Causes of infertility in the endangered Australian endemic plant Borya mirabilis (Boryaceae)
Noushka H. Reiter A C , Neville G. Walsh B and Ann C. Lawrie A D
+ Author Affiliations
- Author Affiliations
A School of Applied Sciences, RMIT University, Bundoora, Vic. 3083, Australia.
B Royal Botanic Gardens Victoria, Birdwood Avenue, Melbourne, Vic. 3004, Australia.
C Present address: Royal Botanic Gardens Victoria, cnr Ballarto Road and Botanic Drive, Cranbourne, Vic. 3977, Australia.
D Corresponding author. Email: aclawrie@rmit.edu.au
Australian Journal of Botany 63(7) 554-565 https://doi.org/10.1071/BT14229
Submitted: 7 September 2014 Accepted: 27 June 2015 Published: 17 August 2015
Abstract
Borya mirabilis Churchill (Boryaceae, Asparagales) is a herbaceous perennial and one of Australia’s most endangered plants. Only one population of four colonies remains, on a rock ledge in the Grampians (Gariwerd) National Park in Victoria, Australia. The reasons why B. mirabilis flowers freely but does not set seed were investigated. Borya mirabilis had a greater proportion of floral abnormalities than other, fertile Borya species. The pollen was often mis-shapen, with ≤ 1% pollen tube formation, but the ovules showed no structural dissimilarity from other, fertile Borya species. The flowers offered a nectar reward and many insects visited the pollen-bearing flowers in the field. Artificial cross-pollination resulted in the first recorded seed for this species. Borya mirabilis has ~66 chromosomes, relative to the diploid number of ~26 in Borya constricta Churchill, strongly suggesting that B. mirabilis is polyploid. Only 4–7% genetic diversity was found within the remaining B. mirabilis field population using 25/60 RAPD primers that showed heterogeneity. An ex-situ nursery collection was found not to contain all genotypes. Recommendations for the conservation of B. mirabilis include capturing all the known genetic diversity in cloned plants in preference over further attempts to produce seed.
Additional keywords: genetic diversity, PCR, polymorphism, polypoidy, RAPD.
References
Adamec L, Tichý M (1997) Flowering of Aldrovanda vesiculosa in outdoor culture in the Czech Republic and isozyme variability of its European populations. Carnivorous Plant Newsletter 26, 99–103.Allen AM, Hiscock SJ (2010) Molecular communication between plant pollen and pistils. In ‘Plant science reviews 2010’. (Ed. D Hemming) pp. 237–248. (CAB International: Wallingford, UK)
Atlas of Living Australia (2007) ‘Occurrence record: VCSB:254. Borya mirabilis: Pincushion Lily.’ (Royal Botanic Gardens Melbourne) Available at: http://biocache.ala.org.au/occurrences/b86cb694-bcf5-493f-b304-442252d3657c [Verified 13 July 2015]
Arrigo N, Barker MS (2012) Rarely successful polyploids and their legacy in plant genomes. Current Opinion in Plant Biology 15, 140–146.
| Rarely successful polyploids and their legacy in plant genomes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XltVKnsr4%3D&md5=2322b5ea7ba4211c9e1348fd8f96c1abCAS | 22480430PubMed |
Blöch C, Weiss-Schneeweiss H, Schneeweiss GM, Barfuss MHJ, Rebernig CA, Villaseñor JL, Stuessy JF (2009) Molecular phylogenetic analyses of nuclear and plastic DNA sequences support dysploid and polyploid chromosome number changes and reticulate evolution in the diversification of Melampodium (Millerieae, Asteraceae). Molecular Phylogenetics and Evolution 53, 220–233.
| Molecular phylogenetic analyses of nuclear and plastic DNA sequences support dysploid and polyploid chromosome number changes and reticulate evolution in the diversification of Melampodium (Millerieae, Asteraceae).Crossref | GoogleScholarGoogle Scholar | 19272456PubMed |
Briggs BG (2002) Chromosome numbers of some native and naturalised plant species in Australia. Telopea 9, 833–835.
| Chromosome numbers of some native and naturalised plant species in Australia.Crossref | GoogleScholarGoogle Scholar |
Burne HM, Yates CJ, Ladd PG (2003) Comparative population structure and reproductive biology of the critically endangered shrub Grevillea althoferorum and two closely related more common congeners. Biological Conservation 114, 53–65.
