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Multiple Origins of Polyploids in the Glycine Tabacina Complex Inferred from Chloroplast DNA Polymorphism (Restriction Fragment Variation/Plant Taxonomy) JEFF J

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Multiple Origins of Polyploids in the Glycine Tabacina Complex Inferred from Chloroplast DNA Polymorphism (Restriction Fragment Variation/Plant Taxonomy) JEFF J Proc. Natl. Acad. Sci. USA Vol. 87, pp. 714-717, January 1990 Botany Multiple origins of polyploids in the Glycine tabacina complex inferred from chloroplast DNA polymorphism (restriction fragment variation/plant taxonomy) JEFF J. DOYLE*, JANE L. DOYLE*, A. H. D. BROWNt, AND J. P. GRACEt *L. H. Bailey Hortorium, 466 Mann Library Building, Cornell University, Ithaca, NY 14853; and tCommonwealth Scientific and Industrial Research Organisation, Division of Plant Industry, GPO Box 1600, Canberra, Australian Capital Territory 2601, Australia Communicated by Charles B. Heiser, Jr., November 13, 1989 (receivedfor review September 8, 1989) ABSTRACT The Glycine tabacina polyploid complex has J.J.D., J.L.D., and A.H.D.B., unpublished data). Studies of been shown to include a minimum of two morphological and restriction endonuclease recognition site variation of mater- crossing groups, which also differ in chloroplast DNA (cpDNA) nally inherited (15) chloroplast DNA (cpDNA) indicate that restriction map and nuclear ribosomal gene repeat phenotype. the two polyploid classes had different chloroplast genome These AAB2B2 and BBB2B2 G. tabacina polyploids contain (plastome) donors; that of the AAB2B2 type belonged to the plastomes referable to the A and B diploid plastome groups of A plastome group of diploid species while the BBB2B2 subgenus Glycine, respectively. Eight different cpDNA variants progenitor was, as expected, a member of the B plastome were observed among the 65 B-type polyploids studied, six of group (16). which were identical for numerous restriction site characters to Most recently, studies of cpDNA variation within the B plastome types found among the highly polymorphic B genome diploid species group of the subgenus have revealed consid- diploid species. It is hypothesized that there have been numer- erable polymorphism, with 25 plastome groups identified ous independent origins of polyploid G. tabacina: at least one (J.J.D. et al., unpublished data). These studies, along with AA x B2B2 event and a minimum of five BB X B2B2 events previous cpDNA studies of the entire subgenus, have pro- involving different BB types as female progenitor. Low vided markers for elucidating the origins and affinities of amounts of cpDNA divergence between diploid and polyploid polyploid G. tabacina accessions. Here we show that the B plastomes and among the plastomes of geographically disjunct group is cpDNA in polyploids suggest that the origin and dispersal of polyploids polyploid polymorphic for variants that are relatively recent events. All hypothesized diploid progen- several cases are identical to those found among diploid itors are native to Australia, while both A- and B-type G. accessions, suggesting that this polyploid taxon had numer- tabacina polyploids occur on islands of the Pacific outside the ous independent origins. range of diploids. The presence of several different plastome types of polyploid G. tabacina in the Pacific islands suggests METHODS AND MATERIALS that several colonization events have occurred. Sixty-five accessions of polyploid G. tabacina were used in this study, most selected from the Commonwealth Scientific Polyploidy has been a significant genetic process in the and Industrial Research Organisation native Australian Gly- evolution offlowering plants. The origin of a polyploid taxon cine collection (listed in Table 1; map coordinates given in is often considered a rare event, however, despite the abun- ref. 16). These accessions were chosen to represent as fully dance of angiosperm species with high, presumably poly- as possible the morphological, geographical, and genetic ploid, chromosome numbers (1, 2), the common natural of the Plants were in the occurrence of unreduced gametes in plants (3), and the often diversity complex. grown green- high frequency of polyploids within plant species (4). The house under uniform conditions. Voucher specimens are availability of molecular markers has recently provided a deposited in the herbarium of the L. H. Bailey Hortorium means of assessing more readily the frequency of polyploid (BH) and in the Herbarium Australiense (CANB). origins, with the result that multiple origins of polyploid taxa DNA was isolated from 0.01-1 g of fresh leaves from indi- are increasingly being noted (5-8). vidual plants by the method of Doyle and Doyle (17). Acces- Glycine subgenus Glycine, the perennial relatives of the sions in Table 1 were screened with a subset of the more than cultivated soybean, comprises 15 currently recognized spe- 50 restriction site characters used in our studies of