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Hdy2009112.Pdf Heredity (2010) 104, 185–190 & 2010 Macmillan Publishers Limited All rights reserved 0018-067X/10 $32.00 www.nature.com/hdy ORIGINAL ARTICLE Molecular evidence for the natural production of homozygous Cupressus sempervirens L. lines by Cupressus dupreziana seed trees JLR Nava1, A Buonamici2, GG Vendramin2 and C Pichot1 1INRA, Unite´ d’Ecologie des Foreˆts Me´diterrane´ennes (UR629), Domaine St Paul, Site Agroparc, Avignon, France and 2Istituto di Genetica Vegetale, Consiglio Nazionale delle Ricerche, Sesto Fiorentino (Firenze), Italy Paternal apomixis was recently reported in the endangered C. sempervirens controlled crosses. A high level of polymorph- Mediterranean cypress, Cupressus dupreziana. This species ism was observed among the diploid all-paternal trees. All but acts as a surrogate mother for the development of all-paternal three individuals exhibited single-band profiles as expected for embryos from pollen grains. C. dupreziana production homozygotes, which may originate from natural diploidization of Cupressus sempervirens haploid or diploid seedlings from of a C. sempervirens haploid embryo or from the fusion of C. sempervirens pollen was also demonstrated. The haploid two male gametes produced by the same C. sempervirens progeny was derived from the embryogenic development of microgametophyte. The three heterozygous seedlings must be haploid gametes, but the origin of the diploid progeny remained derived from the fusion of male gametes produced by two unknown. To determine the ontogenic origin of the diploid different C. sempervirens microgametophytes. These findings C. sempervirens progeny, we analyzed the heterozygozity of offer a unique opportunity in conifers to produce homozygous 63 diploid all-paternal C. sempervirens seedlings using highly lines, highly valuable for genetic analyses or breeding. variable co-dominant nuclear microsatellite markers. The Heredity (2010) 104, 185–190; doi:10.1038/hdy.2009.112; bi-parental inheritance of the markers was checked in published online 26 August 2009 Keywords: androgenesis; dihaploid; surrogate mother; SSR; conifer Introduction species always exhibits a low seed viability rate, which can be related to the abnormalities of its sexual Sexual reproduction is the general rule in higher plants reproductive process. The aberrant meiosis that occurs and animals (Bell, 1982; Barton and Charlesworth, 1998; in both micro and macrospores leads to the development West et al., 1999). However, some species exhibit an of diploid pollen grains (Pichot and El Maaˆtaoui, 2000) apomictic or parthenogenetic reproduction in which the and diploid-based megagametophytes (Pichot et al., offspring derives from only one parent, the mother 1998). The embryogenic ability of C. dupreziana pollen (Foroughi-Wehr and Wenzel, 1993). According to was first demonstrated in inter-specific pollination McKone and Halpern (2003), very rare cases of andro- experiments. All progeny produced by controlled polli- genesis have been observed in animals. So far, Cupressus nation of the Mediterranean cypress (Cupressus sempervi- dupreziana A. Camus (Cupressaceae) is the only plant rens) using C. dupreziana pollen were pure C. dupreziana species where ‘paternal apomixis’ has been reported seedlings (Pichot et al., 2001). Reciprocally, the ability of (Pichot et al., 2001). C. dupreziana to act as a surrogate mother for the Cupressus dupreziana (or Tassili cypress) is a highly development of all-paternal C. sempervirens progeny endangered woody species. It is represented by only one was more recently demonstrated (Pichot et al., 2008). natural population in the Tassili N’Ajjer desert, Algeria, Indeed two-thirds of the seedlings produced by open and the number of surviving individuals is limited to 233 pollinated C. dupreziana trees planted in a South Eastern (Abdoun and Beddiaf, 2002). This species can easily be France collection were pure C. sempervirens individuals. distinguished from C. sempervirens L. (common cypress Most of these seedlings were haploid, which was or Mediterranean cypress) on the basis of a multi-locus consistent with the fact that they would derive from profile obtained using AFLP (Pichot et al., 2008) and haploid C. sempervirens pollen grains without fecunda- nuclear microsatellites (transferred from Sebastiani et al., tion. On the other hand, the remaining seedlings were 2005). The precarious state of the species results from a diploid and their ontogenic origin remained unknown combination of extreme climatic conditions, long-term (Pichot et al., 2008). human pressure and extremely scarce regeneration. The In this paper we infer the genetic origin of the diploid all-paternal C. sempervirens seedlings using codominant microsatellite markers (single sequence repeat (SSR)) for