Gene expression data support the hypothesis that Isoetes rootlets are true roots and not modified leaves

Hetherington, Alexander J.; Emms, David; Kelly, Steven L.; Dolan, Liam

doi:10.1038/s41598-020-78171-y

Cited by 8 publications

(9 citation statements)

References 81 publications

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“…Selfsynteny was then assessed in i-Adhore and Ks values were calculated and plotted for syntenic pairs only using the "wgd syn" tool 81 . To conduct Ks analysis of related species, RNA-seq data was downloaded from the SRA database for Isoetes yunguiensis (SRR6920723) 82 , I. sinensis (SRR1648119) 83 , I. drummondii (SRR4762161), I. echinospora (SRR6853338) 84 , I. lacustris (SRR9620527) 85 , and I. tegetiformans (ERR2040873) 19 . Transcriptomes were assembled using SOAPdenovo-Trans 86 with a k-mer length of 31.…”

Section: Methodsmentioning

confidence: 99%

Underwater CAM photosynthesis elucidated by Isoetes genome

et al. 2021

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To conserve water in arid environments, numerous plant lineages have independently evolved Crassulacean Acid Metabolism (CAM). Interestingly, Isoetes, an aquatic lycophyte, can also perform CAM as an adaptation to low CO2 availability underwater. However, little is known about the evolution of CAM in aquatic plants and the lack of genomic data has hindered comparison between aquatic and terrestrial CAM. Here, we investigate underwater CAM in Isoetes taiwanensis by generating a high-quality genome assembly and RNA-seq time course. Despite broad similarities between CAM in Isoetes and terrestrial angiosperms, we identify several key differences. Notably, Isoetes may have recruited the lesser-known ‘bacterial-type’ PEPC, along with the ‘plant-type’ exclusively used in other CAM and C4 plants for carboxylation of PEP. Furthermore, we find that circadian control of key CAM pathway genes has diverged considerably in Isoetes relative to flowering plants. This suggests the existence of more evolutionary paths to CAM than previously recognized.

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Section: Methodsmentioning

confidence: 99%

Underwater CAM photosynthesis elucidated by Isoetes genome

et al. 2021

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“…This led to the identification of RGF-like sequences from 17 out of 21 transcriptome data. Additional RGF-like sequences were retrieved by searching against the predicted Selaginella moellendorffii proteome and the Isoetes echinospora transcriptome data ( Banks et al, 2011 ; Hetherington et al, 2020 ; Figure 4 and Supplementary Figure 3 ). No RGF-like sequences were found in four species of Lycopodiaceae ( Figure 4 ).…”

Section: Resultsmentioning

confidence: 99%

“…A heavy asterisk indicates that the proteome predicted from the sequenced genome was analyzed for S. moellendorffii ( Banks et al, 2011 ). A dagger indicates that the published transcriptome data was examined for Isoetes echinospora ( Hetherington et al, 2020 ). The 1KP dataset was analyzed for other species.…”

Section: Resultsmentioning

confidence: 99%

“…This study, therefore, searched for RGF-like sequences extensively in all major extant land plant lineages using a large-scale transcriptome data collected by the 1000 Plant Genomes Project (1KP 1 ) as well as other valuable genome and transcriptome resources ( Rensing et al, 2008 ; Banks et al, 2011 ; Goodstein et al, 2012 ; Amborella Genome Project, 2013 ; Fernandez-Pozo et al, 2015 ; Ming et al, 2015 ; Cheng et al, 2017 ; Filiault et al, 2018 ; Dong et al, 2019 ; One Thousand Plant Transcriptomes Initiative, 2019 ; Hetherington et al, 2020 ; Li et al, 2020 ; Zhang J. et al, 2020 ; Zhang L. et al, 2020 ; Geng et al, 2021 ). As a result, more than four hundreds of RGF-like sequences were retrieved from all major extant land plant lineages excepting hornworts.…”

Section: Introductionmentioning

confidence: 99%

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The RGF/GLV/CLEL Family of Short Peptides Evolved Through Lineage-Specific Losses and Diversification and Yet Conserves Its Signaling Role Between Vascular Plants and Bryophytes

Furumizu

Sawa²

2021

Front. Plant Sci.

