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Sorghum Laxiflorum and S. Macrospermum, the Australian Plant Syst. Evol. 249: 233–246 (2004) DOI 10.1007/s00606-004-0210-7 Sorghum laxiflorum and S. macrospermum, the Australian native species most closely related to the cultivated S. bicolor based on ITS1 and ndhF sequence analysis of 25 Sorghum species S. L. Dillon1, P. K. Lawrence1, R. J. Henry2, L. Ross3, H. J. Price4, and J. S. Johnston5 1Australian Tropical Crops and Forages Collection, Queensland Department of Primary Industries and Fisheries, Biloela, QLD, Australia 2Centre for Plant Conservation Genetics, Southern Cross University, Lismore, NSW, Australia 3Dallas, TX, USA 4Department of Soil & Crop Sciences, Texas Agricultural Experiment Station, Texas A&M University, College Station TX, USA 5Department of Entomology, Texas Agricultural Experiment Station, Texas A&M University, College Station TX, USA Received March 8, 2004; accepted June 9, 2004 Published online: October 18, 2004 Ó Springer-Verlag 2004 Abstract. Australian species make up seventeen of relationships within this second lineage remain the world’s twenty-five recognised species of Sor- unresolved. We identified S. laxiflorum and ghum, with the genus separated into five sections: S. macrospermum as the Australian species most Eu-sorghum, Chaetosorghum, Heterosorghum, closely related to cultivated sorghum. Our data Para-sorghum and Stiposorghum. Whereas the support a reduction in the number of subgeneric genetic relationships within section Eu-sorghum sections from five to three: Eu-sorghum (unchanged); are well known, little is known about the genetic a combined Chaetosorghum/Heterosorghum to relationships and crossabilities outside the primary reflect the very close relationship between these genepool. We made a detailed investigation of two species; and a combined Para-sorghum/Stipo- phylogenetic relationships within Sorghum to iden- sorghum section, thereby removing the unclear tify wild species most closely related to cultivated taxonomic and genetic boundaries between these sorghum (with outgroups Zea mays and Saccharum species. officinarum). The ribosomal ITS1 gene of ten species and the chloroplast ndhF gene from nine- Key words: Wild sorghum, phylogeny, ITS1, ndhF, teen species were sequenced. Independent and Poaceae. combined analyses of the ITS1 and ndhF data sets were undertaken. The Eu-sorghum species were resolved into a strongly supported lineage by all Introduction three analyses, and included the Australian natives S. laxiflorum and S. macrospermum in the ITS1 and Australian species of Sorghum make up sev- combined analyses. All remaining sorghum species enteen out of the world’s twenty-five recogni- were resolved into a second well-supported lineage sed Sorghum species, with the genus separated in the combined analyses, although some internal into five taxonomic sections: Eu-sorghum, 234 S. L. Dillon et al.: Sorghum laxiflorum and S. macrospermum closely related to S. bicolor Chaetosorghum, Heterosorghum, Para-sorghum Lazarides, S. bulbosum Lazarides, S. ecarina- and Stiposorghum. The six Eu-sorghum species tum Lazarides, S. exstans Lazarides, S. inter- consist of the cultivated Sorghum bicolor (L.) jectum Lazarides, S. intrans F. Muell. ex Moench,S.x almum Parodi, S. arundinaceum Benth., S. plumosum (R. Br.) P. Beauv., and (Desv.) Stapf,S.x drummondii (Steud.) S. stipoideum (Ewart & Jean White) C. A. Millsp. & Chase, S. halepense (L.) Pers., and Gardner & C. E. Hubb. form the section S. propinquum (Kunth) Hitchc. The Eu-sorgh- Stiposorghum, all being endemic to northern ums originate from Africa and Asia with Australia (Garber 1950, Lazarides et al. 1991). 2n ¼ 20 and 40 chromosomes, and the known The gene pool concept is useful to describe progenitor of cultivated S. bicolor is S. arun- the total pool of different genes within a genus. dinaceum (DeWet and Harlan 1971, Doggett The primary gene pool consists of species that 1976, Duvall and Doebley 1990). Sorghum readily cross producing viable hybrids with drummondii originated from a natural cross chromosomes that freely recombine. The sec- between S. bicolor and S. arundinaceum, while ondary gene pool consists of species with a S. propinquum is reputedly a perennial rhizo- certain degree of hybridisation barriers due to matous form of S. bicolor (Doggett 1976, ploidy differences, chromosome alterations, or Chittenden et al. 1994, Sun et al. 1994). incompatibility genes making gene transfer Sorghum halepense (Johnson grass) is derived difficult. The tertiary gene pool consists of from a doubling of the chromosomes in a species from which gene transfer is very natural cross between S. arundinaceum and difficult due to strong sterility barriers (Harlan S. propinquum, while a natural cross between and de Wet 1971). In Sorghum, the Eu-sorghum S. bicolor and S. halepense gave rise to S. x species form both the primary and secondary almum (Doggett 1976). The close genetic gene pools, while Chaetosorghum, Heterosor- relationships and inter-crossability between ghum, Para-sorghum and Stiposorghum species the Eu-sorghum species are well known form the tertiary gene pool. Advances in (Magoon and Shambulingappa 1961, Wu biotechnology are increasing the use of these 1979, Chittenden et al. 1994, Paterson et al. tertiary genepool species in breeding programs. 