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Polysporangiophyte

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Polysporangiophyte
Temporal range:LlandoveryorWenlockto Recent
Reconstruction ofAglaophyton,illustrating bifurcating axes with terminal sporangia, and rhizoids.
Modern polysporangiophyte,monarch fernis avascular plant.
Scientific classificationEdit this classification
Kingdom: Plantae
Clade: Embryophytes
Clade: Polysporangiophytes
Kenrick & Crane (1997)
Subgroups

Polysporangiophytes,also calledpolysporangiatesor formallyPolysporangiophyta,are plants in which the spore-bearing generation (sporophyte) has branching stems (axes) that bearsporangia.The name literally means 'many sporangia plant'. Thecladeincludes all land plants (embryophytes) except for thebryophytes(liverworts, mosses and hornworts) whose sporophytes are normally unbranched, even if a few exceptional cases occur.[1]While the definition is independent of the presence ofvascular tissue,all living polysporangiophytes also have vascular tissue, i.e., arevascular plantsor tracheophytes. Extinct polysporangiophytes are known that have no vascular tissue and so are not tracheophytes.

Early polysporangiophytes[edit]

History of discovery[edit]

Paleobotanists distinguish between micro- and megafossils. Microfossils are primarilyspores,either single or in groups. Megafossils are preserved parts of plants large enough to show structure, such as stem cross-sections or branching patterns.[2]

Dawson,a Canadian geologist and paleobotanist, was the first to discover and describe a megafossil of a polysporangiophyte. In 1859 he published a reconstruction of aDevonianplant, collected as a fossil from theGaspé regionof Canada, which he namedPsilophytonprinceps.The reconstruction shows horizontal and upright stem-like structures; no leaves or roots are present. The upright stems or axes branch dichotomously and have pairs of spore-forming organs (sporangia) attached to them. Cross-sections of the upright axes showed thatvascular tissuewas present. He later described other specimens. Dawson's discoveries initially had little scientific impact; Taylor et al. speculate that this was because his reconstruction looked very unusual and the fossil was older than was expected.[3]

From 1917 onwards,Robert KidstonandWilliam H. Langpublished a series of papers describing fossil plants from theRhynie chert– a fine-grained sedimentary rock found near the village of Rhynie,Aberdeenshire,now dated to thePragianof the Lower Devonian (around411 to 408million years ago). The fossils were better-preserved than Dawson's, and showed clearly that these early land plants did indeed consist of generally naked vertical stems arising from similar horizontal structures. The vertical stems were dichotomously branched with some branches ending in sporangia.[3]

Since these discoveries, similar megafossils have been discovered in rocks ofSilurianto mid-Devonian age throughout the world, including Arctic Canada, the eastern US, Wales, the Rhineland of Germany, Kazakhstan, Xinjiang and Yunnan in China, and Australia.[4]

As of 2019,Eohostimella,dated to theLlandovery epoch(444 to 433million years ago), is one of the earliest fossils that has been identified as a polysporangiophyte.[5][6]Fossils assigned to the genusCooksonia,which is more certainly a polysporangiophyte, have been dated to the succeedingWenlock epoch(433 to 427million years ago).[7][8]

Taxonomy[edit]

The concept of the polysporangiophytes, more formally called Polysporangiophyta, was first published in 1997 by Kenrick and Crane.[9](The taxobox at the right represents their view of the classification of the polysporangiophytes.) The defining feature of thecladeis that the sporophyte branches and bears multiple sporangia. This distinguishes polysporangiophytes fromliverworts,mossesandhornworts,which have unbranched sporophytes each with a single sporangium. Polysporangiophytes may or may not havevascular tissue– those that do arevascular plantsor tracheophytes.[citation needed]

Prior to that, most of the early polysporangiophytes had been placed in a singleorder,Psilophytales, in theclassPsilophyta, established in 1917 by Kidston and Lang.[10]The livingPsilotaceae,the whisk-ferns, were sometimes added to the class, which was then usually called Psilopsida.[11]

As additional fossils were discovered and described, it became apparent that the Psilophyta were not a homogeneous group of plants. In 1975, Banks expanded on his earlier 1968 proposal that split it into three groups at therankof subdivision.[12][13]These groups have since been treated at the ranks of division,[14]class[15]and order.[16]A variety of names have been used, which the table below summarizes.

