review article The origin and early evolution of plants on land Paul 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 organisms and global environments. A recent surge of interest, catalysed by palaeobotanical discoveries and advances in the systematics of living plants, provides a revised perspective on the evolution of early land plants and suggests new directions for future research. The origin and early diversification of land plants marks an interval Eoembryophytic (mid-Ordovician [early Llanvirn: ϳ476 Myr] to of unparalleled innovation in the history of plant life. From a simple Early Silurian [late Llandovery: ϳ432 Myr])3. Spore tetrads (com- plant body consisting of only a few cells, land plants (liverworts, prising four membrane-bound spores; Fig. 2d) appear over a broad hornworts, mosses and vascular plants) evolved an elaborate two- geographic area in the mid-Ordovician and provide the first good phase life cycle and an extraordinary array of complex organs and evidence of land plants3,26,29. The combination of a decay-resistant tissue systems. Specialized sexual organs (gametangia), stems with wall (implying the presence of sporopollenin) and tetrahedral an intricate fluid transport mechanism (vascular tissue), structural configuration (implying haploid meiotic products) is diagnostic tissues (such as wood), epidermal structures for respiratory gas of land plants. The precise relationships of the spore producers exchange (stomates), leaves and roots of various kinds, diverse within land plants are controversial, but evidence of tetrads and spore-bearing organs (sporangia), seeds and the tree habit had all other spore types (such as dyads) in Late Silurian and Devonian evolved by the end of the Devonian period. These and other megafossils16,30, as well as data on spore wall ultrastructure25 and the innovations led to the initial assembly of plant-dominated terres- structure of fossil cuticles31, support previous suggestions of a land trial ecosystems, and had a great effect on the global environment. flora of liverwort-like plants (Fig. 1c)3. Some early spores and Early ideas on the origin of land plants were based on living cuticles may also represent extinct transitional lineages between groups, but since the discovery of exceptionally well-preserved fossil charophycean algae (Fig. 1a, b) and liverworts (Box 1), but precise plants in the Early Devonian Rhynie Chert, research has focused understanding of their affinities is hindered by the dearth of almost exclusively on the fossil record of vascular plants1,2. During associated megafossils. the 1970s, syntheses of palaeobotanical and stratigraphic data Eotracheophytic (Early Silurian [latest Llandovery: ϳ432 Myr] to emphasized the Late Silurian and Devonian periods as the critical Early Devonian [mid Lochkovian: ϳ402 Myr])3. The early Silurian interval during which the initial diversification of vascular plants (latest Llandovery) marks the beginning of a decline in diversity of occurred1,2, and identified a group of simple fossils (rhyniophytes, tetrads and a rise to dominance of individually dispersed, simple such as Cooksonia and Rhynia) as the likely ancestral forms2. They spores, which are found in several basal land plant groups (such as also supported earlier hypotheses of two main lines of evolution: hornworts, some mosses, and early vascular plants)3. Although one comprising clubmosses (Fig. 1f) and extinct relatives, the other tetrads remain dominant in some Early Devonian localities from including all other living vascular plants (ferns, horsetails and seed northwestern Europe32, the elaboration of simple spores and turn- plants; Fig. 1g–j) and related fossils1,2. During the past two decades, over of spore ‘species’3 provide evidence of increasing land plant the discovery of fossil spores from as far back as the mid-Ordovician diversity and vegetational change. Although spores have been period3, improved knowledge of living green algae4,5, renewed observed in Silurian megafossils, the affinities of most dispersed interest in the phylogenetic position of other relevant groups such forms remain unknown, indicating that substantial land plant as mosses and liverworts5, and advances in molecular systema- diversity is currently undetected in the megafossil record30. tics5–14, together with unexpected new data on the structure and The earliest unequivocal land plant megafossils are from the mid- biology of Silurian and Devonian fossils15–25, have provided a Silurian of northern Europe33, and lowermost Upper Silurian of broader perspective on the origin of a land flora26. These new data Bolivia34 and Australia35, and the uppermost Silurian of