Development and Evolution of Unisexual Flowers: A Review

The development of unisexual flowers has been described in a large number of taxa, sampling the diversity of floral phenotypes and sexual systems observed in extant angiosperms, in studies focusing on floral ontogeny, on the evo-devo of unisexuality, or on the genetic and chromosomal bases of unisexuality. We review here such developmental studies, aiming at characterizing the diversity of ontogenic pathways leading to functionally unisexual flowers. In addition, we present for the first time and in a two-dimensional morphospace a quantitative description of the developmental rate of the sexual organs in functionally unisexual flowers, in a non-exhaustive sampling of angiosperms with contrasted floral morphologies. Eventually, recommendations are provided to help plant evo-devo researchers and botanists addressing macroevolutionary and ecological issues to more precisely select the taxa, the biological material, or the developmental stages to be investigated.

Floral Aromatics of Ptelea: Chemical Identification and Human Response

Many members of the citrus family (Rutaceae) are valued for the aromatic compounds emitted by their flowers. Ptelea species are unusually cold-hardy members of the Rutaceae, but conflicting descriptions of the fragrance of their unisexual flowers may discourage the use of these trees. We analyzed floral volatiles and human response to these chemicals to test the hypothesis that the fragrance of staminate and pistillate flowers of these species differs. Gas chromatography and mass spectrometry showed that most volatile chemicals emitted by flowers of Ptelea trifoliata and Ptelea crenulata are monoterpenes, sesquiterpenes, and esters. Most volatiles were emitted from flowers of both sexes, but ethyl benzoate and estragole were emitted only from pistillate flowers. When concentrations of aromatics differed between sexes, they were higher for pistillate flowers, except for cis-3-hexenyl butanoate and an unidentified terpene. For P. crenulata and P. trifoliata, respectively, 81% and 77% of survey responses were from volunteers who liked the fragrance. Panelists most frequently described the scent of flowers of P. crenulata of both sexes with the words citrus, lime, and sweet. Panelists distinguished between pistillate and staminate flowers of P. trifoliata, describing the odor of pistillate flowers most frequently with the words damp-earthy, spicy, and sweet; staminate flowers were perceived as light, fresh, grassy, and pleasant. This work represents the first analysis of floral volatiles of P. crenulata and resolves conflicting prior reports regarding the floral fragrance of P. trifoliata. We conclude that differences among people rather than the sex of flowers account for conflicting prior reports of floral fragrance. The scents of flowers of P. crenulata and P. trifoliata appeal to most people and are horticultural assets of these trees.

Testing for apomixis in an obligate pollination mutualism

Plants with a small number of specific pollinators may be vulnerable to fluctuations in the availability of those pollinators, which could limit plant reproductive success and even result in extinction. Plants can develop mechanisms to mitigate this risk, such as apomixis. Reproductive assurance mechanisms have been largely ignored in obligate pollination mutualisms (OPMs), that are some of the most specialised of plant-pollinator interactions. Furthermore, although OPMs are often referred to as obligate, this is rarely tested. We performed a flower-bagging experiment to test if the unisexual flowers of Breynia oblongifolia could set fruit in the absence of its highly specialised seed-eating moth pollinators. Surprisingly, many bagged female flowers developed fruits, suggesting apomixis. We therefore conducted a second series of experiments in which we 1) added or excluded pollinators from caged plants; and 2) surveyed a wild population for apomictic reproduction using mother-offspring genotyping. In the absence of pollinators, no fruits developed. In addition, we detected no genetic evidence for apomixis when comparing between mothers and their offspring or between adults in a wild population. We explain the production of fruits in bagged branches by our discovery that B. oblongifolia can retain pollinated female flowers over the winter period. These flowers develop to fruits in the spring in the absence of male flowers or pollinators. Our study thus shows that B. oblongifolia is unable to produce fruit in the absence of its specialist moth pollinators. Thus, the highly specific interaction between plant and pollinators appears to be truly obligate.

