Abstract
Dissecting complex connections between cytogenetic traits (ploidy levels) and plant invasiveness has emerged as a popular research subject in the field of invasion biology. Although recent work suggests that polyploids are more likely to be invasive than their corresponding diploids, the molecular basis underlying the successful invasion of polyploids remains largely unexplored. To this end, we adopted an RNA‐seq and sRNA‐seq approach to describe how polyploids mediate invasiveness differences in two contrasting cytotypes of Solidago canadensis L., a widespread wild hexaploid invader with localized cultivated diploid populations. Our analysis of the leaf transcriptome revealed 116,801 unigenes, of which 12,897 unigenes displayed significant differences in expression levels. A substantial number of these differentially expressed unigenes (DEUs) were significantly associated with the biosynthesis of secondary metabolites, carbohydrate metabolism, lipid metabolism, and environmental adaptation pathways. Gene Ontology term enrichment‐based categorization of DEU‐functions was consistent with this observation, as terms related to single‐organism, cellular, and metabolic processes including catalytic, binding, transporter, and enzyme regulator activity were over‐represented. Concomitantly, 186 miRNAs belonging to 44 miRNA families were identified in the same leaf tissues, with 59 miRNAs being differentially expressed. Furthermore, we discovered 83 miRNA‐target interacting pairs that were oppositely regulated, and a meticulous study of these targets depicted that several unigenes encoding transcription factors, DNA methyltransferase, and leucine‐rich repeat receptor‐like kinases involved in the stress response were greatly influenced. Collectively, these transcriptional and epigenetic data provide new insights into miRNA‐mediated gene expression regulatory mechanisms that may operate in hexaploid cytotypes to favor successful invasion.
Highlights
Amid growing evidence of biological invasion impacts on global biodiversity, ecosystem functioning, species conservation, and even social and economic activities (Dyer et al, 2017; Rejmánek, 2015), there is mounting interest in searching the determining elements underlying the successful invasion of alien species
Among them were an over‐representation of unigenes and coherent miRNA targets relevant to metabolism, plant growth and development, and stress responses, implying that these modified genetic and epigenetic attributes may harbor both biochemical and ecological advantages that were beneficial to the successful invasion of hexaploid cytotypes
4.1 | Unique gene and miRNA expression characteristics might have contributed to the invasiveness of hexaploid cytotypes In Arabidopsis thaliana, only 0.1% differences in gene expression between diploid and autotetraploid were detected (Yu et al, 2010)
Summary
Amid growing evidence of biological invasion impacts on global biodiversity, ecosystem functioning, species conservation, and even social and economic activities (Dyer et al, 2017; Rejmánek, 2015), there is mounting interest in searching the determining elements underlying the successful invasion of alien species. The objectives of our current work are as follows: (a) to characterize the initial expression profiling of genes and miRNAs in two identified ploidy levels, that is, diploid and hexaploid cytotypes of S. canadensis at a genome‐wide scale; (b) to determine key candidate genes and miRNA regulators that may contribute to the successful invasion of hexaploid cytotypes based on gene and miRNA expression divergences, as well as over‐represented functional categories of these candidates; and (c) to explore the strong evidence for the potential genetic roles of epigenetic and transcriptional alterations in the successful invasion of hexaploid cytotypes. Our work provides new insights into miRNA‐mediated gene expression regulatory mechanisms that may be useful to explain the successful invasion of hexaploid cytotypes
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