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Reciprocal Illumination and Fossils Provide Important Perspectives in Plant Evo-devo: Examples from Auxin in Seed-Free Plants

  • Kelly K. S. Matsunaga
  • Alexandru M. F. Tomescu
Chapter

Abstract

The plant hormone auxin plays an integral role in numerous aspects of plant development, from embryogeny through secondary growth, which has raised the question of whether changes in auxin signaling underlie major morphological changes in land plant evolution. However, the majority of available data on auxin action come from studies of angiosperms, and it is unclear to what extent these data can be applied to other plant lineages, particularly seed-free plants. Here we review the current state of knowledge on auxin and its role in seed-free plant development, with a focus on polar auxin transport, and illustrate the value of using reciprocal illumination approaches that integrate the fossil record for understanding the evolution of plant form and development. Our survey reveals that while there are some differences, particularly between lycophytes and euphyllophytes, the general patterns of polar auxin transport and auxin action appear to be shared among all tracheophytes. Based on these data, we provide insights and testable hypotheses on leaf and rooting system evolution among lycophytes, demonstrating the utility of anatomical fingerprints of development. However, we also find that numerous gaps in our understanding of the roles of auxin in seed-free plants remain that stymie further progress. Filling these gaps will require continuing incremental research on seed-free plant development, from anatomy to developmental genetics, but has broad potential for making significant contributions to our understanding of patterns and processes in plant evolution.

Keywords

Auxin Development Evo-devo Fern Fossil Lycophyte Polar auxin transport Tracheophyte 

References

  1. Aida M, Beis D, Heidstra R et al (2004) The PLETHORA genes mediate patterning of the Arabidopsis stem cell niche. Cell 119:109–120PubMedCrossRefGoogle Scholar
  2. Albaum HG (1938) Inhibition due to growth hormones in fern prothallia and sporophytes. Am J Bot 25:124–133CrossRefGoogle Scholar
  3. Aloni R (1995) The induction of vascular tissues by auxin and cytokinin. In: Davies PJ (ed) Plant hormones: physiology, biochemistry, and molecular biology, 2nd edn. Kluwer Academic Publishers, Dordrecht, pp 531–546CrossRefGoogle Scholar
  4. Aloni R (2010) The induction of vascular tissues by auxin. In: Davies PJ (ed) Plant hormones. Springer, Dordrecht, pp 485–506CrossRefGoogle Scholar
  5. Banks HP (1968) The early history of land plants. In: Drake ET (ed) Evolution and environment. Yale University Press, New Haven, pp 73–107Google Scholar
  6. Barkoulas M, Galinha C, Grigg SP et al (2007) From genes to shape: regulatory interactions in leaf development. Curr Opin Plant Biol 10:660–666PubMedCrossRefGoogle Scholar
  7. Barkoulas M, Hay A, Kougioumoutzi E et al (2008) A developmental framework for dissected leaf formation in the Arabidopsis relative Cardamine hirsuta. Nat Genet 40:1136–1141PubMedCrossRefGoogle Scholar
  8. Bateman RM, Hilton J, Rudall PJ (2006) Morphological and molecular phylogenetic context of the angiosperms: contrasting the ‘top-down’ and ‘bottom-up’ approaches used to infer the likely characteristics of the first flowers. J Exp Bot 57:3471–3503PubMedCrossRefGoogle Scholar
  9. Benjamins R, Scheres B (2008) Auxin: the looping star in plant development. Annu Rev Plant Biol 59:443–465PubMedCrossRefGoogle Scholar
  10. Benková E, Michniewicz M, Sauer M et al (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115:591–602PubMedCrossRefGoogle Scholar
