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Foliar ontogeny in Gymnostoma deplancheanum and its evolutionary and ecological significance for scleromorphy and xeromorphy in Casuarinaceae (Fagales)

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The phylogenetically basal genus of the Casuarinaceae, Gymnostoma, from relatively mesic environments, shows morphological and anatomical structures that are precursors to xeromorphic modifications in the derived genera Casuarina and Allocasuarina.

Abstract

Gymnostoma is the basal genus of the Casuarinaceae with a long evolutionary history and a morphology that has changed little over many millions of years. From a wide distribution in the Tertiary of the southern hemisphere, it is now restricted to islands in the Pacific Ocean, the Malesian region and one small area of northeastern Queensland where it occurs in mesic climates, often on poor soils. The unique vegetative morphology it shares with other more derived genera in the family appears to be xeromorphic. Its distribution combined with the fossil evidence that early Tertiary Gymnostoma occurred with other taxa whose morphology indicated they grew in mesic environments implies that the reduction in the photosynthetic organs was not specifically related to growing in xeric environments. It may be related to evolutionary adaptation to growing on nutrient poor substrates that may also suffer from seasonal water deficit. The foliage reduction then served as a pre-adaptation for derived species to help them cope with the aridity that developed on the Australian continent through the later part of the Tertiary. The fusion of the leaves to the stem to form phyllichnia was a precursor which enabled the development of specific adaptations in the derived genera Casuarina and Allocasuarina to improve water conservation, such as stomata restricted to furrows between the phyllichnia and proliferation of structural sclerenchyma that helps prevent cell collapse under drought conditions.

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References

  • Arena DA (2008) Exceptional preservation of plants and invertebrates by phosphatization, Riversleigh, Australia. Palaios 23:495–502

    Article  Google Scholar 

  • Barlow BA (1983) Casuarinas—a taxonomic and biogeographic review. In: Midgley SJ, Turnbull JW, Johnston RD (eds) Casuarina Ecology management and utilization. CSIRO, Melbourne, pp 10–18

    Google Scholar 

  • Bresinsky A, Körner C, Kadereit JW, Neuhaus G, Sonnewald U (2008) Strasburger, Lehrbuch der Botanik, 36th. Spektrum, Heidelberg

    Google Scholar 

  • Carpenter RJ, Macphail MK, Jordan GJ, Hill RS (2015) Fossil evidence for open, Proteaceae-dominated heathlands and fire in the late Cretaceous of Australia. Am J Bot 102:2092–2107

    Article  PubMed  Google Scholar 

  • Christophel DC (1980) Occurrence of Casuarina megafossils in the Tertiary of south-eastern Australia. Aust J Bot 28:249–259

    Article  Google Scholar 

  • de Micco V, Aronne G (2012) Morpho-anatomical traits for plant adaptation to drought. In: Aroca R (ed) Plant responses to drought stress. Springer, Berlin, pp 37–61

    Chapter  Google Scholar 

  • Dilcher DL, Christophel DC, Bhagwandin HO, Scriven LJ (1990) Evolution of the Casuarinaceae: morphological comparisons of some extant species. Am J Bot 77:338–355

    Article  Google Scholar 

  • Dörken VM, Parsons RF (2017) Morpho-anatomical studies on the leaf reduction in Casuarina (Casuarinaceae): the ecology of xeromorphy. Trees 31:1165–1177

    Article  Google Scholar 

  • Dörken VM, Ladd PG, Parsons RF (2018) The foliar change from seedlings to adults in Allocasuarina (Casuarinaceae): the evolutionary and ecological aspects of leaf reduction, xeromorphy and scleromorphy. Feddes Rep 129(3):193–222

    Article  Google Scholar 

  • Duhoux E, Franche C, Bogusz D, Diouf D, Le VQ, Gherbi H, Sougoufara B, Le Roux C, Dommergues Y (1996) Casuarina and Allocasuarina species. In: Bajaj YPS (ed) Biotechnology in agriculture and forestry, vol 35. Trees IV. Springer, Berlin

    Google Scholar 

  • Edwards C, Sanson GD, Aranwela N, Read J (2000) Relationships between sclerophylly, leaf biomechanical properties and leaf anatomy in some Australian heath and forest species. Plant Biosyst 134:261–277

    Article  Google Scholar 

  • Flores EM (1977) Developmental studies in Casuarina (Casuarinaceae). III. The anatomy of the mature branchlet. Rev Biol Trop 25:65–87

    Google Scholar 

  • Gaudeul M, Rouhan G, Gardner MF, Hollingsworth PM (2012) AFLP markers provide insights into the evolutionary relationships and diversification of New Caledonian Araucaria species (Araucariaceae). Am J Bot 99:68–81

    Article  PubMed  Google Scholar 

  • Gerlach D (1984) Botanische Mikrotomtechnik, eine Einführung, 2nd edn. Thieme, Stuttgart

