A new approach for modelling water transport in fossil plants

In: IAWA Journal

ABSTRACT

The origin of xylem in the Silurian was a major step in plant evolution, leading to diverse growth forms with various mechanical and hydraulic properties. In the fossil record, these properties can only be investigated using models based on extant plant physiology. Regarding hydraulics, previous studies have considered either the properties of a single tracheid or of a set of independent tubes. Here, we use the analogy between the flow of water under tension in a plant and an electrical circuit to develop an extension of Wilson’s single tracheid model to the tissue scale. Upscaling to the tissue-level allows considering wood as a heterogeneous tissue by taking into account differences in tracheid density and the presence of rays. The new model provides a more biologically accurate representation of fossil wood hydraulic properties. The single tracheid and new tissue models are applied to two conspecific specimens of Callixylon (Progymnospermopsida, Archeopteridales) from the Late Devonian of Morocco. Differences are shown at the tissue level that cannot be suspected at the single tracheid level. Callixylon represents the first trees with a conifer-like wood and is a major component of Late Devonian floras world-wide. Our results show that the anatomical disparity of its wood might have led to hydraulic plasticity, allowing growth in various environmental conditions. More generally, the new tissue-model suggests that the various combinations of tracheid and ray sizes present in Palaeozoic plants might have led to a higher variety of ecophysiologies than suspected based solely on the properties of individual tracheids.

  • AlgeoTJ, SchecklerSE, MaynardJB. 2001. Effects of the Middle to Late Devonian spread of vascular land plants on weathering regimes, marine biotas and global climate. In: GenselPG, EdwardsD (eds.), Plants invade the land. Evolutionary & Environmental perspectives: 213–236. Columbia University Press, New York.

    • Search Google Scholar
    • Export Citation
  • BeckCB. 1962. Plants of the New Albany Shale. II. Callixylon arnoldii sp. nov. Brittonia14: 322–327. DOI: .

  • BeckCB. 1964. Predominance of Archaeopteris in Upper Devonian flora of western Catskills and adjacent Pennsylvania. Bot. Gaz.125: 126–128. DOI: .

  • BeckCB, CoyK, SchmidR. 1982. Observations on the fine structure of Callixylon wood. Am. J. Bot.69: 54–76. DOI: .

  • ChaveJ, CoomesD, JansenS, LewisSL, SwensonNG, ZanneAE. 2009. Towards a world-wide wood economics spectrum. Ecology Letters12: 351–366. DOI: .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • ChoatB, CobbAR, JansenS. 2008. Structure and function of bordered pits: new discoveries and impacts on whole-plant hydraulic function. New Phytol. 177: 608–626. DOI:

    • Crossref
    • Search Google Scholar
    • Export Citation
  • CichanMA. 1986. Conductance in the wood of selected Carboniferous plants. Paleobiology12: 302–310. DOI: .

  • ComstockJP, SperryJS. 2000. Tansley Review No. 119. Theoretical considerations of optimal conduit length for water transport in vascular plants. New Phytol. 148: 195–218. DOI: .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • CornetL, GerrienneP, Meyer-BerthaudB, PrestianniC. 2012. A Middle Devonian Callixylon (Archaeopteridales) from Ronquières, Belgium. Rev. Palaeobot. Palynol.183: 1–8. DOI: .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • CruiziatP, CochardH, AméglioT. 2002. Hydraulic architecture of trees: main concepts and results. Ann. For. Sci.59: 723–752. DOI: .

  • DecombeixA-L, Meyer-BerthaudB, GaltierJ. 2011. Transitional changes in arborescent lignophytes at the Devonian-Carboniferous boundary. J. Geol. Soc.168: 547–557. DOI: .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • EdwardsD.2003. Xylem in early tracheophytes. Plant Cell Environ.26: 57–72. DOI: .

  • EllmoreGS, EwersFW. 1985. Hydraulic conductivity in trunk xylem of elm, Ulmus americana. IAWA J.6: 303–307. DOI: .

  • GerrienneP, GenselPG, Strullu-DerrienC, LardeuxH, SteemansP, PrestianniC. 2011. A simple type of wood in two Early Devonian plants. Science333: 837. DOI: .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • HackeUG, SperryJS, PittermannJ. 2004. Analysis of circular bordered pit function. II. Gymnosperm tracheids with torus-margo pit membranes. Am. J. Bot.91: 386–400. DOI: .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • HajekP, KurjakD, von WühlischG, DelzonS, SchuldtB. 2016. Intraspecific variation in wood anatomical, hydraulic, and foliar traits in ten European beech provenances differing in growth yield. Front. Plant Sci.7: 791. DOI: .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • KenrickP, WellmanCH, SchneiderH, EdgecombeGD. 2012. A timeline for terrestrialization: consequences for the carbon cycle in the Palaeozoic. Phil. Trans. Roy. Soc. B: Biol. Sci.367: 519–536. DOI: .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • KimHK, ParkJ, HwangI. 2014. Investigating water transport through the xylem network in vascular plants. J. Experim. Bot.65: 1895–1904. DOI: .

