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Cited by 280Plant Molecular Biology ResearchChromosomal and Genetic VariationsGenetic Mapping and Diversity in Plants and Animals

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Comparative Genomics of Flowering Time Pathways Using Brachypodium distachyon as a Model for the Temperate Grasses

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Higgins, Janet A., Bailey, Paul C., Laurie, David A.·2010·PLoS ONE
DOI 10.1371/journal.pone.0010065PMC PMC2856676
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Abstract

Brachypodium distachyon (Brachypodium) is a model for the temperate grasses which include important cereals such as barley, wheat and oats. Comparison of the Brachypodium genome (accession Bd21) with those of the model dicot Arabidopsis thaliana and the tropical cereal rice (Oryza sativa) provides an opportunity to compare and contrast genetic pathways controlling important traits. We analysed the homologies of genes controlling the induction of flowering using pathways curated in Arabidopsis Reactome as a starting point. Pathways include those detecting and responding to the environmental cues of day length (photoperiod) and extended periods of low temperature (vernalization). Variation in these responses has been selected during cereal domestication, providing an interesting comparison with the wild genome of Brachypodium. Brachypodium Bd21 has well conserved homologues of circadian clock, photoperiod pathway and autonomous pathway genes defined in Arabidopsis and homologues of vernalization pathway genes defined in cereals with the exception of VRN2 which was absent. Bd21 also lacked a member of the CO family (CO3). In both cases flanking genes were conserved showing that these genes are deleted in at least this accession. Segmental duplication explains the presence of two CO-like genes in temperate cereals, of which one (Hd1) is retained in rice, and explains many differences in gene family structure between grasses and Arabidopsis. The conserved fine structure of duplications shows that they largely evolved to their present structure before the divergence of the rice and Brachypodium. Of four flowering-time genes found in rice but absent in Arabidopsis, two were found in Bd21 (Id1, OsMADS51) and two were absent (Ghd7, Ehd1). Overall, results suggest that an ancient core photoperiod pathway promoting flowering via the induction of FT has been modified by the recruitment of additional lineage specific pathways that promote or repress FT expression.

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Figures

Figure 1 Genetic pathways controlling flowering in Arabidopsis, rice and temperate grasses. Arrows show promoting effects, T-bars show repressing effects. Environmental cues are shown as lower case letters in square boxes; v is extended cold (vernalization); ld is long days; sd is short days; am is ambient (non-vernalizing) temperature. Genes are shown in italics and proteins in non-italics in ovals. Proteins are clearly involved at all stages but we make this distinction only in cases where separate controls are known to exist for transcription and protein function or stability. # indicates inhibition of protein function. The pathways were compiled from the following reviews [1], [2], [3], [4], [5], [6], [7], [8], [9], [11], [12], [13], [14], [16], [17], [18], [19] plus individual articles referenced in the text. Box A. In Arabidopsis genes assigned to pathways are shown in colour (photoperiod pathway in green, vernalization pathway in blue, autonomous pathway in light blue). Flowering pathway integrators are shown in red. Triple headed arrows indicate activation by red or blue light. Box B. Rice genes identified as homologues of those in Arabidopsis are shown in black. Ambiguous homology is indicated with a question mark. Genes with published roles in photoperiod regulated flowering are shown in green and orthologues of pathway integrators in red. Box C. In the temperate grasses box Brachypodium genes identified as homologues of those of Arabidopsis or rice are shown in black. The VRN2 and CO3 genes from barley and wheat are also included. Genes with published roles in photoperiod or vernalization regulated flowering in barley or wheat are shown in green or blue, respectively, and orthologues of pathway integrators in red. In B and C likely orthologues of Arabidopsis genes are shown in equivalent positions within the figure (e.g. Hd1 is the rice orthologue of CO and Hd3a and RFT1 are rice orthologues of FT). Tables 1 and S1 gives information on gene names and synonyms. Square brackets in box B show