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Parthenocarpy in horticultural crop plants is an important trait with agricultural value for various industrial purposes as well as direct eating quality. Here, we demonstrate a breeding strategy to generate parthenocarpic tomato plants using the CRISPR/Cas9 system. We optimized the CRISPR/Cas9 system to introduce somatic mutations effectively into SlIAA9 —a key gene controlling parthenocarpy—with mutation rates of up to 100% in the T0 generation. Furthermore, analysis of off-target mutations using deep sequencing indicated that our customized gRNAs induced no additional mutations in the host genome. Regenerated mutants exhibited morphological changes in leaf shape and seedless fruit—a characteristic of parthenocarpic tomato. And the segregated next generation (T1) also showed a severe phenotype associated with the homozygous mutated genome. The system developed here could be applied to produce parthenocarpic tomato in a wide variety of cultivars, as well as other major horticultural crops, using this precise and rapid breeding technique.

Sexual populations should be vulnerable to invasion and replacement by ecologically similar asexual females because asexual lineages have higher per capita growth rates. However, as asexual genotypes become common, they may also become disproportionately infected by parasites. The Red Queen hypothesis postulates that high infection rates in the common asexual clones could periodically favor the genetically diverse sexual individuals and promote the short‐term coexistence of sexual and asexual populations. Testing this idea requires comparison of competing sexual and asexual lineages that are attacked by natural parasites. To date no such data have been available. Here, we report on long‐term dynamics and parasite coevolution in a “mixed” (sexual and asexual) population of snails (Potamopyrgus antipodarum). We found that, within 7–10 years, the most common clones were almost completely replaced by initially rare clones in two different habitats, while sexuals persisted throughout the study period. The common clones, which were initially more resistant to infection, also became more susceptible to infection by sympatric (but not allopatric) parasites over the course of the study. These results are consistent with the Red Queen hypothesis and show that the coevolutionary dynamics predicted by the theory may also favor sexual reproduction in natural populations.

Apomixis is a naturally occurring mode of asexual reproduction in flowering plants that results in seed formation without the involvement of meiosis or fertilization of the egg. Seeds formed on an apomictic plant contain offspring genetically identical to the maternal plant. Apomixis has significant potential for preserving hybrid vigor from one generation to the next in highly productive crop plant genotypes. ApomicticPennisetum/Cenchrusspecies, members of the Poaceae (grass) family, reproduce by apospory. Apospory is characterized by apomeiosis, the formation of unreduced embryo sacs derived from nucellar cells of the ovary and, by parthenogenesis, the development of the unreduced egg into an embryo without fertilization. InPennisetum squamulatum (L.) R.Br., apospory segregates as a single dominant locus, the aposporyspecific genomic region (ASGR). In this study, we demonstrate that thePsASGR-BABY BOOM-like(PsASGR-BBML) gene is expressed in egg cells before fertilization and can induce parthenogenesis and the production of haploid offspring in transgenic sexual pearl millet. A reduction ofPsASGR-BBMLexpression in apomictic F₁ RNAi transgenic plants results in fewer visible parthenogenetic embryos and a reduction of embryo cell number compared with controls. Our results endorse a key role forPsASGR-BBMLin parthenogenesis and a newly discovered role for a member of the BBM-like clade of APETALA 2 transcription factors. Induction of parthenogenesis byPsASGR-BBMLwill be valuable for installing parthenogenesis to synthesize apomixis in crops and will have further application for haploid induction to rapidly obtain homozygous lines for breeding.

Hybridization is a common evolutionary process with multiple possible outcomes. In vertebrates, interspecific hybridization has repeatedly generated parthenogenetic hybrid species. However, it is unknown whether the generation of parthenogenetic hybrids is a rare outcome of frequent hybridization between sexual species within a genus or the typical outcome of rare hybridization events. Darevskia is a genus of rock lizards with both hybrid parthenogenetic and sexual species. Using capture sequencing, we estimate phylogenetic relationships and gene flow among the sexual species, to determine how introgressive hybridization relates to the origins of parthenogenetic hybrids. We find evidence for widespread hybridization with gene flow, both between recently diverged species and deep branches. Surprisingly, we find no signal of gene flow between parental species of the parthenogenetic hybrids, suggesting that the parental pairs were either reproductively or geographically isolated early in their divergence. The generation of parthenogenetic hybrids in Darevskia is, then, a rare outcome of the total occurrence of hybridization within the genus, but the typical outcome when specific species pairs hybridize. Our results question the conventional view that parthenogenetic lineages are generated by hybridization in a window of divergence. Instead, they suggest that some lineages possess specific properties that underpin successful parthenogenetic reproduction.

Many parthenogenetically reproducing animals produce offspring not clonally but through different mechanisms collectively referred to as automixis. Here, meiosis proceeds normally but is followed by a fusion of meiotic products that restores diploidy. This mechanism typically leads to a reduction in heterozygosity among the offspring compared to the mother. Following a derivation of the rate at which heterozygosity is lost at one and two loci, depending on the number of crossovers between loci and centromere, a number of models are developed to gain a better understanding of basic evolutionary processes in automictic populations. Analytical results are obtained for the expected neutral genetic variation, effective population size, mutation–selection balance, selection with overdominance, the spread of beneficial mutations, and selection on crossover rates. These results are complemented by numerical investigations elucidating how associative overdominance (two off-phase deleterious mutations at linked loci behaving like an overdominant locus) can in some cases maintain heterozygosity for prolonged times, and how clonal interference affects adaptation in automictic populations. These results suggest that although automictic populations are expected to suffer from the lack of gene shuffling with other individuals, they are nevertheless, in some respects, superior to both clonal and outbreeding sexual populations in the way they respond to beneficial and deleterious mutations. Implications for related genetic systems such as intratetrad mating, clonal reproduction, selfing, as well as different forms of mixed sexual and automictic reproduction are discussed.

