporting the association of self-fertilization and colonizing ability are also briefly reviewed and the potential bias in interpretation is discussed. Lastly, a recent theoretical model analysing the link between colonizing ability and self-fertilization is considered.
Evolutionary predictions are actually more complex than Baker's intuitive arguments. It appears that Baker's Law encompasses a variety of ecological scenarios, which cannot be considered a priori as equivalent. Questioning what has been considered as self-evident for more than 50 years seems a reasonable objective to analyse in-depth dispersal and mating system traits.
Self-fertilization; dispersal; syndrome; Baker's Law; empirical data; models
The trailing edges of species ranges are becoming a subject of increasing interest as the environment changes due to global warming. Trailing edge populations are likely to face extinction because of a decline in numbers and an inability to evolve new adaptations with sufficient speed. Discussions of character change in the trailing edge have focused on physiological, exomorphic and phenological traits. The mating pattern within populations has not been part of the discourse, in spite of the fact that the mating pattern may affect the ability of populations to respond to environmental change and to maintain their sizes. In this paper, the case is made that a substantial increase in self-fertilization rates may occur via plastic responses to stress.
Scope and Conclusions
Small populations on the trailing edge are especially vulnerable to environmental change because of inadequate levels of cross-fertilization. Evidence is presented that a deficiency of cross-seed production is due to inadequate pollinator services and a paucity of self-incompatibility alleles within populations. Evidence also is presented that if plants are self-compatible, self-fertilization may compensate in part for this deficiency through a stress-induced increase in levels of self-compatibility and stress-induced alterations in floral morphology that elevate self-pollination. Whereas increased self-fertility may afford populations the time to adapt to their changing environments, it can be concluded that increased selfing is not a panacea for the ills of environmental change, because it will lead to substantial reductions in genetic diversity, which may render adaptation unlikely.
Environmental change; mating system; phenotypic plasticity; self-fertilization; self-pollination; trailing edge
The ‘gynodioecy–dioecy pathway’ is considered to be one of the most important evolutionary routes from hermaphroditism to separate sexes (dioecy). Despite a large accumulation of evidence for female seed fertility advantages in gynodioecious species (females and hermaphrodites coexist) in support of the first step in the gynodioecy–dioecy pathway, we still have very little evidence for the second step, i.e. the transition from gynodioecy to dioecy.
We review the literature to evaluate whether basic predictions by theory are supported. To establish whether females' seed fertility advantage and frequencies are sufficient to favour the invasion of males, we review these for species along the gynodioecy–dioecy pathway published in the last 5 years. We then review the empirical evidence for predictions deriving from the second step, i.e. hermaphrodites' male fertility increases with female frequency, selection favours greater male fertility in hermaphrodites in gynodioecious species, and, where males and hermaphrodites coexist with females (subdioecy), males have greater male fertility than hermaphrodites. We review how genetic control and certain ecological features (pollen limitation, selfing, plasticity in sex expression and antagonists) influence the trajectory of a population along the gynodioecy–dioecy pathway.
Females tend to have greater seed fertility advantages over hermaphrodites where the two coexist, and this advantage is positively correlated with female frequency across species, as predicted by theory. A limited number of studies in subdioecious species have demonstrated that males have an advantage over hermaphrodites, as also predicted by theory. However, less evidence exists for phenotypic selection to increase male traits of hermaphrodites or for increasing male function of hermaphrodites in populations with high female frequency. A few key case studies underline the importance of examining multiple components of male fertility and the roles of pollen limitation, selfing and plasticity, when evaluating advantages. We conclude that we do not yet have a full understanding of the transition from gynodioecy to dioecy.
Breeding system; dioecy; gynodioecy; male fertility; pollen limitation; plasticity; sex ratio; sexual systems; subdioecy; trioecy
The field of plant mating-system evolution has long been interested in understanding why selfing evolves from outcrossing. Many possible mechanisms drive this evolutionary trend, but most research has focused upon the transmission advantage of selfing and its ability to provide reproductive assurance when cross-pollination is uncertain. We discuss the shared conceptual framework of these ideas and their empirical support that is emerging from tests of their predictions over the last 25 years.
These two hypotheses are derived from the same strategic framework. The transmission advantage hypothesis involves purely gene-level selection, with reproductive assurance involving an added component of individual-level selection. Support for both of these ideas has been garnered from population-genetic tests of their predictions. Studies in natural populations often show that selfing increases seed production, but it is not clear if this benefit is sufficient to favour the evolution of selfing, and the ecological agents limiting outcross pollen are often not identified. Pollen discounting appears to be highly variable and important in systems where selfing involves multiple floral adaptations, yet seed discounting has rarely been investigated. Although reproductive assurance appears likely as a leading factor facilitating the evolution of selfing, studies must account for both seed and pollen discounting to adequately test this hypothesis.
