Biology subjects

Scharmann, M.

Publications and source records attributed to Scharmann, M..

7 recordsLinked to original sources

bioRxiv2024

Genomic imprinting in an early-diverging angiosperm reveals ancient mechanisms for seed initiation in flowering plants

The evolution of the seed habit marks a pivotal innovation of the spermatophytes. Angiosperms further refined this trait by coupling the development of seed accessory structures to fertilization, optimizing resource allocation. Here, we demonstrate that post-fertilization auxin production is an evolutionarily conserved mechanism for seed initiation in angiosperms. We also provide evidence that this pathway likely emerged from a switch from maternal to paternal control after the divergence of angiosperms from their gymnosperm ancestors. Our study thus brings new insights into the evolutionary origins of the endosperm, which was a determining feature for the rapid rise to dominance of flowering plants.

plant biology↗

bioRxiv2023

Subgenome dominance shapes novel gene evolution in the decaploid pitcher plant Nepenthes gracilis

Subgenome dominance after whole-genome duplication generates distinction in gene number and expression at the level of chromosome sets, but it remains unclear how this process may be involved in evolutionary novelty. Here, we generated a chromosome-scale genome assembly of the Asian pitcher plant Nepenthes gracilis to analyze how its novel traits (dioecy and carnivorous pitcher leaves) are linked to genomic evolution. We found a decaploid karyotype with five complete sets of syntenic chromosomes (2n = 10x = 80) yet with a clear indication of subgenome dominance and highly diploidized gene contents. The male-linked and pericentromerically located region on the putative sex chromosome was identified in a recessive subgenome and was found to harbor three transcription factors involved in flower and pollen development, including a likely neofunctionalized LEAFY duplicate. Transcriptomic and syntenic analyses of carnivory-related genes suggested that the paleopolyploidization events seeded genes that subsequently formed tandem clusters in recessive subgenomes with specific expression in the digestive zone of the pitcher, where specialized cells digest prey and absorb derived nutrients. Novel gene evolution in recessive subgenomes is likely to be prevalent because duplicates were enriched with Nepenthes-specific genes with tissue-specific expression, including those expressed in trapping pitchers. Thus, subgenome dominance likely contributed to evolutionary novelty by allowing recessive subgenomes experiencing relaxed purifying selection to serve as a preferred host of novel tissue-specific duplicates. Our results provide insight into how polyploids, which may frequently be evolutionary dead-ends, have given rise to novel traits in exceptionally thriving high-ploidy lineages.

plant biology↗

bioRxiv2023

Genomic evidence for rapid speciation and gene flow between sympatric carnivorous Nepenthes pitcher plants

Speciation can result from both neutral and adaptive processes, but their relative importance and the factors exerting selective pressures are incompletely understood. In theory, interspecific gene flow could suffice to reverse speciation, or else erode neutral divergence and expose traits and underlying genes whose divergence is due to selection. Hence, introgression can shed light on selection during the speciation process. Here we study mixed assemblages of carnivorous Nepenthes pitcher plants, which frequently produce natural hybrids yet maintain distinct phenotypes. Using ddRAD-seq markers, we characterize divergence and introgression for eight Nepenthes species that grow sympatrically in communities of three to seven species at four locations in Southeast Asia, totalling 22 populations. The sympatric species fell into two discrete classes of high and low divergence. Five lineages with high divergence displayed little recent introgression in tests of location-dependent allele sharing (ABBA-BABA) despite the presence of some natural hybrids. However, all five lineages appear to have introgressed in the more distant past, as revealed by coalescent models with Approximate Bayesian Computation. In the same locations occur three further sympatric species with low genetic divergence. These incipient species also showed some natural hybrids, but in addition both ABBA-BABA tests and ABC suggested very recent or ongoing introgression, raising the question how divergence is maintained in these hybrid zones. One trait possibly involved in maintenance of divergence against gene flow might be the carnivorous pitcher traps, whose morphology showed greater divergence than expected under neutral evolution (Pst-Fst) in the introgressing species pair N. hemsleyana and N. rafflesiana t.f..

evolutionary biology↗

bioRxiv2023

Adaptive evolution of carnivory in Nepenthes pitcher plants: a comparative transcriptomics and proteomics perspective

While trait diversity associated with evolutionary radiations is easily recognized, their function and adaptive relevance often remain elusive. Here we study the evolution of carnivory genes in Nepenthes, an iconic radiation of carnivorous pitcher plants. We investigate 13 species chosen to represent the diversity of nutrient acquisition strategies, geography and climates covered by the genus. Using a combination of proteomics and transcriptomics, we discovered that Nepenthes secrete hundreds of enzymes and antimicrobial proteins into their digestive fluids. Further genes related to plant carnivory were uncovered by analyses of gene expression changes induced by experimental feeding of starved Nepenthes traps. Feeding status appears to affect the relative abundance of nearly 35% of all expressed genes, and may be accompanied by a strong physiological shift away from photosynthesis towards heterotrophy, proteolysis, and protein synthesis. Among the many thousand genes showing signatures of adaptive evolution in sequence or expression level within the Nepenthes radiation, the secreted pitcher fluid proteins and the carnivory-related genes were over-represented. A bias towards carnivory genes, and towards trap-expressed genes versus leaf-expressed genes, was also observed among the genes differing in expression in a young pair of sister species. Together, our results suggest that the molecular basis of the carnivorous syndrome was disproportionally targeted by positive selection during the Nepenthes radiation. This study demonstrates how the evolutionary relevance of putative key traits can be tested at the level of underlying genes.

