Piecing together the eophytes - a new group of ancient plants containing cryptospores.
Devonian
cryptospores
eophytes
food-conducting cells
fossil
phloem
sieve element
Journal
The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884
Informations de publication
Date de publication:
02 2022
02 2022
Historique:
received:
03
05
2021
accepted:
18
08
2021
pubmed:
23
11
2021
medline:
25
3
2022
entrez:
22
11
2021
Statut:
ppublish
Résumé
The earliest evidence for land plants comes from dispersed cryptospores from the Ordovician, which dominated assemblages for 60 million years. Direct evidence of their parent plants comes from minute fossils in Welsh Borderland Upper Silurian to Lower Devonian rocks. We recognize a group that had forking, striated axes with rare stomata terminating in valvate sporangia containing permanent cryptospores, but their anatomy was unknown especially regarding conducting tissues. Charcoalified fossils extracted from the rock using HF were selected from macerates and observed using scanning electron microscopy. Promising examples were split for further examination and compared with electron micrographs of the anatomy of extant bryophytes. Fertile fossil axes possess central elongate cells with thick walls bearing globules, occasional strands and plasmodesmata-sized pores. The anatomy of these cells best matches desiccation-tolerant food-conducting cells (leptoids) of bryophytes. Together with thick-walled epidermal cells and extremely small size, these features suggest that these plants were poikilohydric. Our new data on conducting cells confirms a combination of characters that distinguish the permanent cryptospore-producers from bryophytes and tracheophytes. We therefore propose the erection of a new group, here named the Eophytidae (eophytes).
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1440-1455Commentaires et corrections
Type : CommentIn
Informations de copyright
© 2021 The Authors. New Phytologist © 2021 New Phytologist Foundation.
Références
Barclay WJ, Davies JR, Hillier RD, Waters RA. 2015. Lithostratigraphy of the old red sandstone successions of the Anglo-Welsh basin. British geological survey research report. Keyworth, UK: British Geological Survey.
Boyce CK. 2008. How green was Cooksonia? The importance of size in understanding the early evolution of physiology in the vascular plant lineage. Paleobiology 34: 179-194.
Brodribb TJ, Carriquí M, Delzon S, McAdam SAM, Holbrook NM. 2020. Advanced vascular function discovered in a widespread moss. Nature Plants 6: 273-279.
Burgess ND. 1991. Silurian cryptospores and miospores from the type Llandovery area, south-west Wales. Palaeontology 34: 575-599.
Burr FA, Evert RF. 1973. Some aspects of sieve element structure and development in Selaginella kraussiana. Protoplasma 78: 81-97.
Cavalier-Smith T. 2018. Kingdom Chromista and its eight phyla: a new synthesis emphasising periplastid protein targeting, cytoskeletal and periplastid evolution, and ancient divergences. Protoplasma 255: 297-357.
Chase MW, Reveal JL. 2009. A phylogenetic classification of the land plants to accompany APG III. Botanical Journal of the Linnean Society 161: 122-127.
Duckett JG, Ligrone R, Renzaglia K, Pressel S. 2014. Pegged and smooth rhizoids in complex thalloid liverworts (Marchantiopsida): Structure, function and evolution. Botanical Journal of the Linnean Society 174: 68-92.
Duckett JG, Pressel S. 2018. The evolution of the stomatal apparatus: intercellular spaces and sporophyte water relations in bryophytes-two ignored dimensions. Philosophical Transactions of the Royal Society B: Biological Sciences 373: 20160498.
Edwards D. 2003. Xylem in early tracheophytes. Plant, Cell & Environment 26: 57-72.
Edwards D. 2004. Embryophytic sporophytes in the Rhynie and Windyfield cherts. Transactions of the Royal Society of Edinburgh Earth Sciences 94: 397-410.
Edwards D, Axe L. 2000. Novel conducting tissues in Lower Devonian plants. Botanical Journal of the Linnean Society 134: 383-399.
Edwards D, Axe L. 2004. Anatomical evidence in the detection of the earliest wildfires. Palaios 19: 113-128.
Edwards D, Axe L, Duckett JG. 2003. Diversity in conducting cells in early land plants and comparisons with extant bryophytes. Botanical Journal of the Linnean Society 141: 297-347.
Edwards D, Fanning U, Richardson JB. 1994. Lower Devonian coalified sporangia from Shropshire: Salopella Edwards & Richardson and Tortilicaulis Edwards. Botanical Journal of the Linnean Society 116: 89-110.