three maize genes with known flowering time effects. Notes: *1 TOC1 represses PRR9, PRR7 and PRR5 [130]. *2 SUF4 interacts with FRI and FRL1. LD blocks SUF4 action to reduce FLC expression [110]. *3 Cerdan and Chory [131] identified PFT1 and proposed that it promotes flowering by a photoperiod independent pathway activating FT. The model here follows Wollenberg et al. [132] who propose an alternative in which PFT1 acts by repressing Pfr phytochrome signalling. *4 SWR1 is a protein complex including SWC6, ARP6 and PIE1. *5 CO expression from phloem-specific promoters complements the co mutation, but expression from meristem-specific promoters does not. CO triggers flowering from the phloem by the cell-autonomous activation of FT expression [133]. *6 High temperatures (27°C vs 23°C) in short days induce flowering by a mechanism that requires FT and gibberellic acid and likely involves MAF1 (FLM). High temperature induction of flowering is independent of the photoperiod pathway but is repressed by FLC and by autonomous pathway mutations that increase FLC levels [122]. Kumar and Wigge [123] showed that ambient temperature responses, including the activation of FT, involve the replacement of histone H2A.Z with H2A in nucleosomes. Mutation of ARP6 (part of the SWR1 complex) blocks this process. The late-flowering phenotype of dominant fwa mutants is caused by hypomethylation in the FWA locus leading to ectopic expression of a homeodomain leucine zipper (HD-ZIP) protein. The FWA protein interacts with FT protein and so ectopic expression of FWA delays flowering by impairing FT function [134]. FWA is not expressed during the vegetative phase in wild type plants and normally has no role in flowering so homologues are not considered in this paper. *7 TWIN SISTER OF FT (TSF) is closely related to FT, is activated by CO, has a similar role in flowering and is repressed by SVP ([135]; reviewed by [4], [102]). *8 Activation of AP1 and LFY requires two paralogous homeobox genes (PENNYWISE (PNY; aka BELLRINGER and REPLUMLESS) and POUND-FOOLISH (PNF)). Double null mutants express SOC1 and FUL but not AP1 or LFY. The double mutants can receive floral inductive signals but do not properly restructure the shoot apical meristem to make flowers [136], [137]. *9 GI promotion of Hd1/CO is shown directly but could act through the FKF1/CDF route as in Arabidopsis. *10 Mayfield et al. [80] found that 14-3-3 proteins physically interact with CO in Arabidopsis. *11 It is unclear if there is a direct connection between OsMADS50 and OsMADS14/15 as well as the connection via Edh1. *12 Ppd-H1 promotion of CO is shown directly but could act through the FKF1/CDF route as in Arabidopsis. *13 Downregulation of VRT2 by vernalization and a role in repressing VRN1 is proposed by Kane et al. [107], [108] but is not supported by Trevaskis et al. [109] so VRT2 is shown in two positions. *14 Shitsukawa et al. [89] found that WSOC1 was expressed preferentially in leaves. Expression was not affected by photoperiod or vernalization but was upregulated in seedlings by a GA treatment. *15 X indicates an unknown target gene [97]. Key to figures of phylogenetic trees A PRANK alignment of protein sequences (shown in the supplementary datasets) was used to construct phylogenetic trees using the neighbor-joining algorithm (subsequently NJ trees) with bootstrap support from 1000 iterations (values of ≥50% shown). Gene identifiers show the species as follows: At for Arabidopsis thaliana, Bradi for Brachypodium distachyon, Os for Orzya sativa (rice), Hv for Hordeum vulgare (barley), Ta for Triticum aestivum (bread wheat), Tm for Triticum monococcum (einkorn wheat), Sb for Sorghum bicolour (sorghum) and Zm for Zea mays (maize). Barley and wheat proteins are highly homologous and usually only one is shown. Gene names follow the identifiers where relevant to the text and genes with known flowering time roles are shown in colour following Figure 1. In several instances we identified pairs of genes in grasses (paralogues) in segmental duplications (SegDup) which likely result from a grass whole genome duplication that predates the divergence of the rice, maize, sorghum, Brachypodium, barley and wheat lineages. These duplication events are shown as solid circles. Similarly, solid diamonds showduplication events in Arabidopsis; these are independent from the duplication event in the grasses. Boxed T shows tandem or closely arranged paralogues resulting from duplications within individual species. Where the protein belongs to a large family we show small clades containing genes of interest selected from analyses of whole families. The clades were