Insights into the molecular evolution of fertilization mechanism in land plants

Sharma, Vijyesh; Clark, Anthony; Kawashima, Tomokazu

doi:10.1007/s00497-021-00414-3

Cited by 15 publications

(9 citation statements)

References 98 publications

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“…Therefore, the transcriptome data suggest that nonangiosperm gene networks widely contribute to the specification and differentiation of the P. patens egg. This is not surprising given the distinct environment in which the egg cell develops and the distinct mechanisms of fertilization (Sharma et al ., 2021).…”

Section: Discussionmentioning

confidence: 99%

The Physcomitrium patens egg cell expresses several distinct epigenetic components and utilizes homologues of BONOBO genes for cell specification

et al. 2022

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Summary Although land plant germ cells have received much attention, knowledge about their specification is still limited. We thus identified transcripts enriched in egg cells of the bryophyte model species Physcomitrium patens, compared the results with angiosperm egg cells, and selected important candidate genes for functional analysis. We used laser‐assisted microdissection to perform a cell‐type‐specific transcriptome analysis on egg cells for comparison with available expression profiles of vegetative tissues and male reproductive organs. We made reporter lines and knockout mutants of the two BONOBO (PbBNB) genes and studied their role in reproduction. We observed an overlap in gene activity between bryophyte and angiosperm egg cells, but also clear differences. Strikingly, several processes that are male‐germline specific in Arabidopsis are active in the P. patens egg cell. Among those were the moss PbBNB genes, which control proliferation and identity of both female and male germlines. Pathways shared between male and female germlines were most likely present in the common ancestors of land plants, besides sex‐specifying factors. A set of genes may also be involved in the switches between the diploid and haploid moss generations. Nonangiosperm gene networks also contribute to the specification of the P. patens egg cell.

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Section: Discussionmentioning

confidence: 99%

The Physcomitrium patens egg cell expresses several distinct epigenetic components and utilizes homologues of BONOBO genes for cell specification

et al. 2022

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“…The monophyletic group of land plants is characterised by a huge variation in reproductive solutions that is the result of successive key evolutionary innovations (Renzaglia et al ., 2000 ; Hackenberg & Twell, 2019 ; Hisanaga et al ., 2019 ; Rensing & Weijers, 2021 ; Sharma et al ., 2021 ). The developmental process controlled by AtMS1 and AtMMD1 , that is tapetum‐assisted microspore and pollen formation facilitating downstream male gametogenesis, is for example a derived trait of angiosperms (Hackenberg & Twell, 2019 ).…”

Section: Introductionmentioning

confidence: 99%

MS1/MMD1 homologues in the moss Physcomitrium patens are required for male and female gametogenesis

et al. 2022

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Summary The Arabidopsis Plant HomeoDomain (PHD) proteins AtMS1 and AtMMD1 provide chromatin‐mediated transcriptional regulation essential for tapetum‐dependent pollen formation. This pollen‐based male gametogenesis is a derived trait of seed plants. Male gametogenesis in the common ancestors of land plants is instead likely to have been reminiscent of that in extant bryophytes where flagellated sperms are produced by an elaborate gametophyte generation. Still, also bryophytes possess MS1/MMD1‐related PHD proteins. We addressed the function of two MS1/MMD1‐homologues in the bryophyte model moss Physcomitrium patens by the generation and analysis of reporter and loss‐of‐function lines. The two genes are together essential for both male and female fertility by providing functions in the gamete‐producing inner cells of antheridia and archegonia. They are furthermore expressed in the diploid sporophyte generation suggesting a function during sporogenesis, a process proposed related by descent to pollen formation in angiosperms. We propose that the moss MS1/MMD1‐related regulatory network required for completion of male and female gametogenesis, and possibly for sporogenesis, represent a heritage from ancestral land plants.

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“…Fertilization of the egg cell by a sperm is an ancient and evolutionarily conserved process in sexual reproduction involving cell fusion facilitators (Sprunck, 2020). Fertilization of the central cell evolved much later and is restricted to the angiosperms (Sharma et al, 2021), thus cell fusion might be less specific. This hypothesis is supported by the observation that the block to polyspermy (fusion of multiple sperm cells with a female gamete) is more stringent in the egg cell than in the central cell (Scott et al, 2008; Nagahara et al, 2020; Tekleyohans and Groß‐Hardt, 2020).…”

Section: Resultsmentioning

confidence: 99%

The egg cell is preferentially fertilized in Arabidopsis double fertilization

Hou

Wang

et al. 2022

JIPB

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In flowering plants (angiosperms), fertilization of the egg cell by one sperm cell produces an embryo, whereas fusion of a second sperm cell with the central cell generates the endosperm. In most angiosperms like Arabidopsis, a pollen grain contains two isomorphic sperm cells required for this double fertilization process. A long‐standing unsolved question is whether the two fertilization events have any preference. A tool to address this question is the usage of the cyclin‐dependent kinase a1 (cdka;1) mutant pollen, which produces a single sperm‐like cell (SLC). Here, we first adopt a complementation‐based fluorescence‐labeling method to successfully separate and collect cdka;1 mutant pollen containing a single SLC. Single‐cell RNA‐sequencing analysis revealed that cdka;1 SLCs show a gene expression profile highly similar to that of sperm cells and not to the generative cell, precursor of the two sperm cells. Pollination assays using a limited number of cdka;1 mutant pollen revealed that in 98.2% of the ovules, single fertilization of the egg cell occurred. Pollination of pistils with excessive cdka;1 mutant pollen allowed the delivery of a second SLC via fertilization recovery, which fertilized the central cell, resulting in 20.7% double‐fertilized ovules. This indicates that cdka;1 SLCs are able to fertilize both the egg and the central cell. Taken together, our findings have answered a long‐standing question and support that preferential fertilization of the egg cell is evident in Arabidopsis.

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Insights into the molecular evolution of fertilization mechanism in land plants

Cited by 15 publications

References 98 publications

The Physcomitrium patens egg cell expresses several distinct epigenetic components and utilizes homologues of BONOBO genes for cell specification

The Physcomitrium patens egg cell expresses several distinct epigenetic components and utilizes homologues of BONOBO genes for cell specification

MS1/MMD1 homologues in the moss Physcomitrium patens are required for male and female gametogenesis

The egg cell is preferentially fertilized in Arabidopsis double fertilization

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