| Comparative population structure and reproductive biology of the critically endangered shrub Grevillea althoferorum and two closely related more common congeners.Crossref | GoogleScholarGoogle Scholar |
Caetano APS, Teixeira SP, Forni-Martins ER, Carmello-Guerreiro SM (2013) Pollen insights into apomictic and sexual Miconia (Miconieae, Melastomataceae). International Journal of Plant Sciences 174, 760–768.
| Pollen insights into apomictic and sexual Miconia (Miconieae, Melastomataceae).Crossref | GoogleScholarGoogle Scholar |
Caponio I, Anton AM, Fortunato RH, Norrmann GA (2012) Ploidy dimorphism and reproductive biology in Stenodrepanum bergii (Leguminosae), a rare South American endemism. Genome 55, 1–7.
| Ploidy dimorphism and reproductive biology in Stenodrepanum bergii (Leguminosae), a rare South American endemism.Crossref | GoogleScholarGoogle Scholar | 22149537PubMed |
Charlesworth D, Willis JH (2009) The genetics of inbreeding depression. Nature Reviews. Genetics 10, 783–796.
| The genetics of inbreeding depression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht1KrtbrI&md5=42cf98097719d114ac33c802b124d762CAS | 19834483PubMed |
Churchill DM (1985) Three new species of Borya Labill. (Liliaceae). Muelleria 6, 1–8.
Churchill DM (1987) Borya. In ‘Flora of Australia. Vol. 45, Hydatellaceae to Liliaceae’. (Ed. AS George) pp. 268–279. (Australian Government Publishing Service: Canberra)
Coates F (2000) ‘Grampians pincushion lily (Borya mirabilis Churchill) recovery plan 2001–2005’. (School of Botany, La Trobe University: Melbourne)
Coates F, Walsh NG, James EA (2002) Threats to the survival of the Grampians pincushion lily (Borya mirabilis, Liliaceae) – a short-range endemic from western Victoria. Australian Systematic Botany 15, 477–483.
| Threats to the survival of the Grampians pincushion lily (Borya mirabilis, Liliaceae) – a short-range endemic from western Victoria.Crossref | GoogleScholarGoogle Scholar |
Coates F, Pritchard A, Moorrees A (2003). ‘Grampians pincushion lily (Borya mirabilis). Action statement no. 149 (Flora and Fauna Guarantee Act 1988)’. (Department of Sustainability and Environment: Melbourne)
Cole CT (2003) Genetic variation in rare and common plants. Annual Review of Ecology Evolution and Systematics 34, 213–237.
| Genetic variation in rare and common plants.Crossref | GoogleScholarGoogle Scholar |
Comai L (2005) The advantages and disadvantages of being polyploid. Nature Reviews. Genetics 6, 836–846.
| The advantages and disadvantages of being polyploid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFygt7%2FO&md5=690b07df46e237cba7a746d558aad99bCAS | 16304599PubMed |
Conran JG (1994) Borya. In ‘Flora of Victoria. Vol. 2’. (Eds NG Walsh, TJ Entwisle) p. 665. (Inkata Press: Melbourne)
Conran JG (1998) Boryaceae. In ‘The families and genera of flowering plants. Vol. III. Monocotyledons: Lilianae (except Orchidaceae)’. (Ed. K Kubitzki) pp. 151–154. (Springer: Berlin)
Cook RE (1983) Clonal plant populations. American Scientist 71, 244–253.
Costa J, Ferrero V, Loureiro J, Castro M, Navarro L, Castro S (2014) Sexual reproduction of the pentaploid, short-styled Oxalis pes-caprae allows the production of viable offspring. Plant Biology 16, 208–214.
| Sexual reproduction of the pentaploid, short-styled Oxalis pes-caprae allows the production of viable offspring.Crossref | GoogleScholarGoogle Scholar |
Crichton RJ, Squirrel J, Woodin SJ, Dalrymple SE, Hollingsworth PM (2012) Isolation of microsatellite primers for Melampyrum sylvaticum (Orobanchaceae), an endangered plant in the United Kingdom. American Journal of Botany 99, e457–e459.
| Isolation of microsatellite primers for Melampyrum sylvaticum (Orobanchaceae), an endangered plant in the United Kingdom.Crossref | GoogleScholarGoogle Scholar | 23115135PubMed |
Cropper S (1993) ‘Management of endangered plants.’ (CSIRO Publishing: Melbourne)
Cropper SC, Calder DM, Tomkinson D (1989) Thelymitra epipactoides F.Muell. (Orchidaceae): the morphology, biology and conservation of an endangered species. Proceedings of the Royal Society of Victoria 101, 89–101.