Edwards D, Kenrick P. 2015. The early evolution of land plants, from fossils to genomics: a commentary on Lang (1937) ‘On the plant-remains from the Downtonian of England and Wales'. Philosophical Transactions of the Royal Society B: Biological Sciences 370: 20140343.
Edwards D, Morris JL, Axe L, Duckett JG, Taylor WA, Kenrick P, Pressel S. 2021. Earliest records of plant transfer cells in Lower Devonian fossils. New Phytologist. doi: 10.1111/nph.17704.
Edwards D, Morris JL, Richardson JB, Axe L, Davies KL. 2012b. Notes on sporangia and spore masses containing tetrads or monads from the Lower Devonian (Lochkovian) of the Welsh Borderland, U.K. Review of Palaeobotany and Palynology 179: 56-85.
Edwards D, Morris JL, Richardson JB, Kenrick P. 2014. Cryptospores and cryptophytes reveal hidden diversity in early land floras. New Phytologist 202: 50-78.
Edwards D, Richardson JB, Axe L, Davies KL. 2012a. A new group of Early Devonian plants with valvate sporangia containing sculptured permanent dyads. Botanical Journal of the Linnean Society 168: 229-257.
Edwards D, Wellman CH, Axe L. 1999. Tetrads in sporangia and spore masses from the upper Silurian and Lower Devonian of the Welsh Borderland. Botanical Journal of the Linnean Society 130: 111-156.
Evert FE, Mierzwa RJ. 1989. The cell wall-plasmalemma interface in sieve tubes of barley. Planta 177: 24-34.
Field KJ, Duckett JG, Cameron DD, Pressel S. 2015. Stomatal density and aperture in non-vascular land plants are non-responsive to above-ambient atmospheric CO2 concentrations. Annals of Botany 115: 915-922.
Glasspool IJ, Edwards D, Axe L. 2006. Charcoal in the Early Devonian: a wildfire-derived Konservat-Lagerstätte. Review of Palaeobotany and Palynology 142: 131-136.
Gray J. 1985. The microfossil record of early land plants: advances in understanding of early terrestrialization, 1970-1984. Philosophical Transactions of the Royal Society of London B 309: 167-195.
Gray J. 1993. Major Paleozoic land plant evolutionary bio-events. Palaeogeography, Palaeoclimatology, Palaeoecology 104: 143-169.
Gray J, Boucot AJ. 1971. Early Silurian spore tetrads from New York: earliest New World evidence for vascular plants? Science 173: 918-921.
Habgood KS. 2000. Two cryptospore-bearing land plants from the Lower Devonian (Lochkovian) of the Welsh Borderland. Botanical Journal of the Linnean Society 133: 203-227.
Harris BJ, Harrison CJ, Hetherington AM, Williams TA. 2020. Phylogenomic evidence for the monophyly of bryophytes and the reductive evolution of stomata. Current Biology 30: 2001-2012.e2002.
Hébant C. 1977. The conducting tissues of bryophytes. Vaduz, Germany: Cramer.
Jensen KH, Berg-Sørensen K, Bruus H, Holbrook NM, Liesche J, Schulz A, Zwieniecki MA, Bohr T. 2016. Sap flow and sugar transport in plants. Reviews of Modern Physics 88: 35007.
Johnson NG. 1985. Early Silurian palynomorphs from the Tuscarora Formation in central Pennsylvania and their paleobotanical and geological significance. Review of Palaeobotany and Palynology 45: 307-360.
Kenrick P, Crane PR. 1991. Water-conducting cells in early fossil land plants: implications for the early evolution of tracheophytes. Botanical Gazette 152: 335-356.
Kenrick P, Crane PR. 1997. The origin and early diversification of land plants: a cladistic study. Washington, DC, USA: Smithsonian Institution Press.
Kenrick P, Edwards D, Dales RC. 1991. Novel ultrastructure in water-conducting cells of the Lower Devonian plant Sennicaulis hippocrepiformis. Palaeontology 34: 751-766.
Kubásek J, Hájek T, Duckett J, Pressel S, Šantrůček J. 2021. Moss stomata do not respond to light and CO2 concentration but facilitate carbon uptake by sporophytes: a gas exchange, stomatal aperture, and 13C-labelling study. New Phytologist 230: 1815-1828.
