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Barfuss, M. H. J.

Publications and source records attributed to Barfuss, M. H. J..

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Closely related facultative and constitutive CAM phenotypes show little transcriptomic overlap in the subgenus Tillandsia

Crassulacean acid metabolism (CAM) is a water-efficient photosynthetic strategy involving a coordinated suite of complex traits including metabolic, anatomical and regulatory aspects that shift across the diel cycle. While CAM has evolved repeatedly in land plants, the evolutionary routes enabling this convergence remain elusive. Whereas the same core CAM (de)carboxylation genes are consistently involved, a key question is whether distinct CAM phenotypes also depend on a shared set of auxiliary genes, reflecting a quantitative continuum of expression, or whether they can instead emerge through divergent or redundant peripheral solutions. The bromeliad subgenus Tillandsia, with diverse photosynthetic strategies, offers an ideal system to explore this question. Using physiological and transcriptomic analyses of well-watered and water-limited accessions of two closely related species, we characterized facultative and constitutive CAM. By comparing orthologous gene expression and orthogroup recruitment, we found that while both species performed CAM upon water-withholding, transcriptional shifts in pathways related to stomatal movement, sugar/malate transport, aquaporins and starch metabolism showed minimal overlap. Core enzymes involved in the CAM (de)carboxylation cycle exhibited broadly shared expression patterns, yet the facultative CAM species uniquely up-regulated PPC2 at night instead of the canonical CAM-related PEPC ortholog PPC1. Our study reveals that, while the expression of certain core CAM enzymes is conserved, the surrounding transcriptional architecture can differ substantially even between closely related species. This supports a model in which CAM evolves through a mosaic recruitment of functionally equivalent, yet non-orthologous genes - underscoring its flexible and modular genetic architecture. These insights advance our understanding of the mechanisms enabling the repeated evolution of CAM and its capacity to facilitate adaptive diversification.

evolutionary biology↗

The explosive radiation of the Neotropical Tillandsia subgenus Tillandsia (Bromeliaceae) has been facilitated by pervasive hybridization

The recent rapid radiation of Tillandsia subgenus Tillandsia (Bromeliaceae) provides an attractive system to study the drivers and constraints of species diversification. This species-rich Neotropical monocot clade includes predominantly epiphytic species displaying vast phenotypic diversity. Recent in-depth phylogenomic work revealed that the subgenus originated within the last 7 MY, with one major expansion from South into Central America within the last 5 MY. However, disagreements between phylogenies and lack of resolution at shallow nodes suggest that hybridization may have occurred throughout the radiation, together with frequent incomplete lineage sorting and rapid gene family evolution. We used whole-genome resequencing data to explore the evolutionary history of representative ingroup species employing both tree-based and network approaches. Our results indicate that lineage co-occurrence does not predict relatedness and confirm significant deviations from a tree-like structure, coupled with pervasive gene tree discordance. Focusing on hybridization, ABBA-BABA and related statistics were used to infer the rates and relative timing of events, while topology weighting uncovered high heterogeneity of the phylogenetic signal along the genome. High rates of hybridization within and among subclades suggest that, contrary to previous hypotheses, the expansion of subgenus Tillandsia into Central America proceeded through several dispersal events, punctuated by episodes of diversification and gene flow. Network analysis revealed reticulation as a plausible propeller during radiation and establishment across different ecological niches. This work contributes a plant example of prevalent hybridization during rapid species diversification, supporting the hypothesis that interspecific gene flow facilitates explosive diversification.

evolutionary biology↗

Short structural variation fuelled CAM evolution within an explosive bromeliad radiation

1.The subgenus Tillandsia (Bromeliaceae) belongs to one of the fastest radiating clades in the plant kingdom and is characterised by the repeated evolution of Crassulacean Acid Metabolism (CAM). Despite its complex genetic basis, this water-conserving trait has evolved independently across many plant families and is regarded as a key innovation trait and driver of ecological diversification in Bromeliaceae. By producing high-quality genome assemblies of a Tillandsia species pair displaying divergent photosynthetic phenotypes, and combining genome-wide investigations of synteny, TE dynamics, sequence evolution, gene family evolution and temporal differential expression, we were able to pinpoint the genomic drivers of CAM evolution in Tillandsia. Several large-scale rearrangements associated with karyotype changes between the two genomes and a highly dynamic TE landscape shaped the genomes of Tillandsia. However, our analyses show that rewiring of photosynthetic metabolism is mainly obtained through regulatory evolution rather than coding sequence evolution, as CAM-related genes are differentially expressed across a 24-hour cycle between the two species, but are no candidates of positive selection. Gene orthology analyses reveal that CAM-related gene families manifesting differential expression underwent accelerated gene family expansion in the constitutive CAM species, further supporting the view of gene family evolution as a driver of CAM evolution.

evolutionary biology↗

Taxon-specific or universal? Using target capture to study the evolutionary history of a rapid radiation

Target capture has emerged as an important tool for phylogenetics and population genetics in non-model taxa. Whereas developing taxon-specific capture probes requires sustained efforts, available universal kits may have a lower power to reconstruct relationships at shallow phylogenetic scales and within rapidly radiating clades. We present here a newly-developed target capture set for Bromeliaceae, a large and ecologically-diverse plant family with highly variable diversification rates. The set targets 1,776 coding regions, including genes putatively involved in key innovations, with the aim to empower testing of a wide range of evolutionary hypotheses. We compare the relative power of this taxon-specific set, Bromeliad1776, to the universal Angiosperms353 kit. The taxon-specific set results in higher enrichment success across the entire family, however, the overall performance of both kits to reconstruct phylogenetic trees is relatively comparable, highlighting the vast potential of universal kits for resolving evolutionary relationships. For more detailed phylogenetic or population genetic analyses, e.g. the exploration of gene tree concordance, nucleotide diversity or population structure, the taxon-specific capture set presents clear benefits. We discuss the potential lessons that this comparative study provides for future phylogenetic and population genetic investigations, in particular for the study of evolutionary radiations.

evolutionary biology↗

Genomic footprints of repeated evolution of CAM photosynthesis in tillandsioid bromeliads

The adaptive radiation of Bromeliaceae (pineapple family) is one of the most diverse among Neotropical flowering plants. Diversification in this group was facilitated by several key innovations including the transition from C3 to CAM photosynthesis. We used a phylogenomic approach complemented by differential gene expression (RNA-seq) and targeted metabolite profiling to address the patterns and mechanisms of C3/CAM evolution in the extremely species-rich bromeliad genus Tillandsia and related taxa. Evolutionary analyses at a range of different levels (selection on protein-coding genes, gene duplication and loss, regulatory evolution) revealed three common themes driving the evolution of CAM: response to heat and drought, alterations to basic carbohydrate metabolism, and regulation of organic acid storage. At the level of genes and their products, CAM/C3 shifts were accompanied by gene expansion of a circadian regulator, re-programming of ABA-related gene expression, and adaptive sequence evolution of an enolase, effectively linking carbohydrate metabolism to ABA-mediated stress response. These changes include several pleiotropic regulators, which facilitated the evolution of correlated adaptive traits during a textbook adaptive radiation.

genomics↗