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Abstract BackgroundLeaf economics theory holds that physiological constraints to photosynthesis have a role in the coordinated evolution of multiple leaf traits, an idea that can be extended to carnivorous plants occupying a particular trait space that is constrained by key costs and benefits. Pitcher traps are modified leaves that may face steep photosynthetic costs: a high-volume, three-dimensional tubular structure may be less efficient than a flat lamina. While past research has investigated the photosynthetic costs of pitchers, the exact suite of constraints shaping pitcher trait variation remain under-explored, including constraints to carnivorous function. ScopeIn this review, we describe various constraints arising from the dual photosynthetic and carnivorous functions of pitchers arising from developmental, functional, budgetary and environmental factors. In addition, we identify the data required to establish the leaf economics spectrum (LES) for carnivorous pitcher plants (CPPs), and – owing to the multifunctional roles of pitcher leaves – discuss difficulties in placing pitchers onto existing frameworks. ConclusionBecause pitcher traps serve multiple functions, both photosynthesis and nutrient acquisition (carnivory), they are difficult to place in the context of the LES, especially in light of a current lack of trait data. We describe a spectrum across the independent CPP lineages in approaches to balancing carnivory–photosynthesis tradeoffs. Future efforts to collect relevant data can clarify the forces that shape observed pitcher trait variation, and increase understanding of principles that may be ultimately generalized to other plants. 

Abstract Cases of convergent adaptation, especially between close relatives within a lineage, provide insights into constraints underlying the mechanisms of evolution. We examined this in the carnivorous plant family Lentibulariaceae, with its highly divergent trap designs but shared need for prey digestion, by generating a chromosome-level genome assembly for Pinguicula gigantea, the giant butterwort. Our work confirms a history of whole-genome duplication in the genus and provides strong phylogenomic evidence for a sister-group relationship between Lentibulariaceae and Acanthaceae. The genome also reveals that a key digestive adaptation, the expansion of cysteine protease genes active in digestion, was achieved through independent tandem duplications in the butterwort (Pinguicula) and its close relative, the bladderwort (Utricularia). Most of these parallel expansions arose in non-homologous regions of the two genomes, with a smaller subset located on homologous blocks. This study provides clear genomic evidence for convergent evolution and illustrates how similar selective pressures can repeatedly shape genomes in analogous ways. 

Abstract Living in nutrient-poor environments, the carnivorous Venus flytrapDionaea muscipulacaptures animal prey to compensate for this deficiency. Stimulation of trigger hairs located on the inner trap surface elicits an action potential (AP). While two consecutive APs result in fast trap closure in wildtype (WT) plants, sustained AP generation by the insect struggling to escape the trap leads to jasmonic acid (JA) biosynthesis, formation of the digestive “stomach”, and release of enzymes needed to decompose the victim. TheDionaea muscipulaDYSCALCULIA (DYSC) mutant is able to fire touch-induced APs, but unlike WT plants, it does not snap-close its traps after two consecutive APs. Moreover, DYSC plants fail to properly initiate the JA pathway in response to mechanostimulation and even wounding, a well-known JA-dependent process conserved among plants. As demonstrated in previous studies, this DYSC mutant defect is associated with impaired decoding of mechanostimulation (i.e. touch) -induced Ca²⁺signals. External JA application to the trap, however, restores slow trap closure and digestive gland function in DYSC, while rapid trap closure is JA-independent and cannot be rescued by exogenous JA application. Higher frequency mechanostimulation and thus more APs, however, revealed that DYSC is still able to close its traps, albeit much slower than WT plants. To reveal the molecular underpinnings of DYSC’s delayed trap movement, we generated a chromosome-scaleDionaeagenome assembly and profiled gene expression. The refined transcriptomic analysis uncovered widespread misregulation of cell wall-related genes in DYSC, implicating altered cell wall plasticity in the sluggish mutant. Cell indentation studies by atomic force microscopy revealed a strictly localized and strikingly enhanced stiffening of the cell wall for DYSC that may hinder rapid trap closure and snap buckling. Together, these genomic, transcriptomic, and biophysical data identify cell wall elasticity as a key constraint on voltage and Ca²⁺dependent trap kinetics. This finding documents the interrelationship between mechanosensing and Ca²⁺signaling in the ultrafast capture organ of the Venus flytrap. 