Dickinson H (1995) Dry stigmas, water and self-incompatibility in Brassica. Sexual Plant Reproduction 8, 1–10.
Drury RA, Wellington EA (1980) ‘Carleton’s histological technique.’ (5th edn) (Oxford University Press: Oxford, UK)
Duffy KJ, Stout JC (2008) The effects of plant density and nectar reward on bee visitation to the endangered orchid Spiranthes romanzoffiana. Acta Oecologica 34, 131–138.
| The effects of plant density and nectar reward on bee visitation to the endangered orchid Spiranthes romanzoffiana.Crossref | GoogleScholarGoogle Scholar |
Erdtman G (1952) ‘Pollen morphology and plant taxonomy in angiosperms.’ (Chronica Botanica Co.: Waltham, MA, USA)
Faber-Langendoen D, Nichols J, Master L, Snow K, Tomaino A, Bittman R, Hammerson G, Heidel B, Ramsay L, Teucher A, Young B (2012). ‘NatureServe conservation status assessments: methodology for assigning ranks.’ (NatureServe: Arlington, VA, USA) Available at http://www.natureserve.org/biodiversity-science/publications/natureserve-conservation-status-assessments-methodology-assigning [Verified 14 June 2015].
Felsenstein J (1993) ‘PHYLIP (Phylogeny Inference Package) version 3.5c.’ (Department of Genetics, University of Washington, Seattle) Available at: http://evolution.genetics.washington.edu/phylip.html [Verified 13 July 2015]
Fialová M, Jandová M, Ohryzek J, Duchoslav M (2014) Biology of the polyploid geophyte Allium oleraceum (Amaryllidaceae): variation in size, sexual and asexual reproduction and germination within and between tetra-, penta- and hexaploid cytotypes. Flora 209, 312–324.
| Biology of the polyploid geophyte Allium oleraceum (Amaryllidaceae): variation in size, sexual and asexual reproduction and germination within and between tetra-, penta- and hexaploid cytotypes.Crossref | GoogleScholarGoogle Scholar |
Forster PI, Thompson EJ (1997) Borya inopinata (Anthericaceae), a new species of resurrection plant from north Queensland. Austrobaileya 4, 597–600.
Franklin AL, Filion WG (1985) A new technique for retarding fading of fluorescence: DPX-BME. Stain Technology 60, 125–135.
Gaff DF (1987) Desiccation tolerant plants in South America. Oecologia 74, 133–136.
| Desiccation tolerant plants in South America.Crossref | GoogleScholarGoogle Scholar |
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 |
Garay LA (1970) A reappraisal of the genus Oncidium Sw. Taxon 19, 443–467.
| A reappraisal of the genus Oncidium Sw.Crossref | GoogleScholarGoogle Scholar |
Gray A (1996) Genetic diversity and its conservation in natural populations of plants. Biodiversity Letters 3, 71–80.
| Genetic diversity and its conservation in natural populations of plants.Crossref | GoogleScholarGoogle Scholar |
Gross CL, Caddy HAR (2006) Are differences in breeding mechanisms and fertility among populations contributing to rarity in Grevillea rhizomatosa (Proteaceae)? American Journal of Botany 93, 1791–1799.
| Are differences in breeding mechanisms and fertility among populations contributing to rarity in Grevillea rhizomatosa (Proteaceae)?Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3MrnsleqsQ%3D%3D&md5=7188e0edb95a9749d94eb28720f31e33CAS | 21642125PubMed |
Gross CL, Nelson PA, Haddadchi A, Fatemi M (2012) Somatic mutations contribute to genotypic diversity in sterile and fertile populations of the threatened shrub, Grevillea rhizomatosa (Proteaceae). Annals of Botany 109, 331–342.