  11. Bennett T (2015) PIN proteins and the evolution of plant development. Trends Plant Sci 20:498–507PubMedCrossRefGoogle Scholar
  12. Bennett T, Hines G, Leyser O (2014) Canalization: what the flux? Trends Genet 30:41–48PubMedCrossRefGoogle Scholar
  13. Berleth T (2001) Top-down and inside-out: directionality of signaling in vascular and embryo development. J Plant Growth Regul 20:14–21CrossRefGoogle Scholar
  14. Berleth T, Sachs T (2001) Plant morphogenesis: long-distance coordination and local patterning. Curr Opin Plant Biol 4:57–62PubMedCrossRefGoogle Scholar
  15. Berleth T, Mattsson J, Hardtke CS (2000) Vascular continuity and auxin signals. Trends Plant Sci 5:387–393PubMedCrossRefGoogle Scholar
  16. Beveridge CA, Mathesius U, Rose RJ et al (2007) Common regulatory themes in meristem development and whole-plant homeostasis. Curr Opin Plant Biol 10:44–51PubMedCrossRefGoogle Scholar
  17. Björklund S, Antti H, Uddestrand I et al (2007) Cross-talk between gibberellin and auxin in development of Populus wood: gibberellin stimulates polar auxin transport and has a common transcriptome with auxin. Plant J 52:499–511PubMedCrossRefGoogle Scholar
  18. Blilou I, Xu J, Wildwater M et al (2005) The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433:39–44PubMedCrossRefGoogle Scholar
  19. Bomfleur B, McLoughlin S, Vajda V (2014) Fossilized nuclei and chromosomes reveal 180 million years of genomic stasis in royal ferns. Science 343:1376–1377PubMedCrossRefGoogle Scholar
  20. Bomfleur B, Grimm GW, McLoughlin S (2017) The fossil Osmundales (Royal Ferns) – a phylogenetic network analysis, revised taxonomy, and evolutionary classification of anatomically preserved trunks and rhizomes. PeerJ 5:e3433PubMedPubMedCentralCrossRefGoogle Scholar
  21. Bower FO (1885) On the development and morphology of Phylloglossum drummondii. Phil Trans R Soc Lond 176:665–678CrossRefGoogle Scholar
  22. Bower FO (1935) Primitive land plants, also known as the Archegoniatae. Macmillan, LondonGoogle Scholar
  23. Boyce CK (2005a) Patterns of segregation and convergence in the evolution of fern and seed plant leaf morphologies. Paleobiology 31:117–140CrossRefGoogle Scholar
  24. Boyce CK (2005b) The evolutionary history of roots and leaves. In: Holbrook NM, Zwieniecki MA (eds) Vascular transport in plants. Elsevier, Amsterdam, pp 479–499CrossRefGoogle Scholar
  25. Boyce CK (2010) The evolution of plant development in a paleontological context. Curr Opin Plant Biol 13:102–107PubMedCrossRefGoogle Scholar
  26. Boyce CK, Knoll AH (2002) Evolution of developmental potential and the multiple independent origins of leaves in Paleozoic vascular plants. Paleobiology 28:70–100CrossRefGoogle Scholar
  27. Bristow MJ (1962) The controlled in vitro differentiation of callus derived from a fern, Pteris cretica L., into gametophytic or sporophytic tissues. Dev Biol 4:361–375CrossRefGoogle Scholar
  28. Byrne TE, Caponetti JD (1992) Morphogenesis in three cultivars of Boston fern. III. Callus production and plantlet differentiation from cell suspensions. Am Fern J 82:12–22CrossRefGoogle Scholar
  29. Campbell L, Turner S (2017) Regulation of vascular cell division. J Exp Bot 68:27–43PubMedCrossRefGoogle Scholar
  30. Cooke TJ, Poli D, Sztein AE et al (2002) Evolutionary patterns in auxin action. Plant Mol Biol 49:319–338PubMedCrossRefGoogle Scholar
  31. Cooke TJ, Poli D, Cohen JD (2004) Did auxin play a crucial role in the evolution of novel body plans during the late Silurian – early Devonian radiation of land plants? In: Hemsley AR, Poole I (eds) The evolution of plant physiology. From whole plants to ecosystems. Elsevier, Amsterdam, pp 85–107CrossRefGoogle Scholar
