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, 131 (4), 1855-67

The Evolution of CONSTANS-like Gene Families in Barley, Rice, and Arabidopsis

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The Evolution of CONSTANS-like Gene Families in Barley, Rice, and Arabidopsis

Simon Griffiths et al. Plant Physiol.

Abstract

The CO (CONSTANS) gene of Arabidopsis has an important role in the regulation of flowering by photoperiod. CO is part of a gene family with 17 members that are subdivided into three classes, termed Group I to III here. All members of the family have a CCT (CO, CO-like, TOC1) domain near the carboxy terminus. Group I genes, which include CO, have two zinc finger B-boxes near the amino terminus. Group II genes have one B-box, and Group III genes have one B-box and a second diverged zinc finger. Analysis of rice (Oryza sativa) genomic sequence identified 16 genes (OsA-OsP) that were also divided into these three groups, showing that their evolution predates monocot/dicot divergence. Eight Group I genes (HvCO1-HvCO8) were isolated from barley (Hordeum vulgare), of which two (HvCO1 and HvCO2) were highly CO like. HvCO3 and its rice counterpart (OsB) had one B-box that was distantly related to Group II genes and was probably derived by internal deletion of a two B-box Group I gene. Sequence homology and comparative mapping showed that HvCO1 was the counterpart of OsA (Hd1), a major determinant of photoperiod sensitivity in rice. Major genes determining photoperiod response have been mapped in barley and wheat (Triticum aestivum), but none corresponded to CO-like genes. Thus, selection for variation in photoperiod response has affected different genes in rice and temperate cereals. The peptides of HvCO1, HvCO2 (barley), and Hd1 (rice) show significant structural differences from CO, particularly amino acid changes that are predicted to abolish B-box2 function, suggesting an evolutionary trend toward a one-B-box structure in the most CO-like cereal genes.

Figures

Figure 1
Figure 1
Exon/intron structure of barley CONSTANS-like genes. The respective sizes of the genes in base pairs are shown together with the positions of domains discussed in the text. Positions of CCT domain subclones used for library screening (#) and single-copy subclones used for genetic mapping (*) are also shown. Structures and gene sizes for CO, Hd1, and S12756 are from sequence accessions listed in Table I. The inset shows the residues forming the exon boundaries. HvCO3a and b are alternatively spliced forms (see text). The intron position of S12569 was determined by alignment with rice genomic sequence.
Figure 2
Figure 2
Alignment of predicted peptides of CONSTANS and related genes from Arabidopsis, barley, and rice. a, Amino termini and B-box domains. Conserved C and H residues and consensus spacing (Xn) defining B-box domains (Borden, 1998; Robson et al., 2001) are shown below. Residues altered in co-2 to co-7 mutant alleles or deleted in co-1 (Robson et al., 2001) are shown above. Boxed residues distinguish COL3- to COL5-like peptides from the most CO-like group. b, Middle region. Alignments of whole sequences are shown for CO, Hd1, HvCO1, and HvCO2. Small conserved motifs found in other CO-like genes are shown in boxes (see text for details). The underlined region is predicted to form coiled structures in Hd1 and HvCO1 but not in CO. c, CCT and COOH domains. Residues affected in co mutant alleles (Robson et al., 2001) are shown above. GenBank accession numbers for the sequences used in this figure are listed in Table I. Barley sequences are the Igri allele in all cases except for HvCO7, where sequence was from CI16151.
Figure 3
Figure 3
Phylogenetic analysis of CO-like genes. NJ trees of CCT domain nucleotides (a) or concatenated B-box and CCT domain nucleotides (b) are shown. Genetic distances were calculated using the Kimura two-parameter model and excluded nucleotides at the third position in each codon. Bootstrap values from 1,000 replicates were used to assess the robustness of the trees. The domain structures of each gene in b is also shown. B1 and B2 are CO-like B-boxes (white rectangles) or other zinc finger domains (solid rectangles). M1 to M4, Conserved middle region domains shown in Figure 2b; T, Carboxy-terminal domain shown in Figure 2c. Intron positions confirmed by alignment with cDNAs or reverse transcription-PCR products are shown as solid arrowheads. Introns predicted from genomic sequence are show as white arrowheads.
Figure 4
Figure 4
Genetic map locations of CONSTANS-like genes in barley and rice. 1, Genetic map lengths of barley chromosomes 1H, 2H, 5H, 6H, and 7H from Qi et al. (1996) indicating the approximate positions of partial maps that are drawn to larger scale. Solid ovals show positions of centromeres derived from other published maps. 2, Genetic map lengths of rice chromosomes 2, 3, 4, 6, and 9 from Harushima et al. (1998) indicating the approximate positions of the partial maps. Solid ovals show positions of centromeres. 3 to 13, Partial maps showing CO-like gene locations. Triticeae maps have markers to the right, and rice maps have markers to the left. 3, Barley: Igri × Triumph (Laurie et al., 1995 plus additional markers; Ppd, Sgh, and eps are loci for photoperiod response, vernalization response, or quantitative trait locus [QTL] for earliness, respectively, from the same paper). 4, H. bulbosum: PB1 × PB11 (Salvo-Garrido et al., 2001); 5, Wheat: Chinese Spring × Synthetic group 2 map (Gale et al., 1995). 6, Barley: Captain × H. spontaneum (2H from Laurie et al., 1993; 7HS from Dunford et al., 1995). 7, Barley: Bonus × H. spontaneum (Laurie et al., 1996). 8, Triticum monococcum (Dubcovsky et al., 1996). 9, Wheat: Group 7 map (Van Deynze et al., 1995). 10, Rye Ds2 × RxL10 (Devos et al., 1993). 11, Rice: IR20 × 63-83 (Quarrie et al., 1997, plus additional markers). 12, Rice: Nipponbare × Kasalath (Harushima et al., 1998). Map locations of Xrgs3574, Xrgs12569, and Xrgc60910 are from Song et al. (1998); Hd1 from Yano et al. (2000). 13, Rice (Causse et al., 1994). Positions of OsE and OsL are by alignment with genomic sequence (Table I).
Figure 5
Figure 5
CCT domain and COOH region peptides in distantly related green plants. Angiosperms: Arabidopsis CO (X94937) and rice Hd1 Ginbouzou allele (AB041840). Gynmosperm: Pinus radiata (AF001136); this gene has similarities to COL3 to COL5 group gene because it has the conserved W, V, and VT B-box residues boxed in Figure 2a. Moss: P. patens (3′ ESTs BJ167752 [1] and BJ166101 [2]; 5′ sequences from the same clones reveal B-box residues). Unicellular green alga: C. reinhardii (ESTs BI529290, BI716177, and BI727274 all give this translation). The CCT domain and COOH region of the Arabidopsis TOC1 gene (AF272039) are included for comparison.

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