| Somatic mutations contribute to genotypic diversity in sterile and fertile populations of the threatened shrub, Grevillea rhizomatosa (Proteaceae).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC387oslOntQ%3D%3D&md5=c79784af24796ea46353a9ae29a10a22CAS | 22080138PubMed |
Heslop-Harrison J, Heslop-Harrison Y (1970) Evaluation of pollen viability by enzymatically induced fluorescence: intracellular hydrolysis of fluorescein diacetate. Biotechnic & Histochemistry 45, 115–120.
| Evaluation of pollen viability by enzymatically induced fluorescence: intracellular hydrolysis of fluorescein diacetate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3cXkt1ajtrg%3D&md5=e7f57f92fe8fc659b6dfdb1bd5884c29CAS |
Hoffmann AA, Parsons PA (1991) ‘Evolutionary genetics and environmental stress.’ (Oxford University Press: Oxford, UK)
Holmes GD, James EA, Hoffmann AA (2009) Divergent levels of genetic variation and ploidy among populations of the rare shrub, Grevillea repens (Proteaceae). Conservation Genetics 10, 827–837.
| Divergent levels of genetic variation and ploidy among populations of the rare shrub, Grevillea repens (Proteaceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXntlShu78%3D&md5=a4ae9fcbcf391971f5b8c7a629075966CAS |
Honnay O, Jacquemyn H, Roldán-Ruiz I, Hermy M (2006) Consequences of prolonged clonal growth on local and regional genetic structure and fruiting success of the forest perennial Maianthemum bifolium. Oikos 112, 21–30.
| Consequences of prolonged clonal growth on local and regional genetic structure and fruiting success of the forest perennial Maianthemum bifolium.Crossref | GoogleScholarGoogle Scholar |
James SH, Keighery GK, Moorrees A, Waycott M (1999) Genomic coalescence in a population of Laxmannia sessiliflora (Angiospermae, Anthericaceae): an association of lethal polymorphism, self-pollination and chromosome number reduction. Heredity 82, 364–372.
| Genomic coalescence in a population of Laxmannia sessiliflora (Angiospermae, Anthericaceae): an association of lethal polymorphism, self-pollination and chromosome number reduction.Crossref | GoogleScholarGoogle Scholar | 10383654PubMed |
Janssen T, Bremer K (2004) The age of major monocot groups inferred from 800+ rbcL sequences. Botanical Journal of the Linnean Society 146, 385–398.
| The age of major monocot groups inferred from 800+ rbcL sequences.Crossref | GoogleScholarGoogle Scholar |
Keighery GJ (1984a) Chromosome counts of Australian Liliaceae. Feddes Repertorium 95, 523–532.
Keighery GJ (1984b) The Johnsonieae (Liliaceae): biology and classification. Flora 175, 103–108.
Keighery GJ (1987) Laxmannia. In ‘Flora of Australia. Vol. 45. Hydatellaceae to Liliaceae’. (Ed. AS George) pp. 254–264. (Australian Government Publishing Service: Canberra)
Kimpton SK, James EA, Drinnan AN (2002) Reproductive biology and genetic marker diversity in Grevillea infecunda (Proteaceae), a rare plant with no known seed production. Australian Systematic Botany 15, 485–492.
| Reproductive biology and genetic marker diversity in Grevillea infecunda (Proteaceae), a rare plant with no known seed production.Crossref | GoogleScholarGoogle Scholar |
Kohout M, Coates F (2010) ‘Recovery plan for Borya mirabilis in Victoria.’ (Department of Sustainability and Environment: Melbourne)
Kramer AT, Havens K (2009) Plant conservation genetics in a changing world. Trends in Plant Science 14, 599–607.
| Plant conservation genetics in a changing world.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlGhsrjO&md5=45f86100705950294c16c9972a325e5aCAS | 19748300PubMed |
Lamont BB, Klinkhamer PGL, Witkowski ETF (1993) Population fragmentation may reduce fertility to zero in Banksia goodii – a demonstration of the Allee effect. Oecologia 94, 446–450.
| Population fragmentation may reduce fertility to zero in Banksia goodii – a demonstration of the Allee effect.Crossref | GoogleScholarGoogle Scholar |
Larson BMH, Barrett SCH (2000) A comparative analysis of pollen limitation in flowering plants. Biological Journal of the Linnean Society. Linnean Society of London 69, 503–520.
| A comparative analysis of pollen limitation in flowering plants.Crossref | GoogleScholarGoogle Scholar |
López-Almansa JC, Pannell JR, Gil L (2003) Female sterility in Ulmus minor (Ulmaceae): a hypothesis invoking the cost of sex in a clonal plant. American Journal of Botany 90, 603–609.
