Phylogenetic analysis of the Australian Salicornioideae (Chenopodiaceae) based on morphology and nuclear DNA
K. A. Shepherd A D , T. D. Macfarlane B and M. Waycott CA School of Plant Biology, Faculty of Natural and Agricultural Sciences, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia.
B Department of Conservation and Land Management, Brain Street, Manjimup, WA 6258, Australia.
C School of Tropical Biology, James Cook University, Townsville, Qld, 4811, Australia.
D Corresponding author. Email: shepherd@cyllene.uwa.edu.au
Australian Systematic Botany 18(1) 89-115 https://doi.org/10.1071/SB04031
Submitted: 5 August 2004 Accepted: 31 December 2004 Published: 29 March 2005
Abstract
The Salicornioideae Kostel. are distinctive among the Chenopodiaceae Venet.. However, their phylogenetic relationships are poorly understood. Analyses of morphological and molecular characters were undertaken to evaluate relationships within the subfamily and to test the monophyly of the endemic Australian genera Halosarcia Paul G. Wilson, Pachycornia Hook.f., Sclerostegia Paul G. Wilson, Tecticornia Hook.f. and Tegicornia Paul G. Wilson. Kalidium Moq. and Halopeplis Bunge ex Ung.-Sternb. of the tribe Halopeplideae were used as outgroup representatives in the morphological analysis and resolved sister to the tribe Salicornieae. Allenrolfea Kuntze; Halocnemum Bieb. and Heterostachys Meyer formed an early branching group sister to a moderately supported clade comprised of the remaining Salicornieae. Only terminal groups of closely related species received significant bootstrap support in this analysis. In contrast, the current tribal classification of the Salicornioideae was not supported in the molecular analysis as Allenrolfea occidentalis Kuntz (tribe Salicornieae) positioned sister to Kalidium foliatum Moq. (tribe Halopeplideae) and the remaining Salicornieae. Three major clades received strong bootstrap support: Microcnemum+Arthrocnemum, Sarcocornia+Salicornia, and the endemic Australian genera. None of the endemic Australian genera was individually supported as monophyletic in either the morphological or the molecular analyses. Subspecies complexes, polyploids and hybrids may contribute to the lack of resolution and apparently high levels of homoplasy in the morphological analysis. A greater understanding of population level processes is required to begin to resolve the phylogeny of this complex group.
Acknowledgments
The authors thank Bernie Dudley, Joseph Maria Montserrat, Javier Rejos, Ian Clarke (Melbourne Royal Botanic Gardens), Tjeerd Bouma and BP Koutstaal for supplying specimens and loan material and to Alex Chapman for sorting material at USA. Thanks go to Grant Whiteman and Steve Hopper for reviewing earlier drafts of the manuscript and to Sharon Platten at the Centre for Microscopy and Microanalysis (UWA) for instruction on the Environmental scanning electron microscope. KS especially thanks Tim Colmer and Terry Macfarlane for supervision while undertaking a PhD at The University of Western Australia and to Paul Wilson for showing the way with the Australian Salicornioideae. This research was supported by an ARC Grant with linkage support from MERIWA, Normandy Mining Limited, Placer (Granny Smith), Acacia Resources, KCGM and the WA Herbarium.
Agardh, JG (1858). ‘Theoria Systematis Plantarum.’ (CWK Gleerup: Lund)
Ball PW
(1964) A taxonomic review of Salicornia in Europe. Feddes Repertorium 69, 1–8.
Ball PW, Tutin TG
(1959) Notes on the annual species of Salicornia in Britain. Watsonia 4, 193–205.
Barlow, B (1982). Cytogenetic systems in Australian arid zone plants. In ‘Evolution of the flora and fauna of arid Australia’. pp. 161–166. (Peacock Publications in association with Australian Systematic Botany Society and ANZAAS South Australian Division Inc.: Frewville, South Australia)
Bentham G, Hooker JD
(1880) Chenopodiaceae. Genera Plantarum 3, 43–78.
Bettenay E
(1962) The salt lake systems and their associated aeolian features in the semi-arid regions of Western Australia. Journal of Soil Science 13, 10–17.
Carine MA, Scotland RW
(2002) Classification of Strobilanthinae (Acanthaceae): trying to classify the unclassifiable? Taxon 51, 259–279.
Carolin RW,
Jacobs SWL, Vesk M
(1982) The chlorenchyma of some members of the Salicornieae (Chenopidiaceae). Australian Journal of Botany 30, 387–392.
Castroviejo S, Coello P
(1980) Datos cariológicos y taxonómicos sobre las Salicorniinae A.J. Scott Ibéricas. Anales del Jardin Botanico de Madrid 37, 41–73.
Castroviejo S, Lago E
(1992) Datos acerca de la hibridación en el género Sarcocornia (Chenopodiaceae). Anales del Jardin Botanico de Madrid 50, 163–170.
Clausen J
(1954) Partial apomixis as an equilibrium system in evolution. Caryologia 6, 469–479.
Connor HE
(1984) Gynodioecism in Sarcocornia quinqueflora (Salicornieae) in New Zealand. New Zealand Journal of Botany 22, 433–439.