Alternative names for Banks' three groups of early polysporangiophytes
Division Subdivision Class Order Informal
Rhyniophyta Rhyniophytina Rhyniopsida (Rhyniophytopsida)[17] Rhyniales rhyniophyte
Zosterophyllophyta Zosterophyllophytina Zosterophyllopsida Zosterophyllales zosterophyll (zosterophyllophyte)
Trimerophyta (Trimerophytophyta)[18] Trimerophytina (Trimerophytophytina) Trimeropsida (Trimerophytopsida) Trimerophytales trimerophyte

For Banks,rhyniophytescomprised simple leafless plants with terminal sporangia (e.g.,Cooksonia,Rhynia) withcentrarchxylem;zosterophyllscomprised plants with lateral sporangia that split distally (away from their attachment) to release their spores, and hadexarchstrands of xylem (e.g.,Gosslingia).Trimerophytescomprised plants with large clusters of downwards curving terminal sporangia that split along their length to release their spores and had centrarch xylem strands (e.g.,Psilophyton).[19]

Research by Kenrick and Crane that established the polysporangiophytes concluded that none of Banks' three groups weremonophyletic.The rhyniophytes included "protracheophytes", which were precursors to vascular plants (e.g.,Horneophyton,Aglaophyton); basal tracheophytes (e.g.,Stockmansella,Rhyniagwynne-vaughanii); and plants allied to the lineages that led to the living club-mosses and allies as well as ferns and seed plants (e.g.,Cooksoniaspecies). The zosterophylls did contain a monophyletic clade, but some genera previously included in the group fell outside this clade (e.g.,Hicklingia,Nothia). The trimerophytes wereparaphyleticstem groupsto both thecrown groupfernsand the crown groupseed plants.[20][21]

Many researchers have urged caution in the classification of early polysporangiophytes. Taylor et al. note that basal groups of early land plants are inherently difficult to characterize since they share many characters with all later-evolving groups (i.e., have multipleplesiomorphies).[14]In discussing the classification of the trimerophytes, Berry and Fairon-Demaret say that reaching a meaningful classification requires "a breakthrough in knowledge and understanding rather than simply a reinterpretation of the existing data and the surrounding mythology".[22]Kenrick and Crane's cladograms have been questioned – see theEvolutionsection below.

As of February 2011,there appears to be no complete Linnean (i.e., rank-based) classification for early polysporangiophytes that is consistent with Kenrick and Crane's cladistic analysis and subsequent research, though Cantino et al. have published aPhylocodeclassification.[23]Banks' three groups continue to be used for convenience.[14]

Phylogeny[edit]

A majorcladisticstudy of land plants was published in 1997 by Kenrick and Crane; this both established the concept of the polysporangiophytes and presented a view of theirphylogeny.[9]Since 1997 there have been continual advances in understanding plant evolution, using RNA and DNA genome sequences and chemical analyses of fossils (e.g., Taylor et al. 2006[24]), resulting in revisions to this phylogeny.

In 2004, Crane et al. published a simplifiedcladogramfor the polysporangiophytes (which they call polysporangiates), based on a number of figures in Kenrick and Crane (1997).[10]Their cladogram is reproduced below (with some branches collapsed into 'basal groups' to reduce the size of the diagram). Their analysis is not accepted by other researchers; for example Rothwell and Nixon say that the broadly defined fern group (moniliforms or monilophytes) is not monophyletic.[25]

polysporangiophytes

†Horneophytopsida(Caia,Horneophyton,Tortilicaulis)

†Aglaophyton

tracheophytes

†Rhyniaceae(Huvenia,Rhynia,Stockmansella)

† basal groups (Aberlemniacaledonica[=Cooksonia caledonica],Cooksonia pertoni)

 † basal groups 

Cooksoniacambrensis,Renalia,Sartilmania,Uskiella,Yunia

lycophytes
       

†Hicklingia

 †basal groups 

Adoketophyton,Discalis,Distichophytum(=Rebuchia),Gumuia,Huia,Zosterophyllummyretonianum,Z. llanoveranum, Z. fertile

 †'core'zosterophylls 

Zosterophyllumdivaricatum,Tarella,Oricilla,Gosslingia,Hsua,Thrinkophyton,Protobarinophyton,Barinophytonobscurum,B. citrulliforme,Sawdonia,Deheubarthia,Konioria,Anisophyton,Serrulacaulis,Crenaticaulis