identified either by using an online interrogatory tree of the transcription factor family using known flowering-time genes as query sequences [98] or from the family trees shown in the supplementary material. Key to figures of segmental duplications In these figures the size and spacing of genes in the respective genomic sequences is shown to the physical scale indicated in each figure. The components of each half of the duplication are grouped under the bars at the top of the figure. For example, Figure 3 shows part of rice chromosome 3 which is colinear with part of Brachypodium chromosome 1 and is related to part of rice chromosome 7 by segmental duplication. This section of rice 7 is colinear with a separate section of Brachypodium 1. Identifiers and names of flowering-time genes and their homologues are shown, with colours following Figure 1. Gene identifiers are also shown at the top and bottom of each segment to allow orientation to the respective genome browsers. The segmental duplications are recognized by conserved genes (black boxes connected by black lines). Some figures have grey boxes which show genes that are not conserved across the duplication in all species. Within these regions, other genes are conserved between species but not across the duplication (red boxes connected by red lines). These are deletion/insertion events that occurred after the duplication arose but before the divergence of the respective species. Genes in yellow are not conserved across species and represent candidates for deletion/insertion events that occurred after species divergence. Hypothetical genes and sequences annotated as transposons are excluded. In most cases the segmental duplications extend further than shown as we only use those portions that are relevant to the relationships of the flowering-time genes discussed in the text.
Figure 1 Genetic pathways controlling flowering in Arabidopsis, rice and temperate grasses. Arrows show promoting effects, T-bars show repressing effects. Environmental cues are shown as lower case letters in square boxes; v is extended cold (vernalization); ld is long days; sd is short days; am is ambient (non-vernalizing) temperature. Genes are shown in italics and proteins in non-italics in ovals. Proteins are clearly involved at all stages but we make this distinction only in cases where separate controls are known to exist for transcription and protein function or stability. # indicates inhibition of protein function. The pathways were compiled from the following reviews [1], [2], [3], [4], [5], [6], [7], [8], [9], [11], [12], [13], [14], [16], [17], [18], [19] plus individual articles referenced in the text. Box A. In Arabidopsis genes assigned to pathways are shown in colour (photoperiod pathway in green, vernalization pathway in blue, autonomous pathway in light blue). Flowering pathway integrators are shown in red. Triple headed arrows indicate activation by red or blue light. Box B. Rice genes identified as homologues of those in Arabidopsis are shown in black. Ambiguous homology is indicated with a question mark. Genes with published roles in photoperiod regulated flowering are shown in green and orthologues of pathway integrators in red. Box C. In the temperate grasses box Brachypodium genes identified as homologues of those of Arabidopsis or rice are shown in black. The VRN2 and CO3 genes from barley and wheat are also included. Genes with published roles in photoperiod or vernalization regulated flowering in barley or wheat are shown in green or blue, respectively, and orthologues of pathway integrators in red. In B and C likely orthologues of Arabidopsis genes are shown in equivalent positions within the figure (e.g. Hd1 is the rice orthologue of CO and Hd3a and RFT1 are rice orthologues of FT). Tables 1 and S1 gives information on gene names and synonyms. Square brackets in box B show three maize genes with known flowering time effects. Notes: *1 TOC1 represses PRR9, PRR7 and PRR5 [130]. *2 SUF4 interacts with FRI and FRL1. LD blocks SUF4 action to reduce FLC expression [110]. *3 Cerdan and Chory [131] identified PFT1 and proposed that it promotes flowering by a photoperiod independent pathway activating FT. The model here follows Wollenberg et al. [132] who propose an alternative in which PFT1 acts by repressing Pfr phytochrome signalling. *4 SWR1 is a protein complex including SWC6, ARP6 and PIE1. *5 CO expression from phloem-specific promoters complements the co mutation, but expression from meristem-specific promoters does not. CO triggers flowering from the phloem by the cell-autonomous activation of FT expression [133]. *6 High