  32. Cúneo NR, Andreis RR (1983) Estudio de un bosque de licofitas en la Formación Nueva Lubecka, Pérmico de Chubut, Argentina. Implicancias paleoclimáticas y paleogeográficas. Ameghiniana 20:132–140Google Scholar
  33. Cusick F (1954) Experimental and analytical studies of pteridophytes. XXV. Morphogenesis in Selaginella willdenowii Baker. II. Angle-meristems and angle-shoots. Ann Bot 18:171–181CrossRefGoogle Scholar
  34. De Rybel B, Moller B, Yoshida S et al (2013) A bHLH complex controls embryonic vascular tissue establishment and indeterminate growth in Arabidopsis. Dev Cell 24:426–437PubMedCrossRefGoogle Scholar
  35. de Vries J, Fischer AM, Roettger M et al (2016) Cytokinin-induced promotion of root meristem size in the fern Azolla supports a shoot-like origin of euphyllophyte roots. New Phytol 209:705–720PubMedCrossRefGoogle Scholar
  36. Deb Y, Marti D, Frenz M et al (2015) Phyllotaxis involves auxin drainage through leaf primordia. Development 142:1992–2001PubMedCrossRefGoogle Scholar
  37. Decombeix A-L, Taylor EL, Taylor TN (2010) Epicormic shoots in a Permian gymnosperm from Antarctica. Int J Plant Sci 171:772–782CrossRefGoogle Scholar
  38. Dengler NG (2001) Regulation of vascular development. J Plant Growth Regul 20:1–13CrossRefGoogle Scholar
  39. Dengler NG (2006) The shoot apical meristem and development of vascular architecture. Can J Bot 84:1660–1671CrossRefGoogle Scholar
  40. Dettmer J, Elo A, Helariutta Y (2009) Hormone interactions during vascular development. Plant Mol Biol 69:347–360PubMedCrossRefGoogle Scholar
  41. Durbak A, Yao H, McSteen P (2012) Hormone signaling in plant development. Curr Opin Plant Biol 15:92–96PubMedCrossRefGoogle Scholar
  42. Edwards D (1994) Toward an understanding of pattern and process in the growth of early vascular plants. In: Ingram DS, Hudson A (eds) Shape and form in plants and fungi. Academic Press & Linnean Society, London, pp 39–59Google Scholar
  43. Esau K (1965) Plant anatomy, 2nd edn. Wiley & Sons, New YorkGoogle Scholar
  44. Escapa IH, Catalano SA (2013) Phylogenetic analysis of Araucariaceae: integrating molecules, morphology, and fossils. Int J Plant Sci 174:1153–1170CrossRefGoogle Scholar
  45. Fabregas N, Formosa-Jordan P, Confraria A et al (2015) Auxin influx carriers control vascular patterning and xylem differentiation in Arabidopsis thaliana. PLoS Genet 11:e1005183PubMedPubMedCentralCrossRefGoogle Scholar
  46. Finet C, Jaillais Y (2012) AUXOLOGY: when auxin meets plant evo-devo. Dev Biol 369:19–31PubMedCrossRefGoogle Scholar
  47. Floyd SK, Bowman JL (2006) Distinct developmental mechanisms reflect the independent origins of leaves in vascular plants. Curr Biol 16:1911–1917PubMedCrossRefGoogle Scholar
  48. Floyd SK, Bowman JL (2010) Gene expression patterns in seed plant shoot meristems and leaves: homoplasy or homology? J Plant Res 123:43–55PubMedCrossRefGoogle Scholar
  49. Frankenberg JM, Eggert DA (1969) Petrified Stigmaria from North America: part I. Stigmaria ficoides, the underground portions of Lepidodendraceae. Palaeontographica B 128:1–47Google Scholar
  50. Friedman WE, Moore RC, Purugganan MD (2004) The evolution of plant development. Am J Bot 91:1726–1741PubMedCrossRefGoogle Scholar
  51. Friml J, Vieten A, Sauer M et al (2003) Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426:147–153PubMedCrossRefGoogle Scholar
  52. Fujinami R, Yamada T, Nakajima A et al (2017) Root apical meristem diversity in extant lycophytes and implications for root origins. New Phytol 215:1210–1220PubMedCrossRefGoogle Scholar
  53. Gensel PG (1975) A new species of Sawdonia with notes on the origin of microphylls and lateral sporangia. Am J Bot 136:50–62Google Scholar