north- indicate that the early diversification of land plants substantially western China36. Early assemblages include clubmosses (such as pre-dates the Late Silurian to Early Devonian, and suggest that the Baragwanathia) and related early fossils (such as zosterophylls, main basal lineages originated over a period of more than 100 some species of Cooksonia), and various other plants of uncertain million years (Myr). affinity (such as Salopella and Hedeia; Fig. 3). These data document an influx into land plant communities of diverse but generally small Patterns in the early fossil record (usually less than 10 cm tall) organisms related to vascular plants Evidence on the origin and diversification of land plants has come (Fig. 3). Exceptions to the generally small size include the clubmoss mainly from dispersed spores and megafossils. Gray recognized Baragwanathia37 and the large and much-branched Pinnatiramosus three new plant-based epochs (Eoembryophytic, Eotracheophytic from the early Silurian of China38. The habit and branching of and Eutracheophytic) spanning the origin and early establishment Pinnatiramosus is similar to that of green algae in the Caulerpales, of land plants: each is characterized by the relative abundance of but the presence of tracheid-like tubes is inconsistent with this spore types and megafossils3. This synthesis highlights diversifica- interpretation39. Additional details, including conclusive data on tion and floral change in the Ordovician and Silurian3,27,28, and reproductive structures, are needed to clarify the relationships of emphasizes a major discrepancy between evidence from spores and this enigmatic plant. megafossils: unequivocal land plant megafossils are first recognized Data from northern Europe, Siberia, Podolia (southwestern in the fossil record roughly 50 Myr after the appearance of land plant Ukraine), Libya, Vietnam, Bolivia, Australia and Xinjiang and spores. Yunnan (China) document increasing land plant diversity into Nature © Macmillan Publishers Ltd 1997 NATURE | VOL 389 | 4 SEPTEMBER 1997 33 review article 33–36,40 the base of the Devonian . These fossils, together with the among land plants, including the capacity to produce sporo- relative chronology implicit in current hypotheses of relationship, pollenin, cutin, phenolic compounds and the glycolate oxidase imply a minimum mid-Silurian origin for several important vas- pathway4,48. However, the absence of well-developed sporophytes, cular plant groups (Box 1; Fig. 4). gametophytes with sexual organs of land plant type, cuticle and Eutracheophytic (Early Devonian [late Lochkovian: ϳ398 Myr] to non-motile, airborne, sporopollenin-walled spores suggests that mid-Permian [ϳ256 Myr])3. In the Early Devonian (late Lochko- these innovations evolved during the transition to the land4,18. In vian) the diversity of spores and megafossils increased contrast to animal groups, the entire multicellular diploid phase of dramatically29,40–42. Early assemblages include the classic floras the plant life cycle probably evolved in a terrestrial setting. from the Rhynie Chert20,43,44, the Gaspe´ Peninsula of eastern The transition from an aqueous to a gaseous medium exposed Canada43,44, New York State43,44, the Rhine Valley of Germany45, plants to new physical conditions that resulted in key physiological Belgium46, Australia35 and Yunnan Province (China)33, which docu- and structural changes. Important metabolic pathways leading to ment a substantial increase in vascular plant diversity, including the lignins, flavenoids, cutins and plant hormones in vascular plants appearance and early diversification of many important living probably arose from pre-existing elements of primary metabolism groups. in charophycean algae and bryophytes4. Although the evolution of these pathways is poorly understood, possible phenolic precursors Building a land plant have been detected in charophycean algae4,31, and elements of auxin Phylogenetic studies favour a single origin of land plants from metabolism have been recognized in mosses and hornworts49. charophycean green algae (Box 1). Based on the ecology of living Phylogenetic studies predict that early land plants were small and species, a freshwater origin of land plants seems likely, but direct morphologically simple, and this hypothesis is borne out by fossil evidence from the fossil record is inconclusive as mid-Palaeozoic evidence (Fig. 3). Early fossils bear a strong resemblance to the charophytes are found in both freshwater and, more commonly, simple spore-producing phase of living mosses and liverworts (Fig. marine facies47. Living charophycean algae (Fig. 1a, b) possess 1d, e and 5)16,26,50,51, and