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Callose in Sporogenesis: Novel Composition of the Inner Spore Wall in Hornworts

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Callose in Sporogenesis: Novel Composition of the Inner Spore Wall in Hornworts See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/339085007 Callose in sporogenesis: novel composition of the inner spore wall in hornworts Article in Plant Systematics and Evolution · April 2020 DOI: 10.1007/s00606-020-01631-5 CITATION READS 1 134 5 authors, including: Karen S Renzaglia Renee Lopez-Smith Southern Illinois University Carbondale Southern Illinois University Carbondale 152 PUBLICATIONS 3,894 CITATIONS 9 PUBLICATIONS 61 CITATIONS SEE PROFILE SEE PROFILE Amelia Merced International Institute of Tropical Forestry 22 PUBLICATIONS 163 CITATIONS SEE PROFILE Some of the authors of this publication are also working on these related projects: Evolution of land plants View project Induction of stress response and toxicity threshold of Azolla caroliniana in response to AgNP View project All content following this page was uploaded by Renee Lopez-Smith on 27 April 2020. The user has requested enhancement of the downloaded file. Plant Systematics and Evolution (2020) 306:16 https://doi.org/10.1007/s00606-020-01631-5 ORIGINAL ARTICLE Callose in sporogenesis: novel composition of the inner spore wall in hornworts Karen S. Renzaglia1 · Renee A. Lopez1 · Ryan D. Welsh1 · Heather A. Owen2 · Amelia Merced3 Received: 27 September 2019 / Accepted: 8 January 2020 © Springer-Verlag GmbH Austria, part of Springer Nature 2020 Abstract Sporogenesis is a developmental process that defnes embryophytes and involves callose, especially in the production of the highly protective and recalcitrant spore/pollen wall. Until now, hornworts, leptosporangiate ferns and homosporous lycophytes are the only major plant groups in which the involvement of callose in spore development is equivocal. Through aniline blue fuorescence and immunogold labeling in the transmission electron microscope, we provide indisputable evi- dence for the presence of callose in the spore wall of fve hornwort genera, but not in the derived Dendroceros, an epiphyte that produces multicellular spores. We present evidence that callose appears in the developing spore wall and is retained throughout development as a wall constituent of the intine or inner spore wall, a novel location for this polysaccharide in embryophytes. In endosporic and multicellular spores/pollen of Dendroceros, the liverwort Pellia, and Arabidopsis, callose appears in the newly formed cell walls only following the frst mitotic division. Further probing for other wall polymers in hornworts reveals the presence of cellulose (Calcofuor fuorescence) in the spore intine, aperture and around the equatorial girdle. Further immunogold labeling with monoclonal antibodies identifes pectin and hemicellulose in hornwort intines. The persistence of callose, a typically transient cell wall constituent, with cellulose, pectins and hemicellulose in the intine, supports specialized functions of callose in spores of hornworts that include reduced water loss when spores are dry and mechanical fexibility to withstand desiccation. Keywords Bryophyte · Callose · Cell wall · Hornwort · Intine · Spore Introduction diagnostic feature of land plants, spores were instrumental to the successful colonization and radiation of embryophytes Callose is a 1-3-β-glucan cell wall polysaccharide that serves nearly 500 million years ago (Renzaglia et al. 2000, 2007; diverse essential functions in plant development, reproduc- Ligrone et al. 2012). Indeed, thick-walled fossil spores tion and stress responses (Piršelová and Matušíková 2013). (cryptospores) provided the frst evidence of plant life on Among the key processes that require this wall polymer is land 40 million years prior to the appearance of plant mac- sporogenesis, a process that culminates in single-celled mei- rofossils (Brown and Lemmon 2011). In non-seed plants otic spores that are encased in highly durable sporopollenin- such as bryophytes, spores play a role similar to seeds in containing walls (Brown et al. 2015). As a signature and that they function as the chief dispersal and perennating structures, remaining dormant for decades as they establish or reestablish populations when habitats become available. Handling Editor: Louis P. Ronse De Craene. Therefore, understanding the intricacies of sporogenesis is * Renee A. Lopez important not only in unraveling early plant evolution but [email protected] also in ascertaining the function of key cell wall polysac- charides across plant groups and over time. 1 Department of Plant Biology, Southern Illinois University Sporogenesis involves the sequential development of Carbondale, Carbondale, IL, USA special cell walls that organize and guide the building of 2 Department of