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The Structure and Function of Xylem in Seed-Free Vascular Plants: An Evolutionary Perspective

  • Jarmila Pittermann
  • James E. Watkins
  • Katharine L. Cary
  • Eric Schuettpelz
  • Craig Brodersen
  • Alan R. Smith
  • Alex Baer

Abstract

Water transport in seed-free vascular plants such as ferns and lycopods occurs through strands of primary xylem. In roots, rhizomes and fronds, the xylem and phloem are packaged in steles comprising either a single vascular bundle (protostele) or many such bundles (dictyosteles) that are variously arranged throughout the segment. Seed-free vascular plants, ferns in particular, are ecologically and morphologically diverse yet very little is known about the structure and function of their xylem. With few exceptions, the xylem of seed-free vascular plants consists of tracheids that are longer and wider than those of conifers, with abundant scalariform pitting present on conduit walls. Recent work indicates that the xylem of seed-free vascular plants may be at least as efficient as that of conifers and angiosperms due to large tracheids, tight conduit packing and permeable pit membranes. Hydraulic benefits may be amplified in some polyploids which exhibit significantly longer tracheids. However, the presence of adaptive xylem does not fully compensate for the absence of a cambial layer, secondary xylem and vessels. Indeed, developmental and in part vascular limits constrain the diversity of seed-free plant morphospace, especially as compared to angiosperms. The fossil record indicates that extinct lineages of seed-free vascular plants had more diverse xylem structures as well as secondary xylem. Few studies have addressed the resistance of seed-free vascular plants to drought-induced cavitation but given the recent evolution of fern epiphytes, ferns may be well adapted to episodic water deficit. Available data indicate that in ferns and lycophytes, narrow tracheids are less vulnerable to air entry than large ones; by extension, species with smaller conduits, such as epiphytes, may be less susceptible to cavitation. The functional significance of stelar arrangements of fern petioles is largely unexplored but mapping stelar patterns onto the fern phylogeny reveals that in the more derived eupolypod lineages, selection has favoured the evolution of simpler, less divided vascular networks.

Keywords

Water transport Cavitation Primary xylem Tracheid Fern Lycophyte Pteridophytes Stele Epiphytes Polyploidy Pit membrane 

Notes

Acknowledgments

We sincerely thank Dr. Uwe Hacke for the opportunity to contribute to this volume and for his comments on the manuscript. Dr. Robbin Moran’s assistance with preparation of Fig. 1.11 is much appreciated. The National Science Foundation is gratefully acknowledged for support of this work (JP, IOS-1258186).

References

  1. Agashe SN (1968) Phloem studies in the pteridophytes, part I. Equisetum. Am Fern J 58:74–77Google Scholar
  2. Alder NN, Pockman WT, Sperry JS, Nuismer S (1997) Use of centrifugal force in the study of xylem cavitation. J Exp Bot 48:665–674Google Scholar
  3. Arakaki M, Christin P-A, Nyffeler R, Lendel A, Eggli U, Ogburn RM, Spriggs E, Moore MJ, Edwards EJ (2011) Contemporaneous and recent radiations of the world’s major succulent plant lineages. Proc Natl Acad Sci U S A 108:8379–8384PubMedCentralPubMedGoogle Scholar
  4. Baack EJ, Stanton ML (2005) Ecological factors influencing tetraploid speciation in snow buttercups (Ranunculus adoneus): niche differentiation and tetraploid establishment. Evolution 59:1936–1944PubMedGoogle Scholar