Leebens-Mack JH, Barker MS, Carpenter EJ, Deyholos MK, Gitzendanner MA, Graham SW, Grosse I, Li Z, Melkonian M, Mirarab S et al. 2019. One thousand plant transcriptomes and the phylogenomics of green plants. Nature 574: 679-685.
Ligrone R, Duckett JG. 1994. Thallus differentiation in the marchantialean liverwort Asterella wilmsii (Steph.) with particular reference to longitudinal arrays of endoplasmic microtubules in the inner cells. Annals of Botany 73: 577-586.
Ligrone R, Duckett JG. 1996. Development of water-conducting cells in the antipodal liverwort Symphyogyna africana (Metzgeriales). New Phytologist 132: 603-615.
Ligrone R, Duckett JG, Renzaglia KS. 2000. Conducting tissues and phyletic relationships of bryophytes. Philosophical Transactions of the Royal Society B: Biological Sciences 355: 795-813.
Ligrone R, Duckett JG, Renzaglia KS. 2012. Major transitions in the evolution of early land plants: a bryological perspective. Annals of Botany 109: 851-871.
Lucas WJ, Groover A, Lichtenberger R, Furuta K, Yadav S-R, Helariutta Y, He X-Q, Fukuda H, Kang J, Brady SM et al. 2013. The plant vascular system: evolution, development and functions. Journal of Integrative Plant Biology 55: 294-388.
Merced A, Renzaglia KS. 2017. Structure, function and evolution of stomata from a bryological perspective. Bryophyte Diversity and Evolution 39: 7-20.
Miller CJ, Duckett JG. 1979. A study of stellar ultrastructure in the heterosporous fern Marsilea quadrifolia L. Annals of Botany 44: 231-238.
Mishler BD, Churchill SP. 1985. Transition to a land flora: phylogenetic relationships of the green algae and bryophytes. Cladistics 1: 305-328.
Morris JL, Edwards D, Richardson JB. 2018. The advantages and frustration of a plant Lagerstätte as illustrated by a new taxon from the Lower Devonian of the Welsh Borderland, UK. In: Krings M, Harper CJ, Cuneo NR, Rothwell GW, eds. Transformative Paleobotany: papers to commemorate the life and legacy of Thomas N Taylor. London, UK: Academic Press, 49-67.
Morris JL, Edwards D, Richardson JB, Axe L. 2012. New dyad-producing plants from the Lower Devonian (Lochkovian) of the Welsh Borderland. Botanical Journal of the Linnean Society 169: 569-595.
Morris JL, Edwards D, Richardson JB, Axe L, Davies KL. 2011. New plant taxa from the Lower Devonian (Lochkovian) of the Welsh Borderland, with a hypothesis on the relationship between hilate and trilete spore producers. Review of Palaeobotany and Palynology 167: 51-81.
Morris JL, Puttick MN, Clark JW, Edwards D, Kenrick P, Pressel S, Wellman CH, Yang Z, Schneider H, Donoghue PCJ. 2018. The timescale of early land plant evolution. Proceedings of the National Academy of Sciences, USA 115: E2274-E2283.
Niklas KJ. 1992. Plant biomechanics: an engineering approach to plant form and function. Chicago, IL, USA: University of Chicago Press.
Pirani JR, Prado J. 2012. Embryopsida, a new name for the class of land plants. Taxon 61: 1096-1098.
Pressel S, Duckett JG, Ligrone R, Proctor MCF. 2009. Effects of de- and rehydration in desiccation-tolerant liverworts: a cytological and physiological study. International Journal of Plant Sciences 170: 182-199.
Pressel S, Ligrone R, Duckett JG. 2006. Effects of de- and rehydration on food-conducting cells in the moss Polytrichum formosum: a cytological study. Annals of Botany 98: 67-76.
Pressel S, Renzaglia KS, Clymo RS, Duckett JG. 2018. Hornwort stomata do not respond actively to exogeneous and environmental cues. Annals of Botany 122: 45-57.
Proctor MCF, Oliver MJ, Wood AJ, Alpert P, Stark LR, Cleavitt NL, Mishler BD. 2007. Desiccation-tolerance in bryophytes: a review. Bryologist 110: 595-621.
Puttick MN, Morris JL, Williams TA, Cox CJ, Edwards D, Kenrick P, Pressel S, Wellman CH, Schneider H, Pisani D et al. 2018. The interrelationships of land plants and the nature of the ancestral embryophyte. Current Biology 28: 733-745.
