An overview of actinorhizal plants in Africa
Maher Gtari A and Jeffrey O. Dawson B C
+ Author Affiliations
- Author Affiliations
A Laboratoire Microorganismes et Biomolécules Actives, Département de Biologie, Faculté des Sciences de Tunis, 2092 Tunis, Tunisia.
B Department of Natural Resources and Environmental Sciences, 1316 Plant Sciences Laboratory, University of Illinois at Urbana–Champaign, 1201 South Dorner Drive, Urbana, IL 61801, USA.
C Corresponding author. Email: jdawson2@illinois.edu
This paper originates from a presentation at the 16th International Meeting on Frankia and Actinorhizal Plants, Oporto, Portugal, 5–8 September 2010.
Functional Plant Biology 38(9) 653-661 https://doi.org/10.1071/FP11009
Submitted: 12 January 2011 Accepted: 24 June 2011 Published: 16 August 2011
Abstract
A compilation and synthesis of information derived from plant databases and other sources on the occurrence, diversity and geographic distribution of actinorhizal plants in Africa is presented in this review. Actinorhizal plants are a specific group of non-leguminous, woody dicots having symbiotic, nitrogen-fixing root nodules that are induced on roots of actinorhizal plant species by soil actinomycetes of the genus Frankia. There is a lack of basic information on actinorhizal plants in Africa compared with other major land masses in the world. Results indicate that most, if not all, African countries and climatic regions have native or introduced actinorhizal species. A synthesis of available information indicates that there are six families, nine genera and 38 reported species of actinorhizal plants in Africa. Of these, 21 species are native and 17 are exotic. The families and corresponding number of species in each genus are: Betulaceae (native Alnus glutinosa (1), exotic Alnus (2)); Casuarinaceae (exotic Casuarina (5), exotic Allocasuarina (3), exotic Gymnostoma deplancheana (1)); Coriariaceae (native Coriaria myrtifolia (1)); Myricaceae (native Morella (19), exotic Morella cerifera (1)); Rhamnaceae (exotic Ceanothus caeruleus (1), exotic Colletia paradoxa (1)); and Elaeagnaceae (exotic Eleaegnus angustifolia (1)). Four reports of native, actinorhizal Ceanothus species in Africa found in the database were determined to be false, instead, being non-actinorhizal species. Widespread plantings of exotic Casuarinaceae have been introduced into tropical and arid zones of Africa as multipurpose trees, especially in arid regions where native species do not occur. There is a diverse assemblage of native species of Morella in Africa, mostly shrubs or small trees, which provide medicine, other useful chemicals and wildlife habitat. Many native Morella species are isolated in montane islands, apparently leading to greater speciation than in Eurasia from where the genus migrated into Africa. The current status and knowledge of African actinorhizal plants indicates a need to focus research on their biogeography, biology, ecology, genetics and use.
Additional keywords: actinorhiza, African plants, Frankia, nitrogen fixation, nitrogen-fixing trees.
References
Alapetite GP (1979) Flore de la Tunisie. Edition du Ministère de l’enseignement supérieur et de la recherche scientifique et le Ministère de l’agriculture. République Tunisienne.Allan HH (1961) Coriariaceae. In ‘Flora of New Zealand. Vol. 1’. (Ed. LB Moore) pp. 300–305. (Government Printer: Wellington, New Zealand)
Basinger J, Dilcher D (1984) Ancient bisexual flowers. Science 224, 511–513.
| Ancient bisexual flowers.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cvisVOqsw%3D%3D&md5=5bd899d78f26299eb0c10f2d22a9a9abCAS |
Becking JH (1977) Dinitrogen-fixing associations in higher plants other than legumes. In ‘A Treatise on dinitrogen fixation. Sec. III Biology’. (Eds RWF Hardy, WS Silver) pp. 185–275. (John Willey & Sons: NY)
Benecke U (1970) Nitrogen fixation by Alnus viridis (Chaix) DC. Plant and Soil 33, 30–48.