temperatures (27°C vs 23°C) in short days induce flowering by a mechanism that requires FT and gibberellic acid and likely involves MAF1 (FLM). High temperature induction of flowering is independent of the photoperiod pathway but is repressed by FLC and by autonomous pathway mutations that increase FLC levels [122]. Kumar and Wigge [123] showed that ambient temperature responses, including the activation of FT, involve the replacement of histone H2A.Z with H2A in nucleosomes. Mutation of ARP6 (part of the SWR1 complex) blocks this process. The late-flowering phenotype of dominant fwa mutants is caused by hypomethylation in the FWA locus leading to ectopic expression of a homeodomain leucine zipper (HD-ZIP) protein. The FWA protein interacts with FT protein and so ectopic expression of FWA delays flowering by impairing FT function [134]. FWA is not expressed during the vegetative phase in wild type plants and normally has no role in flowering so homologues are not considered in this paper. *7 TWIN SISTER OF FT (TSF) is closely related to FT, is activated by CO, has a similar role in flowering and is repressed by SVP ([135]; reviewed by [4], [102]). *8 Activation of AP1 and LFY requires two paralogous homeobox genes (PENNYWISE (PNY; aka BELLRINGER and REPLUMLESS) and POUND-FOOLISH (PNF)). Double null mutants express SOC1 and FUL but not AP1 or LFY. The double mutants can receive floral inductive signals but do not properly restructure the shoot apical meristem to make flowers [136], [137]. *9 GI promotion of Hd1/CO is shown directly but could act through the FKF1/CDF route as in Arabidopsis. *10 Mayfield et al. [80] found that 14-3-3 proteins physically interact with CO in Arabidopsis. *11 It is unclear if there is a direct connection between OsMADS50 and OsMADS14/15 as well as the connection via Edh1. *12 Ppd-H1 promotion of CO is shown directly but could act through the FKF1/CDF route as in Arabidopsis. *13 Downregulation of VRT2 by vernalization and a role in repressing VRN1 is proposed by Kane et al. [107], [108] but is not supported by Trevaskis et al. [109] so VRT2 is shown in two positions. *14 Shitsukawa et al. [89] found that WSOC1 was expressed preferentially in leaves. Expression was not affected by photoperiod or vernalization but was upregulated in seedlings by a GA treatment. *15 X indicates an unknown target gene [97]. Key to figures of phylogenetic trees A PRANK alignment of protein sequences (shown in the supplementary datasets) was used to construct phylogenetic trees using the neighbor-joining algorithm (subsequently NJ trees) with bootstrap support from 1000 iterations (values of ≥50% shown). Gene identifiers show the species as follows: At for Arabidopsis thaliana, Bradi for Brachypodium distachyon, Os for Orzya sativa (rice), Hv for Hordeum vulgare (barley), Ta for Triticum aestivum (bread wheat), Tm for Triticum monococcum (einkorn wheat), Sb for Sorghum bicolour (sorghum) and Zm for Zea mays (maize). Barley and wheat proteins are highly homologous and usually only one is shown. Gene names follow the identifiers where relevant to the text and genes with known flowering time roles are shown in colour following Figure 1. In several instances we identified pairs of genes in grasses (paralogues) in segmental duplications (SegDup) which likely result from a grass whole genome duplication that predates the divergence of the rice, maize, sorghum, Brachypodium, barley and wheat lineages. These duplication events are shown as solid circles. Similarly, solid diamonds showduplication events in Arabidopsis; these are independent from the duplication event in the grasses. Boxed T shows tandem or closely arranged paralogues resulting from duplications within individual species. Where the protein belongs to a large family we show small clades containing genes of interest selected from analyses of whole families. The clades were identified either by using an online interrogatory tree of the transcription factor family using known flowering-time genes as query sequences [98] or from the family trees shown in the supplementary material. Key to figures of segmental duplications In these figures the size and spacing of genes in the respective genomic sequences is shown to the physical scale indicated in each figure. The components of each half of the duplication are grouped under the bars at the top of the figure. For example, Figure 3 shows part of rice chromosome 3 which is colinear with part of Brachypodium chromosome 1 and is related to part of rice chromosome 7 by segmental duplication. This section of rice 7 is colinear with a separate section of Brachypodium 1. Identifiers and