Balanophora genomes display massively convergent evolution with other extreme holoparasites and provide novel insights into parasite–host interactions

Chen, Xiaoli; Fang, Dongming; Xu, Yuxing; Duan, Kunyu; Yoshida, Satoko; Yang, Shuai; Sahu, Sunil Kumar; Fu, Hui; Guang, Xuanmin; Liu, Min; Wu, Chenyu; Liu, Yang; Mu, Weixue; Chen, Yewen; Fan, Yannan; Wang, Fang; Peng, Shufeng; Shi, Dishen; Wang, Yayu; Yu, Runxian; Zhang, Wen; Bai, Yuqing; Liu, Zhong-Jian; Yan, Qiaoshun; Liu, Xin; Xu, Xun; Yang, Huanming; Wu, Jianqiang; Graham, Sean W.; Liu, Huan

doi:10.1038/s41477-023-01517-7

Cited by 13 publications

(3 citation statements)

References 102 publications

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“…Parasitic species are ubiquitous in nature, and trait loss and the associated genetic basis has been a hot topic in their evolution, as longterm host dependence may lead to the loss of some traits, especially nutrient-related pathways 14,15 . For example, in parasitic plants, prevalent gene loss involved in photosynthesis, nutrient uptake, flowering regulation, defense response, and root development were found [16][17][18][19] . In parasitic worms, a large-scaled genome analysis of parasitic nematodes and platyhelminths revealed the widespread losses of metabolic pathways and differential pathway coverage across different evolutionary clades 20 .…”

Section: Introductionmentioning

confidence: 99%

Genomic signatures associated with the evolutionary loss of egg yolk in parasitoid wasps

Zhao,

Liu,

Yang

et al. 2024

Preprint

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Losing or regressing traits has occurred repeatedly throughout evolutionary history in response to changing living environments. In parasitoid wasps, a mega-diverse group of insects in Hymenoptera, the loss or reduction of yolk in eggs has been reported in numerous species, and this phenotypic change is likely to have evolved as a response to the shift from ectoparasitism to endoparasitism. However, the genetic basis of this trait loss and the impact of trait loss on genome evolution are still poorly understood. Here, we perform comparative genomic analysis of 64 hymenopteran insects, and observe that a conserved insect yolk protein gene vitellogenin (Vg) was repeatedly lost in 23 endoparasitoids, representing five independent loss events in five families. Whole genome alignments suggest the loss of Vgs was probably associated with genome rearrangements. We also discover the gene losses, relaxed selection, and protein structural variations of Vg receptor genes (VgRs) in the Vg loss lineages, showing the obviously functional biased patterns of gene loss. Our hypothesis test further reveals that the ecto-to-endo transition is not the main reason for the Vg losses and the subsequent evolution of VgRs. In addition, we find a number of parallel and convergent genomic changes including gene family evolution and gene selection related to transport, development, and metabolism in the independent Vg loss lineages. And these changes may have facilitated the embryonic development in these lineages. Together, our findings uncover the genomic basis of a unique trait loss in parasitoid wasps. More broadly, our study enhances our understanding of yolk loss evolution outside mammals, highlighting a potential evolutionary trend when an alternative nutrient source is available for the embryonic development.

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Section: Introductionmentioning

confidence: 99%

Genomic signatures associated with the evolutionary loss of egg yolk in parasitoid wasps

Zhao,

Liu,

Yang

et al. 2024

Preprint

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“…Biologists have long been fascinated by striking phenotypic similarities among distantly related organisms exposed to similar ecological pressures (1). Research on the molecular basis of these convergent phenotypes has yielded critical insights into the predictability of evolution (2)(3)(4)(5). Most comparative work on this issue has focused on morphological and physiological traits, such as independently derived coloration (6) or high-altitude tolerance (7).…”

Section: Main Text Introductionmentioning

confidence: 99%

Repeated behavioral evolution is associated with targeted convergence of gene expression in cavity-nesting songbirds

