Angiosperms (flowering plants) are by far the most diverse land plant group with over 300,000 species. The sudden appearance of diverse angiosperms in the fossil record was referred to by Darwin as the “abominable mystery,” hence contributing to the heightened interest in angiosperm evolution. Angiosperms display wide ranges of morphological, physiological, and ecological characters, some of which have probably influenced their species richness. The evolutionary analyses of these characteristics help to address questions of angiosperm diversification and require well resolved phylogeny. Following the great successes of phylogenetic analyses using plastid sequences, dozens to thousands of nuclear genes from next-generation sequencing have been used in angiosperm phylogenomic analyses, providing well resolved phylogenies and new insights into the evolution of angiosperms. In this review we focus on recent nuclear phylogenomic analyses of large angiosperm clades, orders, families, and subdivisions of some families and provide a summarized Nuclear Phylogenetic Tree of Angiosperm Families. The newly established nuclear phylogenetic relationships are highlighted and compared with previous phylogenetic results. The sequenced genomes of Amborella, Nymphaea, Chloranthus, Ceratophyllum, and species of monocots, Magnoliids, and basal eudicots, have facilitated the phylogenomics of relationships among five major angiosperms clades. All but one of the 64 angiosperm orders were included in nuclear phylogenomics with well resolved relationships except the placements of several orders. Most families have been included with robust and highly supported placements, especially for relationships within several large and important orders and families. Additionally, we examine the divergence time estimation and biogeographic analyses of angiosperm on the basis of the nuclear phylogenomic frameworks and discuss the differences compared with previous analyses. Furthermore, we discuss the implications of nuclear phylogenomic analyses on ancestral reconstruction of morphological, physiological, and ecological characters of angiosperm groups, limitations of current nuclear phylogenomic studies, and the taxa that require future attention.

Fruit functions in seed protection and dispersal and belongs to many dry and fleshy types, yet their evolutionary pattern remains unclear in part due to uncertainties in the phylogenetic relationships among several orders and families. Thus we used nuclear genes of 502 angiosperm species representing 231 families to reconstruct a well supported phylogeny, with resolved relationships for orders and families with previously uncertain placements. Using this phylogeny as a framework, molecular dating supports a Triassic origin of the crown angiosperms, followed by the emergence of most orders in the Jurassic and Cretaceous and their rise to ecological dominance during the Cretaceous Terrestrial Revolution. The robust phylogeny allowed an examination of the evolutionary pattern of fruit and ovary types, revealing a trend of parallel carpel fusions during early diversifications in eudicots, monocots, and magnoliids. Moreover, taxa in the same order or family with the same ovary type can develop either dry or fleshy fruits with strong correlations between specific types of dry and fleshy fruits; such associations of ovary, dry and fleshy fruits define several ovary-fruit “modules” each found in multiple families. One of the frequent modules has an ovary containing multiple ovules, capsules and berries, and another with an ovary having one or two ovules, achenes (or other single-seeded dry fruits) and drupes. This new perspective of relationships among fruit types highlights the closeness of specific dry and fleshy fruit types, such as capsule and berry, that develop from the same ovary type and belong to the same module relative to dry and fleshy fruits of other modules (such as achenes and drupes). Further analyses of gene families containing known genes for ovary and fruit development identified phylogenetic nodes with multiple gene duplications, supporting a possible role of whole-genome duplications, in combination with climate changes and animal behaviors, in angiosperm fruit and ovary diversification.

The woody bamboos (Bambusoideae) exhibit distinctive biological traits within Poaceae, such as highly lignified culms, rapid shoot growth, monocarpic mass flowering and nutlike or fleshy caryopses. Much of the remarkable morphological diversity across the subfamily exists within a single hexaploid clade, the paleotropical woody bamboos (PWB), making it ideal to investigate the factors underlying morphological evolution in woody bamboos. However, the origin and biogeographical history of PWB remain elusive, as does the effect of environmental factors on the evolution of their morphological characters. We generated a robust and time-calibrated phylogeny of PWB using single nucleotide polymorphisms retrieved from optimized double digest restriction site associated DNA sequencing, and explored the evolutionary trends of habit, inflorescence, and caryopsis type in relation to environmental factors including climate, soil, and topography. We inferred that the PWB started to diversify across the Oligocene–Miocene boundary and formed four major clades, that is, Melocanninae, Racemobambosinae s.l. (comprising Dinochloinae, Greslanlinae, Racemobambosinae s.str. and Temburongiinae), Hickeliinae and Bambusinae s.l. (comprising Bambusinae s.str. plus Holttumochloinae). The ancestor of PWB was reconstructed as having erect habit, indeterminate inflorescence and basic caryopsis. The characters including climbing/scrambling habit, determinate inflorescence, and nucoid/bacoid caryopsis have since undergone multiple changes and reversals during the diversification of PWB. The evolution of all three traits was correlated with, and hence likely influenced by, aspects of climate, topography, and soil, with climate factors most strongly correlated with morphological traits, and soil factors least so. However, topography had more influence than climate or soil on the evolution of erect habit, whereas both factors had greater effect on the evolution of bacoid caryopsis than did soil. Our results provide novel insights into morphological diversity and adaptive evolution in bamboos for future ecological and evolutionary research.