names of flowering-time genes and their homologues are shown, with colours following Figure 1. Gene identifiers are also shown at the top and bottom of each segment to allow orientation to the respective genome browsers. The segmental duplications are recognized by conserved genes (black boxes connected by black lines). Some figures have grey boxes which show genes that are not conserved across the duplication in all species. Within these regions, other genes are conserved between species but not across the duplication (red boxes connected by red lines). These are deletion/insertion events that occurred after the duplication arose but before the divergence of the respective species. Genes in yellow are not conserved across species and represent candidates for deletion/insertion events that occurred after species divergence. Hypothetical genes and sequences annotated as transposons are excluded. In most cases the segmental duplications extend further than shown as we only use those portions that are relevant to the relationships of the flowering-time genes discussed in the text.CC BY · PubMed Central
Figure 2 Phylogenetic relationships within gene families containing circadian clock associated proteins. A) NJ tree of Heading date6 (Hd6) and related CASEIN KINASE IIα proteins (whole protein alignment; Dataset S2). B) NJ tree of ZEITLUPE and related proteins (whole protein alignment; Dataset S3). C) NJ tree of EARLY FLOWERING 3 and related proteins (whole protein alignment; Dataset S4). D) NJ tree of EARLY FLOWERING 4 and related proteins (whole protein alignment; Dataset S5).
Figure 2 Phylogenetic relationships within gene families containing circadian clock associated proteins. A) NJ tree of Heading date6 (Hd6) and related CASEIN KINASE IIα proteins (whole protein alignment; Dataset S2). B) NJ tree of ZEITLUPE and related proteins (whole protein alignment; Dataset S3). C) NJ tree of EARLY FLOWERING 3 and related proteins (whole protein alignment; Dataset S4). D) NJ tree of EARLY FLOWERING 4 and related proteins (whole protein alignment; Dataset S5).CC BY · PubMed Central
Figure 3 Phylogenetic relationship of PRR proteins. A) NJ tree of PSEUDO-RESPONSE REGULATOR proteins based on alignment of the PSEUDO-RECEIVER (PF00072) and CCT (PF06203) domains; Dataset S6; Full length Barley sequences; Dataset S1). B) Structure of a segmental duplication originally defined in rice using RFLP markers [138] that contains the PRR37 (Ppd-H1, Hd2) and PRR73 genes.
Figure 3 Phylogenetic relationship of PRR proteins. A) NJ tree of PSEUDO-RESPONSE REGULATOR proteins based on alignment of the PSEUDO-RECEIVER (PF00072) and CCT (PF06203) domains; Dataset S6; Full length Barley sequences; Dataset S1). B) Structure of a segmental duplication originally defined in rice using RFLP markers [138] that contains the PRR37 (Ppd-H1, Hd2) and PRR73 genes.CC BY · PubMed Central
Figure 4 Phylogenetic relationship of CDF proteins. NJ tree of CYCLING DOF FACTOR proteins (whole protein alignment; Dataset S7). The CDF subgroup was identified with an online interrogatory tree using known Arabidopsis flowering-time genes as query sequences [93]. Wheat DOF proteins were taken from Shaw et al. [139] and include three (green arrows) whose expression patterns resembled that of Arabidopsis CDFs involved in flowering.
Figure 4 Phylogenetic relationship of CDF proteins. NJ tree of CYCLING DOF FACTOR proteins (whole protein alignment; Dataset S7). The CDF subgroup was identified with an online interrogatory tree using known Arabidopsis flowering-time genes as query sequences [93]. Wheat DOF proteins were taken from Shaw et al. [139] and include three (green arrows) whose expression patterns resembled that of Arabidopsis CDFs involved in flowering.CC BY · PubMed Central
Figure 5 Phylogenetic relationship of CO proteins and physical maps of the CO1 and CO2 gene regions. A) NJ tree of CONSTANS and related proteins (whole protein alignment; Dataset S8). This diagram does not contain the diverged group IV CO-like proteins defined by Griffiths et al. [51] as these are described in Figure 11. B) Structure of the segmental duplication containing the CO1 and CO2 genes of the grasses. C) Amino-acid sequences of B-box1 and the start of B-box2 from rice, barley, Brachypodium and sorghum proteins. Blue arrows – conserved C residues not present in B-box 2 of the temperate species. Red arrows – conserved C and H residues missing from B-box 1 of the sorghum CO2 protein. Conserved amino acids defining B-boxes are shown below. D) Colinear segments of rice chromosome 9 and Brachypodium chromosome 4 showing the absence of the CO3 gene from Brachypodium.
