Summary
The advent of embryophytes (land plants) is among the most important evolutionary breakthroughs in Earth history. It irreversibly changed climates and biogeochemical processes on a global scale; it allowed all eukaryotic terrestrial life to evolve and to invade nearly all continental environments. Before this work, the earliest unequivocal embryophyte traces were late Darriwilian (late Middle Ordovician; c. 463–461 million yr ago (Ma)) cryptospores from Saudi Arabia and from the Czech Republic (western Gondwana).
Here, we processed Dapingian (early Middle Ordovician, c. 473–471 Ma) palynological samples from Argentina (eastern Gondwana).
We discovered a diverse cryptospore assemblage, including naked and envelope‐enclosed monads and tetrads, representing five genera.
Our discovery reinforces the earlier suggestion that embryophytes first evolved in Gondwana. It indicates that the terrestrialization of plants might have begun in the eastern part of Gondwana. The diversity of the Dapingian assemblage implies an earlier, Early Ordovician or even Cambrian, origin of embryophytes. Dapingian to Aeronian (Early Silurian) cryptospore assemblages are similar, suggesting that the rate of embryophyte evolution was extremely slow during the first c. 35–45 million yr of their diversification. The Argentinean cryptospores predate other cryptospore occurrences by c. 8–12 million yr, and are currently the earliest evidence of plants on land.
The advent of wood (secondary xylem) is a major event of the Paleozoic Era, facilitating the evolution of large perennial plants. The first steps of wood evolution are unknown. We describe two small Early Devonian (407 to 397 million years ago) plants with secondary xylem including simple rays. Their wood currently represents the earliest evidence of secondary growth in plants. The small size of the plants and the presence of thick-walled cortical cells confirm that wood early evolution was driven by hydraulic constraints rather than by the necessity of mechanical support for increasing height. The plants described here are most probably precursors of lignophytes.
The emergence of the seed habit in the Middle Paleozoic was a decisive evolutionary breakthrough. Today, seed plants are the most successful plant lineage, with more than 250,000 living species. We have identified a middle Givetian (385 million years ago) seed precursor from Belgium predating the earliest seeds by about 20 million years. Runcaria is a small, radially symmetrical, integumented megasporangium surrounded by a cupule. The megasporangium bears an unopened distal extension protruding above the multilobed integument. This extension is assumed to be involved in anemophilous pollination. Runcaria sheds new light on the sequence of character acquisition leading to the seed.
Recent molecular clock data suggest with highest probability a Cambrian origin of Embryophyta (also called land plants), indicating that their terrestrialization most probably started about million years ago. The fossil record of the 'Cambrian explosion' was limited to marine organisms and not visible in the plant fossil record. The most significant changes in early land plant evolution occurred during the Ordovician. For instance, the earliest bryophytelike cryptospores and the oldest fragments of the earliest land plants come from the Middle and Late Ordovician, respectively. Organic geochemistry studies on biomarker compositions hint at a transition from green algae to land plants during the 'Great Ordovician Biodiversification Event' (GOBE). The colonization of the terrestrial realms by land plants clearly had an impact on marine ecosystems. Interactions between the terrestrial and marine biospheres have been proposed and the radiation of land plants potentially impacted on CO2 and O2 concentrations and on global climate. In addition, the shift of strontium isotopes during the Ordovician is probably linked to changing terrestrial landscapes, affected by the first massive land invasion of eukaryotic terrestrial life. The land plants seem unaffected by the first global mass extinction at the end of the Ordovician that eliminated many marine invertebrate taxa.
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