RH17 restricts reproductive fate and represses autonomous seed coat development in sexual Arabidopsis.

Plant sexual and asexual reproduction through seeds (apomixis) is tightly controlled by complex gene regulatory programs, which are not yet fully understood. Recent findings suggest that RNA helicases are required for plant germline development. This resembles their crucial roles in animals, where they are involved in controlling gene activity and the maintenance of genome integrity. Here, we identified previously unknown roles of Arabidopsis RH17 during reproductive development. Interestingly, RH17 is involved in repression of reproductive fate and of elements of seed development in the absence of fertilization. In lines carrying a mutant rh17 allele, development of supernumerary reproductive cell lineages in the female flower tissues (ovules) was observed, occasionally leading to formation of two embryos per seed. Furthermore, seed coat, and putatively also endosperm development, frequently initiated autonomously. Such induction of several features phenocopying distinct elements of apomixis by a single mutation is unusual and suggests that RH17 acts in regulatory control of plant reproductive development. Furthermore, an in-depth understanding of its action might be of use for agricultural applications.

Distinct geographic parthenogenesis in spite of niche conservatism and a single ploidy level: A case of Rubus ser. Glandulosi (Rosaceae).

Asexual organisms often differ in their geographic distributions from their sexual relatives. This phenomenon, termed geographic parthenogenesis, has long been known, but the underlying factors behind its diverse patterns have been under dispute. Particularly problematic is an association between asexuality and polyploidy in most taxa. Here, we present a new system of geographic parthenogenesis on the tetraploid level, promising new insights into this complex topic. We used flow cytometric seed screen and microsatellite genotyping to characterise the patterns of distribution of sexuals and apomicts and genotypic distributions in Rubus ser. Glandulosi across its range. Ecological modelling and local-scale vegetation and soil analyses were used to test for niche differentiation between the reproductive groups. Apomicts were detected only in North-western Europe, sexuals in the rest of the range in Europe and West Asia, with a sharp borderline stretched across Central Europe. Despite that, we found no significant differences in ecological niches. Genotypic richness distributions suggested independence of the reproductive groups and a secondary contact. We argue that unless a niche differentiation (resulting from polyploidy and/or hybridity) evolves, the main factors behind the patterns of geographic parthenogenesis in plants are phylogeographic history and neutral microevolutionary processes, such as clonal turnover.

Differential expression and evolutionary diversification of RNA helicases in Boechera sexual and apomictic reproduction.

In higher plants, sexual reproduction is characterized by meiosis of the first cells of the germlines, and double fertilization of the egg and central cell after gametogenesis. In contrast, in apomicts of the genus Boechera, meiosis is omitted or altered and only the central cell requires fertilization, while the embryo forms parthenogenetically from the egg cell. To deepen the understanding of the transcriptional basis underlying these differences, we applied RNA-seq to compare expression in reproductive tissues of different Boechera accessions. This confirmed previous evidence of an enrichment of RNA helicases in plant germlines. Furthermore, few RNA helicases were differentially expressed in female reproductive ovule tissues harboring mature gametophytes from apomictic and sexual accessions. For some of these genes, we further found evidence for a complex recent evolutionary history. This included a homolog of Arabidopsis thaliana FASCIATED STEM4 (FAS4). In contrast to AtFAS4, which is a single-copy gene, FAS4 is represented by three homologs in Boechera, suggesting a potential for subfunctionalization to modulate reproductive development. To gain first insights into functional roles of FAS4, we studied Arabidopsis lines carrying mutant alleles. This identified the crucial importance of AtFAS4 for reproduction, as we observed developmental defects and arrest during male and female gametogenesis.

Apomixis and the paradox of sex in plants.

