Register      Login
Australian Journal of Botany Australian Journal of Botany Society
Southern hemisphere botanical ecosystems
RESEARCH ARTICLE

Survival strategies of the root tuberous geophyte Chamaescilla corymbosa in a Mediterranean-climate rock-outcrop environment

Michael W. Shane A B and John S. Pate A
+ Author Affiliations
- Author Affiliations

A School of Plant Biology (M084), Faculty of Science, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia.

B Corresponding author. Email: michael.shane@uwa.edu.au

Australian Journal of Botany 63(6) 497-511 https://doi.org/10.1071/BT14220
Submitted: 4 September 2014  Accepted: 6 June 2015   Published: 3 August 2015

Abstract

This field-based study aimed to identify adaptive traits that operate interactively and sequentially towards survival and growth of the perennial geophyte Chamaescilla corymbosa when inhabiting shallow soils on exposed granite outcrops in south-western Australia. During an annual cycle of growth and dormancy, we measured changes in biomass partitioning, mineral nutrient concentrations in root tubers, leaves, roots and seed. Anatomical and histochemical analyses of fleshy-root tubers included identification and quantification of key carbohydrate and free amino acid reserves. During the course of the growing season, developing root tubers accumulated fructans, raffinose and sucrose to maximal concentration at the onset of summer dormancy. Water content of root tubers was similar in summer or winter (79% or 84%, respectively). Accumulation of carbohydrates and development of a lignified and suberised hypodermis are likely to protect aestivating root tubers from desiccation during hot, dry summer. Assimilates and mineral resources acquired in the winter growing season were shown to be preferentially allocated for new tuber production, as opposed to sexual reproduction. Accumulation of key nitrogenous solutes and phosphorus in root tubers before dormancy suggested an adaptive response of the species to soils with inherently low concentrations of available nutrients. Experiments on field-grown populations showed the species to be responsive to delayed commencement of seasonal growth by reducing size and number of root tubers; however, plants still survived until the next growing season. Results are discussed against previous studies of other geophytes on rock outcrops and other similarly testing environments.

Additional keywords: Asparagaceae, drought resistance, inselbergs, perennial monocotyledon, resource carry-over, root tubers.


References

Brundrett MC, Enstone DE, Peterson CA (1988) A berberine–aniline blue fluorescent staining procedure for suberin, lignin, and callose in plant tissue. Protoplasma 146, 133–142.
A berberine–aniline blue fluorescent staining procedure for suberin, lignin, and callose in plant tissue.Crossref | GoogleScholarGoogle Scholar |

Dixon KW, Kuo J, Pate JS (1983) Storage reserves of the seed-like, aestivating organs of geophytes inhabiting granite outcrops in south-western Australia. Australian Journal of Botany 31, 85–103.
Storage reserves of the seed-like, aestivating organs of geophytes inhabiting granite outcrops in south-western Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXhsVSmur8%3D&md5=75e7070d26e0ed00461e2488a401f3eeCAS |

Gaff DF, Churchill DM (1976) Borya nitida Labill.: an Australian species in the Liliaceae with desiccation tolerant leaves. Australian Journal of Botany 24, 209–224.
Borya nitida Labill.: an Australian species in the Liliaceae with desiccation tolerant leaves.Crossref | GoogleScholarGoogle Scholar |

Gandin A, Gutjahr S, Dizengremel P, Lapointe L (2011) Source–sink imbalance increases with growth temperature in the spring geophyte Erythronium americanum. Journal of Experimental Botany 62, 3467–3479.
Source–sink imbalance increases with growth temperature in the spring geophyte Erythronium americanum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXoslOmu74%3D&md5=45704357a4e1f096545639aca13dd48eCAS | 21335435PubMed |

Gibson N, Keighery GJ, Lyons MN, Webb A (2004) Terrestrial flora and vegetation of the Western Australian wheatbelt. Records of the Western Australian Museum Supplement No. 67, 139–189.

Groom PK, Lamont BB (1995) Leaf morphology and life form influence water relations of Hakea species on different soil substrates within southwestern Australia. Acta Oecologica 16, 609–620.

Guy C (1990) Freezing stress tolerance: role of protein metabolism. Annual Review of Plant Physiology and Plant Molecular Biology 41, 187–223.
Freezing stress tolerance: role of protein metabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXksFGkurY%3D&md5=df1e3a1c54dd413860909fb712554ac5CAS |

Hendry G (1987) The ecological significance of fructan in a contemporary flora. New Phytologist 106, 201–216.
The ecological significance of fructan in a contemporary flora.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXktlKmt7Y%3D&md5=bac98dfdd354720a13d0bd081b38f8beCAS |

Hopper SD, Gioia P (2004) The southwest Australian floristic region: evolution and conservation of a global hot spot of biodiversity. Annual Review of Ecology Evolution and Systematics 35, 623–650.
The southwest Australian floristic region: evolution and conservation of a global hot spot of biodiversity.Crossref | GoogleScholarGoogle Scholar |

Hopper SD, Brown AP, Marchant NG (1997) Plants of Western Australian granite outcrops. Journal of the Royal Society of Western Australia 80, 141–158.