  5. Barghoorn ES (1964) Evolution of cambium in geologica time. In: Zimmermann MH (ed) The formation of wood in forest trees. Academic, New York, pp 3–17Google Scholar
  6. Beck CB (1970) The appearance of gymnospermous structure. Biol Rev 45:379–400Google Scholar
  7. Beck CB (2010) An introduction to plant structure and development. Cambridge University Press, Cambridge, p 459Google Scholar
  8. Beck CB, Schmid R, Rothwell G (1982) Stelar morphology and the primary vascular system of seed plants. Bot Rev 48:691–815Google Scholar
  9. Boyce C, Cody G, Fogel M, Hazen R (2003) Chemical evidence for cell wall lignification and the evolution of tracheids in early Devonian plants. Int J Plant Sci 165:691–702.Google Scholar
  10. Bower FO (1923) The ferns (Filicales), vol 1, Analytical examination of the criteria of comparison. Cambridge University Press, Cambridge, p 359Google Scholar
  11. Brodersen CR, McElrone AJ, Choat B, Matthews MA, Shackel KA (2010) The dynamics of embolism repair in xylem: in vivo visualizations using high-resolution computed tomography. Plant Physiol 154:1088–1095PubMedCentralPubMedGoogle Scholar
  12. Brodersen CR, Lee EF, Choat B, Jansen S, Phillips RJ, Shackel KA, McElrone AJ, Matthews MA (2011) Automated analysis of three-dimensional xylem networks using high-resolution-computed-tomography. New Phytol 191:1168–1179PubMedGoogle Scholar
  13. Brodersen CR, Roark LC, Pittermann J (2012) The physiological implications of primary xylem organization in two ferns. Plant Cell Environ 35:1898–1911PubMedGoogle Scholar
  14. Brodersen C, Jansen S, Choat B, Rico C, Pittermann J (2014) Cavitation resistance in seedless vascular plants: the structure and function of interconduit pit membranes. Plant Physiol 165:895–904PubMedCentralPubMedGoogle Scholar
  15. Brodribb TJ, Feild TS (2010) Leaf hydraulic evolution led a surge in leaf photosynthetic capacity during early angiosperm diversification. Ecol Lett 13:175–183PubMedGoogle Scholar
  16. Brodribb TJ, Holbrook NM (2004) Stomatal protection against hydraulic failure: a comparison of co-existing ferns and angiosperms. New Phytol 162:663–670Google Scholar
  17. Brodribb TJ, McAdam SAM (2011) Passive origins of stomatal control in vascular plants. Science 331:582–585PubMedGoogle Scholar
  18. Brodribb TJ, Feild TS, Jordan GJ (2007) Leaf maximum photosynthetic rate and venation are linked by hydraulics. Plant Physiol 144:1890–1898PubMedCentralPubMedGoogle Scholar
  19. Buggs RJA, Pannell JR (2007) Ecological differentiation and diploid superiority across a moving ploidy contact zone. Evolution 61:125–140PubMedGoogle Scholar
  20. Calkin HW, Gibson AC, Nobel PS (1985) Xylem water potentials and hydraulic conductances in eight species of ferns. Can J Bot 63:632–637Google Scholar
  21. Canestraro BK, Moran RC, Watkins JE (2014) Reproductive and physiological ecology of climbing and terrestrial Polybotrya (Dryopteridaceae) at the La Selva Biological Station, Costa Rica. Int J Plant Sci 175:432–441Google Scholar
  22. Carlquist S, Schneider EL (2007) Tracheary elements in ferns: new techniques, observations and concepts. Am Fern J 97:199–211Google Scholar
  23. Choat B, Pittermann J (2009) New insights into bordered pit structure and cavitation resistance in angiosperms and conifers. New Phytol 182:557–560PubMedGoogle Scholar
  24. Choat B, Lahr EC, Melcher PJ, Zwieniecki MA, Holbrook NM (2005) The spatial pattern of air seeding thresholds in mature sugar maple trees. Plant Cell Environ 28:1082–1089Google Scholar
