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

Water-impermeable fruits of the parasitic angiosperm Cassytha filiformis (Lauraceae): confirmation of physical dormancy in Magnoliidae and evolutionary considerations

Niranjan Mahadevan A and K. M. G. Gehan Jayasuriya A B C
+ Author Affiliations
- Author Affiliations

A Department of Botany, University of Peradeniya, Peradeniya, 20400, Sri Lanka.

B Postgraduate Institute of Science, University of Peradeniya, Peradeniya, 20400, Sri Lanka.

C Corresponding author. Email: gejaya@gmail.com

Australian Journal of Botany 61(4) 322-329 https://doi.org/10.1071/BT12275
Submitted: 26 October 2012  Accepted: 1 May 2013   Published: 13 June 2013

Abstract

Physical dormancy (PY) in seeds or fruits has been reported in 17 angiosperm families but not in basal angiosperms, magnoliids or gymnosperms. Here, we report PY in fruits (germination unit) of Cassytha filiformis, a parasitic species in the magnoliid clade. Moisture content of fruits ranged from 10% to 16%, and the seeds are orthodox (desiccation tolerant). Manually scarified fruits increased in mass >80% during imbibition, whereas untreated fruits increased <16%, via only a few fruits imbibing. Thus, the fruits are water impermeable. Dye did not penetrate the lignified palisade layer in the endocarp. Dye tracking of innately non-dormant fruits suggested that the carpellary micropyle is the water gap in C. filiformis fruits. Manual scarification broke dormancy of most, but not all, C. filiformis fruits. Thus, a high percentage of the germination units have PY and a low percentage PY + physiological dormancy. This is the first verified report of PY in the magnoliids; PY is now known to occur in four of the five major angiosperm clades. The evolutionary aspects of PY in Cassytha, an isolated genus in Lauraceae, are discussed.

Additional keywords: basal angiosperm, fruit-coat anatomy, parasitic flowering plant, orthodox storage behaviour, water-impermeable endocarp.


References

Angiosperm Phylogeny Group (APG-III) (2009) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG-III. Botanical Journal of the Linnean Society 161, 105–121.
An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG-III.Crossref | GoogleScholarGoogle Scholar |

Baskin CC, Baskin JM (1998) ‘Seeds: ecology, biogeography, and evolution of dormancy and germination.’ (Academic Press: San Diego, CA)

Baskin JM, Baskin CC (2000) Evolutionary considerations for claims for physical dormancy-break by microbial action and abrasion by soil particles. Seed Science Research 10, 409–413.

Baskin JM, Baskin CC (2004) A classification system for seed dormancy. Seed Science Research 14, 1–16.
A classification system for seed dormancy.Crossref | GoogleScholarGoogle Scholar |

Baskin JM, Baskin CC, Li X (2000) Taxonomy, anatomy and evolution of physical dormancy in seeds. Plant Species Biology 15, 139–152.
Taxonomy, anatomy and evolution of physical dormancy in seeds.Crossref | GoogleScholarGoogle Scholar |

Baskin JM, Baskin CC, Dixon KW (2006) Physical dormancy in the endemic Australian genus Stylobasium, a first report for the family Surianaceae (Fabales). Seed Science Research 16, 229–232.
Physical dormancy in the endemic Australian genus Stylobasium, a first report for the family Surianaceae (Fabales).Crossref | GoogleScholarGoogle Scholar |

Britton T (2002) Impact of Cassytha pubescens R.Br. on the physiology and growth of gorse (Ulex europaeus L.) in south Australia. MSc Thesis, University of Adelaide.

Chang F-R, Chao Y-C, Teng C-M (1998) Chemical constituents from Cassytha filiformis II. Journal of Natural Products 61, 863–866.
Chemical constituents from Cassytha filiformis II.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXktlWjs74%3D&md5=18c503100817f3659edb453bab900e8bCAS | 9677264PubMed |

Clauss MJ, Venable DL (2000) Seed germination in desert annuals: an empirical test of bet-hedging. American Naturalist 155, 168–186.
Seed germination in desert annuals: an empirical test of bet-hedging.Crossref | GoogleScholarGoogle Scholar | 10686159PubMed |