The transmission advantage and reproductive assurance ideas describe components of gene transmission that favour selfing. Future work should move beyond their dichotomous presentation and focus upon understanding whether selection through pollen, seed or both explains the spread of selfing-rate modifiers in plant populations.
Demography; inbreeding depression; mating systems; outcrossing; pollen discounting; pollination; seed discounting
A plant is considered carnivorous if it receives any noticeable benefit from catching small animals. The morphological and physiological adaptations to carnivorous existence is most complex in plants, thanks to which carnivorous plants have been cited by Darwin as ‘the most wonderful plants in the world’. When considering the range of these adaptations, one realizes that the carnivory is a result of a multitude of different features.
This review discusses a selection of relevant articles, culled from a wide array of research topics on plant carnivory, and focuses in particular on physiological processes associated with active trapping and digestion of prey. Carnivory offers the plants special advantages in habitats where nutrient supply is scarce. Counterbalancing costs are the investments in synthesis and the maintenance of trapping organs and hydrolysing enzymes. With the progress in genetic, molecular and microscopic techniques, we are well on the way to a full appreciation of various aspects of plant carnivory.
Sufficiently complex to be of scientific interest and finite enough to allow conclusive appraisal, carnivorous plants can be viewed as unique models for the examination of rapid organ movements, plant excitability, enzyme secretion, nutrient absorption, food-web relationships, phylogenetic and intergeneric relationships or structural and mineral investment in carnivory.
Carnivorous plants; model plants; traps; rapid organ movements; gland functioning; nutrient absorption; action potentials; plant excitability; plant indicators
Stomatal guard cells are the regulators of gas exchange between plants and the atmosphere. Ca2+-dependent and Ca2+-independent mechanisms function in these responses. Key stomatal regulation mechanisms, including plasma membrane and vacuolar ion channels have been identified and are regulated by the free cytosolic Ca2+ concentration ([Ca2+]cyt).
Here we show that CO2-induced stomatal closing is strongly impaired under conditions that prevent intracellular Ca2+ elevations. Moreover, Ca2+ oscillation-induced stomatal closing is partially impaired in knock-out mutations in several guard cell-expressed Ca2+-dependent protein kinases (CDPKs) here, including the cpk4cpk11 double and cpk10 mutants; however, abscisic acid-regulated stomatal movements remain relatively intact in the cpk4cpk11 and cpk10 mutants. We further discuss diverse studies of Ca2+ signalling in guard cells, discuss apparent peculiarities, and pose novel open questions. The recently proposed Ca2+ sensitivity priming model could account for many of the findings in the field. Recent research shows that the stomatal closing stimuli abscisic acid and CO2 enhance the sensitivity of stomatal closing mechanisms to intracellular Ca2+, which has been termed ‘calcium sensitivity priming’. The genome of the reference plant Arabidopsis thaliana encodes for over 250 Ca2+-sensing proteins, giving rise to the question, how can specificity in Ca2+ responses be achieved? Calcium sensitivity priming could provide a key mechanism contributing to specificity in eukaryotic Ca2+ signal transduction, a topic of central interest in cell signalling research. In this article we further propose an individual stomatal tracking method for improved analyses of stimulus-regulated stomatal movements in Arabidopsis guard cells that reduces noise and increases fidelity in stimulus-regulated stomatal aperture responses (
Box 1). This method is recommended for stomatal response research, in parallel to previously adopted blind analyses, due to the relatively small and diverse sizes of stomatal apertures in the reference plant Arabidopsis thaliana.
Stomata; ABA; guard cell; Ca2+; CDPK; calcium sensitivity priming; carbon dioxide; Arabidopsis thaliana
Biological invasions are a major ecological and socio-economic problem in many parts of the world. Despite an explosion of research in recent decades, much remains to be understood about why some species become invasive whereas others do not. Recently, polyploidy (whole genome duplication) has been proposed as an important determinant of invasiveness in plants. Genome duplication has played a major role in plant evolution and can drastically alter a plant's genetic make-up, morphology, physiology and ecology within only one or a few generations. This may allow some polyploids to succeed in strongly fluctuating environments and/or effectively colonize new habitats and, thus, increase their potential to be invasive.
We synthesize current knowledge on the importance of polyploidy for the invasion (i.e. spread) of introduced plants. We first aim to elucidate general mechanisms that are involved in the success of polyploid plants and translate this to that of plant invaders. Secondly, we provide an overview of ploidal levels in selected invasive alien plants and explain how ploidy might have contributed to their success.
Polyploidy can be an important factor in species invasion success through a combination of (1) ‘pre-adaptation’, whereby polyploid lineages are predisposed to conditions in the new range and, therefore, have higher survival rates and fitness in the earliest establishment phase; and (2) the possibility for subsequent adaptation due to a larger genetic diversity that may assist the ‘evolution of invasiveness’. Alternatively, polyploidization may play an important role by (3) restoring sexual reproduction following hybridization or, conversely, (4) asexual reproduction in the absence of suitable mates. We, therefore, encourage invasion biologists to incorporate assessments of ploidy in their studies of invasive alien species.