  25. Christman MA, Sperry JS, Adler F (2009) Testing the “rare pit” hypothesis for xylem cavitation resistance in three species of Acer. New Phytol 182:664–674PubMedGoogle Scholar
  26. Cichan MA (1985a) Vascular cambium and wood development in Carboniferous plants. I. Lepidodendrales. Am J Bot 72:1163–1176Google Scholar
  27. Cichan MA (1985b) Vascular cambium and wood development in Carboniferous plants. II. Sphenophyllum plurifoliatum Williamson and Scott (Sphenophyllales). Bot Gaz 146:395–403Google Scholar
  28. Cichan MA (1986) Conductance in the wood of selected Carboniferous plants. Paleobiology 12:302–310Google Scholar
  29. Coate JE, Schlueter JA, Whaley AM, Doyle JJ (2011) Comparative evolution of photosynthetic genes in response to polyploid and nonpolyploid duplication. Plant Physiol 155:2081–2095PubMedCentralPubMedGoogle Scholar
  30. Coomes DA, Allen RB, Bentley WA et al (2005). The hare, the tortoise and the crocodile: the ecology of angiosperm dominance, conifer persistence and fern filtering. J Ecol 93:918–935.Google Scholar
  31. Creese C, Lee A, Sack L (2011) Drivers of morphological diversity and distribution in the Hawaiian fern flora: trait associations with size, growth form, and environment. Am J Bot 98:1–11Google Scholar
  32. DeBodt S, Maere S, Van de Peer Y (2005) Genome duplication and the origin of angiosperms. Trends Ecol Evol 20:591–597Google Scholar
  33. Domec J-C, Lachenbruch B, Meinzer F, Woodruff D, Warren JM, McCulloh K (2008) Maximum height in a conifer is associated with conflicting requirements for xylem design. Proc Natl Acad Sci U S A 105:12069–12074PubMedCentralPubMedGoogle Scholar
  34. Dubuisson J-Y, Schneider H, Hennequin S (2009) Epiphytism in ferns: diversity and history. C R Biol 332:120–128PubMedGoogle Scholar
  35. Edwards DS (1986) Aglaophyton major, a non-vascular land-plant from the Devonian Rhynie Chert. Bot J Linn Soc 93:173–204Google Scholar
  36. Edwards EJ, Osborne CP, Stromberg CAE, Smith SA, C4 Grasses Consortium (2010) The origins of C4 grasslands: integrating evolutionary and ecosystem science. Science 328:587–591PubMedGoogle Scholar
  37. Fawcett JA, Maere S, Van de Peer Y (2009) Plants with double genomes might have had a better chance to survive the Cretaceous-Tertiary extinction event. Proc Natl Acad Sci U S A 106:5737–5742PubMedCentralPubMedGoogle Scholar
  38. Feild TS, Brodribb TJ, Iglesias A, Chatelet DS, Baresch A, Upchurch GR, Gomez G, Mohr BAR, Coiffard C, Kvacek J, Jaramillo C (2011) Fossil evidence for Cretaceous escalation in angiosperm leaf vein evolution. Proc Natl Acad Sci U S A 108:8363–8366PubMedCentralPubMedGoogle Scholar
  39. Fotedar RL, Shah JJ (1975) Phloem structure and development in Blechnum orientale. Am Fern J 65:52–60Google Scholar
  40. Gaupels F, Buhts A, Knauer T, Deshmukh S, Waller F, Van Bel AJE, Kogel K-H, Kehr J (2008) Adaptation of aphid stylectomy for analyses of proteins and mRNAs in barley phloem sap. J Exp Bot 59:3297–3306PubMedCentralPubMedGoogle Scholar
  41. George L, Bazzaz F (1999) The fern understory as an ecological filter: growth and survival of canopy-tree seedlings. Ecology 80:846–856Google Scholar
  42. Gerrienne P, Gensel PG, Strullu-Derrien C, Lardeux H, Steemans P, Prestianni C (2011) A simple type of wood in two early Devonian plants. Science 33:837Google Scholar
  43. Gullo MAL, Raimondo F, Crisafulli A, Salleo S, Nardini A (2010) Leaf hydraulic architecture and water relations of three ferns from contrasting light habitats. Funct Plant Biol 37:566–574Google Scholar
  44. Hacke UG, Sperry JS, Pockman WT, Davis SD, McCulloh KA (2001) Trends in wood density and structure are linked to prevention of xylem implosion by negative pressure. Oecologia 126:457–461Google Scholar
