Disomic Inheritance, Suppressed Recombination, and Allelic Interactions Govern Apospory in Buffelgrass as Revealed by Genome Mapping

lecular markers within mapping populations (Wendel and Parks, 1984; Torres et al., 1985; McCouch et al., Molecular tools have not identified the gene(s) governing apomixis 1988; Paterson et al., 1988, 1991; Saito et al., 1991; Lytnor have they been used to successfully transfer the trait to important, sexually reproducing food crops. Several molecular studies addressing tle, 1991; Schon et al., 1991; Zivy et al., 1992; Causse et apomixis in grasses have used interspecific and intergeneric hybrids. al., 1994; Chittenden et al., 1994). This loss of specific The failure to recover specific F1 genotypes from these wide crosses genotypes from the progeny may be due to interactions can be caused by unfavorable interactions between the gametes, zybetween genes of the two species within gametes, zygote, embryo, endosperm, and/ or maternal tissue. These interactions gote, embryo, endosperm, or maternal tissue (Hadley can eliminate recombinant genotypes with valuable information toand Openshaw, 1980). Differential viability of offspring wards linkage analyses of the trait. Buffelgrass [Pennisetum ciliare because of allelic interactions has been reported in (L.) Link syn. Cenchrus ciliaris L.], a polymorphic species with intermaize (Zea mays L.)-Tripsacum hybrids (Maguire, fertile apomictic and sexual genotypes, offers an opportunity to genetically map apomixis by means of intraspecific hybrids with euploid 1963), tomato, Lycopersicon esculentum Mill. (Rick, genomes. This study reports a linkage map of the apospory region in 1966), wheat, Triticum aestivum L. (Manabe et al., 1999), buffelgrass. Apospory, classified by progeny testing and cytologically and rice, Oryza sativa L. (Sano, 1990; Cheng et al., 1996; observing megagametophytes, mapped to a single locus in the apomictic Xu et al., 1997; Liu et al., 2001). Because detectable parent’s genome. Two buffelgrass cDNAs (pPAP3A07 and pPAP8C08) recombination in a mapping population is directly reand three previously reported apospory markers (UGT197, QH8, and lated to offspring survival, reports of segregation distorOPC4) were tightly linked (1.4 centimorgans, cM) to the trait. As a tion in pearl millet, Pennisetum glaucum (L.) R. Br. (Liu tetraploid species (2n 4x 36), four copies of each chromosome et al., 1994) and maize (Helentjaris et al., 1986; Gardiner are expected in buffelgrass. A single homolog and two homeologs were identified for the chromosome carrying apospory, indicating the et al., 1993) may negatively affect genetic mapping studformation of two bivalents during meiosis and the disomic inheritance ies of apomixis in these species. of apospory in buffelgrass. Allelic bridges between the parents reMolecular markers have been associated with apovealed suppressed recombination in the apospory linkage group. Segmictic phenotypes in several grass species. One restricregation distortion between a marker on the sexual parent’s homolog tion fragment length polymorphism (RFLP) (UGT197) to the apospory linkage group and a marker on a separate maternal and one random amplified polymorphic DNA (RAPD) linkage group suggested specific allelic combinations in female ga(OPC4) were syntenic with apospory in interspecific metes affect offspring survival in buffelgrass. Pennisetum hybrids (Ozias-Akins et al., 1993). An alien addition line (2n 1 29) derived from a cross between A asexual plant reproduction through seeds, tetraploid pearl millet (2n 4x 28) and P. squamularesults from the parthenogenetic development of tum Fresen. (2n 6x 54) possessed one P. squamulaan unreduced egg cell into a viable embryo (Bashaw tum chromosome, suggesting that a single chromosome and Hanna, 1990). Because apomixis permits the clonal could confer apospory. However, the lack of a homolog propagation of hybrid genotypes, its transfer to cultifor this chromosome to pair with during meiosis prevated crops is of major interest to plant breeding procluded recombination and made this system unsuitable grams. Two types of apomixis, apospory and diplospory, for genetic mapping. occur in grasses. Unreduced embryo sacs arise from Analyses of isozyme, protein, and RAPD markers somatic nucellar cells in apospory and unreduced archedid not identify associations with apospory in buffelgrass sporial cells in diplospory (Asker and Jerling, 1992). (Gustine et al., 1996). This can likely be attributed to The complete body of apomixis literature is abound the small population size and types of markers used. In with conflicting reports. This paper focuses on the mocontrast, a bulked-segregant analysis using RAPDs in lecular analyses of apomixis in grasses, while deferring two different half-sib buffelgrass populations revealed the general subject of apomixis to a recent and extensive two markers (M02-680 and J16-800) tightly linked to review (Savidan, 2000). apospory (Gustine et al., 1997). The two apomictic male Wide hybridizations, which have been used extenparents used to develop the populations gave slightly sively to obtain high polymorphism rates in linkage studdifferent results. M02-680 and J16-800 flanked apospory ies, have often resulted in segregation distortion of moin both populations, but at greater distances in the second population. Interestingly, UGT197 cosegregated with J16-800 in the first population and with apospory R.W. Jessup, Y.-W. Wang, C. Chang, Z. Li, and M.A. Hussey, Dep. of Soil & Crop Sciences, Texas A&M Univ., College Station, TX in the second population. Assuming the reproductive 77843; B.L. Burson, USDA-ARS, College Station, TX 77843; G.B. Burow and A.H. Paterson, Center for Applied Genetic Technologies, Abbreviations: AFLP, amplified fragment length polymorphism; BAC, Dep. Crop and Soil Sciences, Botany, and Genetics, Univ. of Georbacterial artificial chromosome; cM, centimorgan; PCR, polymerase gia, Athens, GA 30602. Received 7 July 2001. *Corresponding author chain reaction; RAPD, random amplified polymorphic DNA; RFLP, ([email protected]). restriction fragment length polymorphism; SCAR, sequence characterized amplified region; SDRF, single dose restriction fragment. Published in Crop Sci. 42:1688–1694 (2002).