| Nitrogen fixation by Alnus viridis (Chaix) DC.Crossref | GoogleScholarGoogle Scholar |
Benson DR, Dawson JO (2007) Recent advances in the biogeography and genecology of symbiotic Frankia and its host plants. Physiologia Plantarum 130, 318–330.
| Recent advances in the biogeography and genecology of symbiotic Frankia and its host plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXns1Oquro%3D&md5=98229d8a39e1f24d06d1142ee69838fbCAS |
Benson DR, Silvester WB (1993) Biology of Frankia strains, actinomycete symbionts of actinorhizal plants. Microbiological Reviews 57, 293–319.
Benson DR, Vanden Heuvel BD, Potter D (2004) Actinorhizal symbioses: diversity and biogeography. In ‘Plant microbiology’. (Ed. M Gillings) pp. 97–127. (BIOS Scientific Publishers Ltd.: Oxford)
Bloem JF, Trytsman G, Smith HJ (2009) Biological nitrogen fixation in resource-poor agriculture in South Africa. Symbiosis 48, 18–24.
| Biological nitrogen fixation in resource-poor agriculture in South Africa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXpsFenur8%3D&md5=e764c4ece3687d2548e9a1ee1a961a51CAS |
Brummitt RK (1999) Proposals to conserve or reject. Report of the Committee for Spermatophyta. Taxon 48, 367–368.
Campbell LD, Holden AM (1984) Miocene Casuarinaceae fossils from Southland and Central Otago, New Zealand. New Zealand Journal of Botany 22, 159–167.
Chen Z, Manchester SR, Sun H (1999) Phylogeny and evolution of the Betulaceae as inferred from DNA sequences, morphology, and paleobotany. American Journal of Botany 86, 1168–1181.
| Phylogeny and evolution of the Betulaceae as inferred from DNA sequences, morphology, and paleobotany.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXlvFals7Y%3D&md5=3b752fbbd2a60d077c42937ab0a43549CAS |
Chianu JN, Nkonya EM, Mairura FS, Chianu JN, Akinnifesi FK (2010) Biological nitrogen fixation and socioeconomic factors for legume production in sub-Saharan Africa: a review. Agronomic Sustainable Development
| Biological nitrogen fixation and socioeconomic factors for legume production in sub-Saharan Africa: a review.Crossref | GoogleScholarGoogle Scholar |
Christophel DC (1980) Occurrence of Casuarina megafossils in the Tertiary of south-eastern Australia. Australian Journal of Botany 28, 249–259.
| Occurrence of Casuarina megafossils in the Tertiary of south-eastern Australia.Crossref | GoogleScholarGoogle Scholar |
Christophel DC (1989) Evolution of the Australian flora through the Tertiary. Plant Systematics and Evolution 162, 63–78.
| Evolution of the Australian flora through the Tertiary.Crossref | GoogleScholarGoogle Scholar |
Clawson ML, Bourret A, Benson DR (2004) Assessing the phylogeny of Frankia-actinorhizal plant nitrogen-fixing root nodule symbioses with Frankia 16S rRNA and glutamine synthetase gene sequences. Molecular Phylogenetics and Evolution 31, 131–138.
| Assessing the phylogeny of Frankia-actinorhizal plant nitrogen-fixing root nodule symbioses with Frankia 16S rRNA and glutamine synthetase gene sequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhvFSks7s%3D&md5=cae8f29503da2376088cc1e77f47d4c1CAS |
Coetzee JA, Muller J (1984) The phytogeographic significance of some extinct Gondwana pollen types from the Tertiary of the south-western Cape (South Africa). Annals of the Missouri Botanical Garden 71, 1088–1099.
| The phytogeographic significance of some extinct Gondwana pollen types from the Tertiary of the south-western Cape (South Africa).Crossref | GoogleScholarGoogle Scholar |
Coetzee J, Praglowski J (1984) Pollen evidence for the occurrence of Casuarina and Myrica in the Tertiary of South Africa. Grana 23, 23–41.