  45. Hacke U, Sperry J, Wheeler J, Castro L (2006) Scaling of angiosperm xylem structure with safety and efficiency. Tree Physiol 26:689–701Google Scholar
  46. Hacke UG, Sperry JS, Feild TS, Sano Y, Sikkema EH, Pittermann J (2007) Water transport in vesselless angiosperms: conducting efficiency and cavitation safety. Int J Plant Sci 168:1113–1126Google Scholar
  47. Hernandez-Hernandez V, Terrazas T, Mehltreter K, Angeles G (2012) Studies of petiolar anatomy in ferns: structural diversity and systematic significance of the circumendodermal band. Bot J Linn Soc 169:596–610Google Scholar
  48. Hietz P, Briones O (1998) Correlation between water relations and within-canopy distribution of epiphytic ferns in a Mexican cloud forest. Oecologia 114:305–316Google Scholar
  49. Jacobsen AL, Ewers FW, Pratt RB, Paddock WA, Davis SA (2005) Do xylem fibers affect vessel cavitation resistance? Plant Physiol 139:546–556PubMedCentralPubMedGoogle Scholar
  50. Jansen S, Choat B, Pletsers A (2009) Morphological variation of intervessel pit membranes and implications to xylem function in angiosperms. Am J Bot 96:409–419PubMedGoogle Scholar
  51. Jensen KH, Liesche J, Bohr T, Schulz A (2012) Universality of phloem transport in seed plants. Plant, Cell Environ 35:1065–1076Google Scholar
  52. Kao RH, Parker IM (2010) Coexisting cytotypes of Arnica cordifolia: morphological differentiation and local-scale distribution. Int J Plant Sci 171:81–89Google Scholar
  53. Kenrick P, Crane PR (1991) Water-conducting cells in early fossil land plants: implications for the early evolution of tracheophytes. Bot Gaz 152:335–356Google Scholar
  54. Kenrick P, Crane PR (1997) The origin and early evolution of plants on land. Nature 389:33–39Google Scholar
  55. Kitin PB, Fujii T, Abe H, Funada R (2004) Anatomy of the vessel network within and between tree rings of Fraxinus lanuginosa (Oleaceae). Am J Bot 91:779–788PubMedGoogle Scholar
  56. Lens F, Sperry JS, Christman MA, Choat B, Rabaey D, Jansen S (2011) Testing hypotheses that link wood anatomy to cavitation resistance and hydraulic conductivity in the genus Acer. New Phytol 190:709–723PubMedGoogle Scholar
  57. Levin DA (1975) Minority cytotype exclusion in local plant populations. Taxon 24:35–43Google Scholar
  58. Li WL, Berlyn GP, Ashton PMS (1996) Polyplolds and their structural and physiological characteristics relative to water deficit in Betula papyrifera (Betulaceae). Am J Bot 83:15–20Google Scholar
  59. Li WD, Biswas DK, Xu H, Xu CQ, Wang XZ, Liu JK, Jiang GM (2009) Photosynthetic responses to chromosome doubling in relation to leaf anatomy in Lonicera japonica subjected to water stress. Funct Plant Biol 36:783–792Google Scholar
  60. Limm EB, Dawson TE (2010) Polystichum munitum (Dryopteridaceae) varies geographically in its capacity to absorb fog water by foliar uptake within the redwood forest ecosystem. Am J Bot 97:1121–1128PubMedGoogle Scholar
  61. Limm EB, Simonin KA, Bothman AG, Dawson TE (2009) Foliar water uptake: a common water acquisition strategy for plants of the redwood forest. Oecologia 161:449–459PubMedCentralPubMedGoogle Scholar
  62. Liu H-M, He L-J, Schneider H (2014). Towards the natural classification of tectarioid ferns: confirming the phylogenetic relationships of Pleocnemia and Pteridrys (eupolypods I). J Syst Evol 52:161–174Google Scholar
  63. Manton I (1950) Problems of cytology and evolution in the Pteridophyta. Cambridge University Press, CambridgeGoogle Scholar
  64. Marrs RH, Watt AS (2006) Biological flora of the British Isles: Pteridium aquilinum (L.) Kuhn. J Ecol 94:1272–1321Google Scholar