Biological invasions; genome size; invasiveness; invasion ecology; polyploidy; whole genome duplication
The large-scale clonal propagation of oil palm (Elaeis guineensis) is being stalled by the occurrence of the mantled somaclonal variation. Indeed, this abnormality which presents a homeotic-like conversion of male floral organs into carpelloid structures, hampers oil production since the supernumerary female organs are either sterile or produce fruits with poor oil yields.
In the last 15 years, the prevailing point of view on the origin of the mantled floral phenotype has evolved from a random mutation event triggered by in vitro culture to a hormone-dependent dysfunction of gene regulation processes. In this review, we retrace the history of the research on the mantled variation in the light of the parallel advances made in the understanding of plant development regulation in model systems and more specifically in the role of epigenetic mechanisms. An overview of the current state of oil palm genomic and transcriptomic resources, which are key to any comparison with model organisms, is given. We show that, while displaying original characteristics, the mantled phenotype of oil palm is morphologically, and possibly molecularly, related to MADS-box genes mutants described in model plants. We also discuss the occurrence of comparable floral phenotypes in other palm species.
Beyond its primary interest in the search for discriminating markers against an economically crippling phenotype, the study of the mantled abnormality also provides a unique opportunity to investigate the regulation of reproductive development in a perennial tropical palm. On the basis of recent results, we propose that future efforts should concentrate on the epigenetic regulation targeting MADS-box genes and transposable elements of oil palm, since both types of sequences are most likely to be involved in the mantled variant phenotype.
Epigenetics; flower development; clonal fidelity; MADS-box; mantled phenotype; somaclonal variation; transposable elements; Elaeis guineensis
The palm family occurs in all tropical and sub-tropical regions of the world. Palms are of high ecological and economical importance, and display complex spatial patterns of species distributions and diversity.
This review summarizes empirical evidence for factors that determine palm species distributions, community composition and species richness such as the abiotic environment (climate, soil chemistry, hydrology and topography), the biotic environment (vegetation structure and species interactions) and dispersal. The importance of contemporary vs. historical impacts of these factors and the scale at which they function is discussed. Finally a hierarchical scale framework is developed to guide predictor selection for future studies.
Determinants of palm distributions, composition and richness vary with spatial scale. For species distributions, climate appears to be important at landscape and broader scales, soil, topography and vegetation at landscape and local scales, hydrology at local scales, and dispersal at all scales. For community composition, soil appears important at regional and finer scales, hydrology, topography and vegetation at landscape and local scales, and dispersal again at all scales. For species richness, climate and dispersal appear to be important at continental to global scales, soil at landscape and broader scales, and topography at landscape and finer scales. Some scale–predictor combinations have not been studied or deserve further attention, e.g. climate on regional to finer scales, and hydrology and topography on landscape and broader scales. The importance of biotic interactions – apart from general vegetation structure effects – for the geographic ecology of palms is generally underexplored. Future studies should target scale–predictor combinations and geographic domains not studied yet. To avoid biased inference, one should ideally include at least all predictors previously found important at the spatial scale of investigation.
Arecaceae; biotic interactions; climate; dispersal limitation; geographic ecology; hydrology; Palmae; spatial scale; species distributions; species richness; soil; topography
The African oil palm (Elaeis guineensis) is a monoecious species of the palm subfamily Arecoideae. It may be qualified as ‘temporally dioecious’ in that it produces functionally unisexual male and female inflorescences in an alternating cycle on the same plant, resulting in an allogamous mode of reproduction. The ‘sex ratio’ of an oil palm stand is influenced by both genetic and environmental factors. In particular, the enhancement of male inflorescence production in response to water stress has been well documented.
This paper presents a review of our current understanding of the sex determination process in oil palm and discusses possible insights that can be gained from other species. Although some informative phenological studies have been carried out, nothing is as yet known about the genetic basis of sex determination in oil palm, nor the mechanisms by which this process is regulated. Nevertheless new genomics-based techniques, when combined with field studies and biochemical and molecular cytological-based approaches, should provide a new understanding of the complex processes governing oil palm sex determination in the foreseeable future. Current hypotheses and strategies for future research are discussed.
Sex determination; oil palm; Elaeis guineensis; inflorescence; monoecious; temporal dioecy; flowering
With more than 90 published studies of pollination mechanisms, the palm family is one of the better studied tropical families of angiosperms. Understanding palm–pollinator interactions has implications for tropical silviculture, agroforestry and horticulture, as well as for our understanding of palm evolution and diversification. We review the rich literature on pollination mechanisms in palms that has appeared since the last review of palm pollination studies was published 25 years ago.