Abstract The inversion of C3 stereochemistry in monoterpenoid indole alkaloids (MIAs), derived from the central precursor strictosidine (3S), is essential for synthesizing numerous 3RMIAs and oxindoles, including the antihypertensive drug reserpine found inRauvolfia serpentina(Indian snakeroot) andRauvolfia tetraphylla(devil pepper) of the plant family Apocynaceae. MIA biosynthesis begins with the reduction of strictosidine aglycone by various reductases, preserving the initial 3Sstereochemistry. In this study, we identify and biochemically characterize a conserved oxidase-reductase pair from the Apocynaceae, Rubiaceae, and Gelsemiaceae families of the order Gentianales: the heteroyohimbine/yohimbine/corynanthe C3-oxidase (HYC3O) and C3-reductase (HYC3R). These enzymes collaboratively invert the 3Sstereochemistry to 3Racross a range of substrates, resolving the long-standing question about the origin of 3RMIAs and oxindole derivatives, and facilitation of reserpine biosynthesis. Notably,HYC3OandHYC3Rare located within gene clusters in both theR. tetraphyllaandCatharanthus roseus(Madagascar periwinkle) genomes, which are partially homologous to an elusive geissoschizine synthase (GS) gene cluster we also identified in these species. InR. tetraphylla, these clusters occur closely in tandem on a single chromosome, likely stemming from a single segmental duplication event, while inC. roseus, a closely related member of rauvolfioid Apocynaceae, they were later separated by a chromosomal translocation. The ancestral genomic context for both clusters can be traced all the way back to common ancestry with grapevine. Given the presence of syntenic GS homologs inMitragyna speciosa(Rubiaceae), the GS cluster, at least in part, probably evolved at the base of the Gentianales, which split from other core eudicots up to 135 million years ago. We also show that the strictosidine biosynthetic gene cluster, required to initiate the MIA pathway, plausibly evolved concurrently. The reserpine biosynthetic cluster likely arose much later in the rauvolfioid lineage of Apocynaceae. Collectively, our work uncovers the genomic and biochemical basis for key events in MIA evolution and diversification, providing insights beyond the well-characterized vinblastine and ajmaline biosynthetic pathways. 

Abstract Over the past 15 years, the D-statistic, a four-taxon test for organismal admixture (hybridization, or introgression) which incorporates single nucleotide polymorphism data with allelic patterns ABBA and BABA, has seen considerable use. This statistic seeks to discern significant deviation from either a given species tree assumption, or from the balanced incomplete lineage sorting that could otherwise defy this species tree. However, while the D-statistic can successfully discriminate admixture from incomplete lineage sorting, it is not a simple matter to determine the directionality of admixture using only four-leaf tree models. As such, methods have been developed that use 5 leaves to evaluate admixture. Among these, the DFOIL method, which tests allelic patterns on the “symmetric” tree S = (((1,2),(3,4)),5), succeeds in finding admixture direction for many five-taxon examples. However, DFOIL does not make full use of all symmetry, nor can DFOIL function properly when ancient samples are included because of the reliance on singleton patterns (such as BAAAA and ABAAA). Here, we take inspiration from DFOIL to develop a new and completely general family of five-leaf admixture tests, dubbed Δ-statistics, that can either incorporate or exclude the singleton allelic patterns depending on individual taxon and age sampling choices. We describe two new shapes that are also fully testable, namely the “asymmetric” tree A = ((((1,2),3),4),5) and the “quasisymmetric” tree Q = (((1,2),3),(4,5)), which can considerably supplement the “symmetric“ S = (((1,2),(3,4)),5) model used by DFOIL. We demonstrate the consistency of Δ-statistics under various simulated scenarios, and provide empirical examples using data from black, brown and polar bears, the latter also including two ancient polar bear samples from previous studies. Recently DFOIL and one of these ancient samples was used to argue for a dominant polar bear → brown bear introgression direction. However, we find, using both this ancient polar bear and our own, that by far the strongest signal using both DFOIL and Δ-statistics on tree S is actually bidirectional gene flow of indistinguishable direction. Further experiments on trees A and Q instead highlight what were likely two phases of admixture: one with stronger brown bear → polar bear introgression in ancient times, and a more recent phase with predominant polar bear → brown bear directionality. Code and documentation available at https://github.com/KalleLeppala/Delta-statistics. 