BACKGROUND: The predominance of sex in eukaryotes, despite the high costs of meiosis and mating, remains an evolutionary enigma. Many theories have been proposed, none of them being conclusive on its own, and they are, in part, not well applicable to land plants. Sexual reproduction is obligate in embryophytes for the great majority of species. SCOPE: This review compares the main forms of sexual and asexual reproduction in ferns and angiosperms, based on the generation cycling of sporophyte and gametophyte (leaving vegetative propagation aside). The benefits of sexual reproduction for maintenance of genomic integrity in comparison to asexuality are discussed in the light of developmental, evolutionary, genetic and phylogenetic studies. CONCLUSIONS: Asexual reproduction represents modifications of the sexual pathway, with various forms of facultative sexuality. For sexual land plants, meiosis provides direct DNA repair mechanisms for oxidative damage in reproductive tissues. The ploidy alternations of meiosis-syngamy cycles and prolonged multicellular stages in the haploid phase in the gametophytes provide a high efficiency of purifying selection against recessive deleterious mutations. Asexual lineages might buffer effects of such mutations via polyploidy and can purge the mutational load via facultative sexuality. The role of organelle-nuclear genome compatibility for maintenance of genome integrity is not well understood. In plants in general, the costs of mating are low because of predominant hermaphroditism. Phylogenetic patterns in the archaeplastid clade suggest that high frequencies of sexuality in land plants are concomitant with a stepwise increase of intrinsic and extrinsic stress factors. Furthermore, expansion of genome size in land plants would increase the potential mutational load. Sexual reproduction appears to be essential for keeping long-term genomic integrity, and only rare combinations of extrinsic and intrinsic factors allow for shifts to asexuality.

Plant kleptomaniacs: geographical genetic patterns in the amphi-apomictic Rubus ser. Glandulosi (Rosaceae) reveal complex reticulate evolution of Eurasian brambles.

BACKGROUND AND AIMS: Rubus ser. Glandulosi provides a unique model of geographical parthenogenesis on a homoploid (2n = 4x) level. We aim to characterize evolutionary and phylogeographical patterns in this taxon and shed light on the geographical differentiation of apomicts and sexuals. Ultimately, we aim to evaluate the importance of phylogeography in the formation of geographical parthenogenesis. METHODS: Rubus ser. Glandulosi was sampled across its Eurasian range together with other co-occurring Rubus taxa (587 individuals in total). Double-digest restriction site-associated DNA sequencing (ddRADseq) and modelling of suitable climate were used for evolutionary inferences. KEY RESULTS: Six ancestral species were identified that contributed to the contemporary gene pool of R. ser. Glandulosi. Sexuals were introgressed from Rubus dolichocarpus and Rubus moschus in West Asia and from Rubus ulmifolius agg., Rubus canescens and Rubus incanescens in Europe, whereas apomicts were characterized by alleles of Rubus subsect. Rubus. Gene flow between sexuals and apomicts was also detected, as was occasional hybridization with other taxa. CONCLUSIONS: We hypothesize that sexuals survived the last glacial period in several large southern refugia, whereas apomicts were mostly restricted to southern France, whence they quickly recolonized Central and Western Europe. The secondary contact of sexuals and apomicts was probably the principal factor that established geographical parthenogenesis in R. ser. Glandulosi. Sexual populations are not impoverished in genetic diversity along their borderline with apomicts, and maladaptive population genetic processes probably did not shape the geographical patterns.

An adventurous journey toward and away from fern apomixis: Insights from genome size and spore abortion patterns.

PREMISE: Apomixis in ferns is relatively common and obligatory. Sterile hybrids may restore fertility via apomixis at a cost of long-term genetic stagnation. In this study, we outlined apomixis as a possible temporary phase leading to sexuality and analyzed factors relating to transitioning to and away from apomixis, such as unreduced and reduced spore formation in apomict and apo-sex hybrid ferns. METHODS: We analyzed the genome size of 15 fern species or hybrids ("taxa") via flow cytometry. The number of reduced and unreduced gametophytes was established as a proxy for viable spore formation of either type. We also calculated the spore abortion ratio (sign of reduced spores) in several taxa, including the apo-sex hybrid Dryopteris × critica and its 16 apomictically formed offspring. RESULTS: Four of 15 sampled taxa yielded offspring variable in genome size. Specifically, each variable taxon formed one viable reduced plant among 12-451 sampled gametophytes per taxon. Thus, haploid spore formation in the studied apomicts was very rare but possible. Spore abortion analyses indicated gradually decreasing abortion (haploid spore formation) over time. In Dryopteris × critica, abortion decreased from 93.8% to mean 89.5% in one generation. CONCLUSIONS: Our results support apomixis as a transitionary phase toward sexuality. Newly formed apomicts hybridize with sexual relatives and continue to form haploid spores early on. Thus, they may get the genomic content necessary for regular meiosis and restore sexuality. If the missing relative goes extinct, the lineage gets locked into apomixis as may be the case with the Dryopteris affinis complex.

