Plant evolution and environmental adaptation unveiled by long-read whole-genome sequencing of<i>Spirodela</i>

An, Dong; Zhou, Yong; Li, Changsheng; Xiao, Qiao; Wang, Tao; Zhang, Yating; Wu, Yongrui; Li, Yubin; Chao, Dai‐Yin; Messing, Joachim; Wang, Wen-Qin

doi:10.1073/pnas.1910401116

Cited by 82 publications

(83 citation statements)

References 53 publications

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“…However, the study of taro genomics has been limited by its relatively large genome size and high heterozygosity (Kokubugata & Konishi, 1999; Soulard et al, 2016). Although the Araceae family comprises approximately 110 genera and more than 3,500 species (Li et al, 2010), the Spirodela polyrhiza (An et al., 2019) genome (158 M), the first assembled to a high‐quality chromosome‐level draft using long‐read sequencing data, provided valuable information for further deciphering other Araceae species. The lack of genome information has undoubtedly restricted the interpretation of molecular mechanisms for taro evolution and metabolic functions.…”

Section: Introductionmentioning

confidence: 99%

A high‐quality genome of taro (Colocasia esculenta (L.) Schott), one of the world's oldest crops

Yin

Jiang

Wang

et al. 2020

Molecular Ecology Resources

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Taro (Colocasia esculenta (L.), Schott), from the Araceae family, is one of the oldest crops with important edible, medicinal, nutritional and economic value. Taro is a highly polymorphic species including diverse genotypes adapted to a broad range of environments, but the taro genome has rarely been investigated. Here, a high‐quality chromosome‐level genome of C. esculenta was assembled using data sequenced by Illumina, PacBio and Nanopore platforms. The assembled genome size was 2,405 Mb with a contig N50 of 400.0 kb and a scaffold N50 of 159.4 Mb. In total, 2,311 Mb (96.09%) of the contig sequences was anchored onto 14 chromosomes to form pseudomolecules, and 2,126 Mb (88.43%) was annotated as repetitive sequences. Of the 28,695 predicted protein‐coding genes, 26,215 genes (91.4%) could be functionally annotated. On the basis of phylogenetic analysis using 769 genes, C. esculenta and Spirodela polyrhiza were placed on one branch of the tree that diverged approximately 73.23 million years ago. The synteny analyses showed that there have been two whole‐genome duplication events in C. esculenta separated by a relatively short gap. According to comparative genome analysis, a larger number (1,189) of distinct gene families and long terminal repeats were enriched in C. esculenta. Our high‐quality taro genome will provide valuable resources for further genetic, ecological and evolutionary analyses of taro or other species in the Araceae.

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Section: Introductionmentioning

confidence: 99%

A high‐quality genome of taro (Colocasia esculenta (L.) Schott), one of the world's oldest crops

Yin

Jiang

Wang

et al. 2020

Molecular Ecology Resources

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“…Most duckweed species rarely flower, instead reproducing primarily by rapid, clonal reproduction that occurs at one of the fastest rates in any angiosperm (3) . The largest duckweed species Spirodela polyrhiza (~1 cm wide) intriguingly has the smallest genome size (~158 megabases) (3)(4)(5) , and several genome assemblies consistently annotate fewer than 20,000 genes (6) . Compared to the Arabidopsis thaliana genome that is roughly the same total genome size, S. polyrhiza has nearly 25% fewer genes.…”