  54. Gensel PG (2008) The earliest land plants. Annu Rev Ecol Evol Syst 39:459–477CrossRefGoogle Scholar
  55. Gensel PG, Andrews HN (1984) Plant life in the Devonian. Praeger, New YorkGoogle Scholar
  56. Gensel PG, Kotyk ME, Basinger JF (2001) Morphology of above- and belowground structures in early Devonian (Pragian–Emsian) plants. In: Gensel PG, Edwards D (eds) Plants invade the land. Columbia University Press, New York, pp 83–102CrossRefGoogle Scholar
  57. Gifford EM, Foster AS (1989) Morphology and evolution of vascular plants, 3rd edn. Freeman, New YorkGoogle Scholar
  58. Gola EM, Jernstedt JA, Zagorska-Marek B (2007) Vascular architecture in shoots of early divergent vascular plants, Lycopodium clavatum and Lycopodium annotinum. New Phytol 174:774–786PubMedCrossRefGoogle Scholar
  59. Hao S, Xue J, Liu Z et al (2007) Zosterophyllum Penhallow around the Silurian-Devonian boundary of northeastern Yunnan, China. Int J Plant Sci 168:477–489CrossRefGoogle Scholar
  60. Harrison CJ (2016) Auxin transport in the evolution of branching forms. New Phytol 215:545.  https://doi.org/10.1111/nph.14333 PubMedCrossRefGoogle Scholar
  61. Harrison CJ (2017) Development and genetics in the evolution of land plant body plans. Philos Trans R Soc B 372:20150490CrossRefGoogle Scholar
  62. Hejnowicz Z, Kurczyńska EU (1987) Occurrence of circular vessels above axillary buds in stems of woody plants. Acta Soc Bot Pol 56:415–419CrossRefGoogle Scholar
  63. Hetherington AJ, Dolan L (2016) The evolution of lycopsid rooting structures: conservatism and disparity. New Phytol 215:538–544PubMedCrossRefGoogle Scholar
  64. Hetherington AJ, Dubrovski JG, Dolan L (2016) Unique cellular organisation in the oldest root meristem. Curr Biol 26:1629–1633PubMedPubMedCentralCrossRefGoogle Scholar
  65. Hou G, Hill JP, Blancaflor EB (2004) Developmental anatomy and auxin response of lateral root formation in Ceratopteris richardii. J Exp Bot 55:685–693PubMedCrossRefGoogle Scholar
  66. Hueber FM (1992) Thoughts on the early lycopsids and zosterophylls. Ann Mo Bot Gard 79:474–499CrossRefGoogle Scholar
  67. Jasper A, Guerra-Sommer M (1999) Licófitas arborescentes in situ como elementos importantes na definição de modelos deposicionais (Formação Rio Bonito - Bacia do Paraná - Brasil). Pesq Geoci 26:49–58Google Scholar
  68. Jernstedt JA, Cutter EG, Lu P (1994) Independence of organogenesis and cell pattern in developing angle shoots of Selaginella martensii. Ann Bot 74:343–355CrossRefGoogle Scholar
  69. Jones AM (1998) Auxin transport: down and out and up again. Science 282:2201–2202PubMedCrossRefGoogle Scholar
  70. Kasprzewska A, Carter R, Swarup R et al (2015) Auxin influx importers modulate serration along the leaf margin. Plant J 83:705–718PubMedPubMedCentralCrossRefGoogle Scholar
  71. Kenrick P, Crane PR (1997) The origin and early diversification of land plants. Smithsonian Institution Press, WashingtonGoogle Scholar
  72. Kenrick P, Strullu-Derrien C (2014) The origin and early evolution of roots. Plant Physiol 166:570–580PubMedPubMedCentralCrossRefGoogle Scholar
  73. Kidston R, Lang WH (1920) On old red sandstone plants showing structure, from the Rhynie Chert Bed, Aberdeenshire. Part III. Asteroxylon mackiei, Kidston and Lang. Trans R Soc Edinb 52:643–680CrossRefGoogle Scholar
  74. Kierzkowski D, Nakayama N, Routier-Kierzkowska A-L et al (2012) Elastic domains regulate growth and organogenesis in the plant shoot apical meristem. Science 335:1096–1099PubMedCrossRefGoogle Scholar
  75. Kwiatkowska D (1992) The relationships between the primary vascular system and phyllotactic patterns of Anagallis arvensis (Primulaceae). Am J Bot 79:904–913CrossRefGoogle Scholar
