Inheritance of Apomeiosis (Diplospory) in Fleabanes (Erigeron

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Inheritance of Apomeiosis (Diplospory) in Fleabanes (Erigeron Heredity (2005) 94, 193–198 & 2005 Nature Publishing Group All rights reserved 0018-067X/05 $30.00 www.nature.com/hdy Inheritance of apomeiosis (diplospory) in fleabanes (Erigeron, Asteraceae) RD Noyes Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, Colorado 80309, USA Unreduced egg formation (apomeiosis) in flowering plants is molecular markers (AFLPs) document the inheritance of the rare except when it is coupled with parthenogenesis to yield maternal genome through unreduced eggs resulting in gametophytic apomixis via apospory or diplospory. Results recombinant but predominantly (77%) tetraploid F1s from genetic mapping studies in diverse apomictic taxa (2n ¼ 4x ¼ 36; 2n þ n,BIII). Quantitative evaluation shows suggest that apomeiosis and parthenogenesis are geneti- continuous variation in the proportion of diplosporous (vs cally linked, a finding that is compatible with the conventional meiotic) ovules (41–89%) in tetraploid F1s despite the rationale that apomeiosis is unlikely to evolve independently presumed equal genetic contribution from the diplosporous because of deleterious fitness consequences. An Erigeron mother. These findings demonstrate the functional indepen- annuus (apomictic)  E. strigosus (sexual) genetic mapping dence of diplospory and suggest that variation in the trait in population, however, included a high proportion of plants that F1s is likely due to segregating paternal modifiers. In were highly apomeiotic (diplosporous) but nonapomictic; that addition, of six aneuploid (4xÀ1, 4xÀ2) F1s, three lack a is, they lacked autonomous seed production. To evaluate the subset of maternal AFLP markers. These plants likely arose function and inheritance of diplospory in Erigeron,a from aberrant megagametogenesis resulting in the loss of diplosporous triploid (2n ¼ 3x ¼ 27) seed parent was crossed maternal chromatin prior to fertilization. with a sexual diploid (2n ¼ 2x ¼ 18) E. strigosus pollen parent Heredity (2005) 94, 193–198. doi:10.1038/sj.hdy.6800597 to produce an F1 of 31 plants. Chromosome numbers and Publishedonline10November2004 Keywords: AFLPs; apomeiosis; apomixis; diplospory; Erigeron Introduction genetically linked (see reviews by Savidan, 2000; Grossniklaus et al, 2001). According to Mogie (1992), this In naturally occurring sexual plants, the formation of result is explained by a single gene model for apomixis in unreduced megagametophytes, or apomeiosis, is infre- which parthenogenesis occurs as a pleiotropic conse- quent except in ephemeral interspecific hybrids. None- quence of apomeiosis. This view is furthered by logical the-less, apomeiosis is considered to be a key step in arguments that apomeiosis and parthenogenesis are polyploid evolution (reviewed in Ramsey and Schemske, unlikely to evolve independently because each trait, 1998). In contrast, apomeiosis achieves high and regular separately, would be deleterious (Asker and Jerling, expression in species that reproduce via gametophytic 1992). This model is controversial, however, because apomixis (Nogler, 1984a; Asker and Jerling, 1992). In apomixis often maps to regions with low recombination. apomicts, the unreduced megagametophyte is formed Therefore, it is possible that these apomixis regions apomeiotically via either apospory (the gametophyte harbor many major or modifying genes affecting distinct arises from a cell of the ovule other than the megaspore aspects of the trait. mother cell (MMC)) or diplospory (the gametophyte Curiously, fertilization of unreduced ovules has often arises directly from the MMC). However, maternal been recorded as a source of 2n þ n (or BIII) ‘off types’ ploidal level is maintained across generations because in progeny tests of apomictic plants (Asker and Jerling, the unreduced egg borne by the megagametophyte 1992). This phenomenon demonstrates that unreduced develops parthenogenetically into an embryo, and eggs produced by apomicts can function normally in progeny are thus genetically identical to the mother crosses. However, our knowledge of the function plant (barring chiasmata prior to restitution). In apo- and inheritance of apomeiotic ovules is limited because micts, the nutritive endosperm may also form autono- few apomeiotic-only plants have been observed in mously, or fertilization of the polar nuclei by a sperm cell nature. For instance, only two known examples of may be required (pseudogamy). naturally occurring apomeiotic plants (in Parthenium Genetic mapping studies in diverse taxa suggest that and Potentilla) are cited in Asker and Jerling (1992; p 82). apomeiosis and parthenogenetic embryo formation are In contrast, apomeiotic plants occur in relatively high frequency in some recently