    Google Scholar 

  • Gersterberger P, Leins P (1978) Rasterelektronenmikroskopische Untersuchungen an Blütenknospen von Physalis philadelphia (Solanaceae). Ber Deutsch Bot Ges 91:381–387

    Google Scholar 

  • Guerin G (2004) Plant macrofossils associated with the Riversleigh macrofauna. Aust Biol 17:55–62

    Google Scholar 

  • Hanelt P (2000) Casuarinales. In: Fukarek F (ed) Urania Pflanzenreich, Blütenpflanzen 1. Urania, Berlin, pp 125–128

    Google Scholar 

  • He T, Lamont BB, Fogliani B (2016) Pre-Gondwanan-breakup origin of Beauprea (Proteaceae) explains its historical presence in New Caledonia and New Zealand. Sci Adv 2:e1501648

    Article  PubMed  PubMed Central  Google Scholar 

  • Heywood VH (1978) Flowering plants of the world. Oxford University Press, Oxford

    Google Scholar 

  • Heywood VH (1982) Blütenpflanzen der Welt. Birkhäuser, Stuttgart

    Google Scholar 

  • Hill RS (1990) Evolution of the modern high latitude southern hemisphere flora. Evidence from the Australian macrofossil record. In: Douglas JG, Christophel DC (eds) Proceedings 3rd IOP conference, Melbourne 1988. A-Z Publishers, Melbourne, pp 31–42

    Google Scholar 

  • Hill RS (1994) History of selected taxa. In: Hill RS (ed) History of the Australia vegetation: Cretaceous to recent. Cambridge University Press, Cambridge, pp 390–420

    Google Scholar 

  • Hill RS, Brodribb TJ (2001) Macrofossil evidence for the onset of xeromorphy in Australian Casuarinaceae and tribe Banksieae (Proteaceae). J Mediterr Ecol 2:127–136

    Google Scholar 

  • Hill RS, Tarran MA, Hill KE, Beer YK (2018) The vegetation history of South Australia. Swainsona 30:9–16

    Google Scholar 

  • Hwang R, Conran JG (2000) Seedling characteristics in the Casuarinaceae. Telopea 8:429–439

    Article  Google Scholar 

  • Jaffre T, Gaulthier D, Rigault F, McCoy S (1994) Les Casuarinacees endemiques. Bois For Trop 242:4

    Google Scholar 

  • Johnson LAS, Wilson KL (1989) Casuarinaceae: a synopsis. In: Crane PR, Blackmore S (eds) Evolution, systematics and fossil history of the Hamamelidae, vol 2. Clarendon Press, Oxford, pp 167–188

    Google Scholar 

  • Johnson LAS, Wilson KL (1993) Casuarinaceae. In: Kubitzki K, Rohwer JG, Bittrich V (eds) The families and genera of vascular plants. vol 2. Flowering plants, dicotyledons: Magnoliid, Hamamelid and Caryophylloid families. Springer, Berlin, pp 237–242

    Google Scholar 

  • Jordan GJ, Brodribb TJ, Blackman CJ, Weston PH (2013) Climate drives vein anatomy in Proteaceae. Am J Bot 100:1483–1493

    Article  PubMed  Google Scholar 

  • Jurzitza G (1987) Anatomie der Samenpflanzen. Thieme, Stuttgart

    Google Scholar 

  • Kubitzki K, Rohwer JG, Bittrich V (1993) The families and genera of vascular plants. vol 2. Flowering plants, dicotyledons: Magnoliid, Hamamelid and Caryophylloid families. Springer, Berlin

    Google Scholar 

  • Ladd PG (1988) The status of Casuarinaceae in Australian forests. In: Frawley KJ, Semple NM (eds) Australia’s ever changing forests. Proceedings of the first national conference on Australian forest history. ADFA, Canberra, pp 63–85

    Google Scholar 

  • Macklin ED (1927) A revision of the “distyla complex” of the genus Casuarina. Trans R Soc S Aust 51:257–286

    Google Scholar 

  • Maggia L, Bousquet J (1994) Molecular phylogeny of the actinorhizal Hamamelidae and relationships with host promiscuity towards Frankia. Mol Ecol 3:459–467

    Article  Google Scholar 

  • McCoy SG (1998) The dynamics of Gymnostoma maquis on ultramafic soils in New Caledonia. PhD thesis, Australian National University, Canberra

  • Moseley MF (1948) Comparative anatomy and phylogeny of the Casuarinaceae. Bot Gaz 110:231–280

    Article  Google Scholar 

  • Natho G, Müller C, Schmidt H (1990) Morphologie und Systematik der Pflanzen, Teil 1 (A-K). Fischer, Stuttgart, pp 144–146

    Google Scholar 

  • Niinemets Ü, Lukjanova A, Sparrow AD, Turnbull MH (2005) Light acclimation of cladode photosynthetic potentials in Casuarina glauca: trade-offs between physiological and structural investments. Funct Plant Biol 32:571–582

    Article  Google Scholar 

  • Poisson J (1874) Recherches sur les Casuarina. Nouvelles Arch Mus d’Hist Nat t.x pp 59–111, pl. IV–VII