Scope and Conclusions
Visitors to palm inflorescences are attracted by rewards such as food, shelter and oviposition sites. The interaction between the palm and its visiting fauna represents a trade-off between the services provided by the potential pollinators and the antagonistic activities of other insect visitors. Evidence suggests that beetles constitute the most important group of pollinators in palms, followed by bees and flies. Occasional pollinators include mammals (e.g. bats and marsupials) and even crabs. Comparative studies of palm–pollinator interactions in closely related palm species document transitions in floral morphology, phenology and anatomy correlated with shifts in pollination vectors. Synecological studies show that asynchronous flowering and partitioning of pollinator guilds may be important regulators of gene flow between closely related sympatric taxa and potential drivers of speciation processes. Studies of larger plant–pollinator networks point out the importance of competition for pollinators between palms and other flowering plants and document how the insect communities in tropical forest canopies probably influence the reproductive success of palms. However, published studies have a strong geographical bias towards the South American region and a taxonomic bias towards the tribe Cocoseae. Future studies should try to correct this imbalance to provide a more representative picture of pollination mechanisms and their evolutionary implications across the entire family.
Palm-pollinator interactions; cantharophily; mellitophily; myophily; co-evolutionary relationships; Arecaceae
New roles for flavonoids, as developmental regulators and/or signalling molecules, have recently been proposed in eukaryotic cells exposed to a wide range of environmental stimuli. In plants, these functions are actually restricted to flavonols, the ancient and widespread class of flavonoids. In mosses and liverworts, the whole set of genes for flavonol biosynthesis – CHS, CHI, F3H, FLS and F3′H – has been detected. The flavonol branch pathway has remained intact for millions of years, and is almost exclusively involved in the responses of plants to a wide array of stressful agents, despite the fact that evolution of flavonoid metabolism has produced >10 000 structures.
Here the emerging functional roles of flavonoids in the responses of present-day plants to different stresses are discussed based on early, authoritative views of their primary functions during the colonization of land by plants. Flavonols are not as efficient as other secondary metabolites in absorbing wavelengths in the 290–320 nm spectral region, but display the greatest potential to keep stress-induced changes in cellular reactive oxygen species homeostasis under control, and to regulate the development of individual organs and the whole plant. Very low flavonol concentrations, as probably occurred in early terrestrial plants, may fully accomplish these regulatory functions.
During the last two decades the routine use of genomic, chromatography/mass spectrometry and fluorescence microimaging techniques has provided new insights into the regulation of flavonol metabolism as well as on the inter- and intracellular distribution of stress-responsive flavonols. These findings offer new evidence on how flavonols may have performed a wide array of functional roles during the colonization of land by plants. In our opinion this ancient flavonoid class is still playing the same old and robust roles in present-day plants.
Auxin transport; early flavonoid genes; evolution of early terrestrial plants; flavonol metabolism; Myb genes; ROS scavengers; stress-responsive flavonoids; sub-cellular flavonoid distribution; UV-B screening
For the Solanaceae-type self-incompatibility, also possessed by Rosaceae and Plantaginaceae, the specificity of self/non-self interactions between pollen and pistil is controlled by two polymorphic genes at the S-locus: the S-locus F-box gene (SLF or SFB) controls pollen specificity and the S-RNase gene controls pistil specificity.
This review focuses on the work from the authors' laboratory using Petunia inflata (Solanaceae) as a model. Here, recent results on the identification and functional studies of S-RNase and SLF are summarized and a protein-degradation model is proposed to explain the biochemical mechanism for specific rejection of self-pollen tubes by the pistil.
The protein-degradation model invokes specific degradation of non-self S-RNases in the pollen tube mediated by an SLF, and can explain compatible versus incompatible pollination and the phenomenon of competitive interaction, where SI breaks down in pollen carrying two different S-alleles. In Solanaceae, Plantaginaceae and subfamily Maloideae of Rosaceae, there also exist multiple S-locus-linked SLF/SFB-like genes that potentially function as the pollen S-gene. To date, only three such genes, all in P. inflata, have been examined, and they do not function as the pollen S-gene in the S-genotype backgrounds tested. Interestingly, subfamily Prunoideae of Rosaceae appears to possess only a single SLF/SFB gene, and competitive interaction, observed in Solanaceae, Plantaginaceae and subfamily Maloideae, has not been observed. Thus, although the cytotoxic function of S-RNase is an integral part of SI in Solanaceae, Plantaginaceae and Rosaceae, the function of SLF/SFB may have diverged. This highlights the complexity of the S-RNase-based SI mechanism. The review concludes by discussing some key experiments that will further advance our understanding of this self/non-self discrimination mechanism.
Competitive interaction; Petunia inflata; Plantaginaceae; protein degradation; Rosaceae; self-incompatibility; S-locus F-box protein; Solanaceae; S-RNase; ubiquitination
Pollination is a crucial step in angiosperm (flowering plant) reproduction. Highly orchestrated pollen–pistil interactions and signalling events enable plant species to avoid inbreeding and outcrossing as a species-specific barrier. In compatible pollination, pollen tubes carrying two sperm cells grow through the pistil transmitting tract and are precisely guided to the ovules, discharging the sperm cells to the embryo sac for fertilization.