| Female sterility in Ulmus minor (Ulmaceae): a hypothesis invoking the cost of sex in a clonal plant.Crossref | GoogleScholarGoogle Scholar | 21659155PubMed |
Luo S, Zhang D, Renner S (2006) Oxalis debilis in China: distribution of flower morphs, sterile pollen and polyploidy. Annals of Botany 98, 459–464.
| Oxalis debilis in China: distribution of flower morphs, sterile pollen and polyploidy.Crossref | GoogleScholarGoogle Scholar | 16735406PubMed |
Lynch AJJ, Barnes RW, Cambecedes J, Vaillancourt RE (1998) Genetic evidence that Lomatia tasmanica (Proteaceae) is an ancient clone. Australian Journal of Botany 46, 25–33.
| Genetic evidence that Lomatia tasmanica (Proteaceae) is an ancient clone.Crossref | GoogleScholarGoogle Scholar |
Masumoto I, Kaneko S, Otake K, Isagi Y (2011) Development of microsatellite markers for Adenophora palustris (Campanulaceae), a critically endangered wetland species in Japan. Conservation Genetics Resources 3, 163–165.
| Development of microsatellite markers for Adenophora palustris (Campanulaceae), a critically endangered wetland species in Japan.Crossref | GoogleScholarGoogle Scholar |
Mayer P (1891) Űber das Forben mit Haematoxylin. Mittheilungen aus der Zoologischen Station zu Neapel 10, 170–186.
Meloni M, Reid A, Caujapé-Castells J, Marrero A, Fernández-Palacios JM, Mesa-Coelo RA, Conti E (2013) Effects of clonality on the genetic variability of rare, insular species: the case of Ruta microcarpa from the Canary Islands. Ecology and Evolution 3, 1569–1579.
| Effects of clonality on the genetic variability of rare, insular species: the case of Ruta microcarpa from the Canary Islands.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3sjktlGmtA%3D%3D&md5=79026cce5fb9599e4a6349cfbda8be08CAS | 23789068PubMed |
Namoff S, Husby CE, Francisco-Ortega J, Noblick LR, Lewis CE, Griffith MP (2010) How well does a botanical garden collection of a rare palm capture the genetic variation in a wild population? Biological Conservation 143, 1110–1117.
| How well does a botanical garden collection of a rare palm capture the genetic variation in a wild population?Crossref | GoogleScholarGoogle Scholar |
Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89, 583–590.
Ohno S (1970) ‘Evolution by gene duplication.’ (Springer-Verlag: Berlin)
Pan JJ, Price JS (2002) Fitness and evolution in clonal plants: the impact of clonal growth. Evolutionary Ecology 15, 583–600.
| Fitness and evolution in clonal plants: the impact of clonal growth.Crossref | GoogleScholarGoogle Scholar |
Pandit MK, Babu CR (2003) The effects of loss of sex in clonal populations of an endangered perennial Coptis teeta (Ranunculaceae). Botanical Journal of the Linnean Society 143, 47–54.
| The effects of loss of sex in clonal populations of an endangered perennial Coptis teeta (Ranunculaceae).Crossref | GoogleScholarGoogle Scholar |
Penet L, Nadot S, Ressayre A, Forchioni A, Dreyer L, Gouyon PH (2005) Multiple developmental pathways leading to a single morph: monosulcate pollen (examples from the Asparagales). Annals of Botany 95, 331–343.
| Multiple developmental pathways leading to a single morph: monosulcate pollen (examples from the Asparagales).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2cnitVOruw%3D%3D&md5=2115d27bfb05c87b40ef7f228f5a96d0CAS | 15567807PubMed |
Reiter N (2008) Borya mirabilis: steps in the recovery of a critically endangered Australian native plant. PhD Thesis, School of Applied Sciences, RMIT University, Melbourne.
Reiter N, Pollard G (2013) The response of Paracaleana disjuncta and Borya mirabilis to wildfire in Victoria. Australasian Plant Conservation 22, 15–17.