 †basal groups 

Nothia,Zosterophyllumdeciduum

 lycopsids 

extant and extinct members

euphyllophytes

†Eophyllophyton

† basal groups (Psilophytoncrenulatum, Ps. dawsonii)

moniliforms(ferns; extant and extinct members)

† basal groups (Pertica,Tetraxylopteris)

spermatophytes(seed plants; extant and extinct members)

More recently, Gerrienne and Gonez have suggested a slightly different characterization of the early diverging polysporangiophytes:[26]

Polysporangiophytes

†'Protracheophytes'

†Paratracheophytes

Eutracheophytes

The paraphyletic protracheophytes, such asAglaophyton,have water-conducting vessels like those of mosses, i.e., without cells containing thickened cell walls. The paratracheophytes, a name intended to replace Rhyniaceae or Rhyniopsida, have 'S-type' water-conducting cells, i.e., cells whose walls are thickened but in a much simpler fashion than those of true vascular plants, the eutracheophytes.[26]

Evolution[edit]

Reconstruction of the sporophyte ofCooksonia pertoni,which Boyce considers too small to be self-sufficient. The axes (stems) are around 0.1 mm in diameter.

If the cladogram above is correct it has implications for the evolution of land plants. The earliest diverging polysporangiophytes in the cladogram are theHorneophytopsida,a clade at the 'protracheophyte' grade that is sister to all other polysporangiophytes. They had essentially an isomorphicalternation of generations(meaning that the sporophytes and gametophytes were equally free living), which might suggest that both the gametophyte-dominant life style of bryophytes and the sporophyte-dominant life style of vascular plants evolved from this isomorphic condition. They were leafless and did not have true vascular tissues. In particular, they did not havetracheids:elongated cells that help transport water and mineral salts, and that develop a thicklignifiedwall at maturity that provides mechanical strength. Unlike plants at thebryophytegrade, their sporophytes were branched.[27]

According to the cladogram, the genusRhyniaillustrates two steps in the evolution of modern vascular plants. Plants have vascular tissue, albeit significantly simpler than modern vascular plants. Their gametophytes are distinctly smaller than their sporophytes (but have vascular tissue, unlike almost all modern vascular plants).[28]

The remainder of the polysporangiophytes divide into two lineages, a deep phylogenetic split that occurred in the early to mid Devonian, around 400 million years ago. Both lineages have developed leaves, but of different kinds. The lycophytes, which make up less than 1% of the species of living vascular plants, have small leaves (microphyllsor more specifically lycophylls), which develop from an intercalarymeristem(i.e., the leaves effectively grow from the base). The euphyllophytes are by far the largest group of vascular plants, in terms of both individuals and species. Euphyllophytes have large 'true' leaves (megaphylls), which develop through marginal or apical meristems (i.e., the leaves effectively grow from the sides or the apex). (Horsetailshave secondarily reduced megaphylls resembling microphylls.)[29]

Both the cladogram derived from Kenrick and Crane's studies and its implications for the evolution of land plants have been questioned by others. A 2008 review by Gensel notes that recently discovered fossil spores suggest that tracheophytes were present earlier than previously thought; perhaps earlier than supposedstem groupmembers. Spore diversity suggests that there were many plant groups, of which no other remains are known. Some early plants may have had heteromorphic alternation of generations, with later acquisition of isomorphic gametophytes in certain lineages.[30]

The cladogram above shows the 'protracheophytes' diverging earlier than the lycophytes; however, lycophytes were present in the Ludfordian stage of the Silurian around430 to 420million years ago,long before the 'protracheophytes' found in theRhynie chert,dated to the Pragian stage of the Devonian around410million years ago.[31]However, it has been suggested that the poorly preservedEohostimella,found in deposits ofEarly Silurianage (Llandovery, around440 to 430million years ago), may be a rhyniophyte.[6]

Boyce has shown that the sporophytes of someCooksoniaspecies and allies ('cooksonioids') had stems that were too narrow to have supported sufficient photosynthetic activity for them to be independent of their gametophytes – inconsistent with their position in the cladogram.[32]

Because thestomatainmosses,hornwortsand polysporangiophytes are viewed as homologous, it has been suggested they belong in a natural group namedstomatophytes.[33]

Theevolutionary history of plantsis far from settled.[citation needed]

Notes and references[edit]

