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Patterns of Gene Duplication and Functional Diversification During The Molecular Phylogenetics and Evolution 44 (2007) 26–41 www.elsevier.com/locate/ympev Patterns of gene duplication and functional diversification during the evolution of the AP1/SQUA subfamily of plant MADS-box genes Hongyan Shan a,b,1, Ning Zhang a,b,1, Cuijing Liu a,b,1, Guixia Xu a,b, Jian Zhang a,b, Zhiduan Chen a,*, Hongzhi Kong a,* a State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, The Chinese Academy of Sciences, Xiangshan, Beijing 100093, People’s Republic of China b Graduate University of the Chinese Academy of Sciences, Beijing 100039, People’s Republic of China Received 19 June 2006; revised 7 February 2007; accepted 19 February 2007 Available online 25 February 2007 Abstract Members of the AP1/SQUA subfamily of plant MADS-box genes play broad roles in the regulation of reproductive meristems, the specification of sepal and petal identities, and the development of leaves and fruits. It has been shown that AP1/SQUA-like genes are angiosperm-specific, and have experienced several major duplication events. However, the evolutionary history of this subfamily is still uncertain. Here, we report the isolation of 14 new AP1/SQUA-like genes from seven early-diverging eudicots and the identification of 11 previously uncharacterized ESTs and genomic sequences from public databases. Sequence comparisons of these and other published sequences reveal a conserved C-terminal region, the FUL motif, in addition to the known euAP1/paleoAP1 motif, in AP1/SQUA-like proteins. Phylogenetic analyses further suggest that there are three major lineages (euAP1,euFUL, and AGL79) in core eudicots, likely resulting from two close duplication events that predated the divergence of core eudicots. Among the three lineages, euFUL is structur- ally very similar to FUL-like genes from early-diverging eudicots and basal angiosperms, whereas euAP1 might have originally been gen- erated through a 1-bp deletion in the exon 8 of an ancestral euFUL-orFUL-like gene. Because euFUL- and FUL-like genes usually have broad expression patterns, we speculate that AP1/SQUA-like genes initially had broad functions. Based on these observations, the evo- lutionary fates of duplicate genes and the contributions of the frameshift mutation and alternative splicing to functional diversity are discussed. Ó 2007 Elsevier Inc. All rights reserved. Keywords: MADS-box gene; The AP1/SQUA subfamily; Evolution; Gene duplication; Alternative splicing; Frameshift mutation; Subfunctionalization 1. Introduction Theissen, 2001; Theissen et al., 1996). Many of the genes in this network encode transcription factors, which can bind Flowers are reproductive structures that characterize to the regulatory region of other genes and activate/repress angiosperms (Endress, 1994). Molecular and genetic stud- their expression (de Folter et al., 2005; Kaufmann et al., ies of model plants, such as Arabidopsis thaliana (Brassica- 2005). Among the regulators involved in floral develop- ceae), Antirrhinum majus (Plantaginaceae), and Petunia ment, the best understood are the MIKCc-type MADS- hybrida (Solanaceae), have indicated that the process of box genes, which encode proteins with a conserved K-box flower formation is controlled by a complex regulatory net- domain, a less-conserved intervening region, and a variable work of numerous genes and pathways (Soltis et al., 2002; C terminus, in addition to the most conserved MADS-box domain (Becker et al., 2003; De Bodt et al., 2003b; Kauf- mann et al., 2005). * Corresponding authors. Fax: +86 10 62590843. E-mail addresses: [email protected] (Z. Chen), [email protected] It has been proposed that floral MADS-box genes can (H. Kong). be grouped into several major groups, or subfamilies, 1 These authors contributed equally to this work. which are the results of several gene duplications (Becker 1055-7903/$ - see front matter Ó 2007 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2007.02.016 H. Shan et al. / Molecular Phylogenetics and Evolution 44 (2007) 26–41 27 and Theissen, 2003; Martinez-Castilla and Alvarez-Buylla, AP1/SQUA-like genes have also been identified from 2003; Nam et al., 2003; Purugganan et al., 1995). Gene other angiosperm species. In general, these genes possess duplication, followed by divergence in coding sequence similar sequence features, expression patterns or gene and expression pattern, thus plays key roles in the innova- functions with one of the four Arabidopsis paralogs. tion and diversification of the regulatory network that For example, in another model species, Antirrhinum determines floral morphology. For example, the earliest majus, the SQUA gene is important for the specification gene duplication events that occurred within the AP3/PI, of floral meristems (Huijser et al., 1992), and DEFH28 AG/STK and SEP subfamilies of MADS-box genes were plays a dual role during the development of both inflo- believed to coincide with the emergence of flowering plants rescences and carpels (Muller et al., 2001). However, this (Aoki et al., 2004; Kim et al., 2004; Kramer et al., 