Is self-incompatibility a reproductive barrier for hybridization in a sympatric species?

PREMISE: Barriers at different reproductive stages contribute to reproductive isolation. Self-incompatibility (SI) systems that prevent self-pollination could also act to control interspecific pollination and contribute to reproductive isolation, preventing hybridization. Here we evaluated whether SI contributes to reproductive isolation among four co-occurring Opuntia species that flower at similar times and may hybridize with each other. METHODS: We assessed whether Opuntia cantabrigiensis, O. robusta, O. streptacantha, and O. tomentosa, were self-compatible and formed hybrid seeds in five manipulation treatments to achieve self-pollination, intraspecific cross-pollination, open pollination (control), interspecific crosses or apomixis, then recorded flowering phenology and synchrony. RESULTS: All species flowered in the spring with a degree of synchrony, so that two pairs of species were predisposed to interspecific pollination (O. cantabrigiensis with O. robusta, O. streptacantha with O. tomentosa). All species had distinct reproductive systems: Opuntia cantabrigiensis is self-incompatible and did not produce hybrid seeds as an interspecific pollen recipient; O. robusta is a dioecious species, which formed a low proportion of hybrid seeds; O. streptacantha and O. tomentosa are self-compatible and produced hybrid seeds. CONCLUSIONS: Opuntia cantabrigiensis had a strong pollen-pistil barrier, likely due to its self-incompatibility. Opuntia robusta, the dioecious species, is an obligate outcrosser and probably partially lost its ability to prevent interspecific pollen germination. Given that the self-compatible species can set hybrid seeds, we conclude that pollen-pistil interaction and high flowering synchrony represent weak barriers; whether reproductive isolation occurs later in their life cycle (e.g., germination or seedling survival) needs to be determined.

One-line hybrid rice with high-efficiency synthetic apomixis and near-normal fertility.

KEY MESSAGE: High-frequency clonal seeds and near-normal fertility were obtained by engineering synthetic apomixis in hybrid rice. The one-line strategy, with the advantage of unnecessary seed production, is the final stage for the hybrid rice development and can be achieved through the fixation of heterosis via artificially inducing apomixis. Recently, synthetic apomixis has been generated in rice by combining MiMe (Mitosis instead of Meiosis) with either the ectopic expression of BABY BOOM (BBM1 or BBM4) or mutation of MATRILINEAL (MTL), resulting in over 95.00% of clonal seeds. However, the frequency of clonal seeds was only 29.20% when AtDD45 promoter was used to drive BBM1. In addition, achieving both a high frequency of clonal seeds and near-normal fertility simultaneously had been elusive in earlier strategies. In this study, using AtDD45 promoter to drive BBM1 expression in combination with the MiMe mutant resulted in the apomixis frequency as high as 98.70%. Even more, employing fusion promoters (AtMYB98_AtDD1_OsECA1-like1) to drive WUS expression in combination with pAtDD45:BBM1 and MiMe could produce clonal seeds at rates of up to 98.21%, the highest seed setting rate reached to 83.67%. Multiple-embryos were observed in clonal lines at a frequency ranging from 3.37% to 60.99%. Transmission of the high frequency of apomixis through skipped generations (atavism) was identified in two clonal lines, even though it remained stable in the majority of clonal lines. These findings significantly advance the pursuit of fixed heterosis in rice through synthetic apomixis, edging closer to its agricultural application.