| Pollen evidence for the occurrence of Casuarina and Myrica in the Tertiary of South Africa.Crossref | GoogleScholarGoogle Scholar |
Côté B, Carlson RW, Dawson JO (1988) Leaf photosynthetic characteristics of seedlings of actinorhizal Alnus spp. and Elaeagnus spp. Photosynthesis Research 16, 211–218.
| Leaf photosynthetic characteristics of seedlings of actinorhizal Alnus spp. and Elaeagnus spp.Crossref | GoogleScholarGoogle Scholar |
Dawson JO (2007) The ecology of actinorhizal plants. In ‘Nitrogen-fixing actinorhizal symbioses. Vol. 6. Nitrogen fixation: applications and research progress’. (Eds K Pawlowski, WE Newton) pp. 199–234. (Springer-Verlag: Dordrecht, The Netherlands)
Diem HG, Gauthier D, Dommergues Y (1983) An effective strain of Frankia from Casuarina sp. Canadian Journal of Botany 61, 2815–2821.
| An effective strain of Frankia from Casuarina sp.Crossref | GoogleScholarGoogle Scholar |
Dilcher DL, Christophel DC, Bhagwandin HO, Scriven LJ (1990) Evolution of the Casuarinaceae: morphological comparisons of some extant species. American Journal of Botany 77, 338–355.
| Evolution of the Casuarinaceae: morphological comparisons of some extant species.Crossref | GoogleScholarGoogle Scholar |
Dillon JT, Baker D (1982) Variation in nitrogenase activity among pure-cultured Frankia strains tested on actinorhizal plants as an induction of symbiotic compatibility. New Phytologist 92, 215–219.
| Variation in nitrogenase activity among pure-cultured Frankia strains tested on actinorhizal plants as an induction of symbiotic compatibility.Crossref | GoogleScholarGoogle Scholar |
Dobignard A, Chatelain C (2010–2011) Synonymic and bibliographic index of North Africa plants. Vol.1 Monocots, Vol. 2 & 3 in prep. African Plants Database (version 3.3.4). Conservatoire et Jardin botaniques de la Villle de Genève and South African National Biodiversity Institute, Pretoria. Available at http://www.ville-ge.ch/musinfo/bd/cjb/africa/ [Verified 11 July 2011]
El-Lakany MH (1983) A review of breeding drought resistant Casuarina for shelterbelt establishment in arid regions with special reference to Egypt. Forest Ecology and Management 6, 129–137.
| A review of breeding drought resistant Casuarina for shelterbelt establishment in arid regions with special reference to Egypt.Crossref | GoogleScholarGoogle Scholar |
El-Lakany MH, Turnbull JW, Brewbaker JL (Eds) (1991) Advances in Casuarina research and utilisation. In ‘Proceedings of the 2nd International Casuarina Workshop’. (American University: Cairo)
Finch J, Marchant R (2011) A palaeoecological investigation into the role of fire and human activity in the development of montane grasslands in East Africa. Vegetation History and Archaeobotany 20, 109–124.
| A palaeoecological investigation into the role of fire and human activity in the development of montane grasslands in East Africa.Crossref | GoogleScholarGoogle Scholar |
Frenguelli J (1943) Restos de Casuarina en el Mioceno de el Mirador, Patagonia central. Notas del Museo de la Plata. Notas del Museo de La Plata. Paleontología 56, 349–354.
Gauthier D, Diem HG, Dommergues Y (1981) In vitro nitrogen fixation by two actinomycete strains isolated from Casuarina nodules. Applied and Environmental Microbiology 41, 306–308.