Dalby D
(1963) Seed dispersal in Salicornia pusilla.
Nature 199, 197–198.
Dalby, D (1975). Salicornia L. In ‘Hybridization and the flora of the British Isles’. pp. 186–188. (Academic Press: London)
Dalby DH
(1962) Chromosome number, morphology and breeding behaviour in the British Salicorniae. Watsonia 5, 150–162.
Danilastos, GD (1993). Microscopy research and technique. In ‘Introduction to the environmental scanning electron microscope instrument’. pp. 354–361. (Wiley-Liss Inc.: New York)
Darlington, CD (1939).
Davy AJ,
Bishop GF, Costa CSB
(2001)
Salicornia L. (Salicornia pusilla J. Woods, S. ramosissima J. Woods, S. europaea L., S. obscura P.W. Ball & Tutin, S. nitens P.W. Ball & Tutin, S. fragilis P.W. Ball & Tutin and S. dolichostachya Moss). Journal of Ecology 89, 681–707.
| Crossref | GoogleScholarGoogle Scholar |
De Deckker P
(1983) Australian salt lakes: their history, chemistry and biota—a review. Hydrobiologia 105, 231–244.
| Crossref | GoogleScholarGoogle Scholar |
Dumortier, DC (1827). ‘Flora Belgica.’ (Tournai: Belgium)
English J
(2004) Ecophysioloy of salinity and waterlogging tolerance in selected species of Halosarcia. PhD thesis.
(The University of Western Australia:
Perth)
Fahn A
(1963) The fleshy cortex of articulated Chenopodiaceae. Journal of the Indian Botanical Society 42a, 39–45.
Fahn A, Arzee T
(1959) Vascularization of articulated Chenopodiaceae and the nature of their fleshy cortex. American Journal of Botany 46, 330–338.
Fahn A, Shchori Y
(1967) The organization of the secondary conducting tissues in some species of the Chenopodiaceae. Phytomorphology 17, 147–154.
Feder N, O’Brien TP
(1968) Plant microtechnique: some principles and new methods. American Journal of Botany 55, 123–142.
Ferguson IK
(1964) Notes on the stigma morphology and flowering behaviour in British Salicornieae. Watsonia 6, 25–27.
de Fraine E
(1912) Anatomy of the genus Salicornia.
Journal of the Linnean Society of London Botany 41, 317–348.
Freitag, H (2000). Salicornia L. In ‘Flora of Turkey and the East Aegean Islands. Supplement 2’. pp. 59–60. (University Press: Edinburgh)
Gorshkova, SG ,
Il’in, MM ,
Knorring, OE ,
Kuzeneva, OI ,
Murav’eva, OA ,
Tolmachev, AI ,
Shishkin, BK ,
Shteinberg, EI ,
and
Vasil’chenko, IT (1970). ‘Centrospermae. Flora of the USSR.’ (Israel Program for Scientific Translations: Jerusalem)
Grant, V (1971). ‘Plant Speciation.’ (Columbia University Press: New York)
Halket AC
(1928) The morphology of Salicornia—an abnormal plant. Annals of Botany 42, 525–536.
Hillis DM, Huelsenbeck JP
(1992) Signal, noise and reliability in molecular phylogenetic analyses. The Journal of Heredity 83, 189–195.
| PubMed |
Jeanmougin F,
Thompson JD,
Gouy M,
Higgins DG, Gibson TJ
(1998) Multiple sequence alignment with Clustal X. Trends in Biochemical Sciences 23, 403–405.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Johnson M
(1980) The origin of Australia’s salt lakes. New South Wales Geological Survey–Records 19, 221–266.
Judd WS, Ferguson IK
(1999) The genera of Chenopodiaceae in the southeastern United States. Harvard Papers in Botany 4, 365–416.
Kadereit G,
Borsch T,
Weising K, Freitag H
(2003) Phylogeny of Amaranthaceae and Chenopodiaceae and the evolution of C4 photosynthesis. International Journal of Plant Sciences 164, 959–986.
| Crossref | GoogleScholarGoogle Scholar |
Kadereit G,
Gotzek D,
Jacobs S, Freitag H
(2005) Origin and age of Australian Chenopodiaceae. Organisms, Diversity and Evolution (in press) 5,
Klak C,
Hedderson TA, Linder HP
(2003) A molecular systematic study of the Lampranthus group (Aizoaceae) based on the chloroplast TrnL-trnF and nuclear ITS and 5S NTS sequence data. Systematic Botany 28, 70–85.
Kosteletzky, V (1835). Chenopodiaceae. In ‘Allgemenine Medizinisch-Pharmazeutische Flora. 4’. pp. 1428–1429. (Prague: Czech Republic)
Kühn, U ,
Bittrich, V ,
Carolin, R ,
Freitag, H ,
Hedge, IC ,
Uotila, P ,
and
Wilson, PG (1993). Chenopodiaceae. In ‘The families and genera of vascular plants. Flowering plants—Dicotyledons. 2’. pp. 253–280. (Springer-Verlag: Berlin)
Levin DA
(2001) The recurrent origin of plant races and species. Systematic Botany 26, 197–204.
