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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.