In Lilium longiflorum pollination, growing pollen tubes utilize two critical mechanisms, adhesion and chemotropism, for directional growth to the ovules. Among several molecular factors discovered in the past decade, two small, secreted cysteine-rich proteins have been shown to play major roles in pollen tube adhesion and reorientation bioassays: stigma/style cysteine-rich adhesin (SCA, approx. 9·3 kDa) and chemocyanin (approx. 9·8 kDa). SCA, a lipid transfer protein (LTP) secreted from the stylar transmitting tract epidermis, functions in lily pollen tube tip growth as well as in forming the adhesive pectin matrix at the growing pollen tube wall back from the tip. Lily chemocyanin is a plantacyanin family member and acts as a directional cue for reorienting pollen tubes. Recent consecutive studies revealed that Arabidopsis thaliana homologues for SCA and chemocyanin play pivotal roles in tip polarity and directionality of pollen tube growth, respectively. This review outlines the biological roles of various secreted proteins in angiosperm pollination, focusing on plant LTPs and chemocyanin.
Angiosperm fertilization; Arabidopsis thaliana; chemocyanin; cysteine-rich peptides (CRPs); Lilium longiflorum; lipid transfer proteins (LTPs); plantacyanins; pollen tube tip growth; stigma/style cysteine-rich adhesin (SCA)
In contrast to animals and lower plants such as mosses and ferns, sperm cells of flowering plants (angiosperms) are immobile and require transportation to the female gametes via the vegetative pollen tube cell to achieve double fertilization. The path of the pollen tube towards the female gametophyte (embryo sac) has been intensively studied in many intra- and interspecific crossing experiments with the aim of increasing the gene pool of crop plants for greater yield, improved biotic and abiotic stress resistance, and for introducing new agronomic traits. Many attempts to hybridize different species or genotypes failed due to the difficulty for the pollen tubes in reaching the female gametophyte. Detailed studies showed that these processes are controlled by various self-incompatible (intraspecific) and cross-incompatible (interspecific) hybridization mechanisms.
Understanding the molecular mechanisms of crossing barriers is therefore of great interest in plant reproduction, evolution and breeding research. In particular, pre-zygotic hybridization barriers related to pollen tube germination, growth, guidance and sperm delivery, which are considered the major hybridization controls in nature and thus also contribute to species isolation and speciation, have been intensively investigated. Despite this general interest, surprisingly little is known about these processes in the most important agronomic plant family, the Gramineae, Poaceae or grasses. Small polymorphic proteins and their receptors, degradation of sterility locus proteins and general compounds such as calcium, γ-aminobutyric acid or nitric oxide have been shown to be involved in progamic pollen germination, adhesion, tube growth and guidance, as well as sperm release. Most advances have been made in the Brassicaceae, Papaveraceae, Linderniaceae and Solanaceae families including their well-understood self-incompatibility (SI) systems. Grass species evolved similar mechanisms to control the penetration and growth of self-pollen to promote intraspecific outcrossing and to prevent fertilization by alien sperm cells. However, in the Poaceae, the underlying molecular mechanisms are still largely unknown.
We propose to develop maize (Zea mays) as a model to investigate the above-described processes to understand the associated intra- and interspecific crossing barriers in grasses. Many genetic, cellular and biotechnological tools including the completion of a reference genome (inbred line B73) have been established in the last decade and many more maize inbred genomes are expected to be available soon. Moreover, a cellular marker line database as well as large transposon insertion collections and improved Agrobacterium transformation protocols are now available. Additionally, the processes described above are well studied at the morphological level and a number of mutants have been described already, awaiting disclosure of the relevant genes. The identification of the first key players in pollen tube growth, guidance and burst show maize to be an excellent grass model to investigate these processes in more detail. Here we provide an overview of our current understanding of these processes in Poaceae with a focus on maize, and also include relevant discoveries in eudicot model species.
Maize; male germline; sperm cell; interspecific crosses; self- and cross-incompatibility; pollen tube growth and guidance; fertilization; reproductive isolation
Background and Aims
Sexual reproduction in angiosperms involves a network of signalling and interactions between pollen and pistil. To promote out-breeding, an additional layer of interactions, involving self-incompatibility (SI), is used to prevent self-fertilization. SI is generally controlled by the S-locus, and comprises allelic pollen and pistil S-determinants. This provides the basis of recognition, and consequent rejection, of incompatible pollen. In Papaver rhoeas, SI involves interaction of pistil PrsS and pollen PrpS, triggering a Ca2+-dependent signalling network. This results in rapid and distinctive alterations to both the actin and microtubule cytoskeleton being triggered in ‘self’ pollen. Some of these alterations are implicated in mediating programmed cell death, involving activation of several caspase-like proteases.