Examining the Needle in the Haystack: Evolutionary Relationships in the Mistletoe Genus Loranthus (Loranthaceae)

Abstract— The genus Loranthus (Loranthaceae) consists of ca. nine Old World species distributed from eastern Asia to Europe. Loranthus, the type of the family, has had a complex taxonomic history that continues today, partly because most mistletoes in the family have resided in this genus. For this reason, there are over 1800 Loranthus species names, the vast majority of which are synonyms for mistletoes in other genera. The present work sampled representatives of nine species considered bona fide members of the genus. Using complete plastome sequences, nuclear ribosomal DNA, and mitochondrial 26S rDNA, phylogenetic gene trees were generated to assess interspecific relationships. The Loranthus plastomes ranged in size from 121 to 125 kb and exhibited the quadripartite structure seen in most Santalales. These plastomes have lost or pseudogenized 24 genes, including all of the NADH dehydrogenase complex, thus reducing the genomes to ca. 90 functional genes. Cladistic analyses of morphological characters were conducted and these trees compared to the molecular trees, thus informing which taxonomic characters best define clades and characterize species within the genus. Two major clades in Loranthus were identified. The Europaeus clade includes the deciduous species L. europaeus, L. grewingkii, L. lambertianus, and L. tanakae mostly distributed above 30° N latitude. The Odoratus clade, mostly distributed below 30° N latitude, included L. guizhouensis, L. kaoi, L. odoratus, and L. pseudo-odoratus. The latter four species are genetically closely related, show percurrent (vs. pseudo-dichotomous) branching, and have evergreen leaves. Unisexual flowers have apparently evolved independently in each of the two clades. Future work should focus upon the species delimitation in the Odoratus clade and whether hybridization is occurring among any members.

Transcriptome Profile Analysis Reveals the Regulation Mechanism of Stamen Abortion in Handeliodendron bodinieri

Handeliodendron bodinieri has unisexual flowers with aborted stamens in female trees, which can be used to study unisexual flower development in tree species. To elucidate the molecular mechanism of stamen abortion underlying sex differentiation, the stage of stamen abortion was determined by semi-thin sections; results showed that stamen abortion occurred in stage 6 during anther development. In addition, differentially expressed transcripts regulating stamen abortion were identified by comparing the transcriptome of female flowers and male flowers with RNA-seq technique. The results showed that 14 genes related to anther development and meiosis such as HbGPAT, HbAMS, HbLAP5, HbLAP3, and HbTES were down-regulated, and HbML5 was up-regulated. Therefore, this information will provide a theoretical foundation for the conservation, breeding, scientific research, and application of Handeliodendron bodinieri.

Sex-biased genes and metabolites explain morphologically sexual dimorphism and reproductive costs in Salix paraplesia catkins

Dioecious species evolved from species with monomorphic sex systems in order to achieve overall fitness gains by separating male and female functions. As reproductive organs, unisexual flowers have different reproductive roles and exhibit conspicuous sexual dimorphism. To date, little is known about the temporal variations in and molecular mechanisms underlying the morphology and reproductive costs of dioecious flowers. We investigated male and female flowers of Salix paraplesia in three flowering stages before pollination (the early, blooming and late stages) via transcriptional sequencing as well as metabolite content and phenotypic analysis. We found that a large number of sex-biased genes, rather than sex-limited genes, were responsible for sexual dimorphism in S. paraplesia flowers and that the variation in gene expression in male flowers intensified this situation throughout flower development. The temporal dynamics of sex-biased genes derived from changes in reproductive function during the different flowering stages. Sexually differentiated metabolites related to respiration and flavonoid biosynthesis exhibited the same bias directions as the sex-biased genes. These sex-biased genes were involved mainly in signal transduction, photosynthesis, respiration, cell proliferation, phytochrome biosynthesis, and phenol metabolism; therefore, they resulted in more biomass accumulation and higher energy consumption in male catkins. Our results indicated that sex-biased gene expression in S. paraplesia flowers is associated with different reproductive investments in unisexual flowers; male flowers require a greater reproductive investment to meet their higher biomass accumulation and energy consumption needs.