Abstract Coffea arabica, an allotetraploid hybrid ofCoffea eugenioidesandCoffea canephora, is the source of approximately 60% of coffee products worldwide, and its cultivated accessions have undergone several population bottlenecks. We present chromosome-level assemblies of a di-haploidC. arabicaaccession and modern representatives of its diploid progenitors,C. eugenioidesandC. canephora. The three species exhibit largely conserved genome structures between diploid parents and descendant subgenomes, with no obvious global subgenome dominance. We find evidence for a founding polyploidy event 350,000–610,000 years ago, followed by several pre-domestication bottlenecks, resulting in narrow genetic variation. A split between wild accessions and cultivar progenitors occurred ~30.5 thousand years ago, followed by a period of migration between the two populations. Analysis of modern varieties, including lines historically introgressed withC. canephora, highlights their breeding histories and loci that may contribute to pathogen resistance, laying the groundwork for future genomics-based breeding ofC. arabica. 

Abstract Ancient whole-genome duplications (WGDs) characterize many large angiosperm lineages, including angiosperms themselves. Prominently, the core eudicot lineage accommodates 70% of all angiosperms and shares ancestral hexaploidy, termedgamma.Gammaarose via two WGDs that occurred early in eudicot history; however, the relative timing of these is unclear, largely due to the lack of high-quality genomes among early-diverging eudicots. Here, we provide complete genomes forBuxus sinica(Buxales) andTetracentron sinense(Trochodendrales), representing the lineages most closely related to core eudicots. We show thatBuxusandTetracentronare both characterized by independent WGDs, resolve relationships among early-diverging eudicots and their respective genomes, and use the RACCROCHE pipeline to reconstruct ancestral genome structure at three key phylogenetic nodes of eudicot diversification. Our reconstructions indicate genome structure remained relatively stable during early eudicot diversification, and reject hypotheses ofgammaarising via inter-lineage hybridization between ancestral eudicot lineages, involving, instead, only stem lineage core eudicot ancestors. 

Abstract Species radiations, despite immense phenotypic variation, can be difficult to resolve phylogenetically when genetic change poorly matches the rapidity of diversification. Genomic potential furnished by palaeopolyploidy, and relative roles for adaptation, random drift and hybridisation in the apportionment of genetic variation, remain poorly understood factors. Here, we study these aspects in a model radiation,Syzygium, the most species-rich tree genus worldwide. Genomes of 182 distinct species and 58 unidentified taxa are compared against a chromosome-level reference genome of the sea apple,Syzygium grande. We show that whileSyzygiumshares an ancient genome doubling event with other Myrtales, little evidence exists for recent polyploidy events. Phylogenomics confirms thatSyzygiumoriginated in Australia-New Guinea and diversified in multiple migrations, eastward to the Pacific and westward to India and Africa, in bursts of speciation visible as poorly resolved branches on phylogenies. Furthermore, some sublineages demonstrate genomic clines that recapitulate cladogenetic events, suggesting that stepwise geographic speciation, a neutral process, has been important inSyzygiumdiversification. 

Abstract Lychee is an exotic tropical fruit with a distinct flavor. The genome of cultivar ‘Feizixiao’ was assembled into 15 pseudochromosomes, totaling ~470 Mb. High heterozygosity (2.27%) resulted in two complete haplotypic assemblies. A total of 13,517 allelic genes (42.4%) were differentially expressed in diverse tissues. Analyses of 72 resequenced lychee accessions revealed two independent domestication events. The extremely early maturing cultivars preferentially aligned to one haplotype were domesticated from a wild population in Yunnan, whereas the late-maturing cultivars that mapped mostly to the second haplotype were domesticated independently from a wild population in Hainan. Early maturing cultivars were probably developed in Guangdong via hybridization between extremely early maturing cultivar and late-maturing cultivar individuals. Variable deletions of a 3.7 kb region encompassed by a pair ofCONSTANS-like genes probably regulate fruit maturation differences among lychee cultivars. These genomic resources provide insights into the natural history of lychee domestication and will accelerate the improvement of lychee and related crops. 

Carnivorous plants are a paradigm of convergent evolution, but their genomes reveal even deeper layers of complexity. Recent work uncovers widespread polyploidy, including the decaploid East Asian pitcher plant (Nepenthes gracilis) genome and hybrid origins for the tetraploid Venus flytrap (Dionaea muscipula) and queen (hexaploid) and Cape (dodecaploid) sundews (Drosera regia and D. capensis, respectively). The bladderwort (Utricularia gibba) experienced extreme genome compaction while retaining otherwise typical gene number, challenging assumptions about genome size. Molecular convergence is conspicuous, from digestive enzyme recruitment to repeated amino acid substitutions under functional constraints. Drosera species further illustrate how centromere type (monocentric versus holocentric) shapes genome architecture. These discoveries position carnivorous plants as models for studying the plasticity and adaptive landscapes of plant genomes, including tradeoffs between local and global gene duplication and intergenic DNA deletion.