Lipshutz,

Hibbins,

Bentz

et al. 2024

Preprint

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Uncovering the genomic bases of phenotypic adaptation is a major goal in biology, but this has been hard to achieve for complex behavioral traits. Here, we leverage the repeated, independent evolution of obligate cavity-nesting in birds to test the hypothesis that the shared pressure to compete for a limited breeding resource drives convergent behavioral evolution via convergent gene regulatory changes in the brain. Using behavioral assays in the field, hormonal measures of free-living subjects, and transcriptome-wide analyses of the brain in wild-captured males and females, we examined five species pairs across five avian families, each including one obligate cavity-nesting species and a related species with an open cup-nesting or otherwise more flexible nest strategy. Results support the hypothesis of behavioral convergence, with higher levels of territorial aggression in obligate cavity-nesters, particularly among females. Levels of testosterone in circulation were not associated with nest strategy or aggression for either sex, but phylogenetic analyses of individual genes and co-regulated gene networks revealed some shared patterns of gene expression, including a nest strategy-related gene network shared across families and two separate networks linked to aggression only in females. Though associated with convergent behavioral evolution, these genes were not significantly enriched for particular functional pathways, and the scope of convergent gene expression evolution was limited to a small percent of the genome. Together, these observations indicate that replicated evolutionary changes in complex behavior arise via a combination of convergent and lineage-specific evolution of gene regulation.

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“…In some plants, such as Cactaceae, Euphorbiaceae, and Casuarinaceae, the leaves have degenerated into spines or membranous structures, and photosynthesis is carried out by the stem [1][2][3][4]. In other groups, like the Orobanchaceae, Balanophoraceae, Rafflesiaceae, Cassytha, and Cuscuta, plants obtain nutrients by parasitizing host plants through specialized structures [5][6][7][8]. Monotropa uniflora absorb nutrients from decaying plant materials through mycorrhizal associations [9,10].…”

Section: Introductionmentioning

confidence: 99%

The Complete Chloroplast Genome of an Epiphytic Leafless Orchid, Taeniophyllum complanatum: Comparative Analysis and Phylogenetic Relationships

Zhou,

Chen,

Wang

et al. 2024

Horticulturae

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Taeniophyllum is a distinct taxon of epiphytic leafless plants in the subtribe Aeridinae of Orchidaceae. The differences in chloroplast genomes between extremely degraded epiphytic leafless orchids and other leafy orchids, as well as their origins and evolution, raise intriguing questions. Therefore, we report the chloroplast genome sequence of Taeniophyllum complanatum, including an extensive comparative analysis with other types of leafless orchids. The chloroplast genome of T. complanatum exhibited a typical quadripartite structure, and its overall structure and gene content were relatively conserved. The entire chloroplast genome was 141,174 bp in length, making it the smallest known chloroplast genome of leafless epiphytic orchids. It encoded a total of 120 genes, including repetitive genes, comprising 74 protein-coding genes, 38 transfer RNA (tRNA) genes, and 8 ribosomal RNA (rRNA) genes. A phylogenetic analysis was conducted on the chloroplast genomes of 43 species belonging to five subfamilies of Orchidaceae. The results showed that the five subfamilies were monophyly, with nearly all segments having a 100% bootstrap value. T. complanatum and Chiloschista were clustered together as a sister group to Phalaenopsis and occupied the highest position in the Epidendroideae. Phylogenetic analysis suggested that T. complanatum and other leafless orchids within the Orchidaceae evolved independently. This study may provide the foundation for research on phylogenetic and structural diversity in leafless epiphytic orchids, thereby enhancing the resources available for chloroplast genome studies in Orchidaceae.

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Balanophora genomes display massively convergent evolution with other extreme holoparasites and provide novel insights into parasite–host interactions

Cited by 13 publications

References 102 publications

Genomic signatures associated with the evolutionary loss of egg yolk in parasitoid wasps

Genomic signatures associated with the evolutionary loss of egg yolk in parasitoid wasps

Repeated behavioral evolution is associated with targeted convergence of gene expression in cavity-nesting songbirds

The Complete Chloroplast Genome of an Epiphytic Leafless Orchid, Taeniophyllum complanatum: Comparative Analysis and Phylogenetic Relationships

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