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Dichotomously branched polysporangiate sporophyte of Psilotum nudum. In spite of its superficial resemblance to fossil rhyniopsids, Psilotum is firmly nested within the monilophytes along with the ferns and horsetails (Qiu et al., 2006, 2007).
Source publication
Background Molecular phylogeny has resolved the liverworts as the earliest-divergent clade of land plants and mosses as the sister group
to hornworts plus tracheophytes, with alternative topologies resolving the hornworts as sister to mosses plus tracheophytes
less well supported. The tracheophytes plus fossil plants putatively lacking lignified va...
Context in source publication
Context 1
... branching pattern of the shoot axis in living polyspor- angiophytes is quite diverse but basically two types can be distinguished: apical (or dichotomous) branching and lateral branching. In apical branching the SAM bifurcates into two, more or less equal and divergent parts (Fig. 5). In lateral branching the main apex produces subordinate SAMs that may develop into shoots some distance behind (Sussex and Kerk, 2001;Harrison et al., 2007). Apical branching is predominant in ferns and lycopsids and is viewed as ancestral in polysporangiophytes, whereas lateral branching is character- istic of seed plants, although ...
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Bryophyte is a non-vascular plant, consisting of three classes: mosses, hornworts, and liverworts. The body forms have a thallus, and some have a leaf-like organ. The class division of the Bryophyte division is base on anatomical and morphological traits, such as meristem tissues, stomata, and vascular tissues. M Bryophyte has no vascular tissue, b...
Stomata are key innovations for the diversification of land plants. They consist of two differentiated epidermal cells or guard cells and a pore between that leads to an internal cavity. Mosses and hornworts are the earliest among extant land plants to have stomata, but unlike those in all other plants, bryophyte stomata are located exclusively on...
Unraveling the phylogenetic relationships between the four major lineages of terrestrial plants (mosses, liverworts, hornworts, and vascular plants) is essential for an understanding of the evolution of traits specific to land plants, such as their complex life cycles, and the evolutionary development of stomata and vascular tissue.
Well supported...
Background
Plant body plans arise by the activity of meristematic growing tips during development and radiated independently in the gametophyte (n) and sporophyte (2n) stages of the life cycle during evolution. Although auxin and its intercellular transport by PIN family efflux carriers are primary regulators of sporophytic shoot development in flo...
Citations
... Liverworts, particularly the dioecious Marchantia polymorpha, are at the forefront of bryophyte studies due to their status as the earliest-diverging clade. M. polymorpha's short life cycle, relatively simple genome and amenability to genetic manipulation, coupled with its critical evolutionary position, make it an ideal model organism 6,7 . In M. polymorpha, specific environmental cues trigger the development of male (antheridiophores) and female (archegoniophores) reproductive structures 8 . ...
... https://doi.org/10.1038/s41477-024-01703-1 100 mM sodium phosphate buffer (pH 7.0), 5 mM K 3 [Fe(CN) 6 ], 5 mM K 4 [Fe(CN) 6 ], 1% Triton X-100 and 1 mg ml −1 X-Gluc. ChlorophyII in the tissue was removed by incubation in 70% ethanol. ...
In bryophytes, sexual reproduction necessitates the release of motile sperm cells from a gametophyte into the environment. Since 1856, this process, particularly in liverworts, has been known to depend on water. However, the molecular mechanism underlying this phenomenon has remained elusive. Here we identify the plasma membrane protein MpMLO1 in Marchantia polymorpha, a model liverwort, as critical for sperm discharge from antheridia. The MpMLO1-expressing tip cells among the sperm-wrapping jacket cells undergo programmed cell death upon antheridium maturation to facilitate sperm discharge after the application of water and even hypertonic solutions. The absence of MpMLO1 leads to reduced cytoplasmic Ca²⁺ levels in tip cells, preventing cell death and consequently sperm discharge. Our findings reveal that MpMLO1-mediated programmed cell death in antheridial tip cells, regulated by cytosolic Ca²⁺ dynamics, is essential for sperm release, elucidating a key mechanism in bryophyte sexual reproduction and providing insights into terrestrial plant evolution.