Corner EJH (1976) ‘The seeds of dicotyledons, 2 vols.’ (Cambridge University Press: Cambridge, UK)

Dassanayaka MD (1983) ‘A revised hand book to the flora of Ceylon.’ (Amerind Publishing Company: New Delhi)

Finch-Savage WE, Leubner-Metzger G (2006) Seed dormancy and the control of germination. New Phytologist 171, 501–523.
Seed dormancy and the control of germination.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XpsVertbw%3D&md5=545ae0dce9d94749c9d4bf86e9bf6784CAS | 16866955PubMed |

French K, Westoby M (1996) Vertebrate-dispersed species in a fire prone environment. Australian Journal of Botany 21, 379–385.

Gama-Arachchige NS, Baskin JM, Geneve RL, Baskin CC (2010) Identification and characterization of the water gap in physically dormant seeds of Geraniaceae, with special reference to Geranium carolinianum. Annals of Botany 105, 977–990.
Identification and characterization of the water gap in physically dormant seeds of Geraniaceae, with special reference to Geranium carolinianum.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3czmtFersg%3D%3D&md5=9e98c1588e6f7393c5dce0fd79c5121aCAS | 20400757PubMed |

Gama-Arachchige NS, Baskin JM, Geneve RL, Baskin CC (2012) The autumn effect: timing of physical dormancy break in seeds of two winter annual species of Geraniaceae by a stepwise process. Annals of Botany 110, 637–651.
The autumn effect: timing of physical dormancy break in seeds of two winter annual species of Geraniaceae by a stepwise process.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38jgsFSntQ%3D%3D&md5=d90f07704525c01b943b9106a1656c0dCAS | 22684684PubMed |

Gworgwor NA, Ndahi WB, Weber HC (2001) Parasitic weeds of north eastern region of Nigeria; a new potential threat to crop production. In ‘Proceedings of BCPC conference on weeds’. (Ed. CJ Leaver) pp. 181–186. (British Crop Protection Council: Brighton, UK)

Haynes AR, Coile NC, Schubert TS (1996) ‘Comparison of two parasitic vines: dodder (Cuscuta) and woe vine (Cassytha).’ Division of Plant Industry Botany Circular 30. (Florida Department of Agriculture Consumer Services: Tallahassee, FL)

Heide-Jørgensen HS (1991) Anatomy and ultrastructure of the haustorium of Cassytha pubescens R.Br. I. The adhesive disk. Botanical Gazette 152, 321–334.
Anatomy and ultrastructure of the haustorium of Cassytha pubescens R.Br. I. The adhesive disk.Crossref | GoogleScholarGoogle Scholar |

Hoet S, Stevigny C, Block S, Opperdoes F, Colson P, Baldeyrou B, Lansiaux A, Bailly C, Quetin-Lecleraq J (2004) Alkaloids from Cassytha filiformis and related aporphines, antitrypanosomal activity, cytotoxicity and interaction with DNA and topoisomerases. Planta Medica 70, 407–413.
Alkaloids from Cassytha filiformis and related aporphines, antitrypanosomal activity, cytotoxicity and interaction with DNA and topoisomerases.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXktlOkurw%3D&md5=d3447bb32c8df4aa72d1a5a285006ee3CAS | 15124084PubMed |

Hutchison JM, Ashton FM (1979) Effect of desiccation and scarification on the permeability and structure of the seed coat of Cuscuta compestris. American Journal of Botany 66, 40–46.
Effect of desiccation and scarification on the permeability and structure of the seed coat of Cuscuta compestris.Crossref | GoogleScholarGoogle Scholar |

International Seed Testing Association (ISTA) (2008) ‘International rules for seed testing.’ (ISTA: Bassersdorf, Switzerland)

Jain JB, Kumane SC, Bhattaccharya S (2006) Medicinal flora of Madhya Pradesh and Chattiggarh: a review. Indian Journal of Traditional Knowledge 5, 237–242.

