Multiflagellated sperm cells of <i>Ceratopteris richardii</i> are bathed in arabinogalactan proteins throughout development

Lopez, Renee A.; Renzaglia, Karen S.

doi:10.3732/ajb.1400424

Cited by 30 publications

(18 citation statements)

References 56 publications

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“…Although ferns receive comparatively little attention and genome sequences of ferns are, so far, unavailable, it is accepted that we need to extend our analyses to more phylogenetic branches (Barker and Wolf, 2010). To date, only few fern species have been used to study developmental processes (Whittier, 1971; Wen et al, 1999; Salmi et al, 2005, 2010; Kaźmierczak, 2010; Lopez and Renzaglia, 2014; Valledor et al, 2014; de Vries et al, 2015). …”

Section: Introductionmentioning

confidence: 99%

Proteogenomic Analysis Greatly Expands the Identification of Proteins Related to Reproduction in the Apogamous Fern Dryopteris affinis ssp. affinis

Grossmann¹,

Fernández

Chaubey

et al. 2017

Front. Plant Sci.

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Performing proteomic studies on non-model organisms with little or no genomic information is still difficult. However, many specific processes and biochemical pathways occur only in species that are poorly characterized at the genomic level. For example, many plants can reproduce both sexually and asexually, the first one allowing the generation of new genotypes and the latter their fixation. Thus, both modes of reproduction are of great agronomic value. However, the molecular basis of asexual reproduction is not well understood in any plant. In ferns, it combines the production of unreduced spores (diplospory) and the formation of sporophytes from somatic cells (apogamy). To set the basis to study these processes, we performed transcriptomics by next-generation sequencing (NGS) and shotgun proteomics by tandem mass spectrometry in the apogamous fern D. affinis ssp. affinis. For protein identification we used the public viridiplantae database (VPDB) to identify orthologous proteins from other plant species and new transcriptomics data to generate a “species-specific transcriptome database” (SSTDB). In total 1,397 protein clusters with 5,865 unique peptide sequences were identified (13 decoy proteins out of 1,410, protFDR 0.93% on protein cluster level). We show that using the SSTDB for protein identification increases the number of identified peptides almost four times compared to using only the publically available VPDB. We identified homologs of proteins involved in reproduction of higher plants, including proteins with a potential role in apogamy. With the increasing availability of genomic data from non-model species, similar proteogenomics approaches will improve the sensitivity in protein identification for species only distantly related to models.

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Section: Introductionmentioning

confidence: 99%

Proteogenomic Analysis Greatly Expands the Identification of Proteins Related to Reproduction in the Apogamous Fern Dryopteris affinis ssp. affinis

Grossmann¹,

Fernández

Chaubey

et al. 2017

Front. Plant Sci.

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“…These two phenomena reflect two observable aberrations as different manifestations of the same defect. In the control, the sperm cell cytoplasm is surrounded by an extracellular matrix in which the gametes develop; this matrix is broken down during differentiation, enabling sperm cells to swim when released (Lopez and Renzaglia 2014 ). The mutant exhibits a persistent extraprotoplasmatic matrix inside the “vesicle” wall (cf.…”

Section: Resultsmentioning

confidence: 99%

HAG1 and SWI3A/B control of male germ line development in P. patens suggests conservation of epigenetic reproductive control across land plants

