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II. 13 Major Events in the Evolution of Land Plants Peter R. Crane and Andrew B. Leslie School of Forestry & Environmental S

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II. 13 Major Events in the Evolution of Land Plants Peter R. Crane and Andrew B. Leslie School of Forestry & Environmental S 11/30/118/9/11- 1 II. 13 Major Events in the Evolution of Land Plants Peter R. Crane and Andrew B. Leslie School of Forestry & Environmental Studies, Yale University OUTLINE 1. Phylogenetic framework 2. Origin and diversification of land plants 3. Origin and diversification of vascular plants 4. Origin and diversification of seed plants 5. Origin and diversification of flowering plants 6. Innovation in the land plant body 7. Innovation in land plant reproduction 8. Co-evolution with animals 9. Patterns of extinction Although land plants represent merely one branch in the eukaryotic tree of life, they are essential to the energetics and functioning of terrestrial ecosystems. Land plants appear to have arisen from a single colonization of the land surface around 450 million years ago. In the early phases of this colonization, plant innovations centered on the elaboration of a new kind of plant body capable of withstanding the rigors of life on land and exploiting the new opportunities that terrestrial existence provided. Subsequently, this phase of vegetative innovation was followed by successive transformations of the reproductive system, for example resulting in seeds and flowers, which facilitated increasingly efficient reproduction and dispersal. The unfolding of land plant diversification from a single origin makes it possible to understand all living groups in a relatively simple phylogenetic framework, in which increasingly less inclusive groups are characterized by successive innovations in plant structure and biology. 11/30/118/9/11- 2 GLOSSARY Alternation of generations – A type of life cycle with multicellular organisms in both the haploid and diploid phases. The diploid phase (sporophyte) produces haploid spores by meiosis that later germinate and develop into the haploid phase (gametophyte), which produces gametes by mitosis. Gamete fusion (fertilization) gives rise to a diploid zygote, and marks the transition from the haploid to diploid phase. Heterospory - The earliest land plants, as well as many living “pteridophytes”, were homosporous, meaning that their sporophytes produced haploid spores of a single size that could each germinate to produce bisexual gametophytes. In contrast, several extinct and extant lineages are heterosporous, meaning they produce two types of spores: larger megaspores, which develop into gametophytes (megagameophytes) that produce only female gametes, and smaller microspores, which develop into gametophytes (microgametophytes) producing only produce male gametes. Typically, these two types of spores are produced in separate sporangia (megasporangia and microsporangia respectively) Seed – The seed can be considered an extreme form of heterospory in which a single megaspore develops within a megasporangium that never opens to release the spore. In seed plants, this megasporangium is further enveloped by a protective covering called the integument, and the whole structure is termed an ovule. The ovule becomes a seed upon fertilization, and at maturity it contains an embryo, an accompanying food source, and a protective seed coat. Vascular tissue – Vascular tissues are specialized cells that transport water and nutrients through the plant body. The xylem, or water conducting tissue, is principally composed of cells called tracheids (or similar but modified cells called fibers or vessels) that are dead at maturity and have walls that are typically thickened by the deposition of the complex biopolymer lignin. The phloem, which conducts sugar and nutrients through the plant, contains living transport cells called sieve cells as well as other cell types. 11/30/118/9/11- 3 1. PHYLOGENETIC FRAMEWORK A phylogenetic framework in which to understand the eleven major groups of living land plants was originally developed from structural data and has been confirmed by analyses based on molecular sequences (Figure 1). Plants are a monophyletic subgroup of eukaryotes defined by the presence of the photosynthetic pigments chlorophylls a and b, the storage of starch in plastids (chloroplasts), and several other features. In addition to land plants, this definition also includes freshwater and marine organisms often grouped together as “green algae” and contrasts with treatments in which plants are defined more narrowly as synonymous with land plants. Molecular and structural data, including characteristics of cell division, support the placement of certain freshwater “charophycean green algae” (Coleochaetae, Chara) as the closest relatives of land plants; these groups together form a clade called the streptophytes. The land plant clade, or