Meristem dormancy in Marchantia polymorpha is regulated by a liverwort-specific miRNA and a clade III SPL gene

Streubel, Susanna; Deiber, Sebastian; Rötzer, Johannes; Mosiołek, Magdalena; Jandrasits, Katharina; Dolan, Liam

doi:10.1016/j.cub.2022.12.062

Cited by 22 publications

(23 citation statements)

References 46 publications

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“…As no experimental data are available for A. agrestis and A. punctatus microtransriptomes, we applied homology-based search to identify miRNA candidates which could target Anthoceros SPL gene transcripts. Mature miRNA sequences from liverwort Pellia endiviifolia (miR156) and M. polymorpha (miR529c and Mpo-miR13) were used as an input sequences (Alaba et al ., 2015; Lin et al ., 2016; Tsuzuki et al ., 2019; Streubel et al ., 2023). Since we did not find any sequences matching to miR156/529c or Mpo-miR13 in both Anthoceros genomes, we used Anthoceros SPL transcript sequences to predict potential target sites which could be recognized by these miRNAs by using psRNATarget server.…”

Section: Resultsmentioning

confidence: 99%

“…The copyright holder for this this version posted February 28, 2023. ; https://doi.org/10.1101/2023.02.27.530190 doi: bioRxiv preprint Streubel and co-workers hypothesized that the miRNA-SPL regulation module involved in the meristem dormancy important for the shade avoidance mechanism evolved independently in the liverwort and angiosperm lineages (Streubel et al, 2023). On the other hand, the authors only focused on the vegetative thallus development and did not show any data connected with the sexual reproduction (Streubel et al 2023). Therefore, it cannot be excluded that the Mpo-MR-13-MpSPL1 module may play a dual role during Marchantia life cycle.…”

Section: Discussionmentioning

confidence: 99%

“…It is worth noting that in the phylogenetic Group 1 only three Arabidopsis SPL genes are under control of evolutionary conserved miR156. Interestingly, Marchantia Mp SPL1 is also regulated by miRNA, however by liverwort specific Mpo-MR-13 (Tsuzuki et al ., 2016; Streubel et al ., 2023). Based on transcriptomic studies it was suggested that this Mpo-MR-13– Mp SPL1 module might be involved in controlling the transition from vegetative to reproductive life cycle.…”

Section: Discussionmentioning

confidence: 99%

“…Characteristic expression pattern of Mp SPL1 has been observed with an explicit expression peak in gametangiophores along with simultaneous down-regulation of Mpo-MR-13 precursors at this developmental stage (Flores-Sandoval et al ., 2018). However, recent functional studies revealed a role of this Mpo-MR-13–Mp SPL1 module in the regulation of meristem dormancy with superior control of this module by PIF-mediated phytochrome signaling (Streubel et al ., 2023). The light signaling modulates the architecture of the thallus branching via Mp SPL2 action which under shade imitating conditions promotes meristem dormancy by repressing meristem activity (Streubel et al ., 2023).…”

Section: Discussionmentioning

confidence: 99%

“…1), where at least one member from the analyzed plant species was assigned to each group. M. polymorpha and both Anthoceros species have only For many plant species, it was shown that among the SPL family, some of the members undergo post-transcriptional gene expression regulation by conserved miRNAs, miR156 or miR529 and Marchantia specific Mpo-miR13 (Streubel et al, 2023). As no experimental data are available for A. agrestis and A. punctatus microtransriptomes, we applied homology-based search to identify miRNA candidates which could target Anthoceros SPL gene transcripts.…”

Section: Comparative Evolutionary Analysis Of Spl Gene Family Between...mentioning

confidence: 99%

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Comparative analysis ofSQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL)gene family between bryophytes and seed plants

Alisha

Szweykowska-Kulińska

Sierocka

2023

Preprint

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SQUAMOSA-PROMOTER BINDING PROTEIN-LIKE (SPL) genes encode plant-specific transcription factors which have been found to be conserved in green plants lineage. SPL proteins are important regulators of diverse plant developmental processes in bryophytes and vascular plants. In our study, we took advantage of available genome sequences of representatives of each bryophyte clade to investigate the relationships of SPL genes between bryophytes and model angiosperm Arabidopsis thaliana. We have identified four SPL genes in each of the two hornworts species, Anthoceros agrestis and Anthoceros punctatus, what is similar to the set of SPL genes present in the liverwort Marchantia polymorpha. Thus, the analyzed hornworts and liverwort genomes encode a minimal set of SPL genes in comparison to other land plants that may resemble an archetype of SPL genes present in the ancestor of land plants. The phylogenetic analysis revealed the presence of four SPL groups. Comparative gene structure analysis showed that SPLs share similar exon-intron organization within the same phylogenetic group with some exceptions in hornworts. While we have identified conserved protein motifs between bryophytes and Arabidopsis in three out of four phylogenetic groups, the motif content differed explicitly in the fourth group. Since current understanding of SPL genes mostly arises from seed plants, the presented comparative and phylogenetic analysis will provide better understanding of SPL gene family from the representatives of the oldest living land plants.