... According to the general anatomy and morphology, it is supposed the earliest terrestrial plants possessed features at the bryophyte grade (Gray, 1985;Ligrone et al., 2012). The earliest land plants found in the macrofossil record exhibit a branched sporophyte bearing terminal sporangia and are thereby classified as polysporangiophytes (Kenrick and Crane, 1991). ...
... conducting cells are absent in hornworts and elusive in liverworts (Ligrone et al., 2012), highlighting the diverse transport mechanisms among mosses and across bryophytes. The lesser stature and less intense demand for translocation of photosynthate in mosses are undoubtedly related to the apparent simplicity of architecture and the minimal elaboration of pores in end wall of moss leptoids compared with tracheophytes. ...
Introduction
Leptoids, the food-conducting cells of polytrichaceous mosses, share key structural features with sieve elements in tracheophytes, including an elongated shape with oblique end walls containing modified plasmodesmata or pores. In tracheophytes, callose is instrumental in developing the pores in sieve elements that enable efficient photoassimilate transport. Aside from a few studies using aniline blue fluorescence that yielded confusing results, little is known about callose in moss leptoids.
Methods
Callose location and abundance during the development of leptoid cell walls was investigated in the moss Polytrichum commune using aniline blue fluorescence and quantitative immunogold labeling (label density) in the transmission electron microscope. To evaluate changes during abiotic stress, callose abundance in leptoids of hydrated plants was compared to plants dried for 14 days under field conditions. A bioinformatic study to assess the evolution of callose within and across bryophytes was conducted using callose synthase (CalS) genes from 46 bryophytes (24 mosses, 15 liverworts, and 7 hornworts) and one representative each of five tracheophyte groups.
Results
Callose abundance increases around plasmodesmata from meristematic cells to end walls in mature leptoids. Controlled drying resulted in a significant increase in label density around plasmodesmata and pores over counts in hydrated plants. Phylogenetic analysis of the CalS protein family recovered main clades (A, B, and C). Different from tracheophytes, where the greatest diversity of homologs is found in clade A, the majority of gene duplication in bryophytes is in clade B.
Discussion
This work identifies callose as a crucial cell wall polymer around plasmodesmata from their inception to functioning in leptoids, and during water stress similar to sieve elements of tracheophytes. Among bryophytes, mosses exhibit the greatest number of multiple duplication events, while only two duplications are revealed in hornwort and none in liverworts. The absence in bryophytes of the CalS 7 gene that is essential for sieve pore development in angiosperms, reveals that a different gene is responsible for synthesizing the callose associated with leptoids in mosses.
... Although some reviews extend the use of the term leptoid to relatively unspecialised parenchymatous cells (Glime 2017a, Woudenberg et al. 2022, most authors working on bryophyte ultrastructure restrict it to the specialized FCCs of polytrichaceous mosses (Ligrone et al. 2000(Ligrone et al. , 2012Pressel et al. 2006), in which ultrastructural studies have revealed a distinctive cytological organization that include plasmodesmata in the end walls, plastids, mitochondria and endoplasmic reticulum-derived vesicles along longitudinal arrays of endoplasmic microtubules, breakdown of the tonoplast, mixing of the vacuolar and cytoplasmic contents and nuclear breakdown. Some of these characteristics are also present in the FCCs of L. canariensis, although no endoplasmic microtubules were observed, a common feature with sieve elements that was also reported by Pressel et al. (2006) in the FCCs (leptoids) of Polytrichastrum formosum (Hedw.) ...
... Seminal phylogenomic work over the last years suggests them to be a monophyletic group (Leebens-Mack et al., 2019;Li et al., 2020;Puttick et al., 2018). Representing one of the two major lineages of land plants, bryophytes are key for inferring traits present in the last common ancestor of land plants and understanding the plant terrestrialization event that occurred about 500 million years ago (Kenrick, 2017;Ligrone et al., 2012;Rensing, 2018). Already before terrestrialization, streptophyte algae, the paraphylum that nowadays includes the closest relatives to the land plants, were likely able to form desiccation-tolerant cells, including akinetes, pre-akinetes, and zygospores (Herburger et al., 2015;McLean & Pessoney, 1971;Pichrtov a et al., 2014). ...
