Introgression is widespread in the radiation of carnivorous Nepenthes pitcher plants

Scharmann, Mathias; Wistuba, Andreas; Widmer, Alex

doi:10.1016/j.ympev.2021.107214

Cited by 9 publications

(6 citation statements)

References 123 publications

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“…fordii , with an estimated tMRCA of 5.61 Ma. This pattern of cyto‐nuclear discordance is common, where species ‘A’ shows an early divergence and forms a separate branch in the nuclear tree, while it tends to be sister to geographically related species ‘B’ and shows a late divergence in the plastid tree (Ali et al., 2016; Folk et al., 2017; Güzel et al., 2021; Lei et al., 2021; Liu et al., 2017; Liu, Campbell, et al., 2020; Nge et al., 2021; Scharmann et al., 2021; Yang et al., 2021). This phenomenon, known as plastid capture, typically arises from hybridization between sympatric species (Acosta & Premoli, 2010).…”

Section: Discussionmentioning

confidence: 99%

“…Evolutionary biologists aim to unravel species relationships using bifurcating trees, where the most recent common ancestor (MRCA), gives rise to only two descendants (Gregory, 2008; Omland et al., 2008; Simpson, 2019). However, gene trees within a species may conflict, making it difficult to deduce the ‘true’ species tree (Degnan et al., 2006; Maddison, 1997; Scharmann et al., 2021). Phylogenetic conflicts in plants are typically explained by two hypotheses: interspecific gene flow (i.e., hybridization and introgression) and incomplete lineage sorting (ILS) (Lin et al., 2019; Wang et al., 2021).…”

Section: Introductionmentioning

confidence: 99%

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Reticulate evolution of the tertiary relict Osmanthus

Li,

Nie

et al. 2023

The Plant Journal

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SUMMARYWhen interspecific gene flow is common, species relationships are more accurately represented by a phylogenetic network than by a bifurcating tree. This study aimed to uncover the role of introgression in the evolution of Osmanthus, the only genus of the subtribe Oleinae (Oleaceae) with its distribution center in East Asia. We built species trees, detected introgression, and constructed networks using multiple kinds of sequencing data (whole genome resequencing, transcriptome sequencing, and Sanger sequencing of nrDNA) combined with concatenation and coalescence approaches. Then, based on well‐understood species relationships, historical biogeographic analyses and diversification rate estimates were employed to reveal the history of Osmanthus. Osmanthus originated in mid‐Miocene Europe and dispersed to the eastern Tibetan Plateau in the late Miocene. Thereafter, it continued to spread eastwards. Phylogenetic conflict is common within the ‘Core Osmanthus’ clade and is seen at both early and late stages of diversification, leading to hypotheses of net‐like species relationships. Incomplete lineage sorting proved ineffective in explaining phylogenetic conflicts and thus supported introgression as the main cause of conflicts. This study elucidates the diversification history of a relict genus in the subtropical regions of eastern Asia and reveals that introgression had profound effects on its evolutionary history.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Reticulate evolution of the tertiary relict Osmanthus

Li,

Nie

et al. 2023

The Plant Journal

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“…For example, the transcriptomic data of Dionaea muscipula , Drosera capensis (Cape sundew), and Nepenthes species were analyzed to elucidate their evolutionary relationships, which showed that the clade contains at least seven independent paleopolyploidy events that lead to the speciation of these angiosperms within the same clade [ 2 ]. Furthermore, it has been recently reported that the post-speciation gene flow and introgression in c. 160 Nepenthes species are widespread throughout the rapid adaptive radiation that is only c. 5 million years old (Mya) based on the phylogenomic analysis of 235 double digest restriction site-associated DNA (ddRAD)-seq and 25 RNA-seq data [ 54 ].…”

Section: Insights From Omics Studiesmentioning

confidence: 99%

Omics Approaches in Uncovering Molecular Evolution and Physiology of Botanical Carnivory

Baharin¹,

Ting²,

Goh³

2023

Plants

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Systems biology has been increasingly applied with multiple omics for a holistic comprehension of complex biological systems beyond the reductionist approach that focuses on individual molecules. Different high-throughput omics approaches, including genomics, transcriptomics, metagenomics, proteomics, and metabolomics have been implemented to study the molecular mechanisms of botanical carnivory. This covers almost all orders of carnivorous plants, namely Caryophyllales, Ericales, Lamiales, and Oxalidales, except Poales. Studies using single-omics or integrated multi-omics elucidate the compositional changes in nucleic acids, proteins, and metabolites. The omics studies on carnivorous plants have led to insights into the carnivory origin and evolution, such as prey capture and digestion as well as the physiological adaptations of trap organ formation. Our understandings of botanical carnivory are further enhanced by the discoveries of digestive enzymes and transporter proteins that aid in efficient nutrient sequestration alongside dynamic molecular responses to prey. Metagenomics studies revealed the mutualistic relationships between microbes and carnivorous plants. Lastly, in silico analysis accelerated the functional characterization of new molecules from carnivorous plants. These studies have provided invaluable molecular data for systems understanding of carnivorous plants. More studies are needed to cover the diverse species with convergent evolution of botanical carnivory.

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“…The genus Nepenthes (Nepenthaceae, Caryophyllales) is highly diverse [12,52,53], and has accumulated approximately 150 species within only c. 5 millions years [54]. Although all Nepenthes produce pitcher traps, there is a large diversity in morphology, biomechanics, and chemistry of the digestive fluid [12,52,53] that corresponds in part to differences in prey spectra.…”

Section: Introductionmentioning

confidence: 99%

Adaptive evolution of carnivory inNepenthespitcher plants: a comparative transcriptomics and proteomics perspective

Scharmann

Metali

Grafe

et al. 2023

Preprint

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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.

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Introgression is widespread in the radiation of carnivorous Nepenthes pitcher plants

Cited by 9 publications

References 123 publications

Reticulate evolution of the tertiary relict Osmanthus

Reticulate evolution of the tertiary relict Osmanthus

Omics Approaches in Uncovering Molecular Evolution and Physiology of Botanical Carnivory

Adaptive evolution of carnivory inNepenthespitcher plants: a comparative transcriptomics and proteomics perspective

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