Although the frequency of ancient hybridization across the Tree of Life is greater than previously thought, little work has been devoted to uncovering the extent, timeline, and geographic and ecological context of ancient hybridization. Using an expansive new dataset of nuclear and chloroplast DNA sequences, we conducted a multifaceted phylogenomic investigation to identify ancient reticulation in the early evolution of oaks (Quercus). We document extensive nuclear gene tree and cytonuclear discordance among major lineages of Quercus and relatives in Quercoideae. Our analyses recovered clear signatures of gene flow against a backdrop of rampant incomplete lineage sorting, with gene flow most prevalent among major lineages of Quercus and relatives in Quercoideae during their initial radiation, dated to the Early-Middle Eocene. Ancestral reconstructions including fossils suggest ancestors of Castanea + Castanopsis, Lithocarpus, and the Old World oak clade probably co-occurred in North America and Eurasia, while the ancestors of Chrysolepis, Notholithocarpus, and the New World oak clade co-occurred in North America, offering ample opportunity for hybridization in each region. Our study shows that hybridization—perhaps in the form of ancient syngameons like those seen today—has been a common and important process throughout the evolutionary history of oaks and their relatives. Concomitantly, this study provides a methodological framework for detecting ancient hybridization in other groups.

Sex chromosomes have evolved independently in numerous lineages across the Tree of Life, in both diploid-dominant species, including many animals and plants, and the less studied haploid-dominant plants and algae. Strict genetic sex determination ensures that individuals reproduce by outcrossing. However, species with separate sexes (termed dioecy in diploid plants, and dioicy in haploid plants) may sometimes evolve different sex systems, and become monoicous, with the ability to self-fertilize. Here, we studied dioicy-monoicy transitions in the ancient liverwort haploid-dominant plant lineage, using three telomere-to-telomere gapless chromosome-scale reference genome assemblies from the Ricciaceae group of Marchantiales. Ancestral liverworts are believed to have been dioicous, with U and V chromosomes (chromosome 9) determining femaleness and maleness, respectively. We confirm the finding that monoicy in Ricciocarpos natans evolved from a dioicous ancestor, and most ancestrally U chromosomal genes have been retained on autosomes in this species. We also describe evidence suggesting the possible re-evolution of dioicy in the genus Riccia, with probable de novo establishment of a sex chromosome from an autosome (chromosome 5), and further translocations of genes from the new sex chromosome to autosomes. Our results also indicated that micro-chromosomes are consistent genomic features, and may have evolved independently from sex chromosomes in Ricciocarpos and Riccia lineages.

Host–pathogen co-evolution shapes resistance (R) proteins and their recognition of pathogen avirulence factors. However, little attention has been paid to naturally occurring genetic diversity in R genes. In this study, 12 Solanum bulbocastanum accessions from the Commonwealth Potato Collection were screened for resistance to Phytophthora infestans, identifying 11 resistant and one susceptible accession. Targeted enrichment sequencing of nucleotide-binding leucine-rich repeat (NLR) genes using RenSeq, followed by diagnostic RenSeq (dRenSeq) analysis, revealed that all accessions except 7650 contained Rpi-blb1/RB variants. Variants in accessions 7641 and 7648 were non-functional, while three novel functional variants were identified. Cloning and functional analysis of Rpi-blb1/RB variants assessed their recognition of the avirulence factor IPI-O1. Three variants were functional, conferring resistance to P. infestans. Variants in accessions 7644 and 7647 also recognized IPI-O4, confirmed in transgenic potatoes. Analysis of a non-functional variant in S. bulbocastanum accession 7648 identified amino acid Ser347 in the nucleotide-binding (NB-ARC) domain as critical for cell-death initiation following IPI-O1 recognition. Predictions from the FunFOLD2 protein–ligand interaction model suggested that Ser347 is essential for ATP binding, suggesting potential inhibition on pentameric resistosome assembly. Western blot analysis revealed that the mutation of Ser347 to Asn markedly compromises the Rpi-blb1/RB protein stability, and co-immunoprecipitation assay further confirmed that this mutation severely disrupts the self-association of CCNB, thereby preventing Rpi-blb1/RB activation. Consistently, substituting Asn347 with serine restored function, underscoring its key role in Rpi-blb1/RB activity. Cell biology experiments demonstrated that Rpi-blb1/RB relocalize to the plasma membrane in response to IPI-O1. This relocalization depends on Ser347, further supporting the idea that its mutation affects resistosome formation, impairing resistance. This study provides an in-depth functional analysis of natural Rpi-blb1/RB diversity, offering insights into NLR protein evolution and resistance mechanisms in potatoes.