Jayasuriya KMGG, Baskin JM, Baskin CC (2008a) Cycling of sensitivity to physical dormancy-break in seeds of Ipomoea lacunosa (Convolvulaceae) and ecological significance. Annals of Botany 101, 341–352.
Cycling of sensitivity to physical dormancy-break in seeds of Ipomoea lacunosa (Convolvulaceae) and ecological significance.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1c%2FnvFahtQ%3D%3D&md5=8e225c966a2713cc252c51af51cf6aa3CAS |

Jayasuriya KMGG, Baskin JM, Geneve RL, Baskin CC, Chien C-T (2008b) Physical dormancy in seeds of the holoparasitic angiosperm Cuscuta australis (Convolvulaceae, Cuscuteae): dormancy-breaking requirements, anatomy of the water gap and sensitivity cycling. Annals of Botany 102, 39–48.
Physical dormancy in seeds of the holoparasitic angiosperm Cuscuta australis (Convolvulaceae, Cuscuteae): dormancy-breaking requirements, anatomy of the water gap and sensitivity cycling.Crossref | GoogleScholarGoogle Scholar |

Jones SR, Lamberton JA (1966) Cassytha alkaloids. I. New aporphine alkaloids from Cassytha filiformis L. Australian Journal of Chemistry 19, 297–302.
Cassytha alkaloids. I. New aporphine alkaloids from Cassytha filiformis L.Crossref | GoogleScholarGoogle Scholar |

Josekutty PC, Wakuk EE, Joseph MJ (2002) Invasive/weedy angiosperms in Kosrae, FSM. Micronesica 6, 61–65.

Koutsovoulou K, Vassiliades D, Yannitsaros A, Thanos CA (2005) Seed germination of Biebersteinia orphanidis Boiss. Proceedings of the Greek Botanical Society 10, 331–337. [in Greek with English abstract]

Li Y-H, Yao D-R (1992) Anatomical and histochemical studies of haustorial development of Cassytha filiformis L. Acta Botanica Sinica 34, 753–757. [in Chinese with English abstract]

Li X, Baskin JM, Baskin CC (1999a) Anatomy of two mechanisms of breaking physical dormancy by experimental treatments in seeds of two North American Rhus species (Anacardiaceae). American Journal of Botany 86, 1505–1511.
Anatomy of two mechanisms of breaking physical dormancy by experimental treatments in seeds of two North American Rhus species (Anacardiaceae).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3Mngs1Gmuw%3D%3D&md5=f6bb4c4ad374f79c283ec914ca8de207CAS | 10562242PubMed |

Li X, Baskin JM, Baskin CC (1999b) Physiological dormancy and germination requirements of seeds of several North American Rhus species. Seed Science Research 9, 237–245.

Linkies A, Graeber K, Knight C, Leubner-Metzger G (2010) The evolution of seeds. New Phytologist 186, 817–831.
The evolution of seeds.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXotVWhtb8%3D&md5=a4785877ff99952bb4ef95e2e76e97adCAS | 20406407PubMed |

McLuckie J (1924) Studies in parasitism. I. A contribution to the physiology of the genus Cassytha. Proceedings of the Linnean Society of New South Wales 49, 55–79.

Mukhtar I, Khokhar I, Mushtaq S (2010) First report on Cassytha filiformis. l. (Lauraceae), a parasitic weed from Lahore, Pakistan. Pakistan Journal of Weed Science 16, 451–457.

Mythili S, Gajalakshmi S, Sathiavelu A, Sridharan TB (2011a) Pharmacological activities of Cassytha filiformis: a review. Asian Journal of Plant Science and Research 1, 77–83.

Mythili S, Sathiavelu A, Sridharan TB (2011b) Antimicrobial activity of selected Indian folk medicinal plants. Journal of Pharmacy Research 4, 1894–1898.

Mythili S, Sathiavelu A, Sridharan TB (2011c) Evaluation of antioxidant activity of Cassytha filiformis. International Journal of Applied Biology and Pharmaceutical Technology 2, 380–385.

Nelson SC (2008) Cassytha filiformis. Plant Disease 42, 1–10.

