Dataset Information

Phylogenetic Patterns of Swainsonine Presence in Morning Glories.

ABSTRACT: Endosymbionts play important roles in the life cycles of many macro-organisms. The indolizidine alkaloid swainsonine is produced by heritable fungi that occurs in diverse plant families, such as locoweeds (Fabaceae) and morning glories (Convolvulaceae) plus two species of Malvaceae. Swainsonine is known for its toxic effects on livestock following the ingestion of locoweeds and the potential for pharmaceutical applications. We sampled and tested herbarium seed samples (n = 983) from 244 morning glory species for the presence of swainsonine and built a phylogeny based on available internal transcribed spacer (ITS) sequences of the sampled species. We show that swainsonine occurs only in a single morning glory clade and host species are established on multiple continents. Our results further indicate that this symbiosis developed ∼5 mya and that swainsonine-positive species have larger seeds than their uninfected conspecifics.

SUBMITTER: Quach QN

PROVIDER: S-EPMC9111539 | biostudies-literature | 2022

REPOSITORIES: biostudies-literature

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Phylogenetic Patterns of Swainsonine Presence in Morning Glories.

Quach Quynh N QN Gardner Dale R DR Clay Keith K Cook Daniel D

Frontiers in microbiology 20220503

Endosymbionts play important roles in the life cycles of many macro-organisms. The indolizidine alkaloid swainsonine is produced by heritable fungi that occurs in diverse plant families, such as locoweeds (Fabaceae) and morning glories (Convolvulaceae) plus two species of Malvaceae. Swainsonine is known for its toxic effects on livestock following the ingestion of locoweeds and the potential for pharmaceutical applications. We sampled and tested herbarium seed samples (<i>n</i> = 983) from 244 m ...[more]

PMID: 35591984

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Project description:BackgroundStorage roots are an ecologically and agriculturally important plant trait that have evolved numerous times in angiosperms. Storage roots primarily function to store carbohydrates underground as reserves for perennial species. In morning glories, storage roots are well characterized in the crop species sweetpotato, where starch accumulates in storage roots. This starch-storage tissue proliferates, and roots thicken to accommodate the additional tissue. In morning glories, storage roots have evolved numerous times. The primary goal of this study is to understand whether this was through parallel evolution, where species use a common genetic mechanism to achieve storage root formation, or through convergent evolution, where storage roots in distantly related species are formed using a different set of genes. Pairs of species where one forms storage roots and the other does not were sampled from two tribes in the morning glory family, the Ipomoeeae and Merremieae. Root anatomy in storage roots and fine roots was examined. Furthermore, we sequenced total mRNA from storage roots and fine roots in these species and analyzed differential gene expression.ResultsAnatomical results reveal that storage roots of species in the Ipomoeeae tribe, such as sweetpotato, accumulate starch similar to species in the Merremieae tribe but differ in vascular tissue organization. In both storage root forming species, more genes were found to be upregulated in storage roots compared to fine roots. Further, we find that fifty-seven orthologous genes were differentially expressed between storage roots and fine roots in both storage root forming species. These genes are primarily involved in starch biosynthesis, regulation of starch biosynthesis, and transcription factor activity.ConclusionsTaken together, these results demonstrate that storage roots of species from both morning glory tribes are anatomically different but utilize a common core set of genes in storage root formation. This is consistent with a pattern of parallel evolution, thus highlighting the importance of examining anatomy together with gene expression to understand the evolutionary origins of ecologically and economically important plant traits.

Project description:BackgroundThe morning glories (Convolvulaceae) are distributed worldwide and produce economically important crops, medicinal herbs, and ornamentals. Members of this family are diverse in morphological characteristics and trophic modes, including the leafless parasitic Cuscuta (dodders). Organelle genomes were generally used for studying plant phylogeny and genomic variations. Notably, plastomes in parasitic plants always show non-canonical features, such as reduced size and accelerated rates. However, few organelle genomes of this group have been sequenced, hindering our understanding of their evolution, and dodder mitogenome in particular.ResultsWe assembled 22 new mitogenomes and 12 new plastomes in Convolvulaceae. Alongside previously known ones, we totally analyzed organelle genomes of 23 species in the family. Our sampling includes 16 leafy autotrophic species and 7 leafless parasitic dodders, covering 8 of the 12 tribes. Both the plastid and mitochondrial genomes of these plants have encountered variations that were rarely observed in other angiosperms. All of the plastomes possessed atypical IR boundaries. Besides the gene and IR losses in dodders, some leafy species also showed gene and intron losses, duplications, structural variations, and insertions of foreign DNAs. The phylogeny reconstructed by plastid protein coding sequences confirmed the previous relationship of the tribes. However, the monophyly of 'Merremieae' and the sister group of Cuscuta remained uncertain. The mitogenome was significantly inflated in Cuscuta japonica, which has exceeded over 800 kb and integrated massive DNAs from other species. In other dodders, mitogenomes were maintained in small size, revealing divergent evolutionary strategies. Mutations unique to plants were detected in the mitochondrial gene ccmFc, which has broken into three fragments through gene fission and splicing shift. The unusual changes likely initially happened to the common ancestor of the family and were caused by a foreign insertion from rosids followed by double-strand breaks and imprecise DNA repairs. The coding regions of ccmFc expanded at both sides after the fission, which may have altered the protein structure.ConclusionsOur family-scale analyses uncovered unusual scenarios for both organelle genomes in Convolvulaceae, especially in parasitic plants. The data provided valuable genetic resources for studying the evolution of Convolvulaceae and plant parasitism.

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Phylogenetic Patterns of Swainsonine Presence in Morning Glories.

Publications

Phylogenetic Patterns of Swainsonine Presence in Morning Glories.

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