Here we review and discuss our current understanding of the cytoskeletal alterations induced in incompatible pollen during SI and their relationship with programmed cell death. We focus on data relating to the formation of F-actin punctate foci, which have, to date, not been well characterized. The identification of two actin-binding proteins that interact with these structures are reviewed. Using an approach that enriched for F-actin from SI-induced pollen tubes using affinity purification followed by mass spectrometry, further proteins were identified as putative interactors with the F-actin foci in an SI situation.
Previously two important actin-binding proteins, CAP and ADF, had been identified whose localization altered with SI, both showing co-localization with the F-actin punctate foci based on immunolocalization studies. Further analysis has identified differences between proteins associated with F-actin from SI-induced pollen samples and those associated with F-actin in untreated pollen. This provides candidate proteins implicated in either the formation or stabilization of the punctate actin structures formed during SI.
This review brings together for the first time, our current understanding of proteins and events involved in SI-induced signalling to the actin cytoskeleton in incompatible Papaver pollen.
Actin cytoskeleton; actin-binding proteins; mass spectrometry; Papaver rhoeas; pollen; self-incompatibility; signalling
The conical epidermal cells found on the petals of most Angiosperm species are so widespread that they have been used as markers of petal identity, but their function has only been analysed in recent years. This review brings together diverse data on the role of these cells in pollination biology.
The published effects of conical cells on petal colour, petal reflexing, scent production, petal wettability and pollinator grip on the flower surface are considered. Of these factors, pollinator grip has been shown to be of most significance in the well-studied Antirrhinum majus/bumble-bee system. Published data on the relationship between epidermal cell morphology and floral temperature were limited, so an analysis of the effects of cell shape on floral temperature in Antirrhinum is presented here. Statistically significant warming by conical cells was not detected, although insignificant trends towards faster warming at dawn were found, and it was also found that flat-celled flowers could be warmer on warm days. The warming observed is less significant than that achieved by varying pigment content. However, the possibility that the effect of conical cells on temperature might be biologically significant in certain specific instances such as marginal habitats or weather conditions cannot be ruled out.
Conical epidermal cells can influence a diverse set of petal properties. The fitness benefits they provide to plants are likely to vary with pollinator and habitat, and models are now required to understand how these different factors interact.
Antirrhinum majus; conical cell; epidermis; floral scent; floral temperature; flower colour; grip; petal; pollination; wettability
Pollen–pistil interactions are an essential prelude to fertilization in angiosperms and determine compatibility/incompatibility. Pollen–pistil interactions have been studied at a molecular and cellular level in relatively few families. Self-incompatibility (SI) is the best understood pollen–pistil interaction at a molecular level where three different molecular mechanisms have been identified in just five families. Here we review studies of pollen–pistil interactions and SI in the Asteraceae, an important family that has been relatively understudied in these areas of reproductive biology.
We begin by describing the historical literature which first identified sporophytic SI (SSI) in species of Asteraceae, the SI system later identified and characterized at a molecular level in the Brassicaceae. Early structural and cytological studies in these two families suggested that pollen–pistil interactions and SSI were similar, if not the same. Recent cellular and molecular studies in Senecio squalidus (Oxford ragwort) have challenged this belief by revealing that despite sharing the same genetic system of SSI, the Brassicaceae and Asteraceae molecular mechanisms are different. Key cellular differences have also been highlighted in pollen–stigma interactions, which may arise as a consequence of the Asteraceae possessing a ‘semi-dry’ stigma, rather than the ‘dry’ stigma typical of the Brassicaceae. The review concludes with a summary of recent transcriptomic analyses aimed at identifying proteins regulating pollen–pistil interactions and SI in S. squalidus, and by implication the Asteraceae. The Senecio pistil transcriptome contains many novel pistil-specific genes, but also pistil-specific genes previously shown to play a role in pollen–pistil interactions in other species.
Studies in S. squalidus have shown that stigma structure and the molecular mechanism of SSI in the Asteraceae and Brassicaceae are different. The availability of a pool of pistil-specific genes for S. squalidus offers an opportunity to elucidate the molecular mechanisms of pollen–pistil interactions and SI in the Asteraceae.
Asteraceae; Senecio; pistil; stigma; pollen; pollen–pistil interactions; self-incompatibility; transcriptome
S-RNase-based self-incompatibility (SI) occurs in the Solanaceae, Rosaceae and Plantaginaceae. In all three families, compatibility is controlled by a polymorphic S-locus encoding at least two genes. S-RNases determine the specificity of pollen rejection in the pistil, and S-locus F-box proteins fulfill this function in pollen. S-RNases are thought to function as S-specific cytotoxins as well as recognition proteins. Thus, incompatibility results from the cytotoxic activity of S-RNase, while compatible pollen tubes evade S-RNase cytotoxicity.