Clonal Reproduction through Seeds in Sight for Crops.

Apomixis or asexual reproduction through seeds, enables the preservation of hybrid vigor. Hybrids are heterozygous and segregate for genotype and phenotype upon sexual reproduction. While apomixis, that is, clonal reproduction, is intuitively antithetical to diversity, it is rarely obligate and actually provides a mechanism to recover and maintain superior hybrid gene combinations for which sexual reproduction would reveal deleterious alleles in less fit genotypes. Apomixis, widespread across flowering plant orders, does not occur in major crop species, yet its introduction could add a valuable tool to the breeder's toolbox. In the past decade, discovery of genetic mechanisms regulating meiosis, embryo and endosperm development have facilitated proof-of-concept for the synthesis of apomixis, bringing apomictic crops closer to reality.

Apomixis: oh, what a tangled web we have!

MAIN CONCLUSION: Apomixis is a complex evolutionary trait with many possible origins. Here we discuss various clues and causes, ultimately proposing a model harmonizing the three working hypotheses on the topic. Asexual reproduction through seeds, i.e., apomixis, is the holy grail of plant biology. Its implementation in modern breeding could be a game-changer for agriculture. It has the potential to generate clonal crops and maintain valuable complex genotypes and their associated heterotic traits without inbreeding depression. The genetic basis and origins of apomixis are still unclear. There are three central hypothesis for the development of apomixis that could be: i) a deviation from the sexual developmental program caused by an asynchronous development, ii) environmentally triggered through epigenetic regulations (a polyphenism of sex), iii) relying on one or more genes/alleles. Because of the ever-increasing complexity of the topic, the path toward a detailed understanding of the mechanisms underlying apomixis remains unclear. Here, we discuss the most recent advances in the evolution perspective of this multifaceted trait. We incorporated our understanding of the effect of endogenous effectors, such as small RNAs, epigenetic regulation, hormonal pathways, protein turnover, and cell wall modification in response to an upside stress. This can be either endogenous (hybridization or polyploidization) or exogenous environmental stress, mainly due to oxidative stress and the corresponding ROS (Reacting Oxygen Species) effectors. Finally, we graphically represented this tangled web.

An exonuclease V homologue is expressed predominantly during early megasporogenesis in apomictic Brachiaria brizantha.

MAIN CONCLUSION: An exonuclease V homologue from apomictic Brachiaria brizantha is expressed and localized in nucellar cells at key moments when these cells differentiate to give rise to unreduced gametophytes. Brachiaria is a genus of forage grasses with economical and agricultural importance to Brazil. Brachiaria reproduces by aposporic apomixis, in which unreduced embryo sacs, derived from nucellar cells, other than the megaspore mother cell (MMC), are formed. The unreduced embryo sacs produce an embryo without fertilization resulting in clones of the mother plant. Comparative gene expression analysis in ovaries of sexual and apomictic Brachiaria spp. revealed a sequence from B. brizantha that showed a distinct pattern of expression in ovaries of sexual and apomictic plants. In this work, we describe a gene named BbrizExoV with strong identity to exonuclease V (Exo V) genes from other grasses. Sequence analysis in signal prediction tools showed that BbrizExoV might have dual localization, depending on the translation point. A longer form to the nucleus and a shorter form which would be directed to the chloroplast. This is also the case for monocot sequences analyzed from other species. The long form of BbrizExoV protein localizes to the nucleus of onion epidermal cells. Analysis of ExoV proteins from dicot species, with exception of Arabidopsis thaliana ExoVL protein, showed only one localization. Using a template-based AlphaFold 2 modelling approach the structure of BbrizExoV in complex with metal and ssDNA was predicted based on the holo structure of the human counterpart. Features predicted to define ssDNA binding but a lack of sequence specificity are shared between the human enzyme and BbrizExoV. Expression analyses indicated the precise site and timing of transcript accumulation during ovule development, which coincides with the differentiation of nucelar cells to form the typical aposporic four-celled unreduced gametophyte. A putative function for this protein is proposed based on its homology and expression pattern.