et al. 2021

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Key message Bryophytes as models to study the male germ line: loss-of-function mutants of epigenetic regulators HAG1 and SWI3a/b demonstrate conserved function in sexual reproduction. Abstract With the water-to-land transition, land plants evolved a peculiar haplodiplontic life cycle in which both the haploid gametophyte and the diploid sporophyte are multicellular. The switch between these phases was coined alternation of generations. Several key regulators that control the bauplan of either generation are already known. Analyses of such regulators in flowering plants are difficult due to the highly reduced gametophytic generation, and the fact that loss of function of such genes often is embryo lethal in homozygous plants. Here we set out to determine gene function and conservation via studies in bryophytes. Bryophytes are sister to vascular plants and hence allow evolutionary inferences. Moreover, embryo lethal mutants can be grown and vegetatively propagated due to the dominance of the bryophyte gametophytic generation. We determined candidates by selecting single copy orthologs that are involved in transcriptional control, and of which flowering plant mutants show defects during sexual reproduction, with a focus on the under-studied male germ line. We selected two orthologs, SWI3a/b and HAG1, and analyzed loss-of-function mutants in the moss P. patens. In both mutants, due to lack of fertile spermatozoids, fertilization and hence the switch to the diploid generation do not occur. Pphag1 additionally shows arrested male and impaired female gametangia development. We analyzed HAG1 in the dioecious liverwort M. polymorpha and found that in Mphag1 the development of gametangiophores is impaired. Taken together, we find that involvement of both regulators in sexual reproduction is conserved since the earliest divergence of land plants.

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“…AGPs in bryophytes are reported to be associated with water conducting cells (Ligrone et al 2002), apical cell extension and differentiation of protonemata, (Lee et al 2005, Kobayashi et al 2011, water balance (Shibaya et al 2005), cell wall regeneration in cultured protoplasts (Shibaya & Sugawara 2007), cell plate formation (Shibaya & Sugawara 2009) and hyaline cell wall deposition in Sphagnum Linnaeus (1753: 1106) ( Kremer et al 2004). Consistent with a role in signaling, AGPs are abundantly expressed during spermatogenesis and oogenesis in Ceratopteris (Lopez & Renzaglia 2014, 2016 and spermatogenesis in Aulacomnium palustre (Hedwig) Schwägrichen (1827: 216) (Lopez-Swalls 2016).…”

Section: Discussionmentioning

confidence: 97%

Cell wall polymers in the Phaeoceros placenta reflect developmental and functional differences across generations

Henry

Ligrone²,

Vaughn³

et al. 2021

BDE

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The placenta of hornworts is unique among bryophytes in the restriction of transfer cells that are characterized by elaborate wall labyrinths to the gametophyte generation. During development, cells around the periphery of the sporophyte foot elongate, forming smooth-walled haustorial cells that interdigitate with gametophyte cells. Using immunogold labeling with 22 antibodies to diverse cell wall polymers, we examined compositional differences in the developmentally and morphologically distinct cell walls of gametophyte transfer cells and sporophyte haustorial cells in the placenta of Phaeoceros. As detected by Calcofluor White fluorescence, cellulose forms the cell wall scaffolding in cells on both sides of the placenta. Homogalacturonan (HG) and rhamnogalacturonan I (RG-I) pectins are abundant in both cell types, and haustorial cells are further enriched in methyl-esterified HGs. The abundance of pectins in placental cell walls is consistent with the postulated roles of these polymers in cell wall porosity and in maintaining an acidic apoplastic pH favorable to solute transport. Xyloglucan hemicellulose, but not mannans or glucuronoxylans, are present in cell walls at the interface between the two generations with a lower density in gametophytic wall ingrowths. Arabinogalactan proteins (AGPs) are diverse along the plasmalemma of placental cells and are absent in surrounding cells in both generations. AGPs in placental cell walls may play a role in calcium binding and release associated with signal transduction as has been speculated for these glycoproteins in other plants. Callose is restricted to thin areas in cell walls of gametophyte transfer cells. In contrast to studies of transfer cells in other systems, no reaction to the JIM12 antibody against extensin was observed in Phaeoceros.

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Multiflagellated sperm cells of Ceratopteris richardii are bathed in arabinogalactan proteins throughout development

Cited by 30 publications

References 56 publications

Proteogenomic Analysis Greatly Expands the Identification of Proteins Related to Reproduction in the Apogamous Fern Dryopteris affinis ssp. affinis

Proteogenomic Analysis Greatly Expands the Identification of Proteins Related to Reproduction in the Apogamous Fern Dryopteris affinis ssp. affinis

HAG1 and SWI3A/B control of male germ line development in P. patens suggests conservation of epigenetic reproductive control across land plants

Cell wall polymers in the Phaeoceros placenta reflect developmental and functional differences across generations

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