Figure 5 Phylogenetic relationship of CO proteins and physical maps of the CO1 and CO2 gene regions. A) NJ tree of CONSTANS and related proteins (whole protein alignment; Dataset S8). This diagram does not contain the diverged group IV CO-like proteins defined by Griffiths et al. [51] as these are described in Figure 11. B) Structure of the segmental duplication containing the CO1 and CO2 genes of the grasses. C) Amino-acid sequences of B-box1 and the start of B-box2 from rice, barley, Brachypodium and sorghum proteins. Blue arrows – conserved C residues not present in B-box 2 of the temperate species. Red arrows – conserved C and H residues missing from B-box 1 of the sorghum CO2 protein. Conserved amino acids defining B-boxes are shown below. D) Colinear segments of rice chromosome 9 and Brachypodium chromosome 4 showing the absence of the CO3 gene from Brachypodium.CC BY · PubMed Central
Figure 6 Phylogenetic relationship of TOE1 and related AP2 family genes a physical maps of the maize Vgt1 region. A) NJ tree of TARGET OF EAT1 and related proteins (whole protein alignment; dataset S9; clade selected from Figure S2 using outgroup root At1g16060). Sequence alignment shows a 15 amino acid deletion in TOE1 and Vgt1 (red bar) that was not found in any Brachypodium or rice gene. The position of the conserved miRNA172 target site is also shown. B) Position of Vgt1 on maize chromosome 8 and colinear regions of rice chromosome 1 and Brachypodium chromosome 2 showing the absence of Vgt1 homologues from rice and Brachypodium.
Figure 6 Phylogenetic relationship of TOE1 and related AP2 family genes a physical maps of the maize Vgt1 region. A) NJ tree of TARGET OF EAT1 and related proteins (whole protein alignment; dataset S9; clade selected from Figure S2 using outgroup root At1g16060). Sequence alignment shows a 15 amino acid deletion in TOE1 and Vgt1 (red bar) that was not found in any Brachypodium or rice gene. The position of the conserved miRNA172 target site is also shown. B) Position of Vgt1 on maize chromosome 8 and colinear regions of rice chromosome 1 and Brachypodium chromosome 2 showing the absence of Vgt1 homologues from rice and Brachypodium.CC BY · PubMed Central
Figure 7 Phylogenetic relationships of TEM, ID1 and Ehd1 proteins. A) NJ tree of TEMPRANILLO and related proteins (whole protein alignment; Dataset S10). The TEM subgroup was identified with an online interrogatory tree using known Arabidopsis flowering-time genes as query sequences [98]. B) Colinear segments of rice chromosome 10 and Brachypodium chromosome 3 showing the absence of Ehd1 from Brachypodium. C) NJ tree of INDETERMINATE1 proteins (using an alignment of the ID domain; Dataset S11). Two related IDD proteins are included to show that ID proteins are a distinct subgroup of the C2H2 zinc-finger transcription factor family (Figure S3).
Figure 7 Phylogenetic relationships of TEM, ID1 and Ehd1 proteins. A) NJ tree of TEMPRANILLO and related proteins (whole protein alignment; Dataset S10). The TEM subgroup was identified with an online interrogatory tree using known Arabidopsis flowering-time genes as query sequences [98]. B) Colinear segments of rice chromosome 10 and Brachypodium chromosome 3 showing the absence of Ehd1 from Brachypodium. C) NJ tree of INDETERMINATE1 proteins (using an alignment of the ID domain; Dataset S11). Two related IDD proteins are included to show that ID proteins are a distinct subgroup of the C2H2 zinc-finger transcription factor family (Figure S3).CC BY · PubMed Central
Figure 8 Phylogenetic relationship of FT and HAP family proteins. A) NJ tree of FLOWERING LOCUS T and related proteins (PEBP (PF01161) domain alignment; Dataset S12). B) NJ tree of HAP3 and related proteins (whole protein alignment; Dataset S13). C) NJ tree of HAP5 and related proteins (whole protein alignment; Dataset S14). In B and C only the HAP3 and HAP5 clades selected from Figure S5 are shown.