Flowering Newsletter 2023.

The word 'fruit' is derived from the latin 'fructus' which itself is said to be derived from 'frui', which means to enjoy. Along those lines, I hope this year's Flowering Newsletter brings a lot of joy, because fruits and seeds feature in multiple articles.

Asexual reproduction through seeds: the complex case of diplosporous apomixis.

Apomixis is considered a potentially revolutionary tool to generate high-quality food at a lower cost and shorter developmental time due to clonal seed production through apomeiosis and parthenogenesis. In the diplosporous type of apomixis, meiotic recombination and reduction are circumvented either by avoiding or failing meiosis or by a mitotic-like division. Here, we review the literature on diplospory, from early cytological studies dating back to the late 19th century to recent genetic findings. We discuss diplosporous developmental mechanisms, including their inheritance. Furthermore, we compare the strategies adopted to isolate the genes controlling diplospory with those to produce mutants forming unreduced gametes. Nowadays, the dramatically improved technologies of long-read sequencing and targeted CRISPR/Cas mutagenesis justify the expectation that natural diplospory genes will soon be identified. Their identification will answer questions such as how the apomictic phenotype can be superimposed upon the sexual pathway and how diplospory genes have evolved. This knowledge will contribute to the application of apomixis in agriculture.

Engineering apomixis in crops.

Apomixis is an asexual mode of reproduction through seeds where progeny are clones of the mother plants. Naturally apomictic modes of reproduction are found in hundreds of plant genera distributed across more than 30 plant families, but are absent in major crop plants. Apomixis has the potential to be a breakthrough technology by allowing the propagation through seed of any genotype, including F1 hybrids. Here, we have summarized the recent progress toward synthetic apomixis, where combining targeted modifications of both the meiosis and fertilization processes leads to the production of clonal seeds at high frequencies. Despite some remaining challenges, the technology has approached a level of maturity that allows its consideration for application in the field.

Advances in genomic characterization of Urochloa humidicola: exploring polyploid inheritance and apomixis.

KEY MESSAGE: We present the highest-density genetic map for the hexaploid Urochloa humidicola. SNP markers expose genetic organization, reproduction, and species origin, aiding polyploid and tropical forage research. Tropical forage grasses are an important food source for animal feeding, with Urochloa humidicola, also known as Koronivia grass, being one of the main pasture grasses for poorly drained soils in the tropics. However, genetic and genomic resources for this species are lacking due to its genomic complexity, including high heterozygosity, evidence of segmental allopolyploidy, and reproduction by apomixis. These complexities hinder the application of marker-assisted selection (MAS) in breeding programs. Here, we developed the highest-density linkage map currently available for the hexaploid tropical forage grass U. humidicola. This map was constructed using a biparental F1 population generated from a cross between the female parent H031 (CIAT 26146), the only known sexual genotype for the species, and the apomictic male parent H016 (BRS cv. Tupi). The linkage analysis included 4873 single nucleotide polymorphism (SNP) markers with allele dosage information. It allowed mapping of the ASGR locus and apospory phenotype to linkage group 3, in a region syntenic with chromosome 3 of Urochloa ruziziensis and chromosome 1 of Setaria italica. We also identified hexaploid haplotypes for all individuals, assessed the meiotic configuration, and estimated the level of preferential pairing in parents during the meiotic process, which revealed the autopolyploid origin of sexual H031 in contrast to apomictic H016, which presented allopolyploid behavior in preferential pairing analysis. These results provide new information regarding the genetic organization, mode of reproduction, and allopolyploid origin of U. humidicola, potential SNPs markers associated with apomixis for MAS and resources for research on polyploids and tropical forage grasses.

Dispersal and establishment traits provide a colonization advantage for a polyploid apomictic plant.