evolutionary biology↗

bioRxiv2021

Evolutionary footprints of a cold relic in a rapidly warming world

With accelerating global warming, understanding the evolutionary dynamics of plant adaptation to environmental change is increasingly urgent. Here we reveal the enigmatic history of the genus Cochlearia (Brassicaceae), a Pleistocene relic that originated from a drought-adapted Mediterranean sister genus during the Miocene. Cochlearia rapidly diversified and adapted to circum-Arctic regions and other cold-characterized habitat types during the Pleistocene. This rapid change in ecological preferences was accompanied by a highly complex, reticulate polyploid evolution, which was apparently triggered by the impact of repeated Pleistocene glaciation cycles. Our results illustrate that two early diversified arctic-alpine diploid gene pools contributed differently to the evolution of this young polyploid genus now captured in a cold-adapted niche. Metabolomics revealed ancestral central carbon metabolism responses to cold in diverse ecotypes, likely due to continuous connections to cold habitats that we hypothesize facilitated widespread parallel adaptation to alpine and subalpine habitats, and which we speculate were coopted from existing drought adaptations. Given the growing scientific interest in adaptive evolution of temperature-related traits, our results provide much-needed taxonomic and phylogenomic resolution of a model system as well as first insights into the origins of its adaptation to cold.

evolutionary biology↗

bioRxiv2021

High rates of evolution preceded shifts to sex-biased gene expression in Leucadendron, the most sexually dimorphic angiosperms

The males and females of many dioecious plants differ in morphological (Dawson and Geber 1999; Barrett and Hough 2013; Tonnabel et al. 2017), physiological (Juvany and Munne-Bosch 2015), life-history (Delph 1999), and defence traits (Cornelissen and Stiling 2005). Ultimately, such sexual dimorphism must largely be due to differential gene expression between the sexes (Ellegren and Parsch 2007), but little is known about how sex-biased genes are recruited and how their expression evolves over time. We measured gene expression in leaves of males and females of ten species sampled across the South African Cape genus Leucadendron, which shows repeated changes in sexual dimorphism and includes the most extreme differences between males and females in flowering plants (Midgley 2010; Barrett and Hough 2013; Tonnabel et al. 2014). Even in the most dimorphic species in our sample, fewer than 2% of genes showed sex-biased gene expression (SBGE) in vegetative tissue, with surprisingly little correspondence between SBGE and vegetative dimorphism across species. The identity of sex-biased genes in Leucadendron was highly species-specific, with a rapid turnover among species. In animals, sex-biased genes often evolve more quickly than unbiased genes in their sequences and expression levels (Ranz et al. 2003; Khaitovich et al. 2005; Ellegren and Parsch 2007; Voolstra et al. 2007; Harrison et al. 2015; Naqvi et al. 2019), consistent with hypotheses invoking rapid evolution due to sexual selection. Our phylogenetic analysis in Leucadendron, however, clearly indicates that sex-biased genes are recruited from a class of genes with ancestrally rapid rates of expression evolution, perhaps due to low evolutionary or pleiotropic constraints. Nevertheless, we also find evidence for adaptive evolution of expression levels once sex bias evolves. Thus, although the expression of sex-biased genes is ultimately responsive to selection, high rates of expression evolution might usually predate the evolution of sex bias.

evolutionary biology↗

bioRxiv2017

Sex-determination and sex chromosomes are shared across the radiation of dioecious Nepenthes pitcher plants

Plants with separate sexes (dioecy) represent a minority but dioecy has evolved multiple times independently in plants. Our understanding of sex determination systems in plants and of the ecological factors and molecular changes associated with the evolution of dioecy remain limited. Here, we study the sex-determination system in dioecious plants that lack heteromorphic sex chromosomes and are not amenable to controlled breeding: Nepenthes pitcher plants. We genotyped wild populations of flowering males and females of three Nepenthes taxa using ddRAD-seq, and sequenced a male inflorescence transcriptome. We developed a novel statistical tool (privacy rarefaction) to distinguish true sex-specificity from stochastic noise in high-throughput sequencing data. Our results support XY-systems in all three Nepenthes taxa and in Silene latifolia which was used as a positive control for its known XY-system. The male-specific region of the Y chromosome showed little conservation among the three Nepenthes taxa, except for the essential pollen development gene DYT1 which was also male-specific in additional taxa. Hence, this homomorphic XY sex-determination system likely has a unique origin older than the crown of the genus Nepenthes at c. 17.7 My. In addition to the characterisation of the previously unknown sex chromosomes of Nepenthes, our work contributes an innovative, highly sensitive statistical method to efficiently detect sex-specific genomic regions in wild populations in general.

evolutionary biology↗