The S-specificity determinants are known, but many questions remain. In this review, the genetics of SI are introduced and the characteristics of S-RNases and pollen F-box proteins are briefly described. A variety of modifier genes also required for SI are also reviewed. Mutations affecting compatibility in pollen are especially important for defining models of compatibility and incompatibility. In Solanaceae, pollen-side mutations causing breakdown in SI have been attributed to the heteroallelic pollen effect, but a mutation in Solanum chacoense may be an exception. This has been interpreted to mean that pollen incompatibility is the default condition unless the S-locus F-box protein confers resistance to S-RNase. In Prunus, however, S-locus F-box protein gene mutations clearly cause compatibility.
Two alternative mechanisms have been proposed to explain compatibility and incompatibility: compatibility is explained either as a result of either degradation of non-self S-RNase or by its compartmentalization so that it does not have access to the pollen tube cytoplasm. These models are not necessarily mutually exclusive, but each makes different predictions about whether pollen compatibility or incompatibility is the default. As more factors required for SI are identified and characterized, it will be possible to determine the role each process plays in S-RNase-based SI.
S-RNase; self-incompatibility; Solanaceae; Rosaceae; Nicotiana; Prunus
Background and Scope
Self-incompatibility (SI) in flowering plants ensures the maintenance of genetic diversity by ensuring outbreeding. Different genetic and mechanistic systems of SI among flowering plants suggest either multiple origins of SI or considerable evolutionary diversification. In the grasses, SI is based on two loci, S and Z, which are both polyallelic: an incompatible reaction occurs only if both S and Z alleles are matched in individual pollen with alleles of the pistil on which they alight. Such incompatibility is referred to as gametophytic SI (GSI). The mechanics of grass GSI is poorly understood relative to the well-characterized S-RNase-based single-locus GSI systems (Solanaceae, Rosaceae, Plantaginaceae), or the Papaver recognition system that triggers a calcium-dependent signalling network culminating in programmed cell death. There is every reason to suggest that the grass SI system represents yet another mechanism of SI. S and Z loci have been mapped using isozymes to linkage groups C1 and C2 of the Triticeae consensus maps in Secale, Phalaris and Lolium. Recently, in Lolium perenne, in order to finely map and identify S and Z, more closely spaced markers have been developed based on cDNA and repeat DNA sequences, in part from genomic regions syntenic between the grasses. Several genes tightly linked to the S and Z loci were identified, but so far no convincing candidate has emerged.
Research and Progress
From subtracted Lolium immature stigma cDNA libraries derived from S and Z genotyped individuals enriched for SI potential component genes, kinase enzyme domains, a calmodulin-dependent kinase and a peptide with several calcium (Ca2+) binding domains were identified. Preliminary findings suggest that Ca2+ signalling and phosphorylation may be involved in Lolium GSI. This is supported by the inhibition of Lolium SI by Ca2+ channel blockers lanthanum (La3+) and verapamil, and by findings of increased phosphorylation activity during an SI response.
Lolium perenne; perennial ryegrass; grasses; Poaceae; self-incompatibility; calcium inhibitors; lanthanum chloride; verapamil
Genetic engineering offers the opportunity to generate unique genetic variation that is either absent in the sexually compatible gene pool or has very low heritability. The generation of transgenic plants, coupled with breeding, has led to the production of widely used transgenic cultivars in several major cash crops, such as maize, soybean, cotton and canola. The process for regulatory approval of genetically engineered crops is slow and subject to extensive political interference. The situation in forage grasses and legumes is more complicated.
Most widely grown forage, turf and bioenergy species (e.g. tall fescue, perennial ryegrass, switchgrass, alfalfa, white clover) are highly self-incompatible and outcrossing. Compared with inbreeding species, they have a high potential to pass their genes to adjacent plants. A major biosafety concern in these species is pollen-mediated transgene flow. Because human consumption is indirect, risk assessment of transgenic forage, turf and bioenergy species has focused on their environmental or ecological impacts. Although significant progress has been made in genetic modification of these species, commercialization of transgenic cultivars is very limited because of the stringent and costly regulatory requirements. To date, the only transgenic forage crop deregulated in the US is ‘Roundup Ready’ (RR) alfalfa. The approval process for RR alfalfa was complicated, involving several rounds of regulation, deregulation and re-regulation. Nevertheless, commercialization of RR alfalfa is an important step forward in regulatory approval of a perennial outcrossing forage crop. As additional transgenic forage, turf and bioenergy crops are generated and tested, different strategies have been developed to meet regulatory requirements. Recent progress in risk assessment and deregulation of transgenic forage and turf species is summarized and discussed.
Forage and turf; bioenergy crops; grass; legume; transgenic plant; gene flow; deregulation; biosafety; transgenesis; alfalfa; creeping bentgrass; Kentucky bluegrass; Roundup Ready
Carnivorous pitcher plants (CPPs) use cone-shaped leaves to trap animals for nutrient supply but are not able to kill all intruders of their traps. Numerous species, ranging from bacteria to vertrebrates, survive and propagate in the otherwise deadly traps. This paper reviews the literature on phytotelmata of CPPs.