Most eukaryotes inherit their mitochondria from only one of their parents. When there are different sexes, it is almost always the maternal mitochondria that are transmitted. Indeed, maternal uniparental inheritance has been reported for the brown alga Ectocarpus but we show in this study that different strains of Ectocarpus can exhibit different patterns of inheritance: Ectocarpus siliculosus strains showed maternal uniparental inheritance, as expected, but crosses using different Ectocarpus species 7 strains exhibited either paternal uniparental inheritance or an unusual pattern of transmission where progeny inherited either maternal or paternal mitochondria, but not both. A possible correlation between the pattern of mitochondrial inheritance and male gamete parthenogenesis was investigated. Moreover, in contrast to observations in the green lineage, we did not detect any change in the pattern of mitochondrial inheritance in mutant strains affected in life cycle progression. Finally, an analysis of field-isolated strains provided evidence of mitochondrial genome recombination in both Ectocarpus species.

Parthenogenesis, or virgin birth, describes a mode of reproduction where an egg develops into an offspring without fertilization, and is observed across various vertebrate taxa, excluding mammals. Obligate parthenogenesis, found in around 100 vertebrate species and 1000 invertebrate species, is relatively rare. Conversely, facultative parthenogenesis, where females can reproduce both sexually and parthenogenetically, is observed in some vertebrates, including elasmobranchs. Notably, this phenomenon in elasmobranchs is mainly documented in captivity, allowing for detailed long-term observation. Specifically, this study reports the first case of facultative parthenogenesis in the common smooth-hound shark Mustelus mustelus , a species classified by IUCN as endangered. Here we show that the juvenile M. mustelus were born through parthenogenesis, exhibiting homozygosity at each genetic marker, consistent with terminal fusion automixis. Remarkably, this finding reveals that parthenogenesis can occur annually in these sharks, alternating between two females, and conclusively excludes long-term sperm storage as a cause. Consequently, this enhances our understanding of parthenogenesis in elasmobranchs and highlights the reproductive flexibility of M. mustelus . Overall, these results contribute to our broader understanding of reproductive strategies in elasmobranchs, which could inform conservation efforts for endangered species.

Abstract Genomes of aphids (family Aphididae) show several unusual evolutionary patterns. In particular, within the XO sex determination system of aphids, the X chromosome exhibits a lower rate of interchromosomal rearrangements, fewer highly expressed genes, and faster evolution at nonsynonymous sites compared with the autosomes. In contrast, other hemipteran lineages have similar rates of interchromosomal rearrangement for autosomes and X chromosomes. One possible explanation for these differences is the aphid's life cycle of cyclical parthenogenesis, where multiple asexual generations alternate with 1 sexual generation. If true, we should see similar features in the genomes of Phylloxeridae, an outgroup of aphids which also undergoes cyclical parthenogenesis. To investigate this, we generated a chromosome-level assembly for the grape phylloxera, an agriculturally important species of Phylloxeridae, and identified its single X chromosome. We then performed synteny analysis using the phylloxerid genome and 30 high-quality genomes of aphids and other hemipteran species. Unexpectedly, we found that the phylloxera does not share aphids’ patterns of chromosome evolution. By estimating interchromosomal rearrangement rates on an absolute time scale, we found that rates are elevated for aphid autosomes compared with their X chromosomes, but this pattern does not extend to the phylloxera branch. Potentially, the conservation of X chromosome gene content is due to selection on XO males that appear in the sexual generation. We also examined gene duplication patterns across Hemiptera and uncovered horizontal gene transfer events contributing to phylloxera evolution.

The BABY BOOM (BBM) AINTEGUMENTA-LIKE (AIL) AP2/ERF domain transcription factor is a major regulator of plant cell totipotency, as it induces asexual embryo formation when ectopically expressed. Surprisingly, only limited information is available on the role of BBM during zygotic embryogenesis. Here we reexamined BBM expression and function in the model plant Arabidopsis thaliana (Arabidopsis) using reporter analysis and newly developed CRISPR mutants. BBM was expressed in the embryo from the zygote stage and also in the maternal (nucellus) and filial (endosperm) seed tissues. Analysis of CRISPR mutant alleles for BBM (bbm-cr) and the redundantly acting AIL gene PLETHORA2 (PLT2) (plt2-cr) uncovered individual roles for these genes in the timing of embryo progression. We also identified redundant roles for BBM and PLT2 in endosperm proliferation and cellularization and the maintenance of zygotic embryo development. Finally, we show that ectopic BBM expression in the egg cell of Arabidopsis and the dicot crops Brassica napus and Solanum lycopersicon is sufficient to bypass the fertilization requirement for embryo development. Together these results highlight roles for BBM and PLT2 in seed development and demonstrate the utility of BBM genes for engineering asexual embryo development in dicot species.