  65. Mauseth JD, Fujii T (1994) Resin-casting: a method for investigating apoplastic spaces. Am J Bot 81:104–110Google Scholar
  66. McCulloh K, Sperry JS, Lachenbruch B, Meinzer FC, Reich PB, Voelker S (2010) Moving water well: comparing hydraulic efficiency in twigs and trunks of coniferous, ring-porous, and diffuse-porous saplings from temperate and tropical forests. New Phytol 186:439–450PubMedGoogle Scholar
  67. Mehltreter K, Walker LR, Sharpe JM (2010) Fern Ecology. Cambridge University Press, New YorkGoogle Scholar
  68. Meyer-Berthaud B, Scheckler SE, Wendt J (1999) Archaeopteris is the earliest known modern tree. Nature 398:700–701Google Scholar
  69. Meyer-Berthaud B, Scheckler SE, Bousquet J-L (2000) The development of Archaeopteris: new evolutionary characters from the structural analysis of an Early Famennian trunk from southeast Morocco. Am J Bot 87:456–468PubMedGoogle Scholar
  70. Moran RC (2008) Diversity, biogeography, and floristics. In: Ranker TA, Haufler CH (eds) Biology and evolution of ferns and lycophytes. Cambridge University Press, Cambridge, pp 367–394Google Scholar
  71. Morrow AC, Dute RR (1998) Development and structure of pit membranes in the rhizome of the woody fern Botrichium dissectum. IAWA J 19:429–441Google Scholar
  72. Mullendore DL, Windt CW, Van As H, Knoblauch M (2010) Sieve tube geometry in relation to phloem flow. Plant Cell 22:579–593PubMedCentralPubMedGoogle Scholar
  73. Nikinmaa E, Sievanen R, Holtta T (2014) Dynamics of leaf gas exchange, xylem and phloem transport, water potential and carbohydrate concentration in a realistic 3-D model tree crown. Ann Bot 114(44):653–666. doi: 10.1093/aob/mcu068 PubMedGoogle Scholar
  74. Niklas KJ (1985) The evolution of tracheid diameter in early vascular plans and its implications on the hydraulic conductance of the primary xylem strand. Evolution 39:1110–1122Google Scholar
  75. Niklas KJ (1992) Plant biomechanics: an engineering approach to plant form and function. University of Chicago Press, Chicago, p 410Google Scholar
  76. Niklas KJ (1999). Evolutionary walks through a land plant morphospace. J Exp Bot 50:39–52.Google Scholar
  77. Niklas KJ (2000) The evolution of plant body plans—a biomechanical perspective. Ann Bot 85:411–438Google Scholar
  78. Niklas K, Smocovitis V (1983) Evidence for a conducting strand in the early Silurian (Llandoverian) plants: implications for the evolution of the land plants. Paleobiology 9:126–137Google Scholar
  79. Niklas KJ, Speck T (2001) Evolutionary trends in safety factors against wind-induced stem failure. Am J Bot 88:1266–1278PubMedGoogle Scholar
  80. Ogura Y (1972) Comparative anatomy of vegetative organs of the pteridophytes. Gebruder Borntraeger, Berlin, p 502Google Scholar
  81. Page CN (2002) Ecological strategies in fern evolution: a neopteridological overview. Rev Palaeobot Palynol 119:1–33Google Scholar
  82. Panshin AJ, de Zeeuw C (1980) Textbook of wood technology. McGraw-Hill, New YorkGoogle Scholar
  83. Pickard WF, Abraham-Shrauner B (2009) A “simplest” steady-state Munch-like model of phloem translocation, with source and pathway and sink. Funct Plant Biol 36:629–644Google Scholar
  84. Pittermann J (2010) The evolution of water transport in plants: an integrated approach. Geobiology 8:112–139PubMedGoogle Scholar
  85. Pittermann J, Sperry JS, Hacke UG, Wheeler JK, Sikkema EH (2005) The torus-margo pit valve makes conifers hydraulically competitive with angiosperms. Science 310:1924PubMedGoogle Scholar