  • Rao AN (1972) Anatomical studies on succulent cladodes in Casuarina equisetifolia. Proc Indian Acad Sci B 76:262–270

    Google Scholar 

  • Read J, Sanson GD (2003) Characterizing sclerophylly: the mechanical properties of a diverse range of leaf types. New Phytol 160:81–99

    Article  Google Scholar 

  • Read J, Sanson GD, de Garine-Wichatitsky M, Jaffre T (2006) Sclerophylly in two contrasting tropical environments: low nutrients vs low rainfall. Am J Bot 93:1601–1614

    Article  PubMed  Google Scholar 

  • Salleo S, Nardini A (2000) Sclerophylly: evolutionary advantage or mere epiphenomenon? Plant Biosyst 134:247–259

    Article  Google Scholar 

  • Schütt P, Schuck HJ, Stimm B (2002) Lexikon der Baum- und Straucharten. Nikol, Hamburg

    Google Scholar 

  • Seddon G (1974) Xerophytes, xeromorphs and sclerophylls: the history of some concepts in ecology. Biol J Linn Soc 6:65–87

    Article  CAS  Google Scholar 

  • Sogo A, Setoguchi H, Noguchi J, Jaffré T, Tobé H (2001) Molecular phylogeny of Casuarinaceae based on rbcL and matK gene sequences. J Plant Res 114:459–464

    Article  CAS  Google Scholar 

  • Solereder H (1908) Systematic anatomy of the dicotyledons. A handbook for laboratories of pure and applied botany, vol 2. Monochlamydeae, Addenda, Concluding remarks. Clarendon Press, Oxford

    Google Scholar 

  • Steane DA, Wilson KL, Hill RS (2003) Using matK sequence data to unravel the phylogeny of Casuarinaceae. Mol Phylogen Evol 28:47–59

    Article  CAS  Google Scholar 

  • Taylor TN, Taylor EL, Krings M (2009) Palaeobotany: the biology and evolution of fossil plants. Academic Press, Burlington

    Google Scholar 

  • Torrey JG, Berg RH (1988) Some morphological features for generic characterization among the Casuarinaceae. Am J Bot 75:864–874

    Article  Google Scholar 

  • Turnbull JW (1990) Taxonomy and genetic variation in Casuarinas. In: El-Lakany MH, Turnbull JW, Brewbaker (eds) Advances in Casuarina research and utilization. In: Proc 2nd Int Casuarina Workshop, Desert Dev Cent, AUC, Cairo, pp 1–11

  • Warrier KCS, Suganthi A, Singh BG (2013) A new record of abnormal phylloclad modification in Casuarina equisetifolia. Int J Agric Sci Res 2:8–11

    Google Scholar 

  • Weiler E, Nover L (2008) Allgemeine und molekulare Botanik. Thieme, Stuttgart

    Book  Google Scholar 

  • Williams RF, Metcalf RA (1985) The genesis of form in Casuarinaceae. Austr J Bot 33:563–578

    Article  Google Scholar 

  • Wilson KL, Johnson LAS (1989) Casuarinaceae. In: George AS (ed) Flora of Australia, vol 3. Hamamelidales to Casuarinales. Australian Government Publishing Service, Canberra, pp 100–174

    Google Scholar 

  • Zamaloa MC, Gandolfo MA, Gonzales CC, Romero EJ, Cuneo NR, Wilf P (2006) Casuarinaceae from the Eocene of Patagonia, Argentina. Int J Plant Sci 167:1279–1289

    Article  Google Scholar 

  • Zimpfer JF, Igual JM, McCarty B, Smyth C, Dawson JO (2004) Casuarina cunninghamiana tissue extracts stimulate the growth of Frankia and differentially alter the growth of other soil microorganisms. J Chem Ecol 30:439–452

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We are grateful to Mrs. Anne Kern (Botanic Garden of the University of Konstanz, Germany) for producing the seedlings. Furthermore, we thank Dr. Michael Laumann and Dr. Paavo Bergmann (Electron Microscopy Center, Department of Biology, University of Konstanz, Germany) for technical support (paraffin technique).

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Authors and Affiliations

  1. Department of Biology, University of Konstanz, M 613, Universitätsstr. 10, 78457, Konstanz, Germany

    V. M. Dörken

  2. School of VLS, Murdoch University, Murdoch, WA, 6150, Australia

    P. G. Ladd

  3. Department of Ecology, Environment and Evolution, La Trobe University, Bundoora, Melbourne, VIC, 3086, Australia

    R. F. Parsons

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Correspondence to V. M. Dörken.

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Dörken, V.M., Ladd, P.G. & Parsons, R.F. Foliar ontogeny in Gymnostoma deplancheanum and its evolutionary and ecological significance for scleromorphy and xeromorphy in Casuarinaceae (Fagales). Trees 33, 653–668 (2019). https://doi.org/10.1007/s00468-018-1806-9

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