  1. ^Harrison, C. Jill; Morris, Jennifer L. (2017)."The origin and early evolution of vascular plant shoots and leaves".Philosophical Transactions of the Royal Society B: Biological Sciences.373(1739): 20160496.doi:10.1098/rstb.2016.0496.PMC5745332.PMID29254961.
  2. ^See, e.g., Edwards, D. & Wellman, C. (2001), "Embryophytes on Land: The Ordovician to Lochkovian (Lower Devonian) Record" inGensel & Edwards 2001,pp. 3–28
  3. ^abTaylor, T.N.; Taylor, E.L. & Krings, M. (2009),Paleobotany, The Biology and Evolution of Fossil Plants(2nd ed.), Amsterdam; Boston: Academic Press,ISBN978-0-12-373972-8,p. 225ff
  4. ^Gensel, P.G. & Edwards, D., eds. (2001),Plants invade the Land: Evolutionary & Environmental Perspectives,New York: Columbia University Press,ISBN978-0-231-11161-4,chapters 2, 6, 7
  5. ^Edwards, D. & Wellman, C. (2001), "Embryophytes on Land: The Ordovician to Lochkovian (Lower Devonian) Record", in Gensel, P. & Edwards, D. (eds.),Plants Invade the Land: Evolutionary and Environmental Perspectives,New York: Columbia University Press, pp. 3–28,ISBN978-0-231-11161-4,p. 4
  6. ^abNiklas, Karl J. (1979), "An Assessment of Chemical Features for the Classification of Plant Fossils",Taxon,28(5/6): 505–516,doi:10.2307/1219787,JSTOR1219787
  7. ^Edwards, D. & Feehan, J. (1980), "Records ofCooksonia-type sporangia from late Wenlock strata in Ireland ",Nature,287(5777): 41–42,Bibcode:1980Natur.287...41E,doi:10.1038/287041a0,S2CID7958927
  8. ^Libertín, Milan; Kvaček, Jiří; Bek, Jiří; Žárský, Viktor & Štorch, Petr (2018),"Sporophytes of polysporangiate land plants from the early Silurian period may have been photosynthetically autonomous",Nature Plants,4(5): 269–271,doi:10.1038/s41477-018-0140-y,PMID29725100,S2CID19151297
  9. ^abKenrick & Crane 1997a,pp. 139–140, 249
  10. ^abCrane, P.R.; Herendeen, P. & Friis, E.M. (2004), "Fossils and plant phylogeny",American Journal of Botany,91(10): 1683–99,doi:10.3732/ajb.91.10.1683,PMID21652317
  11. ^Taylor, Taylor & Krings 2009,p. 226.
  12. ^Banks, H.P. (1968), "The early history of land plants", in Drake, E.T. (ed.),Evolution and Environment: A Symposium Presented on the Occasion of the 100th Anniversary of the Foundation of Peabody Museum of Natural History at Yale University,New Haven, Conn.: Yale University Press, pp. 73–107,cited inBanks 1980
  13. ^Banks, H.P. (1975), "Reclassification of Psilophyta",Taxon,24(4): 401–413,doi:10.2307/1219491,JSTOR1219491
  14. ^abcTaylor, Taylor & Krings 2009,p. 227
  15. ^See, e.g., Berry, C.M. & Fairon-Demaret, M. (2001), "The Middle Devonian Flora Revisited", inGensel & Edwards 2001,pp. 120–139
  16. ^Banks, H.P. (1970),Evolution and Plants of the Past,London: Macmillan Press,ISBN978-0-333-14634-7,p. 57
  17. ^Although this name has appeared in some sources, e.g.,Knoll, Andrew H. (1998-01-01), "Review ofThe Origin and Early Diversification of Land Plants: A Cladistic Studyby Paul Kenrick; Peter Crane ",International Journal of Plant Sciences,159(1): 172–174,doi:10.1086/297535,JSTOR2474949,it appears to be a mistake, as it is not in accord with Article 16 of theInternational Code of Botanical Nomenclature.
  18. ^The name is based on the genusTrimerophyton;Article 16.4 of theInternational Code of Botanical Nomenclatureallows thephytonpart to be omitted before-ophyta,-ophytina,and-opsida.
  19. ^Banks, H.P. (1980), "The role ofPsilophytonin the evolution of vascular plants ",Review of Palaeobotany and Palynology,29:165–176,doi:10.1016/0034-6667(80)90056-1
