The american elm, Ulmus americana (Ulmaceae), is a tall, graceful tree that is native to the eastern United States and adjacent Canada (Bey, 1990). The species has frequently been planted as an ornamental and shade tree throughout temperate parts of the world, but use of the tree as an ornamental has been heavily limited by dutch elm disease, caused by two exotic wilt fungi, Ophiostoma ulmi (Buisman) C Nannf. and O. novo-ulmi Brasier (Brasier, 1991, 2001). Recent screening and breeding work has produced several cultivars that tolerate the disease (Townsend et al., 2005), and work is underway to breed this resistance into a wider variety of genetic backgrounds, with the aim of restoring american elm as an important and useful in both urban and forested landscapes (Pinchot et al., 2017).
Most elm species are diploid, with 2n = 28 (Santamour and Ware, 1997). Polyploids are known in only one elm species, U. americana, with diploid and tetraploid populations known in the wild (Whittemore and Olsen, 2011; Whittemore and Xia, 2017) and two triploids known in cultivation (Santamour and Bentz, 1995; Sherald et al., 1994). Understanding the complex genetics of american elm is important if breeding and selection work is to be carried out efficiently.
The cultivated triploid NPS 3-487 (released commercially as U. americana ‘Jefferson’) was studied by Sherald et al. (1994), who found that 17% of the fruit on the triploid contained viable seed. This figure is low compared with tetraploid U. americana they studied, in which 89% of the fruit contained viable seed, but it is an unusually high figure for a sexually reproducing triploid. This tree is particularly interesting from a horticultural standpoint because it is known to show very high levels of tolerance to dutch elm disease (Townsend et al., 2005). In the course of surveying wild U. americana, a natural pentaploid was found in western Nebraska (discussed subsequently), and this also showed substantial seed set.
Spontaneous triploids and other odd polyploids are known in many groups of plants, but they are normally sexually sterile or nearly so (Grant, 1981). However, some triploids reproduce via apomixis (Whitton et al., 2008) or by unusual chromosomal systems that allow permanent propagation of odd ploidies (Grant, 1981). In cases where triploids set seed sexually, they can serve as a genetic bridge, allowing gene exchange between diploids and tetraploids, both in natural populations and in artificial plant breeding. Transfer of alleles between diploids and tetraploids has played an important evolutionary role in some taxa (Kim et al., 2008). The effectiveness of triploids as a bridge between diploids and tetraploids depends on the fertility of the triploid and the chromosomal complement of the backcrosses (Burton and Husband, 2000; Ramsey and Schemske, 1998). The meager literature on the chromosomal complements of backcrosses between triploids and plants with even ploidy numbers is reviewed by Ramsey and Schemske (1998). Although meiosis in triploids produces a preponderance of aneuploid pollen with ≈1.5 sets of chromosomes, many triploids produce progeny that are euploid or close to euploid. The progeny of triploids fertilized with pollen from tetraploids were predominantly tetraploid [sometimes with one extra or one missing chromosome (i.e., 2n = 4x ± 1)] in the majority of cases, but this varied greatly among taxa, covering the whole range from 100% tetraploid (in Aquilegia chrysantha A. Gray × flabellata Siebold & Zucc.) to 75% aneuploid (in Triticum durum Desf. × Aegilops longissima Schweinf. & Muschl.) (Ramsey and Schemske, 1998).
The progeny of the triploid american elm NPS 3-487 that were described by Sherald et al. (1994) no longer exist, but the original parent tree is alive on the National Mall in Washington, DC, and still producing heavy crops of seed. To test whether these seeds are the result of sexual reproduction and to estimate the chromosomal complement of the seeds, nuclear DNA content was estimated by flow cytometry on a large sample of its seeds. Representative U. americana from surrounding plantings were also analyzed to estimate the ploidy level of the pollen available for fertilizing the triploid. A small sample of seeds was obtained from a wild pentaploid elm from Nebraska, and two tetraploid trees close to it were also analyzed.