Plants adapt to their local environments through natural or artificial selection of optimal phenotypes. Recent advances in genomics and computational biology, which integrate phenotypic and multi-omics data, have facilitated the rapid identification of key genes and allelic variations that underlie these adaptive evolutionary processes. Understanding the underlying molecular mechanisms has significantly enhanced our knowledge of how plants respond to changed habitats, including various biotic and abiotic stresses. In this review, we highlight recent progress in elucidating the genetic basis of phenotypic variation in morphological traits and stress responses, as well as the emergence of new ecotypes, subspecies, and species during adaptive evolution across varied environments. This occurs through allelic divergences in both coding and non-coding regions in both model and non-model plants. Furthermore, the terrestrialization and early diversification of land plants involved the acquisition of additional genes, primarily through horizontal gene transfer and whole-genome duplication, which facilitated the development of complex molecular pathways to adapt to increasingly diverse environments. Finally, we discuss emerging trends and prospects for exploring and utilizing beneficial alleles for environmental adaptation, to guide crop breeding efforts in response to global climate change.

DNAs from the cytoplasmic genomes often communicate with the nuclear genome during regulation, development, and evolution. However, the dynamics of cytonuclear interaction during crop domestication have still been rarely investigated. Here, we examine cytonuclear interactions during grapevine domestication using pan-mitogenome, pan-plastome, and haplotype-resolved nuclear genomes, all assembled from long-read sequences across 33 wild and domesticated grapevine accessions. Structural variation shaped the mitogenomic variation in gene contents, leading to duplications of three specific genes during grapevine domestication (one cox and two rpl genes). Extensive genomic signals of cytonuclear interactions were detected, including a total of 212–431 nuclear–mitochondrial segments (NUMTs) and 95–205 nuclear–plastid segments (NUPTs). These results showed that NUMTs were under strong selection and were more abundant in cultivated grapes, whereas NUPTs dominated in wild grapes, indicating the evolutionary trajectories of cytonuclear interactions during grape domestication. Through Genome-Wide Association Study (GWAS), we identified 84 candidate genes associated with mitochondrial–nuclear genome interactions. Among these, the PFD1 gene acts as a signaling regulator, modulating specific signaling pathways regulated by the mitochondria. Interestingly, there are significantly more cytonuclear interaction genes near NUMTs than in other genomic regions, suggesting NUMT-mediated interactions between the nuclear and mitochondrial genomes. Overall, our study provides evidence that NUMTs promote cytonuclear interaction during grapevine domestication, offering new insight into the impact of cytonuclear interactions on plant evolution, genetics, and breeding.

While many plant lineages display remarkable diversity in morphological form, our understanding of how phenotypic diversity, or disparity, arises in relation to genomic evolution over geologic scales remains poorly understood. Here, we investigated the relationship between phenotypic and genomic evolution in the Fagales, a lineage of woody plants that has been a dominant component of temperate and subtropical forests since the Late Cretaceous. We examine newly generated transcriptomic and trait datasets representing most extant genera and a rich diversity of Cretaceous fossil representatives. Our phylogenomic analyses identify recurrent hotspots of gene duplication and genomic conflict across the order. Our phenotypic analyses showed that the morphospace occupied by Fagales was largely filled by the early Cenozoic, and rates of evolution were highest during the early radiation of the Fagales crown and its major families. These results suggest that Fagales conforms to an “early-burst” model of disparification, with morphospace being filled early in the order's diversification history, and that elevated levels of phenotypic evolution also often correspond to hotspots of gene duplication. Species diversification appears decoupled from patterns of both phenotypic and genomic evolution, highlighting the multidimensional nature of the evolution of plant diversity across geological timescales.

Rates of protein evolution (d_N/d_S) vary widely across the tree of life. In plants, both life-history traits and GC-biased gene conversion (gBGC) are thought to contribute to this variation, although disentangling their individual contributions remains a challenge. Using information on variation in life-history traits and molecular data in 148 species from Poaceae subfamilies Bambusoideae (mostly woody) and Pooideae (exclusively herbaceous), we investigated the relative importance of modes of reproduction and the non-selective forces of gBGC on protein evolutionary rates between the two subfamilies. Elevated rates of protein evolution associated with relaxed purifying selection were more evident in woody bamboos than in Pooideae and were better explained by reproductive modes than by traits that are likely proxies of effective population size. Although gBGC slightly reduced protein evolutionary rates in both subfamilies, its contribution had only a limited effect on molecular divergence between the groups. Forward simulations generally supported our empirical results on the influence of reproductive mode on selection and gBGC. Our findings from two sister lineages of the grass family provide evidence for association between protein evolution and life-history traits governing reproductive mode and enhance understanding of molecular evolution in plants with contrasting reproductive strategies.