PREMISE: Apomictic plants (reproducing asexually through seed) often have larger ranges and occur at higher latitudes than closely related sexuals, a pattern known as geographical parthenogenesis (GP). Explanations for GP include differences in colonizing ability due to reproductive assurance and direct/indirect effects of polyploidy (most apomicts are polyploid) on ecological tolerances. While life history traits associated with dispersal and establishment also contribute to the potential for range expansion, few studies compare these traits in related apomicts and sexuals. METHODS: We investigated differences in early life history traits between diploid-sexual and polyploid-apomictic Townsendia hookeri (Asteraceae), which displays a classic pattern of GP. Using lab and greenhouse experiments, we measured seed dispersal traits, germination success, and seedling size and survival in sexual and apomictic populations from across the range of the species. RESULTS: While theory predicts that trade-offs between dispersal and establishment traits should be common, this was largely not the case in T. hookeri. Apomictic seeds had both lower terminal velocity (staying aloft longer when dropped) and higher germination success than sexual seeds. While there were no differences in seedling size between reproductive types, apomicts did, however, have slightly lower seedling survival than sexuals. CONCLUSIONS: These differences in early life history traits, combined with reproductive assurance conferred by apomixis, suggest that apomicts achieve a greater range through advantages in their ability to both spread and establish.

Alien genome mobilization and fixation utilizing an apomixis mediated genome addition (AMGA) strategy in Pennisetum to improve domestication traits of P. squamulatum.

KEY MESSAGE: An approach to release 'frozen' variability in apomictic species using sexuality of another species, eventually its utilization in crop improvement and de-novo domestication of crop wild relatives is presented. Pennisetum squamulatum, a secondary gene pool species of pearl millet (P. glaucum), harbours many desirable traits. However, it was neither utilized to improve pearl millet fodder traits nor improvement of its own domestication traits was attempted, due to the complexities of genomes and apomictic reproduction. To overcome this, we followed an Apomixis Mediated Genome Addition (AMGA) strategy and utilized the contrasting reproductive capacities (sexuality and apomixis) of both the species to access the otherwise un-available variability embedded in P. squamulatum. Segregating population of interspecific hybrids exhibited significant variability and heterosis for desired morphological, agronomical, and nutritional traits. Elite apomictic and perennial hybrids were evaluated in breeding trials, and eventually a novel grass cultivar was released for commercial cultivation in India. The performance of newly developed cultivar was superior to other adapted perennial grasses of arid and semi-arid rangelands. Through AMGA, the sexuality of one species was successfully utilized to 'release' the 'frozen' variability embedded in another species. Subsequently, the hybrids representing desirable trait combinations were again 'fixed' utilizing the apomixis alleles from the male parent in a back-and-forth apomixis-sexual-apomixis selection cycle. This study also demonstrated the potential of AMGA to improve crop relatives through genomes introgression as well as de novo domestication of new crops from wild species.

Diverged subpopulations in tropical Urochloa (Brachiaria) forage species indicate a role for facultative apomixis and varying ploidy in their population structure and evolution.

BACKGROUND: Urochloa (syn. Brachiaria) is a genus of tropical grasses sown as forage feedstock, particularly in marginal soils. Here we aimed to clarify the genetic diversity and population structure in Urochloa species to understand better how population evolution relates to ploidy level and occurrence of apomictic reproduction. METHODS: We explored the genetic diversity of 111 accessions from the five Urochloa species used to develop commercial cultivars. These accessions were conserved from wild materials collected at their centre of origin in Africa, and they tentatively represent the complete Urochloa gene pool used in breeding programmes. We used RNA-sequencing to generate 1.1 million single nucleotide polymorphism loci. We employed genetic admixture, principal component and phylogenetic analyses to define subpopulations. RESULTS: We observed three highly differentiated subpopulations in U. brizantha, which were unrelated to ploidy: one intermixed with U. decumbens, and two diverged from the former and the other species in the complex. We also observed two subpopulations in U. humidicola, unrelated to ploidy; one subpopulation had fewer accessions but included the only characterized sexual accession in the species. Our results also supported a division of U. decumbens between diploids and polyploids, and no subpopulations within U. ruziziensis and U. maxima. CONCLUSIONS: Polyploid U. decumbens are more closely related to polyploid U. brizantha than to diploid U. decumbens, which supports the divergence of both polyploid groups from a common tetraploid ancestor and provides evidence for the hybridization barrier of ploidy. The three differentiated subpopulations of apomictic polyploid U. brizantha accessions constitute diverged ecotypes, which can probably be utilized in hybrid breeding. Subpopulations were not observed in non-apomictic U. ruziziensis. Sexual Urochloa polyploids were not found (U. brizantha, U. decumbens) or were limited to small subpopulations (U. humidicola). The subpopulation structure observed in the Urochloa sexual-apomictic multiploidy complexes supports geographical parthenogenesis, where the polyploid genotypes exploit the evolutionary advantage of apomixis, i.e. uniparental reproduction and clonality, to occupy extensive geographical areas.