The establishment of moss spores is considered a milestone in plant evolution. They harbor protein networks underpinning desiccation tolerance and accumulation of storage compounds that can be found already in algae and that are also utilized in seeds and pollen. Furthermore, germinating spores must produce proteins that drive the transition through heterotrophic growth to the autotrophic plant. To get insight into the plasticity of this proteome, we investigated it at five timepoints of moss (Physcomitrium patens) spore germination and in protonemata and gametophores. The comparison to previously published Arabidopsis proteome data of seedling establishment showed that not only the proteomes of spores and seeds are functionally related, but also the proteomes of germinating spores and young seedlings. We observed similarities with regard to desiccation tolerance, lipid droplet proteome composition, control of dormancy, and β-oxidation and the glyoxylate cycle. However, there were also striking differences. For example, spores lacked any obvious storage proteins. Furthermore, we did not detect homologs to the main triacylglycerol lipase in Arabidopsis seeds, SUGAR DEPENDENT1. Instead, we discovered a triacylglycerol lipase of the oil body lipase family and a lipoxygenase as being the overall most abundant proteins in spores. This finding indicates an alternative pathway for triacylglycerol degradation via oxylipin intermediates in the moss. The comparison of spores to Nicotiana tabacum pollen indicated similarities for example in regards to resistance to desiccation and hypoxia, but the overall developmental pattern did not align as in the case of seedling establishment and spore germination.
... For bryophytes, studies of the economic trait spectrum have mostly focused on the gametophyte, indicating, e.g., that mass-based nitrogen concentration and maximum photosynthetic rate are positively related, much like in vascular plants (Waite and Sack, 2010;Wang et al., 2014Wang et al., , 2017bWang et al., , 2022Carriquí et al., 2019;Grau-Andrés, Kardol, and Gundale, 2022). Studies on sporophytes usually describe the anatomical and morphological structures of the foot, seta, capsule, and spores for classification purposes or focus on their evolutionary function and development (e.g., Ligrone et al., 2012;Rose et al., 2016). Sporophyte traits reflect the reproductive and dispersal strategies of the moss, in particular when seen in combination with gametophytic traits (Crawford et al., 2009). ...
... In most mosses (except in Sphagnopsida and Andreaea), the spore capsule is supported by a slender, cylindrical seta (Ligrone et al., 2012). The capsule starts to expand and form spores after seta elongation (Stark, 2002). ...
PREMISE OF THE STUDY
Moss sporophytes differ strongly in size and biomass partitioning, potentially reflecting reproductive and dispersal strategies. Understanding how sporophyte traits are coordinated is essential for understanding moss functioning and evolution. This study aimed to answer: 1) how sporophyte size and proportions differ between moss species with and without prominent seta central strands, 2) how seta anatomical and morphological traits are related, and 3) how sporophyte biomass relates to gametophyte biomass and nutrient concentrations.
METHODS
We studied the relationships between seta anatomical and morphological traits, the biomass of seta, capsule, and gametophyte, and carbon, nitrogen, and phosphorus concentrations of 27 subtropical montane moss species.
KEY RESULTS
1) Moss species with prominent seta central strands had larger setae and heavier capsules than those without. 2) With increasing seta length, setae became thicker and more rounded for both groups, while in species with prominent central strands, the area ratio of transport‐cell to epidermis decreased; 3) In both groups, mosses with greater gametophyte biomass tended to have heavier sporophytes, but gametophyte nitrogen and phosphorus concentrations were unrelated to sporophyte traits.
CONCLUSIONS
Our study highlights that seta central strands may have an important functional role and affect the allometry of moss sporophytes. The coordinated variations in sporophyte morphological and anatomical traits follow basic biomechanical principles of cylinder‐like structures and these traits relate only weakly to the gametophyte nutrient concentrations. Research on moss sporophyte functional traits and their relationships to gametophytes is still in its infancy but could provide important insights into their adaptation strategies.
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... The epibasal cell divides transversally, resulting in an embryo with three cells. The upper cell (adjacent to the neck of the archegonium) produces the capsule, the middle cell the seta and foot and the lower cell a haustorium (Bower, 1935;Schertler, 1979;Kato and Akiyama, 2005;Ligrone et al., 2012). In hornworts, the first division of the zygote is vertical, and then other cell divisions give rise to a three-tiered embryo, with the upper tier producing the capsule and the lowest tier the foot (Ligrone et al., 2012). ...
