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Monogenic Inheritance of Apomixis in Two Hieracium Species with Distinct Developmental Mechanisms

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Monogenic Inheritance of Apomixis in Two Hieracium Species with Distinct Developmental Mechanisms Heredity 84 (2000) 228±237 Received 25 June 1999, accepted 22 October 1999 Monogenic inheritance of apomixis in two Hieracium species with distinct developmental mechanisms R. A. BICKNELL* , N. K. BORST & A. M. KOLTUNOWà Crop and Food Research, Private Bag 4704, Christchurch, New Zealand and àC.S.I.R.O. Division of Plant Industry, PO Box 350, Glen Osmond, South Australia 5064, Australia Apomixis, the asexual formation of seed, has been known in angiosperms for more than a century yet the genetic mechanisms that control this trait remain poorly understood. Most members of the genus Hieracium are apomicts, forming predominantly asexual seed. Some purely sexual forms, however, also exist. In this paper we present a study of the inheritance of apomixis using two apomictic species of Hieracium which utilize very dierent forms of megagametogenesis. In both cases the progeny inherited apomixis as a monogenic, dominant trait that could be transferred by both haploid and diploid male gametes. In common with observations from other systems, no diploid apomictic progeny were recovered from these crosses. This appears to have been caused by selection against the survival of diploid zygotes, rather than against the mediation of haploid gametes as has been noted in other systems. Crosses between the two apomicts showed that the dominant determinants in the two forms examined were closely linked, possibly allelic. The signi®cance of these data is discussed with respect to current theories on the associative link between gametophytic apomixis and polyploidy. Keywords: apomixis, apospory, Hieracium, inheritance. Introduction 1992) as ®rst described by Rosenberg (1906). Cytologi- cal comparisons were conducted between vegetatively Plants that reproduce by gametophytic apomixis form propagated isolates of three closely related species, an embryo directly from an egg cell in an unreduced the apomicts H. aurantiacum and H. piloselloides and a embryo sac. In contrast to sexual reproduction, the sexual accession of H. pilosella. Although development processes of meiosis and fertilization are avoided, in the sexual accession was found to be typical of the leading to the formation of genetically uniform progeny Polygonum-type, between the apomictic lines studied (Nogler, 1984a; Koltunow, 1993). Apomixis is therefore signi®cant dierences were recorded in the number and typically de®ned by function as asexual reproduction precocity of aposporous initials formed, and in the through seed (syn. agamospermy) (Nogler, 1984a). The number, morphology, developmental cytology and fates developmental mechanisms employed by dierent apo- of the resultant unreduced embryo sacs. It is apparent mictic species, however, are remarkably varied (Nogler, from these and other unreported data, that many of the 1984a; Koltunow et al., 1995), possibly re¯ecting the developmental details of apospory are quite variable in apparent polyphyletic origin of this trait among ¯ower- Hieracium, and that this variability is expressed between ing plants (see Carman, 1997). Known mechanisms of apospecies, between accessions of an apospecies and apomixis have been categorized in dierent ways. even between ¯orets on an individual capitulum. Typically genera are grouped by similarities to a type- As a complement to this work, the inheritance of mechanism (Asker & Jerling, 1992). From our own apomixis was studied using these three accessions. observations in Hieracium subgenus Pilosella it is Apomixis has been described as a heritable trait in apparent that this form of characterization can be several species (Asker & Jerling, 1992). Dominant misleading (Koltunow et al., 1998). The members of this inheritance for apospory has been described in the grass taxon are reported to form asexual seed by apospory of genera Panicum (Savidan, 1981), Brachiaria (Borges do the Hieracium-type (Nogler, 1984a; Asker & Jerling, Valle et al., 1994) and Pennisetum (Dujardin & Hanna, 1985). The results of Christo (1942) indicate that *Correspondence. E-mail: [email protected] dominant inheritance may also apply in Hieracium 228 Ó 2000 The Genetical Society of Great Britain. APOMIXIS IN HIERACIUM 229 aurantiacum (reviewed by Nogler, 1994). Similarly, P4 and P2 appear to be self-incompatible under cool Gadella (1991) noted that apospory may be inherited winter conditions. Pollinations were conducted without as a dominant factor in H. pilosella. Nogler (1984b) prior emasculation. conducted a detailed study of the inheritance of To ensure the genetic integrity of stocks used, the apospory in Ranunculus auricomus, also concluding that plants were maintained vegetatively, either