Press MC, Phoenix GK (2005) Impacts of parasitic plants on natural communities. New Phytologist 166, 737–751.
Impacts of parasitic plants on natural communities.Crossref | GoogleScholarGoogle Scholar | 15869638PubMed |

Qu X, Baskin JM, Baskin CC (2010) Whole-seed development in Sicyos angulatus (Cucurbitaceae, Sicyeae) and a comparison with the development of water impermeable seeds in five other families. Plant Species Biology 25, 185–192.
Whole-seed development in Sicyos angulatus (Cucurbitaceae, Sicyeae) and a comparison with the development of water impermeable seeds in five other families.Crossref | GoogleScholarGoogle Scholar |

Qu X, Baskin JM, Baskin CC (2012) Combinational dormancy in seeds of Sicyos angulatus (Cucurbitaceae, tribe Sicyeae). Plant Species Biology 27, 119–123.
Combinational dormancy in seeds of Sicyos angulatus (Cucurbitaceae, tribe Sicyeae).Crossref | GoogleScholarGoogle Scholar |

Quetin-Leclercq J, Hoet S, Block S, Wautier MC, Stévigny C (2004) Studies on Cassytha filiformis from Benin: isolation, biological activities and quantification of aporphines. In ‘Proceedings of bioresources towards drug discovery and development’. pp: 81–107. University of Mauritius, Réduit. Available at http://www.farm.ucl.ac.be/Full-texts-FARM/Quetin-Leclercq-2004-1.pdf [Verified 16 May 2013]

Raj B, Singh SDJ, John S, Siddiqua A (2011) Pharmacognostic and preliminary phytochemical screening of Cassytha filiformis. Research Journal of Pharmacognosy and Phytochemistry 3, 151–153.

Rangaswamy NS, Rangan TS (1971) Morphogenic investigations on parasitic angiosperms. IV. Morphogenesis in decotylated embryos of Cassytha filiformis L. Lauraceae. Botanical Gazette 132, 113–119.
Morphogenic investigations on parasitic angiosperms. IV. Morphogenesis in decotylated embryos of Cassytha filiformis L. Lauraceae.Crossref | GoogleScholarGoogle Scholar |

Rao PRM (1980) Seed and fruit anatomy of Cassytha filiformis L. with comments on its systematic position. Israel Journal of Botany 28, 44–49.

Rohwer JG, Rudolph B (2005) The phylogenetic positions of Cassytha, Hypodaphnis, and Neocinnamomum (Lauraceae) based on different analyses of trnK intron sequences. Annals of the Missouri Botanical Garden 92, 153–178.

Sastri RLN (1962) Embryology of Cassytha. Botanical Gazette 123, 197–206.
Embryology of Cassytha.Crossref | GoogleScholarGoogle Scholar |

Schroeder CA (1967) The stem parasite Cassytha filiformis, a botanical relative of avocado. California Avocado Society Yearbook 51, 159–160.

Tsang HS (2010) Cassytha pubescens: germination biology and interactions with native and introduced hosts. MSc Thesis, University of Adelaide.

Van Assche JA, Dubucquoy KLA, Rommens WAF (2003) Seasonal cycles in the germination capacity of buried seeds of some Leguminosae (Fabaceae). New Phytologist 158, 315–323.
Seasonal cycles in the germination capacity of buried seeds of some Leguminosae (Fabaceae).Crossref | GoogleScholarGoogle Scholar |

Venable DL (1985) The evolutionary ecology of seed heteromorphism. American Naturalist 126, 577–595.
The evolutionary ecology of seed heteromorphism.Crossref | GoogleScholarGoogle Scholar |

Visser J (1981) ‘South African parasitic flowering plants.’ (Juta and Company: Capetown, South Africa)

Waterhouse DF (1997) ‘The major invertebrate pests and weeds of agriculture and plantation forestry in the southern and western Pacific.’ Australian Center for International Agricultural Research (AClAR) Monograph No. 44. (Australian Centre for International Agricultural Research: Canberra)

Werth C, Pusateri WP, Eshbaugh WH, Wilson TK (1979) Field observations on the natural history of Cassytha filiformis L. (Lauraceae) in the Bahamas. In ‘Proceedings of second international symposium on parasitic weeds’. (Eds LJ Musselman, AD Worsham, RE Eplee) pp. 94–102. (North Carolina State University: Raleigh, NC)

Wills TJ, Read J (2002) Effects of heat and smoke on germination of soil-stored seed in a south eastern Australian sand heath land. Australian Journal of Botany 50, 197–206.
Effects of heat and smoke on germination of soil-stored seed in a south eastern Australian sand heath land.Crossref | GoogleScholarGoogle Scholar |