  76. Lacombe B, Achard P (2016) Long-distance transport of phytohormones through the plant vascular system. Curr Opin Plant Biol 34:1–8PubMedCrossRefGoogle Scholar
  77. Langdale JA (2008) Evolution of developmental mechanisms in plants. Curr Opin Genet Dev 18:368–373PubMedCrossRefGoogle Scholar
  78. Larsson E, Sitbon F, Ljung K et al (2008) Inhibited polar auxin transport results in aberrant embryo development in Norway spruce. New Phytol 177:356–366PubMedGoogle Scholar
  79. Lev-Yadun S (1996) Circular vessels in the secondary xylem of Arabidopsis thaliana (Brassicaceae). IAWA J 17:31–35CrossRefGoogle Scholar
  80. Lev-Yadun S, Aloni R (1990) Vascular differentiation in branch junctions of trees: circular patterns and functional significance. Trees 4:49–54CrossRefGoogle Scholar
  81. Leyser O (2011) Auxin, self-organisation, and the colonial nature of plants. Curr Biol 21:R331–R337PubMedCrossRefGoogle Scholar
  82. Li C-S, Edwards D (1995) A re-investigation of Halle’s Drepanophycus spinaeformis Goepp. from the Lower Devonian of Yunnan Province, southern China. Bot J Linn Soc 118:163–192Google Scholar
  83. Li C-S, Hueber FM, Hotton CL (2000) A neotype for Drepanophycus spinaeformis Göppert 1852. Can J Bot 78:889–902Google Scholar
  84. Liu C-m, Xu Z-h, Chua N-h (1993) Auxin polar transport is essential for the establishment of bilateral symmetry during early plant embryogenesis. Plant Cell 5:621–630PubMedPubMedCentralCrossRefGoogle Scholar
  85. Lucas WJ, Groover A, Lichtenberger R et al (2013) The plant vascular system: evolution, development and functions. J Integr Plant Biol 55:294–388PubMedCrossRefGoogle Scholar
  86. Lyon AG (1964) Probable fertile region of Asteroxylon mackiei K. and L. Nature 203:1082–1083CrossRefGoogle Scholar
  87. Ma Y, Steeves TA (1992) Auxin effects on vascular differentiation in ostrich fern. Ann Bot 70:277–282CrossRefGoogle Scholar
  88. Matsunaga KKS, Tomescu AMF (2016) Root evolution at the base of the lycophyte clade: insights from an early Devonian lycophyte. Ann Bot 117:585–598PubMedPubMedCentralCrossRefGoogle Scholar
  89. Matsunaga KKS, Tomescu AMF (2017) An organismal concept for Sengelia radicans gen. et sp. nov. – morphology and natural history of an early Devonian lycophyte. Ann Bot 119:1097–1113PubMedCrossRefGoogle Scholar
  90. Matsunaga KKS, Cullen NP, Tomescu AMF (2017) Vascularization of the Selaginella rhizophore: anatomical fingerprints of polar auxin transport with implications for the deep fossil record. New Phytol 216:419–428PubMedCrossRefGoogle Scholar
  91. Mattsson J, Sung ZR, Berleth T (1999) Responses of plant vascular systems to auxin transport inhibition. Development 126:2979–2991PubMedGoogle Scholar
  92. Meicenheimer RD (1986) Role of parenchyma in Linum usitatissimum leaf trace patterns. Am J Bot 73:1649–1664CrossRefGoogle Scholar
  93. Miyashima S, Sebastian J, Lee J-Y et al (2013) Stem cell function during plant vascular development. EMBO J 32:178–193PubMedCrossRefGoogle Scholar
  94. Moller B, Weijers D (2009) Auxin control of embryo patterning. Cold Spring Harb Perspect Biol 1:a001545PubMedPubMedCentralCrossRefGoogle Scholar
  95. Nakamura T, Gehrke AR, Lemberg J et al (2016) Digits and fin rays share common developmental histories. Nature 537:225–228PubMedPubMedCentralCrossRefGoogle Scholar
  96. Overvoorde P, Fukaki H, Beeckman T (2010) Auxin control of root development. Cold Spring Harb Perspect Biol 2:a001537PubMedPubMedCentralCrossRefGoogle Scholar
  97. Partanen JN, Partanen CR (1963) Observations on the culture of roots of the bracken fern. Can J Bot 41:1657–1661CrossRefGoogle Scholar
  98. Pigg KB (2001) Isoetalean lycopsid evolution: from the Devonian to the present. Am Fern J 91:99–114CrossRefGoogle Scholar