Ingram J, Bartels D (1996) The molecular basis of dehydration tolerance in plants. Annual Review of Plant Physiology and Plant Molecular Biology 47, 377–403.
The molecular basis of dehydration tolerance in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XjtlWgtr0%3D&md5=21b0d650a08d6c70ca2b03622496cd75CAS | 15012294PubMed |

Jensen WA (1962) ‘Botanical Histochemistry.’ (Freeman: San Francisco, CA)

Kamenetsky R, Peterson RL, Melville LH, Machado CF, Bewley JD (2005) Seasonal adaptations of the tuberous roots of Ranunculus asiaticus to desiccation and resurrection by changes in cell structure and protein content. New Phytologist 166, 193–204.
Seasonal adaptations of the tuberous roots of Ranunculus asiaticus to desiccation and resurrection by changes in cell structure and protein content.Crossref | GoogleScholarGoogle Scholar | 15760363PubMed |

Keppel G, Van Niel KP, Wardell-Johnson GW, Yates CJ, Byrne M, Mucina L, Schut GT, Hopper SD, Franklin SE (2012) Refugia: identifying and understanding safe havens for biodiversity under climate change. Global Ecology and Biogeography 21, 393–404.
Refugia: identifying and understanding safe havens for biodiversity under climate change.Crossref | GoogleScholarGoogle Scholar |

Khodorova NV, Miroslavov EA, Shavarda AL, Laberche JC, Boitel-Conti M (2010) Bud development in corydalis (Corydalis bracteata) requires low temperature: a study of developmental and carbohydrate changes. Annals of Botany 105, 891–903.
Bud development in corydalis (Corydalis bracteata) requires low temperature: a study of developmental and carbohydrate changes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmvVWltb4%3D&md5=83571f3b37c5fce69243583e3f6735d8CAS | 20382640PubMed |

Kuo J, Hocking PJ, Pate JS (1982) Nutrient reserves in seeds of selected proteaceous species from south-western Australia. Australian Journal of Botany 30, 231–249.
Nutrient reserves in seeds of selected proteaceous species from south-western Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38Xkt1aksbY%3D&md5=c5904c6e01dc0af0ba1e898e4032e6f3CAS |

Lambers H, Brundrett MC, Raven JA, Hopper SD (2010) Plant mineral nutrition in ancient landscapes: high plant species diversity on infertile soils is linked to functional diversity for nutritional strategies. Plant and Soil 334, 11–31.
Plant mineral nutrition in ancient landscapes: high plant species diversity on infertile soils is linked to functional diversity for nutritional strategies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVaqtbnJ&md5=19baaa1f1509bffcc2ba0630cf658b8dCAS |

Lambers H, Shane MW, Laliberté E, Swarts ND, Teste FP, Zemunik G (2014) Plant mineral nutrition. In ‘Plant life on the sandplains in southwest Australia, a global biodiversity hotspot’. (Ed. H Lambers) pp. 101–127. (UWA Publishing: Perth)

Lapointe L (1998) Fruit development in Trillium. Dependence on stem carbohydrate reserves. Plant Physiology 117, 183–188.
Fruit development in Trillium. Dependence on stem carbohydrate reserves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjsFSktr4%3D&md5=3decc36da3e84fce09b58af3f9f77197CAS | 9576787PubMed |

Marschner H (1995) ‘Mineral nutrition of higher plants.’ 2nd edn. (Academic Press: London)

Mehlich A (1978) New extractant for soil test evaluation of phosphorus, potassium, magnesium, calcium, sodium, manganese and zinc. Communications in Soil Science and Plant Analysis 9, 477–492.
New extractant for soil test evaluation of phosphorus, potassium, magnesium, calcium, sodium, manganese and zinc.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1cXlt1ygs7g%3D&md5=a3fbb4852db3f288fe60407ae69dcb17CAS |

Miller WB (1992) A review of carbohydrate metabolism in geophytes. Acta Horticulturae 325, 239–246.

