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The Evolution Pattern of Rdna ITS in Avena and Phylogenetic Relationship of the Avena Species (Poaceae: Aveneae) YUAN-YING PENG1, 2 , BERNARD R

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The Evolution Pattern of Rdna ITS in Avena and Phylogenetic Relationship of the Avena Species (Poaceae: Aveneae) YUAN-YING PENG1, 2 , BERNARD R Hereditas 147: 183–204 (2010) The evolution pattern of rDNA ITS in Avena and phylogenetic relationship of the Avena species (Poaceae: Aveneae) YUAN-YING PENG 1, 2 , BERNARD R. BAUM2 , CHANG-ZHONG REN 3 , QIAN-TAO JIANG 1 , GUO-YUE CHEN 1 , YOU-LIANG ZHENG4 and YU-MING WEI1 1Triticeae Research Institute, Sichuan Agricultural University, Ya ’ an, Sichuan, PR China 2Agriculture and Agri-Food Canada, Eastern Cereal and Oilseed Research Centre, Ottawa, Ontario, Canada 3Baicheng Academy of Agricultural Sciences, Baicheng, Jilin, PR China 4Key Laboratory of Southwestern Crop Germplasm Utilization, Ministry of Agriculture, Sichuan Agricultural University, Yaan, Sichuan, PR China Peng, Y.-Y., Baum, B. R., Ren, C.-Z., Jiang, Q.-T., Chen, G.-Y., Zheng, Y.-L. and Wei, Y.-M. 2010. The evolution pattern of rDNA ITS in Avena and phylogenetic relationship of the Avena species (Poaceae: Aveneae). – Hereditas 147 : 183–204. Lund, Sweden. eISSN 1601-5223. Received 18 January 2010. Accepted 8 June 2010. Ribosomal ITS sequences are commonly used for phylogenetic reconstruction because they are included in rDNA repeats, and these repeats often undergo rapid concerted evolution within and between arrays. Therefore, the rDNA ITS copies appear to be virtually identical and can sometimes be treated as a single gene. In this paper we examined ITS polymorphism within and among 13 diploid (A and C genomes), seven tetraploid (AB, AC and CC genomes) and four hexaploid (ACD genome) to infer the extent and direction of concerted evolution, and to reveal the phylogenetic and genome relationship among species of Avena . A total of 170 clones of the ITS1-5.8S-ITS2 fragment were sequenced to carry out haplotype and phylogenetic analysis. In addition, 111 Avena ITS sequences retrieved from GenBank were combined with 170 clones to construct a phylogeny and a netwok. We demonstrate the major diver- gence between the A and C genomes whereas the distinction among the A and B/D genomes was generally not possible. High affi n- ity among the Ad genome species A. damascena and the ACD genome species A. fatua was found, whereas the rest of the ACD genome hexaploids and the AACC tetraploids were highly affi liated with the Al genome diploid A. longiglumis . One of the AACC species A. murphyi showed the closest relationship with most of the hexaploid species. Both Cv and Cp genome species have been proposed as paternal donors of the C-genome carrying polyploids. Incomplete concerted evolution is responsible for the observed differences among different clones of a single Avena individual. The elimination of C-genome rRNA sequences and the resulting evolutionary inference of hexaploid species are discussed. Y. M. Wei, Triticeae Research Institute, Sichuan Agricultural University, Ya ’ an 625014, Sichuan, PR China . E-mail: ymwei@sicau. edu.cn The genus Avena L. (Poaceae: Aveneae)) with approxi- evidence available, much is still unknown about the evolu- mately 30 species forming a distinct polyploid series rang- tion of the genus. Despite numerous observations made by ing from diploid through tetraploid to hexaploid with a morphological and cytological studies ( RAJHATHY et al. basic chromosome number of seven ( RAJHATHY and 1966; RAJHATHY and THOMAS 1974; BAUM 1977; LINARES T HOMAS 1974; BAUM 1977; THOMAS 1992; LEGGETT and et al. 1992; THOMAS 1992; LEGGETT and THOMAS 1995), the T HOMAS 1995; KATSIOTIS et al. 2000). All Avena species, application of different molecular techniques has provided with the exception of A. macrostachya , are self-pollinated further information on Avena genome relationships, such annuals, whereas A. macrostachya is a cross-pollinating, as in situ hybridization ( CHEN and ARMSTRONG 1994; quadrivalent-forming, autotetraploid perennial ( MALZEW J ELLEN et al. 1994a; KATSIOTIS et al. 1996; LINARES et al. 1930; BAUM 1968, 1974; BAUM and RAJHATHY 1976; 1998; IRIGOYEN et al. 2001), the use of molecular markers R ODIONOVA et al. 1994; KATSIOTIS et al. 1997). Genome ( SANCHEZ DE LA HOZ and FOMINAYA 1989; ALICCHIO et al. differentiation was initially based on cytological studies 1995; O ’ DONOUGHUE et al. 1995; RONALD et al. 1997; of interspecifi c hybrids and descriptions of species karyo- K IANIAN et al. 1999; NOCELLI et al. 1999; LI et al. 2000a, types ( RAJHATHY and THOMAS 1974; THOMAS 1992; 2000b, 2009; LOSKUTOV and PERCHUK 2000; DROSSOU et al. RODIONOVA et al. 1994; LEGGETT and MARKHAND 1995). 2004; FU and WILLIAMS 2008) and the comparison of Diploid species have either the A or C genome, tetraploids nucleotide sequences ( CHENG et al. 2003; RODIONOV et al. have either the AB or AC genome and the hexaploids have 2005; IRIGOYEN et al. 2006; NIKOLOUDAKIS and KATSIOTIS the ACD genome designation. 