  99. Pigg KB, Rothwell GW (1983) Megagametophyte development in the Chaloneriaceae fam. Nov., permineralized Paleozoic Isoetales (Lycopsida). Bot Gaz 144:295–302CrossRefGoogle Scholar
  100. Poli D (2005) The role of auxin on the evolution of embryo development and axis formation in land plants. PhD Dissertation, University of MarylandGoogle Scholar
  101. Prigge MJ, Clark SE (2006) Evolution of the class III HD-Zip gene family in land plants. Evol Dev 8:350–361PubMedCrossRefGoogle Scholar
  102. Raven JA, Edwards D (2001) Roots: evolutionary origins and biogeochemical significance. J Exp Bot 52:381–401PubMedCrossRefGoogle Scholar
  103. Rayner RJ (1984) New finds of Drepanophycus spinaeformis Goppert from the lower Devonian of Scotland. Trans R Soc Edinb Earth Sci 75:353–363CrossRefGoogle Scholar
  104. Reinhardt D (2005) Phyllotaxis – a new chapter in an old story about beauty and magic numbers. Curr Opin Plant Biol 8:487–493PubMedCrossRefGoogle Scholar
  105. Reinhardt D, Mandel T, Kuhlemeier C (2000) Auxin regulates the initiation and radial position of plant lateral organs. Plant Cell 12:507–518PubMedPubMedCentralCrossRefGoogle Scholar
  106. Reinhardt D, Pesce E-R, Stieger P et al (2003) Regulation of phyllotaxis by polar auxin transport. Nature 426:255–260PubMedCrossRefGoogle Scholar
  107. Robert HS, Grones P, Stepanova AN et al (2013) Local auxin sources orient the apical-basal axis in Arabidopsis embryos. Curr Biol 23:2506–2512PubMedCrossRefGoogle Scholar
  108. Rothwell GW (1995) The fossil history of branching: implications for the phylogeny of land plants. In: Hoch PC, Stephenson AG (eds) Experimental and molecular approaches to plant biosystematics. Missouri Botanical Garden, St. Louis, pp 71–86Google Scholar
  109. Rothwell GW, Erwin DM (1985) The rhizomorph apex of Paurodendron: implications for homologies among the rooting organs of Lycopsida. Am J Bot 72:86–98CrossRefGoogle Scholar
  110. Rothwell GW, Lev-Yadun S (2005) Evidence of polar auxin flow in 375 million-year-old fossil wood. Am J Bot 92:903–906PubMedCrossRefGoogle Scholar
  111. Rothwell GW, Nixon KC (2006) How does the inclusion of fossil data change our conclusions about the phylogenetic history of euphyllophytes? Int J Plant Sci 167:737–749CrossRefGoogle Scholar
  112. Rothwell GW, Tomescu AMF (2017) Structural fingerprints of development at the intersection of evolutionary developmental biology and the fossil record. In: Nuño de la Rosa L, Müller GB (eds) Evolutionary developmental biology – a reference guide. Springer International Publishing, Cham (Switzerland) https://doi.org/10.1007/978-3-319-33038-9_169-1
  113. Rothwell GW, Sanders H, Wyatt SE et al (2008) A fossil record for growth regulation: the role of auxin in wood evolution. Ann Mo Bot Gard 95:121–134CrossRefGoogle Scholar
  114. Rothwell GW, Wyatt SE, Tomescu AMF (2014) Plant evolution at the interface of paleontology and developmental biology: an organism-centered paradigm. Am J Bot 101:899–913PubMedCrossRefGoogle Scholar
  115. Rudall PJ, Hilton J, Bateman RM (2013) Several developmental and morphogenetic factors govern the evolution of stomatal patterning in land plants. New Phytol 200:598–614PubMedCrossRefGoogle Scholar
  116. Runions A, Tsiantis M, Prusinkiewicz P (2017) A common developmental program can produce diverse leaf shapes. New Phytol 216:401–418PubMedPubMedCentralCrossRefGoogle Scholar
  117. Sabatini S, Beis D, Wolkenfelt H et al (1999) An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99:463–472PubMedCrossRefGoogle Scholar
  118. Sachs T (1969) Polarity and the induction of organized vascular tissues. Ann Bot 33:263–275CrossRefGoogle Scholar
  119. Sachs T (1981) The control of the patterned differentiation of vascular tissues. Adv Bot Res 9:151–262CrossRefGoogle Scholar