... The upper cell (adjacent to the neck of the archegonium) produces the capsule, the middle cell the seta and foot and the lower cell a haustorium (Bower, 1935;Schertler, 1979;Kato and Akiyama, 2005;Ligrone et al., 2012). In hornworts, the first division of the zygote is vertical, and then other cell divisions give rise to a three-tiered embryo, with the upper tier producing the capsule and the lowest tier the foot (Ligrone et al., 2012). The bryophyte embryo is relatively long and narrow, and as the development of the capsule begins the embryo becomes greatly elongated (Fig. 1a). ...
In this review, we explore the origin of the rudimentary embryo, its relationship to other kinds of plant embryos and its role in the diversification of angiosperms. Rudimentary embryos have a length:width ratio of ≤2.0, and they have organs, including cotyledon(s) and a primary root. A literature survey failed to reveal rudimentary embryos in the pre-angiosperms, suggesting that this kind of embryo is an angiosperm invention. Although proembryos of some gymnosperms and angiosperms have a length:width ratio of ≤2.0, they have not formed meristems or organs. Thus, rudimentary embryos are not proembryos. During the development of rudimentary embryos in monocots and dicots (all non-monocots), the growth pattern of the epicotyledonary cells differs, resulting in differences in the placement of the shoot meristem and in one versus two cotyledons, respectively, but the embryo size is similar. Rudimentary embryos grow inside the seed prior to germination, which is true for linear-underdeveloped embryos, including those in some gymnosperms. Rudimentary embryos served as the starting point for the great diversification of embryos, and ultimately of seeds, in angiosperms, and they are still present in many families of extant angiosperms. The rudimentary embryo is part of the syndrome of changes, including increased speed of pollen germination and pollen tube growth, simplification of the female gametophyte, development of endosperm and elimination of multiple embryo production from each zygote, that distinguish angiosperm seed production from that of gymnosperms. We conclude that the rudimentary embryo was one of many new developments of angiosperms that contributed to their great success on earth.
... The bryophyte Physcomitrium patens (formerly Physcomitrella patens; Medina et al., 2019), which diverged from angiosperms approximately 0.5 billion years ago, has features of ancestral land plants and has been key to our understanding of land plant evolution (Rensing et al., 2020). This plant comprises a two-dimensional (2D) spreading mat of basal assimilatory filaments (chloronemata) and foraging filaments (caulonemata) that comprise foodconducting cells necessary for resource acquisition in dry habitats (reviewed in Ligrone et al., 2012). Once a filamentous plant is established, a proportion of caulonemal cells divide asymmetrically to produce three-dimensional (3D) upright leafy shoots, known as gametophores, which bear the reproductive organs (Harrison et al., 2009;Rensing et al., 2020;Thelander et al., 2018). ...
... Chloronemal cells can self-renew or may differentiate to form foraging caulonemal cells (reviewed in Jaeger & Moody, 2021). Caulonemata are specialised filaments made up of food-conducting cells (FCCs) with features similar to tracheophyte sieve elements (reviewed in Ligrone et al., 2012). The switch to caulonemal growth is regulated by resource availability, but is also controlled by a balance between auxin, which promotes caulonemata, and CK, which inhibits caulonemal growth (reviewed in Kofuji & Hasebe, 2014). ...
... Among these numerous innovations, early land plants evolved structures that enabled the acquisition of nutrients in dry habitats. In P. patens, these structures are the FCCcontaining caulonemal filaments (reviewed in Ligrone et al., 2012). The evolution of 3D growth was another critical innovation in early land plants. ...