  • LancashireJR, EnnosAR. 2002. Modelling the hydrodynamic resistance of bordered pits. J. Experim. Bot.53: 1485–1493. DOI: .

  • LemoigneY, IrinaA, SnigirevskayaN. 1983. Révision du genre Callixylon Zalessky 1911 (Archaeopteris) du Dévonien. Palaeontographica186B: 81–120.

    • Search Google Scholar
    • Export Citation
  • Martínez-VilaltaJ, MencucciniM, ÁlvarezX, CamachoJ, LoepfeL, PiñolJ. 2012. Spatial distribution and packing of xylem conduits. Am. J. Bot.99: 1189–1196. DOI: .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Meyer-BerthaudB, SchecklerSE, BousquetJ-L. 2000. The development of Archaeopteris: New evolutionary characters from the structural analysis of an Early Famennian trunk from southeast Morocco. Am. J. Bot.87: 456–468. DOI: .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Meyer-BerthaudB, SchecklerSE, WendtJ. 1999. Archaeopteris is the earliest modern tree. Nature398: 700–701. DOI: .

  • Meyer-BerthaudB, SoriaA, DecombeixA-L. 2010. The land plant cover in the Devonian: a reassessment of the evolution of the tree habit. In: VecoliM, ClémentG, Meyer-BerthaudB (eds.), The terrestrialization process: modelling complex interactions at the biospheregeosphere interface: 59–70. Geological Society, London, Special Publ. DOI: .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • MorrisH, PlavcováL, CveckoP, FichtlerE, GillinghamMAF, Martínez-CabreraHI, McGlinnD, WheelerE, ZhengJ, ZiemińskaK, JansenS. 2016. A global analysis of parenchyma tissue fractions in secondary xylem of seed plants. New Phytol.209: 1553–1565. DOI: .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • OrlovaOA, JurinaA. 2011. Genus Callixylon Zalessky (Archaeopteridophyta): main criteria for distinguishing its species and revision of its species composition. Paleontological J.45: 580 –589.

    • Search Google Scholar
    • Export Citation
  • PfautschS, HölttäT, MencucciniM. 2015. Hydraulic functioning of tree stems – Fusing ray anatomy, radial transfer and capacitance. Tree Physiol.35: 706–722. DOI: .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • PittermannJ, LimmE, RicoC, ChristmanMA. 2011. Structure–function constraints of tracheidbased xylem. A comparison of conifers and ferns. New Phytol.192: 449–461. DOI: .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • PittermannJ, SperryJS, HackeUG, WheelerJK, SikkemaEH. 2006. Inter-tracheid pitting and the hydraulic efficiency of conifer wood: the role of tracheid allometry and cavitation protection. Am. J. Bot.93: 1265–1273. DOI: .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • PittermannJ, StuartSA, DawsonTE, MoreauA. 2012. Cenozoic climate change shaped the evolutionary ecophysiology of the Cupressaceae conifers. Proc. Nat. Acad. Sci.109: 9647–9652. DOI: .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • RavenJA. 1984. Physiological correlates of the morphology of early vascular plants. Bot. J. Linn. Soc.88: 105–126. DOI: .

  • RavenJA. 1993. The evolution of vascular plants in relation to quantitative functioning of dead water-conducting cells and stomata. Biological Review68: 337–363.

    • Search Google Scholar
    • Export Citation
  • ReidDEB, SilinsU, MendozaC, LieffersVJ. 2005. A unified nomenclature for quantification and description of water conducting properties of sapwood xylem based on Darcy’s law. Tree Physiol.25: 993–1000. DOI: .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • RosnerS.2013. Hydraulic and biomechanical optimization in Norway spruce trunkwood – A review. IAWA J.34: 365–390. DOI: .

  • RothA, MosbruggerV. 1996. Numerical studies of water conduction in land plants: evolution of early stele types. Paleobiology22: 411–421. DOI: https://www.jstor.org/stable/2401097.