  120. Sachs T (1991) Pattern formation in plant tissues. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  121. Sachs T, Cohen D (1982) Circular vessels and the control of vascular differentiation in plants. Differentiation 21:22–26CrossRefGoogle Scholar
  122. Sanders HL, Langdale JA (2013) Conserved transport mechanisms but distinct auxin responses govern shoot patterning in Selaginella kraussiana. New Phytol 198:419–428PubMedCrossRefGoogle Scholar
  123. Sanders H, Rothwell GW, Wyatt SE (2009) Key morphological alterations in the evolution of leaves. Int J Plant Sci 170:860–868CrossRefGoogle Scholar
  124. Sanders H, Rothwell GW, Wyatt SE (2011) Parallel evolution of auxin regulation in rooting systems. Pl Syst Evol 291:221–225CrossRefGoogle Scholar
  125. Sawchuk MG, Scarpella E (2013) Polarity, continuity, and alignment in plant vascular strands. J Integr Plant Biol 55:824–834PubMedCrossRefGoogle Scholar
  126. Sawchuk MG, Head P, Donner TJ et al (2007) Time-lapse imaging of Arabidopsis leaf development shows dynamic patterns of procambium formation. New Phytol 176:560–571PubMedCrossRefGoogle Scholar
  127. Scarpella E, Meijer AH (2004) Pattern formation in the vascular system of monocot and dicot plant species. New Phytol 164:209–242CrossRefGoogle Scholar
  128. Scarpella E, Marcos D, Friml J et al (2006) Control of leaf vascular patterning by polar auxin transport. Genes Dev 20:1015–1027PubMedPubMedCentralCrossRefGoogle Scholar
  129. Schweitzer H-J, Giesen P (1980) Uber Taeniophyton inopinatum, Protolycopodites devonicus und Cladoxylon scoparium aus dem Mitteldevon von Wuppertal. Palaeontographica B 173:1–25Google Scholar
  130. Schweitzer H-J (1980) Über Drepanophycus spinaeformis Göppert. Bonner Paläobotan Mitt (Selbstverl d Paläobotan Abt d Inst für Paläontologie d Univ Bonn) 7:1–29Google Scholar
  131. Shubin NH (2008) Your inner fish. Vintage Books, New YorkGoogle Scholar
  132. Smith RP, Guyomarc'h S, Mandel T et al (2006) A plausible model of phyllotaxis. Proc Natl Acad Sci U S A 103:1301–1306PubMedPubMedCentralCrossRefGoogle Scholar
  133. Smith SY, Collinson ME, Rudall PJ et al (2009) Virtual taphonomy using synchrotron tomographic microscopy reveals cryptic features and internal structure of modern and fossil plants. Proc Natl Acad Sci U S A 106:12013–12018PubMedPubMedCentralCrossRefGoogle Scholar
  134. Steeves TA, Briggs WR (1960) Morphogenetic studies on Osmunda cinnamomea L. The auxin relationships of expanding fronds. J Exp Bot 11:45–67CrossRefGoogle Scholar
  135. Stewart WN (1964) An upward look in plant morphology. Phytomorphology 14:120–134Google Scholar
  136. Stewart WN, Rothwell GW (1993) Paleobotany and the evolution of plants, 2nd edn. Cambridge University Press, CambridgeGoogle Scholar
  137. Tomescu AMF (2009) Megaphylls, microphylls and the evolution of leaf development. Trends Plant Sci 14:5–12PubMedCrossRefGoogle Scholar
  138. Tomescu AMF (2011) The sporophytes of seed-free vascular plants – major vegetative developmental features and molecular genetic pathways. In: Fernandez H, Kumar A, Revilla MA (eds) Working with ferns. Issues and applications. Springer, New York, pp 67–94CrossRefGoogle Scholar
  139. Tomescu AMF, Escapa IH, Rothwell GW et al (2017) Developmental programmes in the evolution of Equisetum reproductive morphology: a hierarchical modularity hypothesis. Ann Bot 119:489–505PubMedPubMedCentralCrossRefGoogle Scholar
  140. Tuominen H, Puech L, Fink S et al (1997) A radial concentration gradient of indole-3-acetic acid is related to secondary xylem development in hybrid aspen. Plant Physiol 115:577–585PubMedPubMedCentralCrossRefGoogle Scholar