Martin HA
(1998) Late Cretaceous-Cainozoic palynology of the Poonarunna No. 1 well, Central Australia. Transactions of the Royal Society of South Australia 122, 89–138.
Miller JT,
Andrew RA, Maslin BR
(2002) Towards an understanding of variation in the Mulga complex (Acacia aneura and relatives). Conservation Science Western Australia 4, 19–35.
Moquin-Tandon, A (1840). ‘Chenopodearum Monographica Enumeratio.’ (Paris: France)
Moss CE
(1954) The species of Arthrocnemum and Salicornia in Southern Africa. The Journal of South African Botany 20, 1–22.
O’Callaghan M
(1992) The ecology and identification of the southern African Salicornieae (Chenopodiaceae). South African Journal of Botany 58, 430–439.
Posada, D (1998). Modeltest 3.06—Testing models of evolution.’ (Provo: Utah)
Randell B
(1970) Adaptations in the genetic system of Australian arid zone Cassia species. Australian Journal of Botany 18, 77–97.
Schütze P,
Freitag H, Weising K
(2003) An integrated molecular and morphological study of the subfamily Suaedioideae Ulbr. (Chenopodiaceae). Plant Systematics and Evolution 239, 257–286.
| Crossref | GoogleScholarGoogle Scholar |
Scott AJ
(1977) Reinstatement and revision of Salicorniaceae J. Agardh (Caryophyllales). Botanical Journal of the Linnean Society 75, 357–374.
Shepherd KA
(2005) Systematic analysis of the Australian Salicornioideae (Chenopodiaceae). PhD thesis.
(The University of Western Australia:
Perth)
Shepherd KA, Yan G
(2003) Chromosome number and size variations in the Australian Salicornioideae (Chenopodiaceae)—evidence of polyploidisation. Australian Journal of Botany 51, 441–452.
| Crossref | GoogleScholarGoogle Scholar |
Shepherd KA,
Macfarlane TD, Colmer TD
(2005) Morphology, anatomy and histochemistry of fruits and seeds of the Salicornioideae (Chenopodiaceae). Annals of Botany (in press) ,
| PubMed |
Shepherd KA,
Waycott M, Calladine A
(2004) Radiation of the Australian Salicornioideae (Chenopodiaceae)—based on evidence from nuclear and chloroplast DNA sequences. American Journal of Botany 91, 1387–1397.
Shmida, A (1985). Biogeography of the desert flora. In ‘Hot deserts and arid shrublands. Vol. 12a’. pp. 23–77. (Elsevier: Amsterdam)
Short DC, Colmer TD
(1999) Salt tolerance in the halophyte Halosarcia pergranulata subsp. pergranulata.
Annals of Botany 83, 207–213.
| Crossref | GoogleScholarGoogle Scholar |
Simmons MP, Ochoterena H
(2000) Gaps as characters in sequence-based phylogenetic analysis. Systematic Biology 48, 369–381.
Soriano A
(1946) Halophytaceae nueva familia del Order Cantrospermae. Notas del Museo de la Planta 11, 161–175.
Spegazzini C
(1902) nova addenda ad floram Patagonicam III. Anales del Museo Nacional de Bruenos Aires 7, 137–154.
Stebbins, GL (1971). Chromosomal evolution in higher plants. In ‘A series of student texts in contemporary biology’. pp. 155–199. (Edward Arnold: London)
Swofford, DL (2002). PAUP—Phylogenetic analysis using parsimony. (Sinauer Associates: Sunderland)
Tölken HR
(1967) The species of Arthrocnemum and Salicornia (Chenopodiaceae) in Southern Africa. Bothalia 9, 255–307.
Ulbrich, E (1934). ‘Chenopodiaceae.’ (Wilhelm Engelmann: Berlin)
Ungern-Sternberg, FB (1866). ‘Systematik der Salicornieen.’ (Dorpat: Estonia)
van de Graff WJE,
Crowe RWA,
Bunting JA, Jackson MJ
(1977) Relict early Cainozoic drainages in arid Western Australia. Zeitschrift für Geomorphologie 21, 379–400.
Volkens, G (1892). Chenopodiaceae. In ‘Die Natürlichen Pflanzenfamilien’. pp. 36–91. (Engelmann: Berlin)
Volkens, G (1893). ‘Chenopodiaceae. (Berlin: Germany)
Whiteman G
(2002) The impact of pastoral practice on the genetic diversity of the grass Heteropogon contortus in a semi-arid Australian Rangeland. PhD thesis.
(James Cook University:
Townsville)
Wilson PG
(1972) A taxonomic revision of the genus Tecticornia.
Nuytsia 1, 277–288.
Wilson PG
(1980) A revision of the Australian species of Salicornieae (Chenopodiaceae). Nuytsia 3, 1–154.
Wilson, PG (1984). Chenopodiaceae In ‘Flora of Australia’. pp. 277–309. (Australian Government Publishing Service: Canberra)