Biological Sciences, University of Wisconsin one of the most elaborate and structurally unique walls Milwaukee, Milwaukee, WI, USA known in the plant life cycle. Spore wall construction 3 Institute of Neurobiology, University of Puerto Rico, begins just prior to or during meiosis when a template for San Juan, PR, USA Vol.:(0123456789)1 3 16 Page 2 of 9 K. S. Renzaglia et al. the sculptured spore or pollen wall is organized within the Materials and methods diploid mother cell wall. In many plant groups, including liverworts, heterosporous lycophytes, homosporous ferns Plant species and collections and seed plants, this template contains callose (Wallace et al. 2011; Renzaglia et al. 2015). In seed plants, callose Arabidopsis thaliana Shur is from culture of Donor Stock has been suggested to restrict the primexine matrix that Number CS1601 located at the Arabidopsis Biological is produced by the microspores at the tetrad stage during Resource Center. The species and authorities, locations development. It is within the primexine that the exine pat- and collections for feld collected plants are listed below: tern is established and the pollen wall is formed (Dong Leiosporoceros dussii (Steph.) Hässel, PANAMA, et al. 2005; Nishikawa et al. 2005; Radja et al. 2019). In Villarreal 803a; Anthoceros agrestis Paton, nom. cons. liverworts in contrast, sporopollenin is assembled within prop., ILLINOIS, Renzaglia 4146; Phaeoceros carolini- a callosic template that is replaced progressively as the anus, ILLINOIS, Renzaglia 4139; Notothylas orbicularis, outer spore wall forms (Renzaglia et al. 2015; Brown and ILLINOIS, Long s.n.; Megaceros fagellaris (Mitt.) Steph. Lemmon 1987). In their review of sporogenesis in bryo- AUSTRALIA, Cargill 885 (CANB); Dendroceros crispa- phytes, Brown and Lemmon (1990) reported an absence tus (Hook) Nees, AUSTRALIA, D.C. Cargill 28 (CANB); of callose in sporogenesis of mosses and hornworts. With Pellia epiphylla (L.) Corda, ILLINOIS, Welsh s.n. more careful examination and higher resolution techniques that include immunogold labeling, Schuette et al. (2009) demonstrated that in mosses callose appears late in spore Fluorescence light microscopy and fuorochemical development and is restricted to the aperture in the nearly staining mature spore. This was the frst description of callose as a component of the moss spore wall. No involvement of Live specimens were collected from private land adjacent callose in the deposition of the spore wall has been iden- to the Shawnee National Forest in Jackson County, Illinois tifed in mosses. To date, no studies have unequivocally (37.627721, − 89.260070). In order to detect callose in spores, demonstrated the involvement of callose during any por- excised sporophytes (n = 18) and 1-µm-thick sections were tion of hornwort sporogenesis. Although Ridgeway (1965) collected on slides, covered by 1% aniline blue in 0.067 M reported the absence of callose in all stages of sporogen- Na2HPO4 (pH 8.5), placed in the dark at 4 °C for 3–5 days and esis in hornworts, Neidhart (1979) noted callose as a com- rinsed in bufer. To visualize cellulose, resin-embedded thick ponent of the spore mother cell wall, but did not provide sections (1 µm) were placed on glass slides with a drop of Cal- corroborating evidence. cofuor white (Sigma-Aldrich) stain and a drop of 10% KOH To investigate whether or not callose is found in any stage bufer for 3 min. Controls were made using the respective of hornwort spore development, we conducted a correlated bufers without aniline blue or Calcofuor white. All stained microscopic investigation on sporogenesis in Phaeoceros material was viewed with a Leica DM500B compound micro- carolinianus (Michx.) Prosk. and Notothylas orbicularis scope (excitation flter equipped with ultraviolet fuorescence (Schwein.) Sull. ex A. Gray. The entire process of sporogen- between 360 and 400 nm). Images were collected digitally esis was followed using aniline blue staining with fuores- using a Q-Imaging Retiga 2000R digital camera. For images cence microscopy and immunogold labeling in the transmis- of Arabidopsis, 0.5-µm sections were taken from existing sion electron microscope. Following positive identifcation tissue blocks from a previous study (Paxson-Sowders et al. of callose in the intine, or endospore, of these plants, we 2001). The sections were heat fxed to slides, the resin was probed four additional hornwort genera (Leiosporoceros removed with sodium methoxide (Sutherland and McCully Hässel, Anthoceros L., Megaceros Campb. and Dendroc- 1976), and then sections were mounted in 0.05% aniline blue eros Nees), representing the entire diversity within the in phosphate bufer (Smith and McCully 1978). Material was group. To assess whether other wall polymers co-localized viewed with a Nikon Eclipse 80i compound microscope (exci- with
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