reported crossing experi- ments. In these studies, F1 populations resulting from Correspondence: RD Noyes, Department of Ecology and Evolutionary sexual  apomict crosses include plants that produce Biology, University of Colorado, Boulder, Colorado 80309, USA. E-mail: [email protected] unreduced ovules in the absence of other components of Received 29 February 2004; accepted 31 August 2004; published apomixis. In aposporous Poa pratensis (Poaceae), for online 10 November 2004 example, apomeiotic individuals (identified cytologi- Inheritance of apomeiosis in Erigeron RD Noyes 194 cally) constituted 5% of F1s (Albertini et al, 2001). In of a mapping population resulting from a cross between diplosporous Taraxacum officinale (Asteraceae), six of 19 triploid apomictic E. annuus and sexual diploid F1s (32%) were identified as apomeiotic, producing at E. strigosus (Noyes, 2000). This plant was selected least some 2n þ n and no 2n þ 0 offspring progeny when because it produced 92% unreduced ovules (Figure 2). test-crossed (van Dijk et al, 1999). In Erigeron (Aster- Of its remaining ovules, 3% were apparently meiotic, aceae), diplosporous plants constituted 23% (30/130) of yielding four approximately equal sized, but likely an F1 mapping population generated by crossing chromosomally unbalanced, nuclei from divisions of apomictic E. annuus with sexual E. strigosus. In most of the MMC. The remaining 5% of ovules were aberrant, the diplosporous plants, both reduced and unreduced exhibiting during early megagametogenesis either (1) ovules coexisted in the same plant (the proportion of two relatively large nuclei, as in diplosporous ovules, unreduced ovules ranging from 8 to 100%), suggesting that penetrance of apomeiosis may be influenced by modifiers or genetic balance (Noyes, 2000). Together, abc these three studies support the hypothesis that apomeio- sis may be distinct from other aspects of apomictic development (see review by Grossniklaus et al, 2001). This view is supported by genetic mapping in Erigeron that shows that diplospory and autonomous seed formation map to separate linkage groups (Noyes n and Rieseberg, 2000), and developmental analysis for Tripsacum dactyloides that indicate no functional relation- ship between diplospory and parthenogenesis (Grima- nelli et al, 2003). In this work, the function of apomeiotic (diplosporous) n mn ovules and the inheritance of the trait in Erigeron are considered. A highly diplosporous seed parent was crossed with a sexual diploid to test the function of unreduced ovules. The contributions of paternal and maternal genomes in F1s were evaluated using molecular markers, nc n and the inheritance of diplosporous ovule production was assessed by comparing levels of diplospory, measured quantitatively, in the maternal plant and F1s. Materials and methods A triploid (2n ¼ 27; Figure 1) diplosporous plant lacking seed production (H131) was selected that was a member de ab fn fn en en cd Figure 2 Micrographs of cleared Erigeron megagametophytes. (a) Young sexual (tetrasporic) gametophyte showing four nuclei resulting from meiosis of MMC. (b) Young apomeiotic (diplospor- ous) gametophyte showing two nuclei resulting from mitotic (or mitotic-like) division of MMC. (c) Aberrant gametophyte showing two large nuclei (as in apomeiotic gametophytes) plus two micronuclei. (d) Mature reduced megagametophyte. (e) Mature Figure 1 Micrographs of chromosomes. (a) Sexual diploid pollen unreduced megagametophyte. Micropyle is at the base of each parent (2n ¼ 18). (b) Apomeiotic triploid seed parent (2n ¼ 27). (c) micrograph. en ¼ egg nucleus, mn ¼ micronucleus, n ¼ nucleus, Tetraploid F1 (2n ¼ 36). (d) Aneuploid F1 (2n ¼ 35). Scale bar ¼ 5 mm. nc ¼ nucellus, fn ¼ fusion nucleus. Bar ¼ 10 mm. Heredity Inheritance of apomeiosis in Erigeron RD Noyes 195 plus one or more very small nuclei (micronuclei; cia, CA, USA) and quantified using a Hoefer DyNA Figure 2), or (2) three approximately equal sized nuclei Quant 200 Fluorometer (Amersham Pharmacia Biotech, of uncertain origin but likely resulting from a combina- San Francisco, CA, USA). To evaluate inheritance tion of restitution and reduction following meiosis I. In patterns, Amplified Fragment Length Polymorphisms both aberrant types, nonmaternal (but abnormally (AFLPs) (Vos et al, 1995) were evaluated. Polymorphisms reduced) eggs would likely result. Mature unreduced from six selective primer combinations (Eacc  Maac, megagametophytes of H131 include a normal egg Eacc  Macc, Eacc  Macg, Eacc  Magc, Eacg  Macg, apparatus consisting of two synergids and egg cell, and Eacg  Magc) were generated using standard methods a central cell containing a single large nucleus inferred to (Noyes and Rieseberg, 2000), and PCR products were be derived from the fusion of two polar nuclei (the fusion resolved on an
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