Germishuizen G, Meyer NL (Eds) (2003) ‘Plants of Southern Africa: an annotated checklist.’ (National Botanical Institute: Pretoria)
Gerster G (1960) ‘Sahara.’ (Barrie & Rockcliff Publishers: London)
Ghodhbane-Gtari F, Nouioui I, Chair M, Boudabous A, Gtari M (2010) 16S–23S rRNA intergenic spacer region variability in the genus Frankia. Microbial Ecology 60, 487–495.
| 16S–23S rRNA intergenic spacer region variability in the genus Frankia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht12qtL3J&md5=449e92a9a229228d85357fa4fea0aac2CAS |
Girgis MGZ, Ishac YZ, El-Haddad M, Saleh EA, Diem HG, Dommergues YR (1990) First report on isolation and culture of effective Casuarina-compatible strains of Frankia from Egypt. In ‘2nd International Casuarina Workshop’. (Eds MH El-Lakany, JW Turnbull, JL Brewbaker) pp. 156–164. (American University: Cairo)
González-Henríquez MN, Pérez JDR, Rodriquez CS (1986) ‘Flora y vegetation del archipielago Canario.’ (Edirca, S.L.: Las Palmas de Gran Canaria, Canary Islands)
Good RDO (1930) The geography of the genus Coriaria. New Phytologist 29, 170–198.
| The geography of the genus Coriaria.Crossref | GoogleScholarGoogle Scholar |
Graham A (1987) Tropical american tertiary Xoras and paleoenvironments: Mexico, Costa Rica and Panama. American Journal of Botany 74, 1519–1531.
| Tropical american tertiary Xoras and paleoenvironments: Mexico, Costa Rica and Panama.Crossref | GoogleScholarGoogle Scholar |
Gtari M, Brusetti L, Aouani ME, Daffonchio D, Boudabous A (2002) Frankia nodulating Alnus glutinosa and Casuarinaceae in Tunisia. Annals of Microbiology 52, 145–153.
Gtari M, Brusetti L, Skander G, Mora D, Boudabous A, Daffonchio D (2004) Isolation of Elaeagnus-compatible Frankia from soils collected in Tunisia. FEMS Microbiology Letters 234, 349–355.
| Isolation of Elaeagnus-compatible Frankia from soils collected in Tunisia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjvVGmu7o%3D&md5=362d62067435a7b2f500e27049ac4081CAS |
Gtari M, Daffonchio D, Boudabous A (2007a) Occurrence and diversity of Frankia in Tunisian soil. Physiologia Plantarum 130, 372–379.
| Occurrence and diversity of Frankia in Tunisian soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXns1Oqurc%3D&md5=26866e2073712fd5159cad3e81148632CAS |
Gtari M, Brusetti L, Hassen A, Mora D, Daffonchio D, Boudabous A (2007b) Genetic diversity among Elaeagnus compatible Frankia strains and sympatric-related nitrogen-fixing actinobacteria revealed by nifH sequence analysis. Soil Biology and Biochemistry 39, 372–377.
| Genetic diversity among Elaeagnus compatible Frankia strains and sympatric-related nitrogen-fixing actinobacteria revealed by nifH sequence analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1agtr3J&md5=93067656d6d0d222570e6b4a912000eeCAS |
Hibbs DE, Cromack K (1990) Actinorhizal plants in Pacific Northwest forests. In ‘The biology of Frankia and actinorhizal plants’. (Eds CR Schwintzer, JD Tjepkma) pp. 343–363. (Academic Press: San Diego)
Hill RS, MacPhail MK (1983) Reconstruction of the Oligocene vegetation at Pioneer, northeast Tasmania. Alcheringa 7, 281–299.
| Reconstruction of the Oligocene vegetation at Pioneer, northeast Tasmania.Crossref | GoogleScholarGoogle Scholar |
Huguet V, Ojeda Land E, Garcia-Casanova J, Zimpfer JF, Fernandez MP (2005a) Genetic diversity of Frankia microsymbionts from the relict species Myrica faya (Ait.) and Myrica rivas-martinezii (S.) in Canary Islands and Hawaii. Microbial Ecology 49, 617–625.