Figure 8 Phylogenetic relationship of FT and HAP family proteins. A) NJ tree of FLOWERING LOCUS T and related proteins (PEBP (PF01161) domain alignment; Dataset S12). B) NJ tree of HAP3 and related proteins (whole protein alignment; Dataset S13). C) NJ tree of HAP5 and related proteins (whole protein alignment; Dataset S14). In B and C only the HAP3 and HAP5 clades selected from Figure S5 are shown.CC BY · PubMed Central
Figure 9 Phylogenetic relationship of 14-3-3 and SOC1 proteins. A) NJ tree of 14-3-3 and related proteins (whole protein alignment; Dataset S15). Only the 14-3-3 clade selected from Figure S6 is shown, this includes rice GF14c and Arabidopsis GRF5 (GF14υ) but excludes GRF9 (GF14μ) [80]. B) NJ tree of SUPRESSOR of CONSTANS 1 and related MADS-box proteins (whole protein alignment; Dataset S16). The SOC1 clade, including the MADS51 group, selected from Figure S7 is shown including the OsMADS50 (Q9XJ60) protein which spans Os03g03070 and Os03g03100.
Figure 9 Phylogenetic relationship of 14-3-3 and SOC1 proteins. A) NJ tree of 14-3-3 and related proteins (whole protein alignment; Dataset S15). Only the 14-3-3 clade selected from Figure S6 is shown, this includes rice GF14c and Arabidopsis GRF5 (GF14υ) but excludes GRF9 (GF14μ) [80]. B) NJ tree of SUPRESSOR of CONSTANS 1 and related MADS-box proteins (whole protein alignment; Dataset S16). The SOC1 clade, including the MADS51 group, selected from Figure S7 is shown including the OsMADS50 (Q9XJ60) protein which spans Os03g03070 and Os03g03100.CC BY · PubMed Central
Figure 10 Phylogenetic relationship of FUL/AP1/VRN1 type MADS-box proteins and physical maps of the FUL1 and FUL2 regions. A) NJ tree of VRN1 and related proteins (whole protein alignment; Dataset S17). The FUL/AP1 clade selected from Figure S7 is shown. B) Structure of the segmental duplication containing the FUL1 (VRN1; OsMADS14) and FUL2 (OsMADS15) genes of the grasses.
Figure 10 Phylogenetic relationship of FUL/AP1/VRN1 type MADS-box proteins and physical maps of the FUL1 and FUL2 regions. A) NJ tree of VRN1 and related proteins (whole protein alignment; Dataset S17). The FUL/AP1 clade selected from Figure S7 is shown. B) Structure of the segmental duplication containing the FUL1 (VRN1; OsMADS14) and FUL2 (OsMADS15) genes of the grasses.CC BY · PubMed Central
Figure 11 Phylogenetic relationship of VRN2/ZCCT proteins and physical maps of the VRN2 region. A) Structure of the segmental duplication containing the ZCCT genes. B) NJ tree of ZCCT and related proteins (whole protein alignment; Dataset S18). C) Colinear regions of rice chromosome 7 and Brachypodium chromosome 1 showing the absence of a Ghd7 homologue from Brachypodium.
Figure 11 Phylogenetic relationship of VRN2/ZCCT proteins and physical maps of the VRN2 region. A) Structure of the segmental duplication containing the ZCCT genes. B) NJ tree of ZCCT and related proteins (whole protein alignment; Dataset S18). C) Colinear regions of rice chromosome 7 and Brachypodium chromosome 1 showing the absence of a Ghd7 homologue from Brachypodium.CC BY · PubMed Central
Figure 12 Phylogenetic relationship of FD and related bZIP proteins. NJ tree of FD and related basic region leucine zipper domain proteins (BRLZ (SM00338) domain alignment; Dataset S19). The bZIP clade was identified with an online interrogatory tree using known Arabidopsis flowering-time genes as query sequences [98]. Black arrows show genes with roles in flowering as described in [66], [67], [92], [94].