by divi- the trait was conferred by the inheritance of a single sion of mature plants or through micropropagation dominant determinant. That determinant, however, (Bicknell, 1994). The inheritance studies were conducted could only be transferred in a heterozygotic state in a in a glasshouse at Lincoln, New Zealand, maintained diploid or polyploid gamete. Nogler noted that this with a minimum night temperature of 12°C, minimum mechanism favoured the involvement of a polyploid day temperature of 18°C and maximum day tempera- parent and ensured the formation of a polyploid, ture of 25°C. Flowering was promoted by day-length apomictic zygote. extension lighting, using high pressure sodium vapour There is a very close association between gametophy- lamps with a photoperiod of 16 h (Yeung, 1989). tic apomixis and polyploidy (reviewed in Asker & Jerling, 1992). In common with most other taxa Breeding scheme for the inheritance of apomixis containing gametophytic apomicts, all naturally occur- ring apomictic forms of Hieracium have been recorded The breeding scheme used is detailed in Fig. 1. Inherit- as polyploid (Skalinska, 1970; Gadella, 1991) yet several ance studies with apomictic species are subject to some diploid sexual species are known. The recent recovery of unique constraints. As the trait results in the formation a diploid, apomictic plant of H. aurantiacum (Bicknell & of predominantly maternal seed, apomixis restricts Borst, 1997) indicates, however, that polyploidy is not access to the female gamete, the egg cell. Furthermore, an obligate requirement for the expression of apomixis when a rare hybridization event does occur in these in this taxon. plants either a reduced or an unreduced egg may be The aims of the current study were to determine the used, resulting in the formation of dierent progeny patterns of inheritance in our experimental accessions classes and frustrating the analysis of segregation. To of H. aurantiacum and H. piloselloides, to test for any avoid these diculties crosses were designed using an prejudice against the mediation of haploid gametes in apomict as the staminate parent and a sexual plant as the transmission of dominant alleles conferring apomixis, the recipient. to test for allelism between the two apomicts tested and Initially it was hoped that by using a triploid apomict to karyotype the chromosomes of H. pilosella. as the staminate parent in a cross with a diploid, sexual recipient, the inheritance of apomixis could be studied at the diploid level. Following a cross between the Materials and methods apomictic triploid D3 and the sexual diploid P2, how- ever, most of the progeny were found to be either Plant materials triploid or aneuploid (Table 1, cross 1). The expected Two apomictic biotypes of Hieracium were used, a diploid class was only represented by three weak triploid accession (2n 27, x 9) of H. piloselloides individuals. The triploid progeny of this cross were (designated `D3') and an aneuploid accession (2n therefore chosen for further analysis. Representative 3x + 4 31) of H. aurantiacum (designated `A3.4'). sexual and apomictic hybrid triploid progeny were Preliminary studies using test-crosses and pollen via- backcrossed to the sexual recurrent parent and the BC1 bility stains revealed that both had a high degree of progeny analysed for ploidy and reproductive mode. pollen fertility and that both frequently produced Again, as triploids were the most common progeny class haploid pollen. They were also selected for their in the BC1 populations, they were analysed for the distinctive morphologies. The bright orange ¯owers of inheritance of apomixis. H. aurantiacum and the upright form and strap-shaped Both the apomictic triploid D3 and aneuploid A3.4 leaves of H. piloselloides provided useful marker were then crossed to the sexual tetraploid P4 and the characteristics for con®rming hybridity in the progeny. progeny analysed for ploidy (Table 1, crosses 4 and 7). A3.4 was originally obtained from an adventive pop- Triploids were recovered from both crosses in sucient ulation in Central Otago, South Island, New Zealand, numbers to permit an assessment of the inheritance of and D3 was obtained from a wild population in apomixis. Backcrosses were conducted for both the Steiermark, Austria. Two sexual biotypes were used; a sexual and apomictic triploid progeny classes of the F1, tetraploid accession of H. pilosella from Caen, France using the sexual accession P4 as the recurrent, maternal (designated `P4') and an anther culture-derived diploid parent. The triploid BC1 progeny were analysed for (Bicknell & Borst, 1996) of P4 (designated `P2'). Both the inheritance of apomixis. Linkage between the Ó The Genetical Society of Great Britain, Heredity, 84, 228±237. 230 R. A. BICKNELL ET AL. of the marker in the resistant seedlings was con®rmed by Southern analysis (data not shown). The
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