1998, situation seems to be restricted to core eudicots because 2004; Stellari et al., 2004; Zahn et al., 2005a, 2006). In genes isolated from basal angiosperms (incl. Amborella- angiosperms, key duplication events seem to have also ceae, Nymphaeaceae, Austrobaileyales, monocots, Cer- occurred within the AP1/SQUA, AP3, AG, and AGL2/3/ atophyllaceae, magnoliids, and Chloranthaceae; see 4 lineages before the diversification of core eudicots (Aoki Soltis and Soltis, 2004) have broad expression patterns. et al., 2004; Kim et al., 2004; Kramer et al., 1998, 2004, For example, the Magnolia grandiflora (Magnoliaceae) 2006; Litt and Irish, 2003; Zahn et al., 2005a, 2006). The Ma.gr.AP1 and Eupomatia bennetii (Eupomatiaceae) core eudicots are one of the most successful angiosperm Eu.be.AP1 genes are both highly expressed in bracts groups, comprising the Gunnerales, Berberidopsidales, (or calyptra in Eupomatia), tepals, stamens, carpels and Saxifragales, Santalales, Caryophyllales, rosids (incl. Ara- leaves (Kim et al., 2005a), and the Nuphar advena bidopsis, Medicago, and Populus, etc.), and asterids (incl. (Nymphaeaceae) Nu.ad.AP1 gene is strongly expressed Antirrhinum, Petunia, and Gerbera, etc.) (Soltis and Soltis, in carpels and leaves, with a small amount of transcripts 2004). detected in inner tepals and stamens (Kim et al., 2005b). Among the floral MADS-box genes studied to date, In rice (Oryza sativa; Poaceae), the OsMADS18 gene is members of the AP1/SQUA subfamily are of particular widely expressed in roots, leaves, inflorescences, and all interest to us because they play very important roles in floral organ primordia (Fornara et al., 2004; Masiero the development of inflorescences and flowers. In Arabid- et al., 2002). opsis, there are four AP1/SQUA-like genes, i.e., APET- In addition to the obvious differences in expression pat- ALA1 (AP1), CAULIFLOWER (CAL), FRUITFULL terns, the evolutionary history of AP1/SQUA-like genes (FUL), and AGAMOUS-LIKE 79 (AGL79)(De Bodt also seems to be complicated. Several recent studies indi- et al., 2003a; Parenicova et al., 2003). AP1 was identified cate that the AP1/SQUA subfamily has experienced fre- as both a floral organ identity gene and a floral meristem quent gene duplications and the acquisition of novel identity gene, as strong ap1 mutations cause the conver- sequence structures, making it difficult to understand the sion of sepals into bract-like structures and the concomi- history of this subfamily (Becker and Theissen, 2003; tant formation of additional flowers in the axis of each Johansen et al., 2002; Litt and Irish, 2003; Vandenbussche bract, and weak ap1 mutations result in defects in sepals et al., 2003a). In most previous studies, resolution and reli- and petals (Bowman et al., 1993; Irish and Sussex, 1990; ability of phylogenetic results are likely affected by taxon Mandel et al., 1992). The closest Arabidopsis relative of limitation and long-branch attraction. For instance, in AP1 is CAL, which was generated through a gene dupli- the most complete study to date, Litt and Irish (2003) cation that occurred within the Brassicaceae and acts par- reported that FUL-like genes from monocots (mainly tially redundantly with AP1 in controlling the formation grasses) were resolved as two successively branching clades, of floral meristem (Bowman et al., 1993; Kempin et al., and the Arabidopsis AtFL gene, which is virtually the same 1995; Lawton-Rauh et al., 1999). The cal single mutants as AGL79, was clustered with FUL-like genes from early- do not have obvious abnormalities, but the cal mutation diverging eudicots (mainly Ranunculales and Buxaceae). causes an enhancement of the repeated branching pattern This pattern suggests that two ancient duplications seen in the ap1 floral meristem (Bowman et al., 1993; occurred at an early stage of angiosperm evolution, one Kempin et al., 1995). The FUL gene encodes a protein before the split of monocots from dicots, and the other with a C terminus quite different from those of AP1 before the diversification of eudicots. However, as pointed and CAL (Mandel and Yanofsky, 1995). FUL also plays out by the authors, this pattern could also be an artifact of a role in the control of the floral meristem; in the ap1 cal an uneven substitution rate or biased G–C content. It has ful triple mutants, all floral meristem characters are lost been shown that, due to uneven substitution rate or biased and no flower is formed (Ferrandiz et al., 2000a). In con- G–C content, factors which may potentially skew the trast to CAL, FUL is also expressed in young siliques and results of phylogenetic analysis, especially when the taxa growing leaves, suggestive of its roles in fruit and leaf selected are strongly biased (Kong et al., 2004; Leebens- development (Gu et al., 1998; Mandel and Yanofsky, Mack et al., 2005; Zahn et al., 2005a, 2006). This suggests 1995). The function of AGL79 is not known, although that the evolution of AP1/SQUA-like genes needs to be its transcripts can be detected in roots (De Bodt et al., further examined by including sequences from additional 2003a; Parenicova et al., 2003).
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