The Diversity and Dynamics of Sex Determination in Dioecious Plants

The diversity of inflorescences among flowering plants is captivating. Such charm is not only due to the variety of sizes, shapes, colors, and flowers displayed, but also to the range of reproductive systems. For instance, hermaphrodites occur abundantly throughout the plant kingdom with both stamens and carpels within the same flower. Nevertheless, 10% of flowering plants have separate unisexual flowers, either in different locations of the same individual (monoecy) or on different individuals (dioecy). Despite their rarity, dioecious plants provide an excellent opportunity to investigate the mechanisms involved in sex expression and the evolution of sex-determining regions (SDRs) and sex chromosomes. The SDRs and the evolution of dioecy have been studied in many species ranging from Ginkgo to important fruit crops. Some of these studies, for example in asparagus or kiwifruit, identified two sex-determining genes within the non-recombining SDR and may thus be consistent with the classical model for the evolution of dioecy from hermaphroditism via gynodioecy, that predicts two successive mutations, the first one affecting male and the second one female function, becoming linked in a region of suppressed recombination. On the other hand, aided by genome sequencing and gene editing, single factor sex determination has emerged in other species, such as persimmon or poplar. Despite the diversity of sex-determining mechanisms, a tentative comparative analysis of the known sex-determining genes and candidates in different species suggests that similar genes and pathways may be employed repeatedly for the evolution of dioecy. The cytokinin signaling pathway appears important for sex determination in several species regardless of the underlying genetic system. Additionally, tapetum-related genes often seem to act as male-promoting factors when sex is determined via two genes. We present a unified model that synthesizes the genetic networks of sex determination in monoecious and dioecious plants and will support the generation of hypothesis regarding candidate sex determinants in future studies.

Comparative morphology and ontogenetic patterns of Bdallophytum species (Cytinaceae, Malvales): insight into the biology of an endoparasitic genus

Cytinaceae are root endoparasitic plants with only three genera. Their biology is largely unknown, and most knowledge of the family is based on the Old World genus, Cytinus. Here, we studied all three species of the New World Bdallophytum from Mexico. We describe their morphoanatomy, floral development, and embryology, highlighting the unique traits of Bdallophytum compared with two other genera of the family and members of Malvales. Both B. americanum and B. andrieuxii are dioecious, while B. oxylepis is gynomonoecious. The floral size and the number of floral organs vary within and among species, which appears common in Cytinaceae. The flowers of Bdallophytum exhibit synorganization in sexual organs, a synandrium in male flowers, and a gynostemium in bisexual flowers of B. oxylepis. Unisexual and bisexual flowers are zygomorphic at the early developmental stages. The unisexual flowers become actinomorphic in later development, while the bisexual flowers of B. oxylepis remain zygomorphic. The androecium of Bdallophytum has key traits shared with some Malvales, such as the fused filaments in Malvaceae and Sarcolaenaceae and the connective appendage shared with Dipterocarpaceae. Our results suggest that a unitegmic ovule is a unique trait for Bdallophytum. This is proposed here as a putative synapomorphy for Bdallophytum.

Studies in Andean Ocotea (Lauraceae) V. Species with Unisexual Flowers and Sparsely Appressed-Pubescent or Glabrous Leaves without Domatia Occurring above 1000 m in Altitude

This is the fifth installment of a treatment of Ocotea Aubl. occurring above 1000-m altitude in the Andean countries of Venezuela, Colombia, Ecuador, Peru, and Bolivia. This part covers species with unisexual flowers lacking distinctive characters such as presence of domatia or erect or dense pubescence on leaves. Twenty-six species are treated, of which 12 are new to science. These are O. nidiae van der Werff from Venezuela; O. erugata van der Werff, O. gymnantha van der Werff, and O. lorda van der Werff from Colombia; O. ceronii van der Werff, O. depilis van der Werff, O. homeieri van der Werff, and O. pilosa van der Werff from Ecuador; and O. calcicola van der Werff, O. fulgida van der Werff, O. nana van der Werff, and O. tunquiensis van der Werff from Peru. Ocotea cernua (Nees) Mez is synonymized with O. leptobotra (Ruiz & Pav.) Mez and O. longifolia Kunth is synonymized with O. aurantiodora (Ruiz & Pav.) Mez.