Figure 12 Phylogenetic relationship of FD and related bZIP proteins. NJ tree of FD and related basic region leucine zipper domain proteins (BRLZ (SM00338) domain alignment; Dataset S19). The bZIP clade was identified with an online interrogatory tree using known Arabidopsis flowering-time genes as query sequences [98]. Black arrows show genes with roles in flowering as described in [66], [67], [92], [94].CC BY · PubMed Central
Figure 13 Phylogenetic relationships of FLC, SVP, FRI, VRN5 and polycomb-like proteins. A) NJ tree of FLOWERING LOCUS C and related MADS-box proteins (whole protein alignment; Dataset S20). Only the FLC clade selected from Figure S7 is shown. B) NJ tree of SHORT VEGETATIVE PHASE and related MADS-box proteins (whole protein alignment; Dataset S21). Only the SVP clade selected from Figure S7 is shown. C) NJ tree of FRIGIDA and related proteins (PF07899 domain alignment; Dataset S22). For Arabidopsis a functional FRI sequence (H51) was used. FRI and related clade selected from Figure S9. D) NJ tree of VERNALIZATION5 and related PHD finger proteins (whole protein alignment; Dataset S23). E) NJ tree of Arabidopsis VERNALIZATION2 and related polycomb group proteins (whole protein alignment; Dataset S24).
Figure 13 Phylogenetic relationships of FLC, SVP, FRI, VRN5 and polycomb-like proteins. A) NJ tree of FLOWERING LOCUS C and related MADS-box proteins (whole protein alignment; Dataset S20). Only the FLC clade selected from Figure S7 is shown. B) NJ tree of SHORT VEGETATIVE PHASE and related MADS-box proteins (whole protein alignment; Dataset S21). Only the SVP clade selected from Figure S7 is shown. C) NJ tree of FRIGIDA and related proteins (PF07899 domain alignment; Dataset S22). For Arabidopsis a functional FRI sequence (H51) was used. FRI and related clade selected from Figure S9. D) NJ tree of VERNALIZATION5 and related PHD finger proteins (whole protein alignment; Dataset S23). E) NJ tree of Arabidopsis VERNALIZATION2 and related polycomb group proteins (whole protein alignment; Dataset S24).CC BY · PubMed Central

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Authors
Higgins, J. A., Bailey, P. C., & Laurie, D. A.
Affiliations
John Innes Centre (GB)
Corresponding author
Higgins, Janet A.
ORCID
Venue
PLoS ONE
Publisher
Public Library of Science (PLoS)
Published
2010-04-19
Volume
5
Issue
4
Pages
e10065
ISSN
1932-6203 (ISSN-L)
DOI
10.1371/journal.pone.0010065
PMC
PMC2856676
OpenAlex
W1988145565
Cited by
280
References
139
Citations by year
2026: 6 · 2025: 4 · 2024: 5 · 2023: 7 · 2022: 18 · 2021: 12 · 2020: 17 · 2019: 14 · 2018: 22 · 2017: 15 · 2016: 28 · 2015: 15 · 2014: 18 · 2013: 38 · 2012: 32
FWCI
38.11
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Figshare (submittedVersion, cc-by)
Funders
  • Gatsby Charitable Foundation
  • Biotechnology and Biological Sciences Research Council (BBS/E/J/000CA286)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Molecular Biology Research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Chromosomal and Genetic Variations
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Mapping and Diversity in Plants and Animals
Keywords
flowering time, Brachypodium distachyon, temperate grass, photoperiod pathway, vernalization pathway, autonomous pathway, circadian clock, CONSTANS, segmental duplication, gene family evolution, cereal domestication, Arabidopsis thaliana, rice, gene homology, MADS-box genes
MeSH terms
Poaceae, Temperature, Genes, Plant, Photoperiod, Genome, Plant, Genomics, Flowers, Metabolic Networks and Pathways

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