  86. Pittermann J, Sperry JS, Hacke UG, Wheeler JK, Sikkema EH (2006) Mechanical reinforcement against tracheid implosion compromises the hydraulic efficiency of conifer xylem. Plant Cell Environ 29:1618–1628PubMedGoogle Scholar
  87. Pittermann J, Choat B, Jansen S, Stuart SA, Lynn L, Dawson T (2010) The relationships between xylem safety and hydraulic efficiency in the Cupressaceae: the evolution of pit membrane form and function. Plant Physiol 153:1919–1931PubMedCentralPubMedGoogle Scholar
  88. Pittermann J, Limm E, Rico C, Christman M (2011) Structure function constraints of tracheid-based xylem: a comparison of conifers and ferns. New Phytol 192:449–461PubMedGoogle Scholar
  89. Pittermann J, Stuart SA, Dawson TE, Moreau A (2012) Cenozoic climate change shaped the evolutionary ecophysiology of the Cupressaceae conifers. Proc Natl Acad Sci U S A 109:9647–9652PubMedCentralPubMedGoogle Scholar
  90. Pittermann J, Brodersen C, Watkins JE (2013) The physiological resilience of fern sporophytes and gametophytes: advances in water relations offer new insights into an old lineage. Front Plant Sci. doi: 10.3389/fpls.2013.00285 PubMedCentralPubMedGoogle Scholar
  91. Pockman WT, Sperry JS (1997) Freezing-induced xylem cavitation and the northern limit of Larrea tridentata. Oecologia 109:19–27Google Scholar
  92. Proctor MCF (2012) Light and desiccation responses of some Hymenophyllaceae (filmy ferns) from Trinidad, Venezuela and New Zealand: poikilohydry in a light-limited but low evaporation ecological niche. Ann Bot 109:1019–1026PubMedCentralPubMedGoogle Scholar
  93. Proctor MCF, Tuba Z (2002) Poikilohydry and homoihydry: antithesis or spectrum of possibilities? New Phytol 156:327–349Google Scholar
  94. Ranker TA, Haufler CH (2008) Biology and evolution of ferns and lycophytes. Cambridge University Press, New YorkGoogle Scholar
  95. Raven JA (1984) Physiological correlates of the morphology of early vascular plants. Bot J the Linn Soc 88:105–126Google Scholar
  96. Robinson RC, Sheffield E, Sharpe JM (2010) Problem ferns: their impact and management. In: Mehltreter K, Walker LR, Sharpe JM (eds) Fern ecology. Cambridge University Press, Cambridge, pp 255–322Google Scholar
  97. Rothfels CJ, Sundue MA, Kuo L-Y, Larsson A, Kato M, Schuettpelz E, Pryer KM (2012) A revised family-level classification for eupolypod II ferns (Polypodiidae: Polypodiales). Taxon 61:515–533Google Scholar
  98. Rothwell GW, Karrfalt EE (2008) Growth, development and systematics of ferns: does Botrychium S.L. (Ophioglossales) really produce secondary xylem? Am J Bot 95:414–423PubMedGoogle Scholar
  99. Rothwell GW, Stockey RA (2008) Phylogeny and evolution of ferns: a paleontological perspective. In: Ranker T, Hausler C (eds) Biology and evolution of ferns and lycophytes. Cambridge University Press, CambridgeGoogle Scholar
  100. Rowe N, Speck T (2005) Plant evolutionary forms; an ecological and evolutionary perspective. New Phytol 166:61–72PubMedGoogle Scholar
  101. Rowe N, Isnard S, Speck T (2004) Diversity of mechanical architectures in climbing plants: an evolutionary perspective. J Plant Growth Regul 23:108–128Google Scholar
  102. Salleo S, Lo Gullo MA, Trifilo P, Nardini A (2004) New evidence for a role of vessel-associated cells and phloem in the rapid xylem refilling of cavitated stems of Laurus nobilis L. Plant Cell Environ 27:1065–1076Google Scholar
  103. Schneider H, Pryer KM, Cranfill R, Smith AR, Wolf PG (2002) Evolution of vascular plant body plans: a phylogenetic perspective. In: Cronk QCB, Bateman RM, Hawkins JA (eds) Developmental genetics and plant evolution. Taylor & Francis, London, pp 330–364Google Scholar