Bey, C.F. 1990 Ulmus americana, p. 801–807. In: R.M. Burns and B.H. Honkala (eds.). Silvics of North America, vol. 2, hardwoods. U.S. Dept. Agr., For. Serv., Agr. Hdbk. 654
Burton, T.L. & Husband, B.C. 2000 Fitness differences among diploids, tetraploids, and their triploid progeny in Chamerion angustiflorum: Mechanisms of inviability and implications for polyploid evolution Evolution 54 1182 1191
Chesnay, C., Kumar, A. & Pearce, S.R. 2007 Genetic diversity of SIRE-1 retroelements in annual and perennial Glycine species revealed using SSAP Cell. Mol. Biol. Lett. 12 103 110
Grant, V. 1981 Plant speciation. 2nd ed. Columbia Univ. Press, New York, NY
Hofmeister, W. 1858 Neuere Beobachtungen über Embryobildung der Phanerogamen. Jahrbücher für wissenschaftliche Botanik 1:82–188
Karnosky, D.F., Redenbaugh, M.K. & Westfall, R. 1979 The use of anther culture and polyembryony in improving american elm, p. 91–96. In: R.P. Guries (ed.). Proc. First North Central Tree Improvement Conf., Madison, WI. North Central Tree Improvement Assn., Madison, WI
Kim, M., Cui, M., Cubas, P., Gillies, A., Lee, K., Chapman, M.A., Abbott, R.J. & Coen, E. 2008 Regulatory genes control a key morphological and ecological trait transferred between species Science 322 1116 1119
Korbecka, G., Klinkhamer, P.G.L. & Vrieling, K. 2002 Selective embryo abortion hypothesis revisited—a molecular approach Pl. Biol. (Stuttgart) 4 298 310
Leliveld, J.A. 1935 Cytological studies in the genus Ulmus. II. The embryo sac and seed development in the common dutch elm Recl. Trav. Bot. Neerl. 32 543 573
López-Almansa, J.C., Pannell, J.R. & Gil, L. 2003 Female sterility in Ulmus minor (Ulmaceae): A hypothesis invoking the cost of sex in a clonal plant Amer. J. Bot. 90 603 609
Nawaschin, S. 1898 Uber das Verhalten des Pollenschlauches bei der Ulme Bulletin de l’Académie Impériale des Sciences de Saint Pétersbourg Ser. 5 8 345 358
O’Connell, L.M. & Ritland, K. 2005 Post-pollination mechanisms promoting outcrossing in a self-fertile conifer, Thuja plicata (Cupressaceae) Can. J. Bot. 83 335 342
Pinchot, C.C., Flower, C.E., Knight, K.S., Marks, C., Minocha, R., Lesser, D., Woeste, K., Schaberg, P.G., Baldwin, B., Delatte, D.M., Fox, T.D., Hayes-Plazolles, N., Held, B., Lehtoma, K., Long, S., Mattix, S., Sipes, A. & Slavicek, J.M. 2017 Development of new dutch elm disease–tolerant selections for restoration of the american elm in urban and forested landscapes, p. 53–63. In: R.A. Sniezko, G. Man, V. Hipkins, K. Woeste, D. Gwaze, J.T. Kliejunas, and B.A. McTeague (technical coordinators). Gene conservation of tree species - Banking on the future. U.S. Dept. Agr., For. Serv., Pacific Northwest Res. Sta., Proc. Wkshp. Gen. Tech. Rep. PNW-GTR-963
Ramsey, J. & Schemske, D.W. 1998 Pathways, mechanisms, and rates of polyploidy formation in flowering plants Annu. Rev. Ecol. Syst. 29 467 501
Sherald, J.L., Santamour, F.S. Jr, Hajela, R.K., Hajela, N. & Sticklen, M.B. 1994 A dutch elm disease resistant triploid elm Can. J. For. Res. 24 647 653
Sorensen, F.C. 1982 The roles of polyembryony and embryo viability in the genetic system of conifers Evolution (Lancaster) 36 725 773
Townsend, A.M., Bentz, S.E. & Douglass, L.W. 2005 Evaluation of 19 american elm clones for tolerance to dutch elm disease J. Environ. Hort. 23 21 24
Winieski, J.A. 1960 Artificial hybridization and grafting methods with Ulmus americana, p. 48–51. In: E.J. Schreiner (ed.). Proc. Seventh Northeastern Forest Tree Improvement Conf., Burlington, VT, 18–19 Aug. 1959
Zheng, J.-Y., Li, Y.-Z., Zhou, C.-C., Lu, Y.-S. & Wang, X.-H. 2017 Study on embryology of Ulmus pumila L Bull. Bot. Res. Guangxi 37 651 657