Correspondence: Dr C Pichot, INRA URFM, Domaine St Paul, Site which we verified the nuclear inheritance. In addition to Agroparc, 84914 Avignon Cedex 9, France. E-mail: [email protected] the progeny included in the study by Pichot et al. (2008), Received 5 March 2009; revised 15 June 2009; accepted 13 July 2009; new progeny originating from either open or controlled published online 26 August 2009 pollinations were analyzed. The observed genetic Homozygous cypresses from in planta androgenesis JLR Nava et al 186 profiles allowed inference of the ontogenic origin of planted in a progeny trial near Avignon, South Eastern seedlings. France. Materials and methods Genotyping protocol Genotyping was carried out in two different laboratories, Plant material at CNR-Firenze (Italy) (first set of samples) and at INRA- To determine their genetic origin, 63 diploid all-paternal Avignon (France) (second set of samples). The first set of C. sempervirens-like seedlings derived from C. dupreziana samples included all the seedlings used for the marker seeds were analyzed (Table 1). Most progeny (57) came inheritance analysis and 31 of the 63 diploid all-paternal from open-pollinated C. dupreziana seed trees planted in individual seedlings were derived from C. dupreziana five ex situ collections (South Eastern France) as seed trees. The remaining 32 diploid all-paternal individ- described by Pichot et al. (2008). In three of these five ual seedlings were included in the second set of samples. cypress collections (Avignon, Carpentras and Montpel- DNA was extracted from leaf samples using the DNeasy lier), C. dupreziana seed trees were very close to plant kit (Qiagen, Venlo, The Netherlands). numerous C. sempervirens pollen trees (more than 30). For the first set of samples, PCRs were carried out in In Ruscas collection, the only one C. dupreziana seed tree 25 ml containing 10 ng of DNA, 1 Â PCR reaction buffer was surrounded by more than 50 C. sempervirens and 50 (Promega, Madison, WI, USA), 200 mM of each dNTP, 1-U Cupressus arizonica pollen trees. The last site (Esterel Taq polymerase (GoTaq, Promega), 1.5 mM MgCl2, and collection) was a pure C. dupreziana collection at a 0.2 mM of each primer. The forward primers were labeled distance of about 2 km from the closest C. sempervirens with FAM, HEX or TAMRA. The PCR thermal profile and C. arizonica trees. (except for Cyp258, see Sebastiani et al. (2005)) was as Six progeny produced by controlled pollinations of one follows: denaturation at 94 1C for 5 min followed by C. dupreziana seed tree with pollen collected from three 30 cycles of 94 1C for 30 s, 50 1C for 30 s, 72 1C for 30 s and C. sempervirens trees were also analyzed. Seedling ploidy a final extension of 72 1C for 8 min. PCRs were carried level was assessed by flow-cytometry upon following the out using a Perkin–Elmer GeneAmp 9700 thermal cycler protocol described by Pichot and El Maaˆtaoui (2000). (Applied Biosystems, Foster City, CA, USA). The PCR products were separated by capillary electrophoresis, Molecular marker selection and inheritance with a 400 bp size standard, using MEGABACE 1000 (GE Seedlings were genotyped using seven nuclear micro- Healthcare, Chalfont, St Giles, UK) automatic sequencer. satellites (SSRs) developed for C. sempervirens: Cyp52, Alleles were sized using FRAGMENT PROFILER version Cyp84, Cyp101, Cyp174, Cyp257, Cyp258 and Cyp293 1.2 (GE Healthcare). (Sebastiani et al., 2005). These markers were highly For the second set of samples, three multiplex PCRs polymorphic in C. sempervirens populations (Valgimigli, (Qiagen), Cyp52 (700 nm) þ Cyp84 (800 nm), Cyp101 2005), providing high resolution for paternity analysis (700 nm) þ Cyp174 (800 nm), Cyp257 and Cyp258 and heterozygote detection, but their putative nuclear (700 nm) þ Cyp293 (800 nm), were carried out in 10 ml inheritance had never been verified. As known marker containing 0.2 mg of DNA, 5 ml of PCR Master Mix, 1 mlof inheritance is a prerequisite for studying the genetic Primer Mix (0.2 mM each primer), 1 ml of Q-Solution and origin of progeny, Mendelian segregation of the SSR 1 ml of RNase-free water. Microsatellite loci were markers was tested by analyzing the genotypes of 77 analyzed on a LI-COR (4200 IR2) automatic sequencer. C. sempervirens seedlings from five full-sib families, The size of alleles was determined automatically and including two reciprocal crosses, and the six parents of (or) manually with the SAGA (LI-COR IR2) computer the crosses (see Supplementary information Table 2). software. This material was selected from a C. sempervirens 9 Â 9 To check for consistency in allele size estimation diallele mating design (unpublished data). Leaf samples across the two laboratories, a common set of PCR were collected from 5-year old individual C.
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