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UW-Madison BOTANY 940 - The Origin and Early Evolution of Plants on Land

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Nature © Macmillan Publishers Ltd 1997NATURE|VOL 389|4 SEPTEMBER 1997 33review articleThe origin and early evolution ofplants on landPaul Kenrick & Peter R. Crane........................................................................................................................................................................................................................................................The origin and early evolution of land plants in the mid-Palaeozoic era, between about 480 and 360 million years ago,was an important event in the history of life, with far-reaching consequences for the evolution of terrestrial organismsand global environments. A recent surge of interest, catalysed by palaeobotanical discoveries and advances in thesystematics of living plants, provides a revised perspective on the evolution of early land plants and suggests newdirections for future research.The origin and early diversification of land plants marks an intervalof unparalleled innovation in the history of plant life. From a simpleplant body consisting of only a few cells, land plants (liverworts,hornworts, mosses and vascular plants) evolved an elaborate two-phase life cycle and an extraordinary array of complex organs andtissue systems. Specialized sexual organs (gametangia), stems withan intricate fluid transport mechanism (vascular tissue), structuraltissues (such as wood), epidermal structures for respiratory gasexchange (stomates), leaves and roots of various kinds, diversespore-bearing organs (sporangia), seeds and the tree habit had allevolved by the end of the Devonian period. These and otherinnovations led to the initial assembly of plant-dominated terres-trial ecosystems, and had a great effect on the global environment.Early ideas on the origin of land plants were based on livinggroups, but since the discovery of exceptionally well-preserved fossilplants in the Early Devonian Rhynie Chert, research has focusedalmost exclusively on the fossil record of vascular plants1,2. Duringthe 1970s, syntheses of palaeobotanical and stratigraphic dataemphasized the Late Silurian and Devonian periods as the criticalinterval during which the initial diversification of vascular plantsoccurred1,2, and identified a group of simple fossils (rhyniophytes,such as Cooksonia and Rhynia) as the likely ancestral forms2. Theyalso supported earlier hypotheses of two main lines of evolution:one comprising clubmosses (Fig. 1f) and extinct relatives, the otherincluding all other living vascular plants (ferns, horsetails and seedplants; Fig. 1g–j) and related fossils1,2. During the past two decades,the discovery of fossil spores from as far back as the mid-Ordovicianperiod3, improved knowledge of living green algae4,5, renewedinterest in the phylogenetic position of other relevant groups suchas mosses and liverworts5, and advances in molecular systema-tics5–14, together with unexpected new data on the structure andbiology of Silurian and Devonian fossils15–25, have provided abroader perspective on the origin of a land flora26. These new dataindicate that the early diversification of land plants substantiallypre-dates the Late Silurian to Early Devonian, and suggest that themain basal lineages originated over a period of more than 100million years (Myr).Patterns in the early fossil recordEvidence on the origin and diversification of land plants has comemainly from dispersed spores and megafossils. Gray recognizedthree new plant-based epochs (Eoembryophytic, Eotracheophyticand Eutracheophytic) spanning the origin and early establishmentof land plants: each is characterized by the relative abundance ofspore types and megafossils3. This synthesis highlights diversifica-tion and floral change in the Ordovician and Silurian3,27,28, andemphasizes a major discrepancy between evidence from spores andmegafossils: unequivocal land plant megafossils are first recognizedin the fossil record roughly 50 Myr after the appearance of land plantspores.Eoembryophytic (mid-Ordovician [early Llanvirn: ,476 Myr] toEarly Silurian [late Llandovery: ,432 Myr])3. Spore tetrads (com-prising four membrane-bound spores; Fig. 2d) appear over a broadgeographic area in the mid-Ordovician and provide the first goodevidence of land plants3,26,29. The combination of a decay-resistantwall (implying the presence of sporopollenin) and tetrahedralconfiguration (implying haploid meiotic products) is diagnosticof land plants. The precise relationships of the spore producerswithin land plants are controversial, but evidence of tetrads andother spore types (such as dyads) in Late Silurian and Devonianmegafossils16,30, as well as data on spore wall ultrastructure25and thestructure of fossil cuticles31, support previous suggestions of a landflora of liverwort-like plants (Fig. 1c)3. Some early spores andcuticles may also represent extinct transitional lineages betweencharophycean algae (Fig. 1a, b) and liverworts (Box 1), but preciseunderstanding of their affinities is hindered by the dearth ofassociated megafossils.Eotracheophytic (Early Silurian [latest Llandovery: ,432 Myr] toEarly Devonian [mid Lochkovian: ,402 Myr])3. The early Silurian(latest Llandovery) marks the beginning of a decline in diversity oftetrads and a rise to dominance of individually dispersed, simplespores, which are found in several basal land plant groups (such ashornworts, some mosses, and early vascular plants)3. Althoughtetrads remain dominant in some Early Devonian localities fromnorthwestern Europe32, the elaboration of simple spores and turn-over of spore ‘species’3provide evidence of increasing land plantdiversity and vegetational change. Although spores have beenobserved in Silurian megafossils, the affinities of most dispersedforms remain unknown, indicating that substantial land plantdiversity is currently undetected in the megafossil record30.The earliest unequivocal land plant megafossils are from the mid-Silurian of northern Europe33, and lowermost Upper Silurian ofBolivia34and Australia35, and the uppermost Silurian of north-western China36. Early assemblages include clubmosses (such asBaragwanathia) and related early fossils (such as zosterophylls,some species of Cooksonia), and various other plants of uncertainaffinity (such as Salopella and Hedeia; Fig. 3). These data documentan influx into land plant communities of diverse but generally small(usually less than 10 cm tall) organisms related to vascular plants(Fig. 3). Exceptions to the


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UW-Madison BOTANY 940 - The Origin and Early Evolution of Plants on Land

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