| Genetic diversity of Frankia microsymbionts from the relict species Myrica faya (Ait.) and Myrica rivas-martinezii (S.) in Canary Islands and Hawaii.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2MvnsVOisg%3D%3D&md5=6f95cafd5154d68ab5c8da9b86d14c8cCAS |
Huguet V, Gouy M, Normand P, Zimpfer J, Fernandez MP (2005b) Molecular phylogeny of Myricaceae: a re-examination of host–symbiont specificity. Molecular Phylogenetics and Evolution 34, 557–568.
| Molecular phylogeny of Myricaceae: a re-examination of host–symbiont specificity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXptlCiug%3D%3D&md5=5379a67dea1ea763c1d2902b085b3a55CAS |
Johnson L A S, Wilson KL (1989) Casuarinaceae: a synopsis. In ‘Evolution, systematics and fossil history of the Hamamelidae. Vol. 2: Higher Hamamelidae. Systematics Association Special Vol. No. 40B’. (Eds PR Crane, S Blackmore) pp. 167–188. (Clarendon Press: Oxford)
Jordan GJ (1997) Evidence of plant extinction and diversity from Regatta Point, western Tasmania, Australia. Botanical Journal of the Linnean Society 123, 45–71.
| Evidence of plant extinction and diversity from Regatta Point, western Tasmania, Australia.Crossref | GoogleScholarGoogle Scholar |
Killick DJB (1969) The South African species of Myrica. Bothalia 10, 5–17.
Killick DJB, Polhill RM, Verdcourt B (1998) New combinations in African Myricaceae. Kew Bulletin 53, 993–995.
| New combinations in African Myricaceae.Crossref | GoogleScholarGoogle Scholar |
Lebrun JP, Stork AL (1991–2010) Enumération des plantes à fleurs d’Afrique tropicale et Tropical African Flowering Plants: Ecology and Distribution, vol. 1, 2, 3, 4, 5 in prep. African Plants Database (version 3.3.4). Conservatoire et Jardin botaniques de la Villle de Genève and South African National Biodiversity Institute, Pretoria. Available at http://www.ville-ge.ch/musinfo/bd/cjb/africa/ [Verified 11 July 2011]
Lutzow-Felling CJ, Gadner DE, Markin GP, Smith CW (1995) Myrica faya: review of the biology, ecology, distribution and control. Technical report, University of Hawaii at Manoa, Cooperative National Park Resources Studies Unit, Honolulu.
Mabberely DJ (1988) ‘The plant book.’ (Cambridge University Press: Cambridge)
Macdonald AD (1989) The morphology and relationships of the Myricaceae. In ‘Evolution, systematics and fossil history of the Hamamelidae’. (Eds PR Crane, S Blackmore) pp. 147–165. (Clarendon Press: Oxford)
Maggia L, Nazaret S, Simonet P (1992) Molecular characterization of Frankia isolates from Casuarina equisetifolia root nodules harvested in West Africa (Senegal and Gambia). Acta Oecologica 13, 453–461.
Melville R (1966) Continental drift, mesozoic continents, and the migration of the angiosperms. Nature 211, 116–120.
| Continental drift, mesozoic continents, and the migration of the angiosperms.Crossref | GoogleScholarGoogle Scholar |
Melville R (1981) Vicarious plant distributions and palaeogeography of the Pacific region. In ‘Vicariance biogeography: a critique’. (Eds G Nelson, G Rosen) pp. 283–302. (Columbia University Press: New York)
Miki A (1977) Late Cretaceous pollen and spore floras of northern Japan: composition and interpretation. Journal of the Faculty of Science, Hokkaido University. Series 4, Geology and Mineralogy 17, 399–436.