Section: Introductionmentioning

confidence: 99%

Unusual predominance of maintenance DNA methylation in Spirodela polyrhiza

Harkess

Bewick

et al. 2020

Preprint

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Abstract5-methylcytosine (5mC) is a modified base often described as necessary for the proper regulation of genes and transposons and for the maintenance of genome integrity in plants. However, the extent of this dogma is limited by the current phylogenetic sampling of land plant species diversity. Here, we report that a monocot plant, Spirodela polyrhiza, has lost CG gene body methylation, genome-wide CHH methylation, and the presence or expression of several genes in the highly conserved RNA-directed DNA methylation (RdDM) pathway. It has also lost the CHH methyltransferase CHROMOMETHYLASE 2. Consequently, the transcriptome is depleted of 24-nucleotide, heterochromatic, small interfering RNAs that act as guides for the deposition of 5mC to RdDM-targeted loci in all other currently sampled angiosperm genomes. Although the genome displays low levels of genome-wide 5mC primarily at LTR retrotransposons, CG maintenance methylation is still functional. In contrast, CHG methylation is weakly maintained even though H3K9me2 is present at loci dispersed throughout the euchromatin and highly enriched at regions likely demarcating pericentromeric regions. Collectively, these results illustrate that S. polyrhiza is maintaining CG and CHG methylation mostly at repeats in the absence of small RNAs. S. polyrhiza reproduces rapidly through clonal propagation in aquatic environments, which we hypothesize may enable low levels of maintenance methylation to persist in large populations.Significance StatementDNA methylation is a widespread chromatin modification that is regularly found in all plant species. By examining one aquatic duckweed species, Spirodela polyrhiza, we find that it has lost highly conserved genes involved in methylation of DNA at sites often associated with repetitive DNA, and within genes, however DNA methylation and heterochromatin is maintained during cell division at other sites. Consequently, small RNAs that normally guide methylation to silence repetitive DNA like retrotransposons are diminished. Despite the loss of a highly conserved methylation pathway, and the reduction of small RNAs that normally target repetitive DNA, transposons have not proliferated in the genome, perhaps due in part to the rapid, clonal growth lifestyle of duckweeds.

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“…A possible gene death was observed in the 9509 genome, which is not shared in the corresponding region of the 7498 genome (Appendix S12). A recent resequencing of the 7498 genome (v3) was also searched, which revealed two additional expansin genes unidentified within the v2 genome (An et al , ). Of these 16 expansin genes, transcripts mapping to nine expansins (~56% of the superfamily) were detected under the conditions used by An et al () for PacBio isoform sequencing (Table S1).…”

Section: Resultsmentioning

confidence: 99%

Expansin gene loss is a common occurrence during adaptation to an aquatic environment

et al. 2019

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Expansins comprise a superfamily of plant cell wall loosening proteins that can be divided into four individual families (EXPA, EXPB, EXLA and EXLB). Aside from inferred roles in a variety of plant growth and developmental traits, little is known regarding the function of specific expansin clades, for which there are at least 16 in flowering plants (angiosperms); however, there is evidence to suggest that some expansins have cell-specific functions, in root hair and pollen tube development, for example. Recently, two duckweed genomes have been sequenced (Spirodela polyrhiza strains 7498 and 9509), revealing significantly reduced superfamily sizes. We hypothesized that there would be a correlation between expansin loss and morphological reductions seen among highly adapted aquatic species. In order to provide an answer to this question, we characterized the expansin superfamilies of the greater duckweed Spirodela, the marine eelgrass Zostera marina and the bladderwort Utricularia gibba. We discovered rampant expansin gene and clade loss among the three, including a complete absence of the EXLB family and EXPA-VII. The most convincing correlation between morphological reduction and expansin loss was seen for Utricularia and Spirodela, which both lack root hairs and the root hair expansin clade EXPA-X. Contrary to the pattern observed in other species, four Utricularia expansins failed to branch within any clade, suggesting that they may be the result of neofunctionalization. Last, an expansin clade previously discovered only in eudicots was identified in Spirodela, allowing us to conclude that the last common ancestor of monocots and eudicots contained a minimum of 17 expansins.

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Plant evolution and environmental adaptation unveiled by long-read whole-genome sequencing ofSpirodela

Cited by 82 publications

References 53 publications

A high‐quality genome of taro (Colocasia esculenta (L.) Schott), one of the world's oldest crops

A high‐quality genome of taro (Colocasia esculenta (L.) Schott), one of the world's oldest crops

Unusual predominance of maintenance DNA methylation in Spirodela polyrhiza

Expansin gene loss is a common occurrence during adaptation to an aquatic environment

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