Pitcher Fluid as a Habitat
The volumes of pitchers range from 0·2 mL to 1·5 L. In Nepenthes and Cephalotus, the fluid is secreted by the trap; the other genera collect rain water. The fluid is usually acidic, rich in O2 and contains digestive enzymes. In some taxa, toxins or detergents are found, or the fluid is extremely viscous. In Heliamphora or Sarracenia, the fluid differs little from pure water.
Pitcher inquilines comprise bacteria, protozoa, algae, fungi, rotifers, crustaceans, arachnids, insects and amphibia. The dominant groups are protists and Dipteran larvae. The various species of CPPs host different sets of inquilines. Sarracenia purpurea hosts up to 165 species of inquilines, followed by Nepenthes ampullaria with 59 species, compared with only three species from Brocchinia reducta. Reasons for these differences include size, the life span of the pitcher as well as its fluid.
Inquilines closely interact with their host. Some live as parasites, but the vast majority are mutualists. Beneficial activities include secretion of enzymes, feeding on the plant's prey and successive excretion of inorganic nutrients, mechanical break up of the prey, removal of excessive prey and assimilation of atmospheric N2.
There is strong evidence that CPPs influence their phytotelm. Two strategies can be distinguished: (1) Nepenthes and Cephalotus produce acidic, toxic or digestive fluids and host a limited diversity of inquilines. (2) Genera without efficient enzymes such as Sarracenia or Heliamphora host diverse organisms and depend to a large extent on their symbionts for prey utilization.
Brocchinia; carnivorous plants; Cephalotus; Heliamphora; pitcher inquilines; mutualism; Nepenthes; phytotelm; Sarracenia; symbiosis
Species' life-history and population dynamics are strongly shaped by the longevity of individuals, but life span is one of the least accessible demographic traits, particularly in clonal plants. Continuous vegetative reproduction of genets enables persistence despite low or no sexual reproduction, affecting genet turnover rates and population stability. Therefore, the longevity of clonal plants is of considerable biological interest, but remains relatively poorly known.
Here, we critically review the present knowledge on the longevity of clonal plants and discuss its importance for population persistence. Direct life-span measurements such as growth-ring analysis in woody plants are relatively easy to take, although, for many clonal plants, these methods are not adequate due to the variable growth pattern of ramets and difficult genet identification. Recently, indirect methods have been introduced in which genet size and annual shoot increments are used to estimate genet age. These methods, often based on molecular techniques, allow the investigation of genet size and age structure of whole populations, a crucial issue for understanding their viability and persistence. However, indirect estimates of clonal longevity are impeded because the process of ageing in clonal plants is still poorly understood and because their size and age are not always well correlated. Alternative estimators for genet life span such as somatic mutations have recently been suggested.
Empirical knowledge on the longevity of clonal species has increased considerably in the last few years. Maximum age estimates are an indicator of population persistence, but are not sufficient to evaluate turnover rates and the ability of long-lived clonal plants to enhance community stability and ecosystem resilience. In order to understand the dynamics of populations it will be necessary to measure genet size and age structure, not only life spans of single individuals, and to use such data for modelling of genet dynamics.
Age; community stability; genet size; global change; life history; population dynamics; somatic mutation; vegetative reproduction
It is essential to understand and predict the effects of changing environments on plants. This review focuses on the sexual reproduction of plants, as previous studies have suggested that this trait is particularly vulnerable to climate change, and because a number of ecologically and evolutionarily relevant genes have been identified.
It is proposed that studying gene functions in naturally fluctuating conditions, or gene functions in natura, is important to predict responses to changing environments. First, we discuss flowering time, an extensively studied example of phenotypic plasticity. The quantitative approaches of ecological and evolutionary systems biology have been used to analyse the expression of a key flowering gene, FLC, of Arabidopsis halleri in naturally fluctuating environments. Modelling showed that FLC acts as a quantitative tracer of the temperature over the preceding 6 weeks. The predictions of this model were verified experimentally, confirming its applicability to future climate changes. Second, the evolution of self-compatibility as exemplifying an evolutionary response is discussed. Evolutionary genomic and functional analyses have indicated that A. thaliana became self-compatible via a loss-of-function mutation in the male specificity gene, SCR/SP11. Self-compatibility evolved during glacial–interglacial cycles, suggesting its association with mate limitation during migration. Although the evolution of self-compatibility may confer short-term advantages, it is predicted to increase the risk of extinction in the long term because loss-of-function mutations are virtually irreversible.
Recent studies of FLC and SCR have identified gene functions in natura that are unlikely to be found in laboratory experiments. The significance of epigenetic changes and the study of non-model species with next-generation DNA sequencers is also discussed.
Arabidopsis thaliana; Arabidopsis halleri; climate change; FLC; FLOWERING LOCUS C; phenotypic plasticity; SCR; S-LOCUS CYSTEINE-RICH PROTEIN; evolution of selfing; predictive models; sexual reproduction; SP11; S-LOCUS PROTEIN 11; SRK; S-RECEPTOR KINASE; ecological and evolutionary systems biology