Raven JA. 1977. The evolution of vascular plants in relation to supracellular transport processes. Advances in Botanical Research 5: 153-219.
Raven JA. 1993. The evolution of vascular plants in relation to quantitative functioning of dead water-conducting cells and stomata. Biological Reviews 68: 337-363.
Raven JA. 1999. The minimum size of seeds and spores in relation to the ontogeny of homoiohydric plants. Functional Ecology 13: 5-14.
Raven JA. 2003. Long-distance transport in non-vascular plants. Plant, Cell & Environment 26: 73-85.
Renzaglia K, Browning W, Merced A. 2020. With over 60 independent losses, stomata are expendable in mosses. Frontiers in Plant Science 11: 567. 10.3389/fpls.2020.00567.
Renzaglia KS, Crandall-Stotler B, Pressel S, Duckett JG, Schuette S, Strother PK. 2015a. Permanent spore dyads are not ‘a thing of the past’: on their occurrence in the liverwort Haplomitrium (Haplomitriopsida). Botanical Journal of the Linnean Society 179: 658-669.
Renzaglia KS, Duff RJ, Nickrent DL, Garbary DJ. 2000. Vegetative and reproductive innovations of early land plants: implications for a unified phylogeny. Philosophical Transactions of the Royal Society of London 355: 769-793.
Renzaglia KS, Garbary DJ. 2001. Motile gametes of land plants: diversity, development, and evolution. Critical Reviews in Plant Sciences 20: 107-213.
Renzaglia KS, Lopez RA, Johnson EE. 2015b. Callose is integral to the development of permanent tetrads in the liverwort Sphaerocarpos. Planta 241: 615-627.
Renzaglia KS, Villarreal JC, Piatkowski BT, Lucas JR, Merced A. 2017. Hornwort stomata: architecture and fate shared with 400-million-year-old fossil plants without leaves. Plant Physiology 174: 788-797.
Retallack GJ. 2019. Ordovician land plants and fungi from Douglas Dam, Tennessee. Palaeobotanist 68: 173-205.
Richardson JB. 1988. Late Ordovician and Early Silurian cryptospores and miospores from northeast Libya. In: El-Arnauti A, Owens B, Thusu B, eds. Subsurface palynostratigraphy of northeast Libya. Benghazi, Libya: Garyounis University Publications, 89-109.
Richardson JB. 1996. Taxonomy and classification of some new Early Devonian cryptospores from England. Special Papers in Palaeontology 55: 7-40.
Richardson JB, McGregor DC. 1986. Silurian and Devonian spore zones of the Old Red Sandstone Continent and adjacent regions. Bulletin of the Geological Survey of Canada 364: 1-79.
Robinson-Beers K, Evert RF. 1991. Fine structure of plasmodesmata in mature leaves of sugarcane. Planta 187: 307-318.
Scheirer DC. 1980. Differentiation of bryophyte conducting tissues: structure and histochemistry. Bulletin of the Torrey Botanical Club 107: 298-307.
Scheirer DC. 1990. Mosses. In: Behnke H-D, Sjolund RD, eds. Sieve elements: comparative structure, induction and development. Berlin, Germany: Springer-Verlag, 19-33.
Sousa F, Civáň P, Brazão J, Foster PG, Cox CJ. 2020. The mitochondrial phylogeny of land plants shows support for Setaphyta under composition-heterogeneous substitution models. PeerJ-Life and Environment 8: e8995.
Steemans P. 2000. Miospore evolution from the Ordovician to the Silurian. Review of Palaeobotany and Palynology 113: 189-196.
Steemans P, le Hérissé A, Bozdogan N. 1996. Ordovician and Silurian cryptospores and miospores from southeastern Turkey. Review of Palaeobotany and Palynology 93: 35-76.
Steemans P, Lepot K, Marshall CP, Le Hérissé A, Javaux EJ. 2010. FTIR characterisation of the chemical composition of Silurian miospores (cryptospores and trilete spores) from Gotland, Sweden. Review of Palaeobotany and Palynology 162: 577-590.
Strother PK. 2000. Cryptospores: the origin and early evolution of the terrestrial flora. In: Gastaldo RA, DiMichele WA, eds. Phanerozoic terrestrial ecosystems. Columbus, OH, USA: The Paleontological Society, 3-20.