  104. Schneider H, Schuettpelz E, Pryer KM, Cranfill R, Magallon S, Lupia R (2004) Ferns diversified in the shadow of angiosperms. Nature 428:553–557PubMedGoogle Scholar
  105. Schuettpelz E, Pryer KM (2009) Evidence for a Cenozoic radiation of ferns in an angiosperm-dominated canopy. Proc Natl Acad Sci U S A 106:11200–11205PubMedCentralPubMedGoogle Scholar
  106. Schulte PJ, Gibson AC, Nobel P (1987) Xylem anatomy and hydraulic conductance of Psilotum nudum. Am J Bot 74:1438–1445Google Scholar
  107. Scoffoni C, Rawls M, McKown A, Cochard H, Sack L (2011) Decline in leaf hydraulic conductance with dehydration: relationship to leaf size and venation architecture. Plant Physiol 156:832–843PubMedCentralPubMedGoogle Scholar
  108. Secchi F, Zwieniecki MA (2011) Sensing embolism in xylem vessels: the role of sucrose as a trigger for refilling. Plant Cell Environ 34:514–524PubMedGoogle Scholar
  109. Sessa EB, Zimmer EA, Givnish TJ (2012) Phylogeny, divergence times, and historical biogeography of new world Dryopteris (Dryopteridaceae). Am J Bot 88:730–750Google Scholar
  110. Sessa EB, Givnish TJ (2014) Leaf form and photosynthetic physiology of Dryopteris species distributed along light gradients in eastern North America. Funct Eco 28:108–123Google Scholar
  111. Serbet R, Rothwell GW (1999) Osmunda cinnamomea (Osmundaceae) in the Upper Cretaceous of western North America: additional evidence for exceptional species longevity among filicalean ferns. Int J Plant Sci 160:425–433Google Scholar
  112. Sharpe JM, Mehltreter K (2010) Ecological insights from fern population dynamics. In: Mehltreter K, Walker LR, Sharpe JM (eds) Fern ecology. Cambridge University Press, New York, pp 61–139Google Scholar
  113. Smith AR, Pryer KM, Schuettpelz E, Korall P, Schneider H, Wolf PG (2006) A classification for extant ferns. Taxon 55:705–731Google Scholar
  114. Sperry JS (2003) Evolution of water transport and xylem structure. Int J Plant Sci 164:S115–S127Google Scholar
  115. Sperry JS, Hacke UG, Pittermann J (2006) Size and function in conifer tracheids and angiosperm vessels. Am J Bot 93:1490–1500PubMedGoogle Scholar
  116. Stebbins GL (1971) Chromosomal evolution in higher plants. Addison-Wesley, ReadingGoogle Scholar
  117. Strullu-Derrien C, Kenrick P Tafforeau P, Cochard H, Bonnemain J-L, Le Herisse A, Lardeux H, Badel E (2014) The earliest wood and its hydrualic properties document in c. 407-million-year-old fossils using synchrotron microtomography. Bot J Linn Soc 175:423–437Google Scholar
  118. Taylor TN, Taylor EL, Krings M (2009) Paleobotany. The biology and evolution of fossil plants. Academic, OxfordGoogle Scholar
  119. Testo WL, Watkins JE, Barrington DS (2014) Dynamics of asymmetrical hybridization in North American wood ferns: reconciling patterns of inheritance with gametophyte ecology. New Phytol. doi: 10.1111/nph.13213 PubMedGoogle Scholar
  120. Testo WL, Watkins JE, Pittermann J, Momin R (2015) Pteris X caridadiae (Pteridaceae), a new hybrid fern from Costa Rica. Brittonia doi: 10.1007/s12228-015-9370-8
  121. Tyree MT, Davis SD, Cochard H (1994) Biophysical perspectives of xylem evolution: is there a tradeoff of hydraulic efficiency for vulnerability to cavitation? IAWA J 15:335–360Google Scholar
  122. Vasco A, Moran RC, Ambrose BA (2013) The evolution, morphology, and development of fern leaves. Front Plant Sci 4:345. doi: 10.3389/fpls.2013.00345 PubMedCentralPubMedGoogle Scholar
  123. Veres JS (1990) Xylem anatomy and hydraulic conductance of Costa Rican Blechnum ferns. Am J Bot 77:1610–1625Google Scholar