Reiter N, Weste G, Guest D (2004) The risk of extinction resulting from disease caused by Phytophthora cinnamomi to endangered, vulnerable or rare plant species endemic to the Grampians, western Victoria. Australian Journal of Botany 52, 425–433.
| The risk of extinction resulting from disease caused by Phytophthora cinnamomi to endangered, vulnerable or rare plant species endemic to the Grampians, western Victoria.Crossref | GoogleScholarGoogle Scholar |
Reiter N, Lawrie A, Walsh N (2013) Mycorrhizal associations of Borya mirabilis. Muelleria 31, 81–88.
Rounsaville TJ, Touchell DH, Ranney TG (2011) Fertility and reproductive pathways in diploid and triploid Miscanthus sinensis. HortScience 46, 1353–1357.
Sage TL, Hristova-Sarkovski K, Koehl V, Lyew J, Pontieri V, Bernhardt P, Weston P, Bagha S, Chiu G (2009) Transmitting tissue architecture in basal-relictual angiosperms: implications for transmitting tissue origins. American Journal of Botany 96, 183–206.
| Transmitting tissue architecture in basal-relictual angiosperms: implications for transmitting tissue origins.Crossref | GoogleScholarGoogle Scholar | 21628183PubMed |
San Martin APM, Adamec L, Suda J, Mes THM, Štorchová H (2003) Genetic variation within the endangered species Aldrovanda vesiculosa (Droseraceae) as revealed by RAPD analysis. Aquatic Botany 75, 159–172.
| Genetic variation within the endangered species Aldrovanda vesiculosa (Droseraceae) as revealed by RAPD analysis.Crossref | GoogleScholarGoogle Scholar |
Stevens PF (2013) ‘Angiosperm phylogeny website.’ Ver. 13, 28 September 2013. (Missouri Botanical Garden: St Louis, MO, USA) Available at http://www.mobot.org/MOBOT/research/APweb/ [Verified 14 June 2015].
Sun HQ, Luo YB, Ge S (2003) A preliminary study on pollination biology of an endangered orchid, Changnienia amoena, in Shennongjia. Acta Botanica Sinica 45, 1019–1023.
The Angiosperm Phylogeny Group (2009) An update of the angiosperm phylogeny group classification for the orders and families of flowering plants: APGIII. 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: APGIII.Crossref | GoogleScholarGoogle Scholar |
Vinogradov AE (2003) Selfish DNA is maladaptive: evidence from the plant Red List. Trends in Genetics 19, 609–614.
| Selfish DNA is maladaptive: evidence from the plant Red List.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXosVKrsr8%3D&md5=fb68c91846e1745f96a41ca5d379331bCAS | 14585612PubMed |
Warburton CL, James EA, Fripp YJ, Trueman SJ, Wallace HM (2000) Clonality and sexual reproductive failure in remnant populations of Santalum lanceolatum (Santalaceae). Biological Conservation 96, 45–54.
| Clonality and sexual reproductive failure in remnant populations of Santalum lanceolatum (Santalaceae).Crossref | GoogleScholarGoogle Scholar |
Weekley CW, Race T (2001) The breeding system of Ziziphus celata Judd and D.W. Hall (Rhamnaceae), a rare endemic plant of the Lake Wales Ridge, Florida, USA: implications for recovery. Biological Conservation 100, 207–213.
| The breeding system of Ziziphus celata Judd and D.W. Hall (Rhamnaceae), a rare endemic plant of the Lake Wales Ridge, Florida, USA: implications for recovery.Crossref | GoogleScholarGoogle Scholar |
Weller SG (1994) The relationship of rarity to plant reproductive biology. In ‘Restoration of endangered species: conceptual issues, planning and implementation’. (Eds ML Bowles, CJ Whelan) pp. 90–117. (Cambridge University Press: Cambridge, UK)
Widholm JM (1972) The use of fluorescein diacetate and phenosafranine for determining viability of cultured plant cells. Biotechnic & Histochemistry 47, 189–194.
| The use of fluorescein diacetate and phenosafranine for determining viability of cultured plant cells.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE383hsVykug%3D%3D&md5=c59a3a1348ec0a05366ac3f3f8de4315CAS |
Yeh FC, Yang R-C, Boyle T, Ye Z-H, Mao JX (1997) ‘Popgene, the user-friendly shareware for population genetic analysis.’ (Molecular Biology and Biotechnology Centre, University of Alberta: Canada) Available at http://www.ualberta.ca/~fyeh/popgene.html [Verified 14 June 2015].