The plant-specific TOPLESS (TPL) family of transcriptional corepressors is integral to multiple angiosperm developmental processes. Despite this, we know little about TPL function in other plants. To address this gap, we investigated the roles TPL plays in the bryophyte Physcomitrium patens, which diverged from angiosperms approximately 0.5 billion years ago. Although complete loss of PpTPL function is lethal, transgenic lines with reduced PpTPL activity revealed that PpTPLs are essential for two fundamental developmental switches in this plant: the transitions from basal photosynthetic filaments (chloronemata) to specialised foraging filaments (caulonemata) and from 2-dimensional to 3-dimensional growth. Using a transcriptomics approach, we integrate PpTPL into the regulatory network governing 3D growth and propose that PpTPLs represent another important class of regulators that are essential for the 2D to 3D developmental switch. Transcriptomics also revealed a previously unknown role for PpTPL in the regulation of flavonoids. Intriguingly, 3D growth and formation of caulonemata were crucial innovations that facilitated the colonization of land by plants; a major transformative event in the history of life on Earth. We conclude that TPL, which existed before the land plants, was co-opted into new developmental pathways, enabling phytoterrestrialisation and the evolution of land plants.
... Polar organizers (Brown andLemmon 2007, 2011), oil bodies (Asakawa 1995;Duckett and Ligrone 1995), and elaters (Asakawa 1995;Duckett and Ligrone 1995) are traits that distinguish liverworts from other two lineages. The apomorphies of mosses include multicellular protonema and rhizoids, spiral leafy organization of the mature gametophyte, and a distinct apical cell segmentation pattern (Ligrone et al. 2012). Moreover, hornworts have certain unique characteristics such as a pyrenoid in the chloroplast and thylakoid arrangement system (Vaughn et al. 1992;Renzaglia et al. 2009). ...
Model organisms are commonly employed in research as convenient tools for studying diverse biological processes. Plant research relied on several non-model plants until the Arabidopsis thaliana was developed as powerful model for identifying genes and determining their functions. To study the genetics of unique processes in different species, few other model photosynthetic organisms have recently been established, including Synechocystis sp. PCC 6803, Anabaena sp. PCC 7120, Chlamydomonas reinhardatii, Oryza sativa, Zea mays, Triticum dicoccoides, Populus trichocarpa, and Picea abies. However, when it comes to answering different biological problems, each of the current model plants has its own set of advantages and disadvantages, and many questions about land plant adaptation strategies at the level of morpho-physiology, development, and stress mitigation could not be adequately answered using these models. Furthermore, the high occurrence of embryo lethal mutations rendered studying the molecular basis of 3-dimensional (3-D) growth and gametogenesis unfeasible. Since bryophytes have a low cellular complexity and a dominant haploid gametophytic phase, they could be useful models not only for avoiding the aforementioned drawbacks, but also for functional genomics research and understanding the chronology of land plant evolution. These distinguishing characteristics and the advancement of sequencing technology have led to the development of some bryophytes as modern model plants, including Physcomitrium patens, Marchantia polymorpha, Anthoceros agrestis. Here, we review at how bryophytes became model plants, and how they have been able to answer crucial plant biology-related concerns like stress tolerance and evolutionary developmental (evo-devo) biology that other model plants have not been able to.
... Each row consists of basally arranged meristematic cells that continuously differentiate into the major tissue types towards the apex of the sporophyte. Very little is known about the molecular mechanisms governing the development of this meristem and its evolutionary homology to the multicellular meristems of land plants is highly debated (Ligrone et al., 2012a;Ligrone et al., 2012b;Harrison and Morris, 2018;Fouracre and Harrison, 2022). Nevertheless, the continuous differentiation gradient present along the longitudinal axis of the sporophyte provides an excellent model to understand conserved features of cell fate determination across bryophytes and vascular plants, and potentially the origin of multicellular meristems in vascular plants. ...
The hornworts are a small group of land plants, consisting of only 11 families and approximately 220 species. Despite their small size as a group, their phylogenetic position and unique biology are of great importance. Hornworts, together with mosses and liverworts, form the monophyletic group of bryophytes that is sister to all other land plants (Tracheophytes). It is only recently that hornworts became amenable to experimental investigation with the establishment of Anthoceros agrestis as a model system. In this perspective, we summarize the recent advances in the development of A. agrestis as an experimental system and compare it with other plant model systems. We also discuss how A. agrestis can help to further research in comparative developmental studies across land plants and to solve key questions of plant biology associated with the colonization of the terrestrial environment. Finally, we explore the significance of A. agrestis in crop improvement and synthetic biology applications in general.