Morrison MES, Hamilton AC (1974) Vegetation and climate in the uplands of south-western Uganda during the later Pleistocene Period: II. Forest clearance and other vegetational changes in the Rukiga Highlands during the past 8000 Years. Journal of Ecology 62, 1–31.
| Vegetation and climate in the uplands of south-western Uganda during the later Pleistocene Period: II. Forest clearance and other vegetational changes in the Rukiga Highlands during the past 8000 Years.Crossref | GoogleScholarGoogle Scholar |
Murai S (1964) Phytotaxonomical and geobotanical studies on genus Alnus in Japan (III). Taxonomy of whole world species and distribution of each section. Bulletin of the Government Forest Experiment Station, Tokyo Japan 171, 1–107.
Normand P, Orso S, Cournoyer B, Jeannin P, Chapelon C, Dawson JO, Evtushenko L, Misra AK (1996) Molecular phylogeny of the genus Frankia and related genera and emendation of the family Frankiaceae. International Journal of Systematic Bacteriology 46, 1–9.
| Molecular phylogeny of the genus Frankia and related genera and emendation of the family Frankiaceae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xhtl2ls7s%3D&md5=7aed30ea383af928e8fa1e10844ff2bdCAS |
Normand P, Lapierre P, Tisa LS, Gogarten JP, Alloisio N, Bagnarol E, Bassi CA, Berry AM, Bickhart DM, Choisne N, Couloux A, Cournoyer B, Cruveiller S, Daubin V, Demange N, Francino MP, Goltsman E, Huang Y, Kopp OR, Labarre L, Lapidus A, Lavire C, Marechal J, Martinez M, Mastronunzio JE, Mullin BC, Niemann J, Pujic P, Rawnsley T, Rouy Z, Schenowitz C, Sellstedt A, Tavares F, Tomkins JP, Vallenet D, Valverde C, Wall LG, Wang Y, Medigue C, Benson DR (2007) Genome characteristics of facultatively symbiotic Frankia sp. Strains reflect host range and host plant biogeography. Genome Research 17, 7–15.
| Genome characteristics of facultatively symbiotic Frankia sp. Strains reflect host range and host plant biogeography.Crossref | GoogleScholarGoogle Scholar |
Raven PH, Axelrod DI (1974) Angiosperm biogeography and past continental movements. Annals of the Missouri Botanical Garden 61, 539–673.
| Angiosperm biogeography and past continental movements.Crossref | GoogleScholarGoogle Scholar |
Richardson JE, Fay MF, Cronk QCB, Bowman D, Chase MW (2000) A phylogenetic analysis of Rhamnaceae using rbcL and trnL-F plastid DNA sequences. American Journal of Botany 87, 1309–1324.
| A phylogenetic analysis of Rhamnaceae using rbcL and trnL-F plastid DNA sequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXnt1Ohtrw%3D&md5=b5eb4b531f9cd903921f749d4d7757a4CAS |
Rouvier C, Prin Y, Reddell P, Normand P, Simonet P (1996) Genetic diversity among Frankia strains nodulating members of the family Casuarinaceae in Australia revealed by PCR and restriction fragment length polymorphism analysis with crushed root nodules. Applied and Environmental Microbiology 62, 979–985.
Schuster M (1976) Plate tectonics and its bearing on the geographical origin and dispersal of angiosperms. In ‘Origin and early evolution of angiosperms’. (Ed. CB Beck) pp. 48–138. (Columbia University Press: New York)
Schwencke J, Carú M (2001) Advances in actinorhizal symbiosis: host plant-Frankia interactions, biology, and application in arid land reclamation. A review. Arid Land Research and Management 15, 285–327.
| Advances in actinorhizal symbiosis: host plant-Frankia interactions, biology, and application in arid land reclamation. A review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXntlags74%3D&md5=07eaf61794c6a0760184b26e8b7601a3CAS |
Scriven LJ, Hill RS (1995) Macrofossil Casuarinaceae: their identification and the oldest macrofossil record, Gymnostoma antiquum sp. nov., from the Late Paleocene of New South Wales, Australia. Australian Systematic Botany 8, 1035–1053.
