Origin of sporophyte shoot Ligrone et al 2012 (original) (raw)
Related papers
The origin of the sporophyte shoot in land plants: a bryological perspective
Annals of botany, 2012
† Background Land plants (embryophytes) are monophyletic and encompass four major clades: liverworts, mosses, hornworts and polysporangiophytes. The liverworts are resolved as the earliest divergent lineage and the mosses as sister to a crown clade formed by the hornworts and polysporangiophytes (lycophytes, monilophytes and seed plants). Alternative topologies resolving the hornworts as sister to mosses plus polysporangiophytes are less well supported. Sporophyte development in liverworts depends only on embryonic formative cell divisions. A transient basal meristem contributes part of the sporophyte in mosses. The sporophyte body in hornworts and polysporangiophytes develops predominantly by post-embryonic meristematic activity. † Scope This paper explores the origin of the sporophyte shoot in terms of changes in embryo organization. Pressure towards amplification of the sporangium-associated photosynthetic apparatus was a major driver of sporophyte evolution. Starting from a putative ancestral condition in which a transient basal meristem produced a sporangium-supporting seta, we postulate that in the hornwort -polysporangiophyte lineage the basal meristem acquired indeterminate meristematic activity and ectopically expressed the sporangium morphogenetic programme. The resulting sporophyte body plan remained substantially unaltered in hornworts, whereas in polysporangiophytes the persistent meristem shifted from a mid-embryo to a superficial position and was converted into an ancestral shoot apical meristem with the evolution of sequential vegetative and reproductive growth. † Conclusions The sporophyte shoot is interpreted as a sterilized sporangial axis interpolated between the embryo and the fertile sporangium. With reference to the putatively ancestral condition found in mosses, the sporophyte body plans in hornworts and polysporangiophytes are viewed as the product of opposite heterochronic events, i.e. an anticipation and a delay, respectively, in the development of the sporangium. In either case the result was a pedomorphic sporophyte permanently retaining juvenile characters.
Major transitions in the evolution of early land plants: a bryological perspective
† 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 vascular tissue form the polysporangiophyte clade. † Scope This paper reviews phylogenetic, developmental, anatomical, genetic and paleontological data with the aim of reconstructing the succession of events that shaped major land plant lineages. † Conclusions Fundamental land plant characters primarily evolved in the bryophyte grade, and hence the key to a better understanding of the early evolution of land plants is in bryophytes. The last common ancestor of land plants was probably a leafless axial gametophyte bearing simple unisporangiate sporophytes. Water-conducting tissue, if present, was restricted to the gametophyte and presumably consisted of perforate cells similar to those in the early-divergent bryophytes Haplomitrium and Takakia. Stomata were a sporophyte innovation with the possible ancestral functions of producing a transpiration-driven flow of water and solutes from the parental gametophyte and facilitating spore separation before release. Stomata in mosses, hornworts and polysporangiophytes are viewed as homologous, and hence these three lineages are collectively referred to as the 'stomatophytes'. An indeterminate sporophyte body (the sporophyte shoot) developing from an apical meristem was the key innovation in polysporangiophytes. Poikilohydry is the ancestral condition in land plants; homoiohydry evolved in the sporophyte of polysporangiophytes. Fungal symbiotic associations ancestral to modern arbuscular mycorrhizas evolved in the gametophytic generation before the separation of major present-living lineages. Hydroids are imperforate water-conducting cells specific to advanced mosses. Xylem vascular cells in polysporangiophytes arose either from perforate cells or de novo. Food-conducting cells were a very early innovation in land plant evolution. The inferences presented here await testing by molecular genetics.
Vegetative and reproductive innovations of early land plants: implications for a unified phylogeny
Philosophical Transactions of The Royal Society B: Biological Sciences, 2000
As the oldest extant lineages of land plants, bryophytes provide a living laboratory in which to evaluate morphological adaptations associated with early land existence. In this paper we examine reproductive and structural innovations in the gametophyte and sporophyte generations of hornworts, liverworts, mosses and basal pteridophytes. Reproductive features relating to spermatogenesis and the architecture of motile male gametes are overviewed and evaluated from an evolutionary perspective. Phylogenetic analyses of a data set derived from spermatogenesis and one derived from comprehensive morphogenetic data are compared with a molecular analysis of nuclear and mitochondrial small subunit rDNA sequences.
2012
Adaptive evolution has often been proposed to explain correlations between habitats and certain phenotypes. In mosses, a high frequency of species with specialized sporophytic traits in exposed or epiphytic habitats was, already 100 years ago, suggested as due to adaptation. We tested this hypothesis by contrasting phylogenetic and morphological data from two moss families, Neckeraceae and Lembophyllaceae, both of which show parallel shifts to a specialized morphology and to exposed epiphytic or epilithic habitats. Phylogeny-based tests for correlated evolution revealed that evolution of four sporophytic traits is correlated with a habitat shift. For three of them, evolutionary rates of dual character-state changes suggest that habitat shifts appear prior to changes in morphology. This suggests that they could have evolved as adaptations to new habitats. Regarding the fourth correlated trait the specialized morphology had already evolved before the habitat shift. In addition, several other specialized ''epiphytic'' traits show no correlation with a habitat shift. Besides adaptive diversification, other processes thus also affect the match between phenotype and environment. Several potential factors such as complex genetic and developmental pathways yielding the same phenotypes, differences in strength of selection, or constraints in phenotypic evolution may lead to an inability of phylogeny-based comparative methods to detect potential adaptations.