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Comparative Evolutionary Analysis Of Spl Gene Family Between...mentioning

confidence: 99%

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Comparative analysis ofSQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL)gene family between bryophytes and seed plants

Alisha

Szweykowska-Kulińska

Sierocka

2023

Preprint

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Plasmodesmata dynamics in bryophyte model organisms: secondary formation and developmental modifications of structure and function

Wegner,

Ehlers

2024

Planta

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Main conclusion Developing bryophytes differentially modify their plasmodesmata structure and function. Secondary plasmodesmata formation via twinning appears to be an ancestral trait. Plasmodesmata networks in hornwort sporophyte meristems resemble those of angiosperms. Abstract All land-plant taxa use plasmodesmata (PD) cell connections for symplasmic communication. In angiosperm development, PD networks undergo an extensive remodeling by structural and functional PD modifications, and by postcytokinetic formation of additional secondary PD (secPD). Since comparable information on PD dynamics is scarce for the embryophyte sister groups, we investigated maturating tissues of Anthoceros agrestis (hornwort), Physcomitrium patens (moss), and Marchantia polymorpha (liverwort). As in angiosperms, quantitative electron microscopy revealed secPD formation via twinning in gametophytes of all model bryophytes, which gives rise to laterally adjacent PD pairs or to complex branched PD. This finding suggests that PD twinning is an ancient evolutionary mechanism to adjust PD numbers during wall expansion. Moreover, all bryophyte gametophytes modify their existing PD via taxon-specific strategies resembling those of angiosperms. Development of type II-like PD morphotypes with enlarged diameters or formation of pit pairs might be required to maintain PD transport rates during wall thickening. Similar to angiosperm leaves, fluorescence redistribution after photobleaching revealed a considerable reduction of the PD permeability in maturating P. patens phyllids. In contrast to previous reports on monoplex meristems of bryophyte gametophytes with single initials, we observed targeted secPD formation in the multi-initial basal meristems of A. agrestis sporophytes. Their PD networks share typical features of multi-initial angiosperm meristems, which may hint at a putative homologous origin. We also discuss that monoplex and multi-initial meristems may require distinct types of PD networks, with or without secPD formation, to control maintenance of initial identity and positional signaling.

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Conserved and non-conserved RNA–target modules in plants: lessons for a better understanding of Marchantia development

Pietrykowska,

Alisha,

Aggarwal

et al. 2023

Plant Mol Biol

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A wide variety of functional regulatory non-coding RNAs (ncRNAs) have been identified as essential regulators of plant growth and development. Depending on their category, ncRNAs are not only involved in modulating target gene expression at the transcriptional and post-transcriptional levels but also are involved in processes like RNA splicing and RNA-directed DNA methylation. To fulfill their molecular roles properly, ncRNAs must be precisely processed by multiprotein complexes. In the case of small RNAs, DICER-LIKE (DCL) proteins play critical roles in the production of mature molecules. Land plant genomes contain at least four distinct classes of DCL family proteins (DCL1–DCL4), of which DCL1, DCL3 and DCL4 are also present in the genomes of bryophytes, indicating the early divergence of these genes. The liverwort Marchantia polymorpha has become an attractive model species for investigating the evolutionary history of regulatory ncRNAs and proteins that are responsible for ncRNA biogenesis. Recent studies on Marchantia have started to uncover the similarities and differences in ncRNA production and function between the basal lineage of bryophytes and other land plants. In this review, we summarize findings on the essential role of regulatory ncRNAs in Marchantia development. We provide a comprehensive overview of conserved ncRNA–target modules among M. polymorpha, the moss Physcomitrium patens and the dicot Arabidopsis thaliana, as well as Marchantia-specific modules. Based on functional studies and data from the literature, we propose new connections between regulatory pathways involved in Marchantia’s vegetative and reproductive development and emphasize the need for further functional studies to understand the molecular mechanisms that control ncRNA-directed developmental processes.

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Meristem dormancy in Marchantia polymorpha is regulated by a liverwort-specific miRNA and a clade III SPL gene

Cited by 22 publications

References 46 publications

Comparative analysis ofSQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL)gene family between bryophytes and seed plants

Comparative analysis ofSQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL)gene family between bryophytes and seed plants

Plasmodesmata dynamics in bryophyte model organisms: secondary formation and developmental modifications of structure and function

Conserved and non-conserved RNA–target modules in plants: lessons for a better understanding of Marchantia development

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