2008; NIKOLOUDAKIS et al. 2008; PENG et al. 2008). At the Although there is considerable morphological, bio- diploid level, hybridization among the A and C genome chemical, geographical, cytotaxonomic and molecular species rarely produces interspecifi c hybrids, indicating © 2010 The Authors. This is an Open Access article. DOI: 10.1111/j.1601-5223.2010.02172.x 184 Y.-Y. Peng et al. Hereditas 147 (2010) major genomic differences among these species ( FOMINAYA was thought, ITS polymorphism within individuals is et al. 1988a; LINARES et al. 1992; JELLEN et al. 1993; DROS- quite common ( BALDWIN et al. 1995; WENDEL et al. 1995; SOU et al. 2004). Although some studies have dealt with M UIR and SCHL Ö TTERER 1999, DENDUANGBORIPANT and phylogenetic relationships among species of different C RONK 2000; MAYO L and ROSSELL Ó 2001; ROSSELL Ó et al. ploidy ( FOMINAYA et al. 1988b; FABIJANSKI et al. 1990; 2006, 2007; NIETO FELINER and ROSSELL Ó 2007; ZHANG G UPTA et al. 1992; ALICCHIO et al. 1995; DROSSOU et al. and GE 2007; KIM et al. 2008; G Ö ER and GRIMM 2008; 2004; IRIGOYEN et al. 2006; NIKOLOUDAKIS et al. 2008), the G RIMM and DENK 2008; PILOTTI et al. 2009). In that case, putative diploid donors of Avena polyploids remain uncer- if only one sequenced clone is selected as representative tain, especially for the B genome origin in the AB tetra- of the ITS sequence of one individual, some polymor- ploids and the D genome donor of the ACD hexaploids. phism will not be able to be revealed. Therefore the use of There is now good evidence of the close relationships the ITS as a universal marker should be evaluated on a among the A and D genomes ( CHEN and ARMSTRONG 1994; case by case basis. J ELLEN et al. 1994a, LEGGETT and MARKHAND 1995; Until now, three studies used Avena ITS sequences LINARES et al. 1996, 1998; LOSKUTOV 2008), and the A and (R ODIONOV et al. 2005; NIKOLOUDAKIS and KATSIOTIS 2008; B genomes ( LEGGETT and MARKHAND 1995; KATSIOTIS N IKOLOUDAKIS et al. 2008). In these studies the majority of et al. 1997). Molecular probes differentiated the D genome plant materials contained only one ITS sequence. Although ( LINARES et al. 1998; PENG et al. 2008) and the B genome the studies used more than one accession of some species, ( IRIGOYEN et al. 2001; PENG et al. 2008) from the A genome. unfortunately only one sequence for each accession was Using various molecular techniques, A. strigosa ( CHEN used and pulled into obvious ambiguous consensus and ARMSTRONG 1994; JELLEN et al. 1994a; LEGGETT and sequence for the species as there are many ambiguity M ARKHAND 1995; LINARES et al. 1996), A. canariensis ( LI nucleotide such as S ( ϭ G/C), K ( ϭ G/T) and B ( ϭ G/T/C) et al. 2000b; LOSKUTOV 2008), A. weistii ( LI et al. 2000b; etc. In the present study, using cloning and sequencing of F U and WILLIAMS 2008) and A. longiglumis ( RODIONOV et multiple copies per individual, we examined the nuclear al. 2005; NIKOLOUDAKIS et al. 2008) had been suggested as ribosomal ITS polymorphism within and among 24 Avena the A genome donor of the tetraploid and hexaploid. All species, including 13 diploid species (A and C genomes), of the diploid C genome species have been proposed as seven tetraploids (AB, AC and CC genomes) and four the putative donors of the C genome in the hexaploids hexaploids (ACD genome), to assess the molecular diver- ( RAJHATHY and THOMAS 1974; CHEN and ARMSTRONG 1994; sity among homologous ITS repeats and infer phyloge- J ELLEN et al. 1994b; CHENG et al. 2003; NIKOLOUDAKIS and netic relationships among species in the genus. Specifi cally, K ATSIOTIS 2008). the objectives of this study were (1) to evaluate the evolu- Molecular phylogenetic studies have successfully tionary pattern and the utility of ITS sequence in Avena ; revealed the origins and evolutionary history of polyploids (2) to reveal relationships among the Avena genomes; and in plants, clarifi ed the nature of different polyploids and (3) to elucidate the phylogenetic relationships between the identifi ed their parental lineages and the hybridization diploid and polyploid species. events involved in their formation ( WENDEL 2000; SOLTIS et al. 2003; LIU et al. 2006). Among the available nuclear METHODS sequences, internal transcribed spacer (ITS) sequences have been used successfully in studying phylogenetic and Plant material and DNA isolation genomic relationships of plants at lower taxonomic levels Twenty fi ve Avena accessions, representing 13 diploid, ( HAMBY and ZIMMER 1992; BALDWIN 1993; BALDWIN et al. seven tetraploid and four hexaploid taxa, with different 1995; HSIAO et al. 1995; SANG et al. 1995; WENDEL et al. genomic combinations (A, C, AB, AC and ACD) were 1995; VOLKOV et al. 1999; ZHANG and SANG 1999; FELINER included in this study (Table 1). All seed material were et al. 2004; LIU et al. 2006). Ribosomal DNA are found in provided by Agriculture and Agri-Food Canada (AAFC) multiple copies arranged in tandem arrays in the genome and the National Small Grains Collection, Agriculture where they appear to undergo rapid concerted evolution Research Service (ARS) and United States Department of and where as a result all copies appear to be virtually iden- Agriculture (USDA).
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