  124. Warner DA, Edwards GE (1993) Effects of polyploidy on photosynthesis. Photosynth Res 35:135–147PubMedGoogle Scholar
  125. Watkins JE, Cardelús CL (2009) Habitat differentiation of ferns in a lowland tropical rain forest. Am Fern J 3:162–175Google Scholar
  126. Watkins JE, Cardelus CL (2012) Ferns in an Angiosperm world: Cretaceous radiation into the epiphytic niche and diversification on the forest floor. Int J Plant Sci 173:695–710Google Scholar
  127. Watkins JE, Mack MC, Sinclair T, Mulkey SS (2007a) Ecological and evolutionary consequences of desiccation tolerance in tropical fern gametophytes. New Phytol 176:708–717PubMedGoogle Scholar
  128. Watkins JE, Mack MC, Mulkey SS (2007b) Gametophyte ecology and demography of epiphytic and terrestrial tropical ferns. Am J Bot 94:701–708PubMedGoogle Scholar
  129. Watkins JE, Rundel P, Cardelus CL (2007c) The influence of life form on carbon and nitrogen relationships in tropical rainforest ferns. Oecologia 153:225–232PubMedGoogle Scholar
  130. Watkins JE, Holbrook NM, Zwieniecki MA (2010) Hydraulic properties of fern sporophytes: consequences for ecological and evolutionary diversification. Am J Bot 97:2007–2019PubMedGoogle Scholar
  131. Wheeler JW, Sperry JS, Hacke UG, Hoang N (2005) Intervessel pitting and cavitation in woody Rosaceae and other vesseled plants: a basis for a safety vs. efficiency trade-off in xylem transport. Plant Cell Environ 28:800–812Google Scholar
  132. White RA, Weidlich WH (1995) Organization of the vascular system in the stems of Diplazium and Blechnum (Filicales). Am J Bot 82:982–991Google Scholar
  133. Wilson JP (2013) Modeling 400 million year of plant hydraulics. Paleontol Soc Pap 19:1–20Google Scholar
  134. Wilson JP, Fischer WW (2010) Hydraulics of Asteroxylon mackei, an early Devonian vascular plant, and the early evolution of water transport tissue in terrestrial plants. Geobiology 9:121–130Google Scholar
  135. Wilson JP, Knoll AH (2010) A physiologically explicit morphospace for tracheid-based water transport in modern and extinct seed plants. Paleobiology 36:335–355Google Scholar
  136. Wilson JP, Knoll AH, Holbrook NM, Marshall CR (2008) Modeling fluid flow in Medullosa, an anatomically unusual Carboniferous seed plant. Paleobiology 34:472–493Google Scholar
  137. Wood TE, Takebayashi N, Barker MS, Mayrose I, Greenspoon PB, Rieseberg LH (2009) The frequency of polyploid speciation in vascular plants. Proc Natl Acad Sci U S A 106:13875–13879PubMedCentralPubMedGoogle Scholar
  138. Zimmermann M, Tomlinson PB (1974) Vascular patterns in palm stems: variations of the Raphis principle. J Arnold Arb 55:402–424Google Scholar
  139. Zimmermann M, Tyree MT (2002) Xylem structure and the ascent of sap. Springer, BerlinGoogle Scholar
  140. Zwieniecki MA, Melcher PJ, Holbrook NM (2001) Hydraulic properties of individual xylem vessels of Fraxinus americana. J Exp Bot 52:257–264PubMedGoogle Scholar

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© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Jarmila Pittermann
    • 1
  • James E. Watkins
    • 2
  • Katharine L. Cary
    • 1
  • Eric Schuettpelz
    • 3
  • Craig Brodersen
    • 4
  • Alan R. Smith
    • 5
  • Alex Baer
    • 1
  1. 1.Department of Ecology and Evolutionary BiologyUniversity of CaliforniaSanta CruzUSA
  2. 2.Department of BiologyColgate UniversityHamiltonUSA
  3. 3.Department of Botany National Museum of Natural HistorySmithsonian InstitutionWashington, DCUSA
  4. 4.School of Forestry and Environmental StudiesYale UniversityNew HavenUSA
  5. 5.University HerbariumUniversity of CaliforniaBerkeleyUSA

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