    • Search Google Scholar
    • Export Citation
  • RothA, MosbruggerV, NeugebauerHJ. 1994. Efficiency and evolution of water transport systems in higher plants: a modelling approach. I. The earliest land plants. Philos. Trans. Roy. Soc. London B345: 137–152. DOI: .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • RothA, MosbruggerV, WunderlinA. 1998. Computer simulations as a tool for understanding the evolution of water transport systems in land plants: a review and new data. Rev. Palaeobot. Palynol.102: 79–99. DOI: .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • SchultePJ, GibsonAC. 1988. Hydraulic conductance and tracheid anatomy in six species of extant seed plants. Canad. J. Bot.66: 1073–1079. DOI: .

  • SchultePJ, GibsonAC, NobelPS. 1987. Xylem anatomy and hydraulic conductance of Psilotum nudum. Am. J. Bot.74: 1438–1445. DOI: .

  • SperryJS, DonnellyJR, TyreeMT. 1988. A method for measuring hydraulic conductivity and embolism in xylem. Plant Cell Environ.11: 35–40. DOI: .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • SperryJS, HackeUG. 2004. Analysis of circular bordered pit function. I. Angiosperm vessels with homogeneous pit membranes. Am. J. Bot.91: 369–385. DOI: .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • SperryJS, MeinzerFC, McCullohKA. 2008. Safety and efficiency conflicts in hydraulic architecture: scaling from tissues to trees. Plant Cell Environ.31: 632–645. DOI: .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • SperryJS, StillerV, HackeUG. 2003. Xylem hydraulics and the soil–plant–atmosphere continuum. Agronomy J.95: 1362–1370.

  • SpicerR, GrooverA. 2010. Evolution of development of vascular cambia and secondary growth. New Phytol.186: 577–592. DOI: .

  • Strullu-DerrienC, KenrickP, BadelE, CochardH, TafforeauP. 2013. An overview of the hydraulic systems in early land plants. IAWA J.34: 333–351. DOI: .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Strullu-DerrienC, KenrickP, TafforeauP, CochardH, BonnemainJ-L, LeHérisséA, LardeuxH, BadelE. 2014. The earliest wood and its hydraulic properties documented in c. 407-million-year-old fossils using synchrotron microtomography. Bot. J. Linn. Soc.175: 423–437. DOI: .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • TanrattanaM, Meyer-BerthaudB, DecombeixA-L. 2018. Callixylon wendtii sp. nov., a new species of archeopteridalean progymnosperm from the Late Devonian of Anti-Atlas, Morocco. Earth and Environmental Science Transactions of the Royal Society of Edinburgh.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • TyreeMT. 1997. The Cohesion-Tension theory of sap ascent: current controversies. J. Experim. Bot.48: 1753–1765. DOI: .

  • TyreeMT, EwersFW. 1991. The hydraulic architecture of trees and other woody plants. New Phytol.119: 345–360. DOI: .

  • TyreeMT, ZimmermannMH. 2002. Xylem structure and the ascent of sap. Ed. 2. Springer, Berlin. 283 pp. DOI: .

  • Van den HonertTH. 1948. Water transport in plants as a catenary process. Discussions of the Faraday Society3: 146–153. DOI: .

  • VenturasMD, SperryJS, HackeUG. 2017. Plant xylem hydraulics: what we understand, current research, and future challenges. J. Integrative Plant Biol.59: 356–389. DOI: .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • WilsonJP. 2013. Modeling 400 million years of plant hydraulics. In: BushAM, PrussSB, PayneJL (eds.), Ecosystem paleobiology and geobiology; The Paleontological Society Short Course, October 26, 2013: 1–20. The Paleontological Society Papers. DOI: .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • WilsonJP. 2016. Hydraulics of Psilophyton and evolutionary trends in plant water transport after terrestrialization. Rev. Palaeobot. Palynol.227: 65–76. DOI: .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • WilsonJP, KnollAH. 2010. A physiologically explicit morphospace for tracheid-based water transport in modern and extinct seed plants. Paleobiology36: 335–355. DOI: .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • WilsonJP, KnollAH, HolbrookNM, MarshallCR. 2008. Modeling fluid flow in Medullosa, an anatomically unusual Carboniferous seed plant. Paleobiology34: 472–493. DOI: https://www.jstor.org/stable/20445610.

    • Search Google Scholar
    • Export Citation
  • ZimmermannMH. 1983. Xylem structure and the ascent of sap. Springer-Verlag, Berlin. 143 pp. DOI:

  • ZwienieckiMA, HolbrookNM. 1998. Diurnal variation in xylem hydraulic conductivity in white ash (Fraxinus americana L.), red maple (Acer rubrum L.) and red spruce (Picea rubens Sarg.). Plant Cell Environ. 21: 1173–1180. DOI: .

    • Crossref
    • Search Google Scholar
    • Export Citation

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