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Short secreted plant peptides act as key signaling molecules and control a plethora of developmental and physiological processes. The ROOT GROWTH FACTOR (RGF)/GOLVEN (GLV)/CLE-Like (CLEL) family of peptides was discovered to be involved in root development in Arabidopsis thaliana. In contrast to active research efforts, which have been revealing receptors and downstream signaling components, little attention has been paid to evolutionary processes that shaped the RGF signaling system as we know it in angiosperms today. As a first step toward understanding how RGF signaling emerged and evolved, this study aimed to elucidate the phylogenetic distribution and functional conservation of RGF-like sequences. Using publicly available, genome and transcriptome data, RGF-like sequences were searched in 27 liverworts, 22 mosses, 8 hornworts, 23 lycophytes, 23 ferns, 38 gymnosperms, and 8 angiosperms. This led to the identification of more than four hundreds of RGF-like sequences in all major extant land plant lineages except for hornworts. Sequence comparisons within and between taxonomic groups identified lineage-specific characters. Notably, one of the two major RGF subgroups, represented by A. thaliana RGF6/GLV1/CLEL6, was found only in vascular plants. This subgroup, therefore, likely emerged in a common ancestor of vascular plants after its divergence from bryophytes. In bryophytes, our results infer independent losses of RGF-like sequences in mosses and hornworts. On the other hand, a single, highly similar RGF-like sequence is conserved in liverworts, including Marchantia polymorpha, a genetically tractable model species. When constitutively expressed, the M. polymorpha RGF-like sequence (MpRGF) affected plant development and growth both in A. thaliana and M. polymorpha. This suggests that MpRGF can exert known RGF-like effects and that MpRGF is under transcriptional control so that its potent activities are precisely controlled. These data suggest that RGFs are conserved as signaling molecules in both vascular plants and bryophytes and that lineage-specific diversification has increased sequence variations of RGFs. All together, our findings form a basis for further studies into RGF peptides and their receptors, which will contribute to our understandings of how peptide signaling pathways evolve.

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“…As a result, rootlet scars are arranged regularly on both sides of the furrow (Bierhorst, 1971;Paolillo, 1982). It has been suggested that rootlets are modified leaves (Karrfalt, 1980;Stubblefield and Rothwell, 1981) in rhizomorphic lycophytes (sensu Kenrick and Crane, 1997) including Isoetaceae, while transcriptome data in Isoetes did not provide a clue supporting the homology between rootlets and leaves (Hetherington et al, 2020).…”

Section: Future Perspective To Understand a Common Body Plan In Lycop...mentioning

confidence: 99%

Shared body plans of lycophytes inferred from root formation of Lycopodium clavatum

Ito

Fujinami²,

Imaichi³

et al. 2022

Front. Ecol. Evol.

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Late Silurian to early Devonian lycophytes had prostrate aerial axes, while subordinate organs or subterranean axes were formed around the dichotomies of the axes. The subterranean axes are hypothesized to have evolved into root-bearing axes (rhizophores) and roots in extant Selaginellaceae and Lycopodiaceae, respectively. Consistent with this hypothesis, rhizophores are formed on the dichotomies of shoots in Selaginellaceae. However, it has remained unclear whether roots are borne in the same position in Lycopodiaceae. In addition, roots form endogenously in the stem, but no data are available regarding the tissues in stem from which they arise. In this study, we tracked the root development in the clubmoss, Lycopodium clavatum, based on anatomical sections and 3D reconstructed images. The vascular tissue of the stem is encircled by ground meristem, which supplies cortical cells outwardly by periclinal divisions. A linear parenchymatous tissue is present on the ventral side of vascular cylinder, which we call “ventral tissue” in this study. We found that root primordia are formed endogenously on the ventral side of stem, possibly from the ventral tissue. In addition, roots always initiate at positions close to dichotomies of stem. The root-initiating position supports the suggestion that Lycopodium roots share a body plan with the subterranean organs of the hypothesized ancestry.

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Gene expression data support the hypothesis that Isoetes rootlets are true roots and not modified leaves

Cited by 8 publications

References 81 publications

Underwater CAM photosynthesis elucidated by Isoetes genome

Underwater CAM photosynthesis elucidated by Isoetes genome

The RGF/GLV/CLEL Family of Short Peptides Evolved Through Lineage-Specific Losses and Diversification and Yet Conserves Its Signaling Role Between Vascular Plants and Bryophytes

Shared body plans of lycophytes inferred from root formation of Lycopodium clavatum

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