Early evolution of the vascular plant body plan — the missing mechanisms
The complex body plan of modern vascular plants evolved by modification of simple systems of branching axes which originated from the determinate vegetative axis of a bryophyte grade ancestor. Understanding body plan evolution and homologies has implications for land plant phylogeny and requires resolution of the specific developmental changes and their evolutionary sequence. The branched sporophyte may have evolved from a sterilized bryophyte sporangium, but prolongation of embryonic vegetative growth is a more parsimonious explanation. Research in the bryophyte model system Physcomitrella points to mechanisms regulating sporophyte meristem maintenance, indeterminacy, branching and the transition to reproductive development. These results can form the basis for hypotheses to identify and refine the nature and sequence of changes in development that occurred during the evolution of the indeterminate branched sporophyte from an unbranched bryophyte-grade sporophyte.
New Phytologist, 1998
This light-and electron-microscope study of four species of Sphagnum reveals that stem elongation involves meristematic activities unique to the group and hitherto unrecognized. The internal tissue of the mature stem arises by the concerted activity of an apical (primary) and a subapical (secondary) meristem. The primary meristem comprises the immediate derivatives of the single apical cell. Following a small number of divisions, the primary derivatives differentiate into highly vacuolate parenchymatous cells with a storied arrangement. Subsequently, the large vacuoles are replaced by numerous small vacuoles and the cells then divide repeatedly, by transverse septa, producing files of about nine short cells. Finally, ninefold elongation of these secondary cells is responsible for extension growth of the main stem below the mature capitulum. An early step in primary differentiation is the confinement of pre-existing plasmodesmata to distinct pitted areas. Further enlargement of the cells during primary and secondary differentiation involves the thickening of non-pitted wall areas, followed by expansion and thinning out, while the pitted areas remain virtually unchanged. A cortical array of microtubules is regularly found in association with non-pitted wall areas, while the unexpanded pitted areas are associated with smooth endoplasmic reticulum showing continuity with desmotubules. Though sharing much the same cytology as the conducting cells in bryoid mosses, in terms of their development the central stem cells in Sphagnum are not homologous with those of other mosses. The unique mode of stem development may be an important factor in the ecological success of Sphagnum.
Multiple innovations underpinned branching form diversification in mosses
The New phytologist, 2017
Broad-scale evolutionary comparisons have shown that branching forms arose by convergence in vascular plants and bryophytes, but the trajectory of branching form diversification in bryophytes is unclear. Mosses are the most species-rich bryophyte lineage and two sub-groups are circumscribed by alternative reproductive organ placements. In one, reproductive organs form apically, terminating growth of the primary shoot (gametophore) axis. In the other, reproductive organs develop on very short lateral branches. A switch from apical to lateral reproductive organ development is proposed to have primed branching form diversification. Moss gametophores have modular development and each module develops from a single apical cell. Here we define the architectures of 175 mosses by the number of module classes, branching patterns and the pattern in which similar modules repeat. Using ancestral character state reconstruction we identify two stages of architectural diversification. During a firs...
Molecular Phylogenetics and Evolution, 2012
Morphological characters from the gametophyte and sporophyte generations have been used in land plants to infer relationships and construct classifications, but sporophytes provide the vast majority of data for the systematics of vascular plants. In bryophytes both generations are well developed and characters from both are commonly used to classify these organisms. However, because morphological traits of gametophytes and sporophytes can have different genetic bases and experience different selective pressures, taxonomic emphasis on one generation or the other may yield incongruent classifications. The moss order Hookeriales has a controversial taxonomic history because previous classifications have focused almost exclusively on either gametophytes or sporophytes. The Hookeriales provide a model for comparing morphological evolution in gametophytes and sporophytes, and its impact on alternative classification systems. In this study we reconstruct relationships among mosses that are or have been included in the Hookeriales based on sequences from five gene regions, and reconstruct morphological evolution of six sporophyte and gametophyte traits that have been used to differentiate families and genera. We found that the Hookeriales, as currently circumscribed, are monophyletic and that both sporophyte and gametophyte characters are labile. We documented parallel changes and reversals in traits from both generations. This study addresses the general issue of morphological reversals to ancestral states, and resolves novel relationships in the Hookeriales.
American Journal of Botany, 2010
Mosses arguably possess the most structurally complex sporangia of any extant land plants, a consequence of being the monosporangiophyte lineage most strongly adapted to terrestrial environments. Morphological and functional variation in the mechanisms that regulate spore release in one of the major classes of mosses, the Polytrichopsida, is largely unexplored, while recent research indicates that the most distinctive structure, the peristome, has evolved independently in the Polytrichopsida and in other mosses. The genus Polytrichastrum was separated from Polytrichum on the basis of such sporangial characters, although the critical features had until recently only been examined using light microscopy, and strong evidence from molecular data indicated that Polytrichastrum as currently circumscribed is polyphyletic. Here we use Bayesian ancestral character state reconstruction in conjunction with extensive scanning electron micrographic studies to elucidate probable morphology at ancestral nodes and defi ne natural taxa. As well as clarifying the structure, evolution, and aspects of development of the peristome -epiphragm complex in this highly prominent group of mosses, the results provide a basis for a revised phylogenetic taxonomy in which the species of Polytrichastrum sect. Aporotheca are recognized once more within Polytrichum .