The origin of novel traits is recognized as an important process underlying many major evolutionary radiations. We studied the genetic basis for the evolution of haustoria, the novel feeding organs of parasitic flowering plants, using comparative transcriptome sequencing in three species of Orobanchaceae. Around 180 genes are upregulated during haustorial development following host attachment in at least two species, and these are enriched in proteases, cell wall modifying enzymes, and extracellular secretion proteins. Additionally, about 100 shared genes are upregulated in response to haustorium inducing factors prior to host attachment. Collectively, we refer to these newly identified genes as putative “parasitism genes.” Most of these parasitism genes are derived from gene duplications in a common ancestor of Orobanchaceae and Mimulus guttatus, a related nonparasitic plant. Additionally, the signature of relaxed purifying selection and/or adaptive evolution at specific sites was detected in many haustorial genes, and may play an important role in parasite evolution. Comparative analysis of gene expression patterns in parasitic and nonparasitic angiosperms suggests that parasitism genes are derived primarily from root and floral tissues, but with some genes co-opted from other tissues. Gene duplication, often taking place in a nonparasitic ancestor of Orobanchaceae, followed by regulatory neofunctionalization, was an important process in the origin of parasitic haustoria.

Horizontal gene transfer (HGT) is the transfer of genetic material across species boundaries and has been a driving force in prokaryotic evolution. HGT involving eukaryotes appears to be much less frequent, and the functional implications of HGT in eukaryotes are poorly understood. We test the hypothesis that parasitic plants, because of their intimate feeding contacts with host plant tissues, are especially prone to horizontal gene acquisition. We sought evidence of HGTs in transcriptomes of three parasitic members of Orobanchaceae, a plant family containing species spanning the full spectrum of parasitic capabilities, plus the free-living Lindenbergia. Following initial phylogenetic detection and an extensive validation procedure, 52 highconfidence horizontal transfer events were detected, often from lineages of known host plants and with an increasing number of HGT events in species with the greatest parasitic dependence. Analyses of intron sequences in putative donor and recipient lineages provide evidence for integration of genomic fragments far more often than retro-processed RNA sequences. Purifying selection predominates in functionally transferred sequences, with a small fraction of adaptively evolving sites. HGT-acquired genes are preferentially expressed in the haustorium-the organ of parasitic plants-and are strongly biased in predicted gene functions, suggesting that expression products of horizontally acquired genes are contributing to the unique adaptive feeding structure of parasitic plants.

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The apple cultivar ‘Honeycrisp’ has superior fruit quality traits, cold hardiness, and disease resistance, making it a popular breeding parent. However, it suffers from several physiological disorders, production, and postharvest issues. Despite several available apple genome sequences, understanding of the genetic mechanisms underlying cultivar-specific traits remains lacking. Here, we present a highly contiguous, fully phased, chromosome-level genome of ‘Honeycrisp’ apples, using PacBio HiFi, Omni-C, and Illumina sequencing platforms, with two assembled haplomes of 674 Mbp and 660 Mbp, and contig N50 values of 32.8 Mbp and 31.6 Mbp, respectively. Overall, 47,563 and 48,655 protein-coding genes were annotated from each haplome, capturing 96.8–97.4% complete BUSCOs in the eudicot database. Gene family analysis reveals most ‘Honeycrisp’ genes are assigned into orthogroups shared with other genomes, with 121 ‘Honeycrisp’-specific orthogroups. This resource is valuable for understanding the genetic basis of important traits in apples and related Rosaceae species to enhance breeding efforts.