Apomictic fern fathers: an experimental approach to the reproductive characteristics of sexual, apomict, and hybrid fern gametophytes.

PREMISE: Apomixis and hybridization are two essential and complementary factors in the evolution of plants, including ferns. Hybridization combines characteristics from different species, while apomixis conserves features within a lineage. When combined, these two processes result in apo-sex hybrids. The conditions leading to the formation of these hybrids are poorly understood in ferns. METHODS: We cultivated spores from 66 fern samples (43 apomicts, 7 apo-sex hybrids, and 16 sexuals), and measured their development in vitro over 16 weeks. We evaluated germination, lateral meristem formation rates, sexual expression, and production of sporophytes and then compared ontogenetic patterns among the three groups. RESULTS: The three examined groups formed antheridia (male gametangia) but differed in overall gametophyte development. Sexual species created archegonia (female, 86% of viable samples), but no sporophytes. Apomicts rarely created nonfunctional archegonia (8%) but usually produced apogamous sporophytes (75%). Surprisingly, apomictic and sexual species showed similar development speed. The sexually reproducing parents of viable studied hybrids formed about twice as many meristic gametophytes as the apomictic parents (39% vs. 20%, respectively). CONCLUSIONS: We present the most thorough comparison of gametangial development of sexual and apomictic ferns, to date. Despite expectations, apomictic reproduction might not lead to earlier sporophyte formation. Apomicts produce functional sperm and thus can contribute this type of gamete to their hybrids. The development patterns found in the parents of hybrids indicate a possible increase of hybridization rates by antheridiogens. The apo-sex hybrids always inherit the apomictic reproductive strategy and are thus capable of self-perpetuation.

The Boechera model system for evolutionary ecology.

Model systems in biology expand the research capacity of individuals and the community. Closely related to Arabidopsis, the genus Boechera has emerged as an important ecological model owing to the ability to integrate across molecular, functional, and eco-evolutionary approaches. Boechera species are broadly distributed in relatively undisturbed habitats predominantly in western North America and provide one of the few experimental systems for identification of ecologically important genes through genome-wide association studies and investigations of selection with plants in their native habitats. The ecologically, evolutionarily, and agriculturally important trait of apomixis (asexual reproduction via seeds) is common in the genus, and field experiments suggest that abiotic and biotic environments shape the evolution of sex. To date, population genetic studies have focused on the widespread species B. stricta, detailing population divergence and demographic history. Molecular and ecological studies show that balancing selection maintains genetic variation in ~10% of the genome, and ecological trade-offs contribute to complex trait variation for herbivore resistance, flowering phenology, and drought tolerance. Microbiome analyses have shown that host genotypes influence leaf and root microbiome composition, and the soil microbiome influences flowering phenology and natural selection. Furthermore, Boechera offers numerous opportunities for investigating biological responses to global change. In B. stricta, climate change has induced a shift of >2 weeks in the timing of first flowering since the 1970s, altered patterns of natural selection, generated maladaptation in previously locally-adapted populations, and disrupted life history trade-offs. Here we review resources and results for this eco-evolutionary model system and discuss future research directions.