1995, Stenhouse et al. 1997). Direct evaluation of pest and disease resis- The section Chaetosorghum contains the tances in non-primary wild sorghum species single species S. macrospermum E. D. Garber (sections Chaetosorghum, Heterosorghum, that is endemic to a small area in the Northern Para-sorghum and Stiposorghum) have been Territory of Australia. Sorghum laxiflorum undertaken over the last twenty years (Bapat F. M. Bailey forms the section Heterosorghum, and Mote 1982, Karunakar et al. 1994, is native to northern Australia and Papua New Franzmann and Hardy 1996, Sharma and Guinea, and is geographically more diverse Franzmann 2001, Kamala et al. 2002, Komo- than its close relative S. macrospermum (Gar- long et al. 2002). These studies show that many ber 1950, Lazarides et al. 1991, Dillon et al. Australian native species of Sorghum contain 2001). The section Para-sorghum contains the valuable genes conferring resistances to pests seven species. S. grande Lazarides, S. leioclad- (Australian species are non-hosts to the sor- um (Hack.) C. E. Hubb., S. matarankense E. ghum midge [Stenodiplosis sorghicola Coquil- D. Garber & Snyder, S. nitidum (Vahl) Pers., lett]) and diseases already in Australia. S. purpureo-sericeum (Hochst. ex. A. Rich.) Importantly, these species have resistances to Asch. & Schweinf., S. timorense (Kunth) Buse some pests (shoot fly [Atherigona soccata and S. versicolor Andersson with these species Rondani], greenbug [Schizaphis graminum native to northern monsoonal Australia, Afri- Rondani], stem borer [Chilo partellus Swinhoe] ca and Asia (Garber 1950, Lazarides et al. etc) and diseases (sorghum downy mildew 1991, Phillips 1995). Sorghum amplum Laza- [Peronosclerospora sorghi (Weston & Uppal) rides, S. angustum S. T. Blake, S. brachypodum C.G. Shaw] etc) currently not present in S. L. Dillon et al.: Sorghum laxiflorum and S. macrospermum closely related to S. bicolor 235 Australia. These non-primary wild Sorghum encodes the ND5 protein of the chloroplast species are therefore valuable sources of genes NADH dehydrogenase involved in chloroplast that could confer resistance to many pests and respiration (Ferguson 1999, Kim and Jansen diseases currently affecting cultivated sorghum 1995, Bohs and Olmstead 1997). The ndhF has production. However, the phylogenetic rela- a relatively high rate of molecular evolution tionships that exist between the cultivated and and provides three times more phylogenetic wild species must be established to act as a information than other chloroplast genes guide to using these wild species for breeding. because of its length and sequence divergence Whereas the phylogenetic relationships (Olmstead and Sweere 1994, Kim and Jansen within section Eu-sorghum (primary and sec- 1995). The highest rate of variability has been ondary gene pools) are well known, little is shown in the 3¢ end of the gene, with 60% of known about the phylogenetic relationships the nucleotide substitutions and all of the and crossabilities of the tertiary genepool alignment gaps positioned there (Olmstead and species. Recent research has attempted to Sweere 1994, Clark et al. 1995, Catala´n et al. determine the phylogenetic relationships 1997). The ndhF gene has delineated closely between primary and non-primary Sorghum related species within many plant groups species, however many relationships within the including sunflower, solanum and Poaceae genus remain unresolved (Sun et al. 1994, (Clark et al. 1995, Kim and Jansen 1995, Spangler et al. 1999, Dillon et al. 2001, Neyland and Urbatsch 1996, Bohs and Olm- Spangler 2003). stead 1997, Catala´n et al. 1997, Spangler et al. The ribosomal ITS1 work by Dillon et al. 1999, Catala´n and Olmstead 2000, Spangler (2001) attempted to determine the phyloge- 2003). Because ndhF gene sequences were able netic relationships between all 25 Sorghum to elucidate relationships between closely species, and obtained two distinct lineages. related Poaceae species, we decided to use this The Eu-sorghum species were all closely related gene to further resolve the phylogenetic rela- with strong statistical support, with most tionships between the Australian native sorgh- Australian native species in a separate lineage. ums. Many of the relationships between the Aus- To fully determine the phylogenetic rela- tralian
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