| Macrofossil Casuarinaceae: their identification and the oldest macrofossil record, Gymnostoma antiquum sp. nov., from the Late Paleocene of New South Wales, Australia.Crossref | GoogleScholarGoogle Scholar |
Silvester WB (1976) Ecological and economic significance of the non-legume symbiosis, In ‘Proceedings of the 1st International Symposium on Nitrogen Fixation’. (Eds WE Newton, CJ Nyman) pp. 489–506. (Washington State University Press: Pullman)
Silvester WB, Harris SL (1989) Nodule structure and nitrogenase activity of Coriaria arborea in response to varying P02 –. Plant and Soil 118, 97–109.
| Nodule structure and nitrogenase activity of Coriaria arborea in response to varying P02 –.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXmtFajtLo%3D&md5=543993a95dac69cef8853a5348a9c0baCAS |
Simonet P, Navarro E, Rouvier C, Reddell P, Zimpfer J, Dommergues Y, Bardin R, Combarro P, Hamelin J, Domenach AM, Gourbiere F, Prin Y, Dawson JO, Normand P (1999) Co-evolution between Frankia populations and host plants in the family Casuarinaceae and consequent patterns of global dispersal. Environmental Microbiology 1, 525–533.
| Co-evolution between Frankia populations and host plants in the family Casuarinaceae and consequent patterns of global dispersal.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3Mzit1Wksw%3D%3D&md5=7d4100d6d187923c6cbe60f2e99aa289CAS |
Skog LE (1972) The genus Coriaria (Coriariaceae) in the western hemisphere. Rhodora 74, 242–253.
Soltis DE, Soltis PS (2000) Contributions of plant molecular systematics to studies of molecular evolution. Plant Molecular Biology 42, 45–75.
| Contributions of plant molecular systematics to studies of molecular evolution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXht1Gku7Y%3D&md5=3fc38620970f66e770dd537c47f56ec2CAS |
Stevens PF (2001) Angiosperm phylogeny website. Ver. 9. Available at http://www.mobot.org/MOBOT/research/APweb/ [Verified 11 July 2011].
Swensen SM (1996) The evolution of actinorhizal symbioses: evidence for multiple origins of the symbiotic association. American Journal of Botany 83, 1503–1512.
| The evolution of actinorhizal symbioses: evidence for multiple origins of the symbiotic association.Crossref | GoogleScholarGoogle Scholar |
The Plant List (2010) The Plant List. Ver. 1. Online database is copyrighted by the Royal Botanic Gardens, Kew and Missouri Botanical Garden on behalf of The Plant List (TPL) and its contributors. Available at http://www.theplantlist.org/ [Verified 30 June 2011].
Welsh A, Mirza B-S, Rieder J-P, Paschke MW, Hahn D (2009a) Diversity of frankiae in root nodules of Morella pensylvanica grown in soils from five continents. Systematic and Applied Microbiology 32, 201–210.
| Diversity of frankiae in root nodules of Morella pensylvanica grown in soils from five continents.Crossref | GoogleScholarGoogle Scholar |
Welsh AK, Dawson JO, Gottfried GJ, Hahn D (2009b) Diversity of Frankia populations in root nodules of geographically isolated Arizona alder trees in central Arizona (United States). Applied and Environmental Microbiology 75, 6913–6918.
| Diversity of Frankia populations in root nodules of geographically isolated Arizona alder trees in central Arizona (United States).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsVGrs7%2FO&md5=4e4faccca697b14c4356bce997415a7aCAS |
Yokoyama J, Suzuki M, Iwatsuki K, Hasebe M (2000) Molecular phylogeny of Coriaria, with special emphasis on the disjunct distribution. Molecular Phylogenetics and Evolution 14, 11–19.
| Molecular phylogeny of Coriaria, with special emphasis on the disjunct distribution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXisFenuw%3D%3D&md5=c7736bcaa5e12b8c2efed055f9cbd2e8CAS |