Strother PK, Al-Hajri S, Traverse A. 1996. New evidence for land plants from the lower Middle Ordovician of Saudi Arabia. Geology 24: 55-58.
Strother PK, Traverse A. 1979. Plant microfossils from Llandoverian and Wenlockian rocks of Pennsylvania. Palynology 3: 1-22.
Strother PK, Traverse A, Vecoli M. 2015. Cryptospores from the Hanadir Shale Member of the Qasim Formation, Ordovician (Darriwilian) of Saudi Arabia: taxonomy and systematics. Review of Palaeobotany and Palynology 212: 97-110.
Taylor WA. 1995. Ultrastructure of Tetrahedraletes medinensis (Strother and Traverse) Wellman and Richardson from the Upper Ordovician of southern Ohio. Review of Palaeobotany and Palynology 85: 183-187.
Taylor WA. 1996. Ultrastructure of lower Paleozoic dyads from southern Ohio. Review of Palaeobotany and Palynology 92: 269-279.
Taylor WA. 1997. Ultrastructure of lower Paleozoic dyads from southern Ohio II: Dyadospora murusattenuata, functional and evolutionary considerations. Review of Palaeobotany and Palynology 97: 1-8.
Tomescu AMF, Wyatt SE, Hasebe M, Rothwell GW. 2014. Early evolution of the vascular plant body plan - the missing mechanisms. Current Opinion in Plant Biology 2014: 126-136.
Turgeon R. 2010. The role of phloem loading reconsidered. Plant Physiology 152: 1817-1823.
Turland NJ, Wiersema JH, Barrie FR, Greuter W, Hawksworth DL, Herendeen PS, Knapp S, Kusber W-H, Li D-Z, Marhold K et al., 2018. International Code of Nomenclature for algae, fungi, and plants (Shenzhen Code) adopted by the Nineteenth International Botanical Congress Shenzhen, China, July 2017. Regnum Vegetabile. Glashütten, Germany: Koeltz Botanical Books.
Van Bel AJE. 2003. The phloem, a miracle of ingenuity. Plant, Cell & Environment 26: 125-149.
Warmbrodt RD, Evert RF. 1974. Structure and development of the sieve element in the stem of Lycopodium lucidulum. American Journal of Botany 61: 267-277.
Warmbrodt RD, Evert RF. 1979. Comparative leaf structure of six species of eusporangiate and protoleptosporangiate ferns. Botanical Gazette 140: 153-167.
Wellman CH. 1996. Cryptospores from the type area of the Caradoc series in Southern Britain. Special Papers in Palaeontology 55: 103-136.
Wellman CH, Ball AC. 2021. Early land plant phytodebris. In: Marret F, O’Keefe J, Osterloff J, Pound M, Shumilovskikh L eds. Applications of non-pollen palynomorphs: from palaeoenvironmental reconstructions to biostratigraphy. London, UK: Geological Society. Special Publications 511.
Wellman CH, Edwards D, Axe L. 1998a. Permanent dyads in sporangia and spore masses from the Lower Devonian of the Welsh Borderland. Botanical Journal of the Linnean Society 127: 117-147.
Wellman CH, Edwards D, Axe L. 1998b. Ultrastructure of laevigate hilate spores in sporangia and spore masses from the Upper Silurian and Lower Devonian of the Welsh Borderland. Philosophical Transactions of the Royal Society of London, B 353: 1983-2004.
Wellman CH, Gray J. 2000. The microfossil record of early land plants. Philosophical Transactions of the Royal Society B: Biological Sciences 355: 717-731.
Wellman CH, Osterloff PL, Mohiuddin U. 2003. Fragments of the earliest land plants. Nature 425: 282-285.
Wellman CH, Steemans P, Vecoli M. 2013. Chapter 29 Palaeophytogeography of Ordovician-Silurian land plants. Geological Society, London, Memoirs 38: 461-476.
Wickett NJ, Goffinet B. 2008. Origin and relationships of the myco-heterotrophic liverwort Cryptothallus mirabilis Malmb. (Metzgeriales, Marchantiophyta). Botanical Journal of the Linnean Society 156: 1-12.
Xue J-Z, Wang Q. 2011. Fusiformitheca, a new name for Fusitheca Wellman, Edwards et Axe, 1998, non Bonorden, 1864. Palaeoworld 20: 98.