variation cies. The entire genus, although presumably an ancient among taxa ofthe diploid B genome group of subgenus Glycine polyploid with 2n = 4x = 40, is fully diploidized and only (J.J.D. et al., unpublished data); accessions marked with aster- three species of subgenus Glycine include neopolyploids (9, isks in Table 1 were screened with a minimum of 45 of these 10). One of these, Glycine tabacina, includes diploids (2n = characters. Digestion with restriction enzymes, gel electropho- 40) that are confined to eastern Australia and polyploids (2n resis, transfer to nylon membranes, hybridization with mung = 80) that occur both sympatrically with the diploids as well bean cpDNA clones (from J. Palmer, Indiana University), and as on islands of the South Pacific and western central Pacific autoradiography were as described elsewhere (15). Cladistic (11-13). Two reproductively isolated types of polyploids are analyses were performed on diploid and polyploid accessions known in the complex and have been designated AAB2B2 and using algorithms available in the HENNIG86 phylogenetic anal- BBB2B2 to indicate that they share one of their two diploid ysis software package (Version 1.5; supplied by J. S. Farris, genomes (11-13). Consistent with this hypothesis, both poly- State University ofNew York, Stony Brook, NY) as described ploids are fixed hybrids for their 18S-25S nuclear rRNA gene elsewhere (J.J.D. et al., unpublished data). Character analyses (rDNA) repeats and share one of their repeat classes (ref. 14; and graphical depiction of cladograms used the CLADOS soft- ware package (K. C. Nixon, personal communication). The publication costs of this article were defrayed in part by page charge payment. This article must therefore be hereby marked "advertisement" Abbreviations: cpDNA, chloroplast DNA; rDNA, nuclear rRNA in accordance with 18 U.S.C. §1734 solely to indicate this fact. genes. 714 Downloaded by guest on October 1, 2021 Botany: Doyle et al. Proc. Natl. Acad. Sci. USA 87 (1990) 715 Table. 1. Geographic origins and plastome designations of G. tabacina polyploid accessions studied Group Origin Accessions 1 New South Wales, Australia 1208, 1234,* 1254, 1313, 1321, 2030, 2511, 2762 Queensland, Australia 378707, 1262, 1862, 2246, 2274, 2279, 2772 Victoria, Australia 2709 South Australia 1706* Western central Pacific 1071, 1072, 1221, 1226, 1284, 1306, 1332, 1338,* 1382, 1714, 1716 South Pacific 1258,* 1863, 1981, 1982, 1984, 1988 2 Australian Capital Territory 1075* New South Wales, Australia 1080,* 1439, 2028, 2029, 2763 Queensland, Australia 2263, 2268, 2715, 2738 Victoria, Australia 2708, 2710 3 New South Wales, Australia 1144, 1255,* 1273,* 1503, 1860, 2765 Queensland, Australia 1861, 2281, 2308 Western central Pacific 2602 4 New South Wales, Australia 1141,* 1312, 1314 5 South Pacific 1205,* 1324, 1325 6 New South Wales, Australia 1329* U South Pacific 1986, 1989 Accessions are listed by Commonwealth Scientific and Industrial Research Organisation Native Australian Glycine Collection numbers (four digits) except 378707, for which the U.S. Department of Agriculture Plant Introduction number is given. Plastome groups (groups 1-6) correspond to origin numbers given in Fig. 2; group U includes the two types unlike any diploid plastome types. *Accessions were screened for variation in a minimum of 45 restriction site characters, while other accessions were screened with a subset of diagnostic markers. RESULTS followed by a restriction site gain in accessions from Australia. However, this same site polymorphism also occurs among All BBB2B2 (B type) G. tabacina accessions were screened populations of Glycine latifolia, a diploid species confined to for several characters that had been found to be diagnostic for Australia; the site character showed no homoplasy in a survey particular plastome types in our studies of cpDNA variation of 74 diploid B genome accessions (J.J.D. et al., unpublished in B genome diploid taxa (J.J.D. et al., unpublished data). data), and the presence of this site in polyploid accessions is Through this procedure, nine different plastome types were as cpDNA from found among the 65 polyploid accessions studied. Represen- interpreted evidence of contribution diploids tatives of several of these types were analyzed with addi- possessing it, rather than of independent origin. tional characters used in the diploid studies; results indicated 1 2 3 4 5 2 3 4 5 that six of the nine types were each identical to different diploid plastome types. A seventh type (G1075) was more closely related to one of these diploid-polyploid pairs than X.h any other polyploid accession. Two accessions, each with a different plastome variant, were unlike plastomes found in toeA- - n-A- 22~-_w w r 22 any of the diploids studied (G1986, G1989). Autoradiograms showing diagnostic restriction site variants for some of these diploid-polyploid pairs are illustrated in Fig. 1; cladistic relationships ofthese
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