Moraes T, Plaxton WC (2000) Purification and characterization of phosphoenolpyruvate carboxylase from Brassica napus (rapeseed) suspension cell cultures. Implications for phosphoenolpyruvate carboxylase regulation during phosphate starvation, and the integration of glycolysis with nitrogen assimilation. European Journal of Biochemistry 267, 4465–4476.
Purification and characterization of phosphoenolpyruvate carboxylase from Brassica napus (rapeseed) suspension cell cultures. Implications for phosphoenolpyruvate carboxylase regulation during phosphate starvation, and the integration of glycolysis with nitrogen assimilation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlt1Gnu7Y%3D&md5=c81b266070d723faed476e0888636f36CAS | 10880970PubMed |

Nikulinsky P, Hopper SD (2008) ‘Life on the rocks. The art of survival.’ 2nd edn. (Fremantle Arts Centre Press: Fremantle, WA)

O’Brien TP, McCully ME (1981) ‘The study of plant structure. Principles and selected methods.’ (Termarcarphi: Melbourne)

Oliveira VF, Silva EA, Zaidan LB, Carvalho MAM (2013) Effects of elevated CO2 concentration and water deficit on fructan metabolism in Viguiera discolour Baker. Plant Biology 15, 471–482.
Effects of elevated CO2 concentration and water deficit on fructan metabolism in Viguiera discolour Baker.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXosVKks7k%3D&md5=7785e594245662232650fa699077b5eeCAS | 22882384PubMed |

Orthen B (2001) Sprouting of the fructan- and starch-storing geophyte Lachenalia minima: effects on carbohydrate and water content within the bulbs. Physiologia Plantarum 113, 308–314.
Sprouting of the fructan- and starch-storing geophyte Lachenalia minima: effects on carbohydrate and water content within the bulbs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXosFynuro%3D&md5=f7bb75ce9298f229ec4c3e22caba76edCAS | 12060274PubMed |

Pate JS, Dixon KW (1982) ‘Tuberous, cormous and bulbous plants: biology of an adaptive strategy in Western Australia.’ (University of Western Australia Press: Perth)

Pate JS, Rasins E, Rullo J, Kuo J (1986) Seed nutrient reserves of Proteaceae with special reference to protein bodies and their inclusions. Annals of Botany 57, 747–770.
Seed nutrient reserves of Proteaceae with special reference to protein bodies and their inclusions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28XksFOqtLc%3D&md5=2003c460dd7dc621957b15d0e5b00e7bCAS |

Peshev D, Vergauwen R, Moglia A, Hileg A, Van den Ende W (2013) Towards understanding vacuolar antioxidant mechanisms: a role for fructans? Journal of Experimental Botany 64, 1025–1038.
Towards understanding vacuolar antioxidant mechanisms: a role for fructans?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjtlGrtro%3D&md5=0cd005fa90643fe389be7ab706d7398fCAS | 23349141PubMed |

Peterson L, Peterson CA, Melville LH (2008) ‘Teaching plant anatomy: through creative laboratory exercises.’ (National Research Council of Canada: Ottawa, Canada)

Pomar F, Caballero N, Pedreño MA, Ros Barceló A (2002) H2O2 generation during the auto‐oxidation of coniferyl alcohol drives the oxidase activity of a highly conserved class III peroxidase involved in lignin biosynthesis. FEBS Letters 529, 198–202.
H2O2 generation during the auto‐oxidation of coniferyl alcohol drives the oxidase activity of a highly conserved class III peroxidase involved in lignin biosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xns1ansbc%3D&md5=6da4d34806a8619dae1f6451e52ab25dCAS | 12372600PubMed |

Porembski S, Barthlott W (2000) Inselbergs: biotic diversity of isolated rock outcrops in tropical and temperate regions. Plant Ecology 151, 19–28.
Inselbergs: biotic diversity of isolated rock outcrops in tropical and temperate regions.Crossref | GoogleScholarGoogle Scholar |

Ruzin SE (1999) ‘Plant microtechnique and microscopy.’ (Oxford University Press: New York, NY)

Shane MW, Fedosejevs ET, Plaxton WC (2013) Reciprocal control of anaplerotic phosphoenolpyruvate carboxylase by in vivo monoubiquitination and phosphorylation in developing proteoid roots of phosphate-deficient harsh Hakea. Plant Physiology 161, 1634–1644.
Reciprocal control of anaplerotic phosphoenolpyruvate carboxylase by in vivo monoubiquitination and phosphorylation in developing proteoid roots of phosphate-deficient harsh Hakea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmt1ygs7s%3D&md5=12fdd85ff54a7f0b1089d79d8e712cb8CAS | 23407057PubMed |

Taleisnik E, Peyrano G, Córdoba A, Arias C (1999) Water retention capacity in root segments differing in the degree of exodermis development. Annals of Botany 83, 19–27.
Water retention capacity in root segments differing in the degree of exodermis development.Crossref | GoogleScholarGoogle Scholar |

Wilson CA, Peterson CA (1983) Chemical composition of the epidermal, hypodermal, endodermal and intervening cortical cell walls of various plant roots. Annals of Botany 51, 759–769.