  141. Turchi L, Baima S, Morelli G et al (2015) Interplay of HD-ZIP II and III transcription factors in auxin-regulated plant development. J Exp Bot 66:5043–5053PubMedCrossRefGoogle Scholar
  142. Vasco A, Smalls TL, Graham SW et al (2016) Challenging the paradigms of leaf evolution: class III HD-Zips in ferns and lycophytes. New Phytol 212:745–758PubMedCrossRefGoogle Scholar
  143. Wabnik K, Robert HS, Smith RS et al (2013) Modeling framework for the establishment of the apical–basal embryonic axis in plants. Curr Biol 23:2513–2518PubMedCrossRefGoogle Scholar
  144. Walters J, Osborne DJ (1979) Ethylene and auxin-induced cell growth in relation to auxin transport and metabolism and ethylene production in the semi-aquatic plant, Regnellidium diphyllum. Planta 146:309–317PubMedCrossRefGoogle Scholar
  145. Walton J (1964) On the morphology of Zosterophyllum and some other early Devonian plants. Phytomorphology 14:155–160Google Scholar
  146. Wang Q, Hasson A, Rossmann S et al (2016) Divide et impera: boundaries shape the plant body and initiate new meristems. New Phytol 209:485–498PubMedCrossRefGoogle Scholar
  147. Wangermann E (1967) The effect of the leaf on differentiation of primary xylem in the internode of Coleus blumei Benth. New Phytol 66:747–754CrossRefGoogle Scholar
  148. Wardlaw CW (1944) Experimental and analytical studies of pteridophytes. IV. Stelar morphology: experimental observations on the relation between leaf development and stelar morphology in species of Dryopteris and Onoclea. Ann Bot 8:387–399CrossRefGoogle Scholar
  149. Wardlaw CW (1946) Experimental and analytical studies of pteridophytes. VII. Stelar morphology: the effect of defoliation on the stele of Osmunda and Todea. Ann Bot 9:97–107CrossRefGoogle Scholar
  150. Wendrich JR, Weijers D (2013) The Arabidopsis embryo as a miniature morphogenesis model. New Phytol 199:14–25PubMedCrossRefGoogle Scholar
  151. White RA (1971) Experimental and developmental studies of the fern sporophyte. Bot Rev 37:509–540CrossRefGoogle Scholar
  152. Wilson JP, Montanez IP, White JD et al (2017) Dynamic Carboniferous tropical forests: new views of plant function and potential for physiological forcing of climate. New Phytol 215:1333.  https://doi.org/10.1111/nph.14700 PubMedCrossRefGoogle Scholar
  153. Wochok ZS, Sussex IM (1973) Morphogenesis in Selaginella. Auxin transport in the stem. Plant Physiol 51:646–650PubMedPubMedCentralCrossRefGoogle Scholar
  154. Wochok ZS, Sussex IM (1974) Morphogenesis in Selaginella. II. Auxin transport in the root (rhizophore). Plant Physiol 53:738–741PubMedPubMedCentralCrossRefGoogle Scholar
  155. Wochok ZS, Sussex IM (1976) Redetermination of cultured root tips to leafy shoots in Selaginella willdenowii. Plant Sci Lett 6:185–192CrossRefGoogle Scholar
  156. Zhou C, Han L, Fu C et al (2013) The trans-acting short interfering RNA3 pathway and NO APICAL MERISTEM antagonistically regulate leaf margin development and lateral organ separation, as revealed by analysis of an argonaute7/lobed leaflet1 mutant in Medicago truncatula. Plant Cell 25:4845–4862PubMedPubMedCentralCrossRefGoogle Scholar
  157. Zhu M, Ahlberg PE (2004) The origin of the internal nostril of tetrapods. Nature 432:94–97PubMedCrossRefGoogle Scholar
  158. Zimmermann W (1938) Die Telometheorie. Biologe 7:385–391Google Scholar
  159. Zimmermann W (1952) Main results of the “Telome theory”. Palaeobotanist 1:456–470Google Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Kelly K. S. Matsunaga
    • 1
  • Alexandru M. F. Tomescu
    • 2
  1. 1.Department of Earth and Environmental SciencesUniversity of MichiganAnn ArborUSA
  2. 2.Department of Biological SciencesHumboldt State UniversityArcataUSA

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