embryophytes, is composed of several major monophyletic groups that are widely used in discussions of plant evolution (Figure 1), including vascular plants (tracheophytes), seed plants (spermatophytes), and flowering plants (angiosperms). There are also corresponding paraphyletic groups (see Chapter II.1) at each level. For example, “green algae” are those plants that are not land plants, “bryophytes” are those land plants that are not vascular plants, “pteridophytes” are those vascular plants that are not seed plants, and “gymnosperms” are those seed plants that are not flowering plants. Analyses of molecular data suggest that living “gymnosperms” (conifers, cycads, Ginkgo, Gnetales) may comprise a monophyletic group although when extinct seed plants are included, “gymnosperms” are clearly paraphyletic. Within flowering plants, phylogenetic analyses support monocots (such as grasses and palm trees) as a monophyletic group, but “dicots” are now known to be paraphyletic. Two major monophyletic groups, eudicots and eumagnoliids, together account for almost all species previously treated as dicots. 2. ORIGIN AND DIVERSIFICATION OF EARLY LAND PLANTS 11/30/118/9/11- 4 Land plants are distinguished from “green algae” by a suite of reproductive and vegetative innovations, many of which are important in overcoming shortages of water. In land plants, the egg is formed and fertilized in a specialized flask-like structure called the archegonium within which the young embryo begins its development. Land plants also have desiccation resistant spore walls impregnated with the complex biopolymer sporopollenin; this enables their reproductive progagules to survive drying and disperse among suitable environments. The land plant body is covered in a waxy cuticle that prevents water loss, and all land plant groups except liverworts also have stomata, which are pores in the cuticle that are used to regulate the exchange of gases and water vapor with the atmosphere. Spore-like microfossils that may have been produced by plants or other eukaryotes are known from as early as the Middle Cambrian (ca. 510 Ma), although their exact affinities are unclear. Spores that were most likely produced by embryophytes appear around the Middle Ordovician (ca. 475 Ma), with forms that are broadly similar to those of some living “bryophytes”. Beginning around the same time, and continuing through much of the Silurian (ca. 443-416 Ma), the fossil record preserves a variety of enigmatic organic sheets and tubes which are suggestive of land plant cuticle and simple water conducting tissues. Such structures provide further evidence that the diversification of early land plants was underway, even though our knowledge of the plants involved is extremely fragmentary (see Chapter II.10). Macroscopic evidence of terrestrial plants is scarce until the Middle to Late Silurian (ca. 420 Ma), when small branching axes bearing multiple sporangia appear in the fossil record. These fossils represent the first known appearance of a major clade, the polysporangiophytes, which exhibit an important innovation in the vegetative plant body. While living “bryophyte” groups (hornworts, liverworts, mosses) produce a morphologically diverse array of sporophytes, they are all small, unbranched structures that bear a single sporangium at their tip. In contrast, the branched sporophytes of polysporangiophytes can produce multiple sporangia from a single embryo. Unlike the situation in “bryophytes”, the larger sporophytes of at least some early polysporangiophytes were also probably nutritionally independent of their corresponding gametophyte. Polysporangiophyte fossils become increasingly common in the latest part 11/30/118/9/11- 5 of the Silurian (ca. 416 Ma) and into the Early Devonian, where a glimpse into early polysporangiate diversity is provided by the classic earliest Devonian Rhynie Chert locality in Scotland (ca. 413 Ma). This assemblage preserves an early terrestrial ecosystem in exquisite detail, including arthropods, fungi, polysporangiophytes, and early representatives of a polysporangiophyte subgroup, the vascular plants, which were to become the most important constituent of later terrestrial ecosystems. 3. ORIGIN AND DIVERSIFICATION OF VASCULAR PLANTS Living vascular plants are distinguished from hornworts, liverworts, and mosses by their specialized vascular tissues (see glossary) and their larger and more elaborate sporophyte. Rhynie Chert polysporangiophytes exhibit a mixture of features that appear to reflect various stages in the evolution of these tissues and structures. The gametophyte and sporophyte of at least some Rhynie Chert plants were similar in size and morphological complexity, which is unlike the lifecycle of any living terrestrial plant and may reflect an intermediate stage between the small sporophytes of “bryophytes” and the earliest polysporangiophytes (some Cooksonia species) and the more elaborate
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