  20. ^Kenrick, Paul & Crane, Peter R. (1997a),The Origin and Early Diversification of Land Plants: A Cladistic Study,Washington, D.C.: Smithsonian Institution Press,ISBN978-1-56098-730-7
  21. ^Kenrick, P. & Crane, P.R. (1997b), "The origin and early evolution of plants on land",Nature,389(6646): 33–39,Bibcode:1997Natur.389...33K,doi:10.1038/37918,S2CID3866183
  22. ^Berry, C. M. & Fairon-Demaret, M. (2001), "The Middle Devonian Flora Revisited", inGensel & Edwards 2001,p. 127
  23. ^Cantino, Philip D.; James A. Doyle; Sean W. Graham; Walter S. Judd; Richard G. Olmstead; Douglas E. Soltis; Pamela S. Soltis; Michael J. Donoghue (2007), "Towards a Phylogenetic Nomenclature of Tracheophyta",Taxon,56(3): 822–846,doi:10.2307/25065865,JSTOR25065865
  24. ^Taylor, D.W.; Li, Hongqi; Dahl, Jeremy; Fago, F.J.; Zinneker, D.; Moldowan, J.M. (2006),"Biogeochemical evidence for the presence of the angiosperm molecular fossil oleanane in Paleozoic and Mesozoic non-angiospermous fossils",Paleobiology,32(2): 179–90,doi:10.1666/0094-8373(2006)32[179:BEFTPO]2.0.CO;2,ISSN0094-8373,S2CID83801635
  25. ^Rothwell, G.W. & Nixon, K.C. (2006), "How Does the Inclusion of Fossil Data Change Our Conclusions about the Phylogenetic History of Euphyllophytes?",International Journal of Plant Sciences,167(3): 737–749,doi:10.1086/503298,S2CID86172890
  26. ^abGerrienne, P. & Gonez, P. (2011), "Early evolution of life cycles in embryophytes: A focus on the fossil evidence of gametophyte/sporophyte size and morphological complexity",Journal of Systematics and Evolution,49:1–16,doi:10.1111/j.1759-6831.2010.00096.x,S2CID29795245
  27. ^Bateman, R.M.; Crane, P.R.; Dimichele, W.A.; Kenrick, P.R.; Rowe, N.P.; Speck, T.; Stein, W.E. (1998), "Early Evolution of Land Plants: Phylogeny, Physiology, and Ecology of the Primary Terrestrial Radiation",Annual Review of Ecology and Systematics,29(1): 263–92,doi:10.1146/annurev.ecolsys.29.1.263,S2CID44508826,p. 270
  28. ^Kerp, H.; Trewin, N.H.; Hass, H. (2004), "New gametophytes from the Early Devonian Rhynie chert",Transactions of the Royal Society of Edinburgh: Earth Sciences,94(4): 411–28,doi:10.1017/s026359330000078x,S2CID128629425
  29. ^Pryer, K.M.; Schuettpelz, E.; Wolf, P.G.; Schneider, H.; Smith, A.R.; Cranfill, R. (2004), "Phylogeny and evolution of ferns (monilophytes) with a focus on the early leptosporangiate divergences",American Journal of Botany,91(10): 1582–98,doi:10.3732/ajb.91.10.1582,PMID21652310,pp. 1582–3
  30. ^Gensel, Patricia G. (2008), "The Earliest Land Plants",Annu. Rev. Ecol. Evol. Syst.,39:459–77,doi:10.1146/annurev.ecolsys.39.110707.173526,pp. 470–2
  31. ^Kotyk, M.E.; Basinger, J.F.; Gensel, P.G.; de Freitas, T.A. (2002), "Morphologically complex plant macrofossils from the Late Silurian of Arctic Canada",Am. J. Bot.,89(6): 1004–1013,doi:10.3732/ajb.89.6.1004,PMID21665700
  32. ^Boyce, C.K. (2008), "How green wasCooksonia?The importance of size in understanding the early evolution of physiology in the vascular plant lineage ",Paleobiology,34(2): 179–194,doi:10.1666/0094-8373(2008)034[0179:HGWCTI]2.0.CO;2,ISSN0094-8373,S2CID36688488
  33. ^Ligrone, R.; Duckett, J.G.; Renzaglia, K.S. (2012)."Major transitions in the evolution of early land plants: a bryological perspective".Annals of Botany.109(5): 851–71.doi:10.1093/aob/mcs017.PMC3310499.PMID22356739.

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