JXB Advance Access originally published online on August 28, 2006
Journal of Experimental Botany 2006 57(13):3379-3386; doi:10.1093/jxb/erl073
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Environmental Perception |
Additional targets of the Arabidopsis autonomous pathway members, FCA and FY
Department of Cell and Developmental Biology, John Innes Centre, Colney Lane, Norwich NR4 7UH, UK
To whom correspondence should be addressed. E-mail: caroline.dean{at}bbsrc.ac.uk
Received 21 March 2006; Accepted 30 May 2006
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Abstract |
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 Top Abstract IntroductionThe floral repressor, FLCRepression of FLC by...FCA interaction with FY...Additional roles for the...ConclusionReferences |
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A central player in the Arabidopsis floral transition is the floral repressor FLC, the MADS-box transcriptional regulator that inhibits the activity of genes required to switch the meristem from vegetative to floral development. One of the many pathways that regulate FLC expression is the autonomous promotion pathway composed of FCA, FY, FLD, FPA, FVE, LD, and FLK. Rather than a hierarchical set of activities the autonomous promotion pathway comprises sub-pathways of genes with different biochemical functions that all share FLC as a target. One sub-pathway involves FCA and FY, which interact to regulate RNA processing of FLC. Several of the identified components (FY, FVE, and FLD) are homologous to yeast and mammalian proteins with rather generic roles in gene regulation. So why do mutations in these genes specifically show a late-flowering phenotype in Arabidopsis? One reason, found during the analysis of fy alleles, is that the mutant alleles identified in flowering screens can be hypomorphic, they still have partial function. A broader role for the autonomous promotion pathway is supported by a microarray analysis which has identified genes mis-regulated in fca mutants, and whose expression is also altered in fy mutants.
Key words: Arabidopsis, autonomous promotion pathway, FCA, FLC, flowering time, FY, microarray, polyadenylation, RNA processing, vernalization
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Introduction |
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TopAbstractIntroductionThe floral repressor, FLCRepression of FLC by...FCA interaction with FY...Additional roles for the...ConclusionReferences |
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The switch to flowering is a major developmental transition in the plant life cycle (Simpson and Dean, 2002). Plants undergo an initial period of vegetative growth and later in development the meristem undergoes a change in fate and enters reproductive development, producing flowers and differentiating the germ line. The timing of this transition is crucial for reproductive success as maximal pollination and seed set occur when environmental conditions are most favourable. Thus, great variability in flowering time has evolved in different plant species and varieties as they have adapted to growth in different conditions. In order to achieve this tight regulation of flowering, multiple pathways have evolved to integrate several environmental and endogenous cues (Battey, 2000; Bernier, 1988). These were elegantly dissected using a physiological approach in a range of plant species, and notable in this respect was the work on photoperiod response analysed in Sinapis alba by Bernier and colleagues (Bernier, 1988; Bernier et al., 1993).
The genetic dissection of flowering time control was greatly facilitated by the focus on Arabidopsis thaliana by many plant scientists. Flowering research in Arabidopsis started in several laboratories in the 1950s, where the focus was on natural variation (Napp-Zinn, 1955), although some mutagenesis was undertaken (Relichová, 1976). However, the induced mutations that have impacted significantly on progress to date were developed by Maarten Koornneef and colleagues in Wageningen (Koornneef et al., 1991). His group identified a series of late-flowering mutations from the rapid-cycling Landsberg erecta parent. Development of map-based gene cloning tools, insertional mutagenesis systems, facile transformation, well-characterized natural variants, extensive mutant collections, and now the full genome sequence have greatly accelerated the dissection of flowering time control in Arabidopsis thaliana. There is now a framework for the regulatory gene hierarchy controlling flowering (Simpson et al., 1999; Boss et al., 2004) and ideas of how it might differ between varieties and species (Simpson and Dean, 2002).
A central regulator in this hierarchy is the floral repressor FLOWERING LOCUS C (FLC) which, together with other floral repressors TERMINAL FLOWER1 (TFL1), TERMINAL FLOWER2 (TFL2), SHORT VEGETATIVE PHASE (SVP), and TARGET OF EAT1/2 (TOE1/2), delays the transition to flowering (Bradley et al., 1997; Sheldon et al., 1999; Hartmann et al., 2000; Gaudin et al., 2001; Aukerman and Sakai, 2003). There has been a great deal of focus on regulation of the expression of the FLC repressor which is regulated by a number of independent pathways (Baurle and Dean, 2006; Henderson and Dean, 2004) (Fig. 1). It is down-regulated by vernalization (through genes VIN3 (Sung and Amasino, 2004), VRN2 (Gendall et al., 2001) and VRN1 (Levy et al., 2002)) and a series of proteins classified as the autonomous promotion pathway. It is up-regulated by a number of genes, including FRIGIDA (FRI) (Johanson et al., 2000), FRIGIDA-LIKE1 (FRL1) (Michaels et al., 2004), EFS (SDS8) (Kim et al., 2005; Zhao et al., 2005), ARP6 (Choi et al., 2005; Deal et al., 2005; Martin-Trillo et al., 2006), and FES1 (Schmitz et al., 2005). In this paper, the focus is on one of those pathways, the autonomous promotion pathway and current understanding of it is reviewed. There is speculation on whether the autonomous promotion pathway has a more generic role than flowering time control and some microarray experiments, aimed at identifying components required for FCA repression of FLC plus targets in addition to FLC, are briefly summarized.
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The floral repressor, FLC |
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TopAbstractIntroductionThe floral repressor, FLCRepression of FLC by...FCA interaction with FY...Additional roles for the...ConclusionReferences |
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FLC is a MADS box transcriptional repressor, expressed predominantly in shoot and root apices and the vasculature. It acts to repress flowering quantitatively through blocking expression of the floral pathway integrators, FLOWERING LOCUS T (FT) and SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 (SOC1) (Michaels and Amasino, 1999; Sheldon et al., 1999, 2000). The mechanism by which it does so is not well understood, although a MADS-box binding site within the SOC1 promoter is required (Hepworth et al., 2002) and it has been found bound in vivo to regulatory sequences of SOC1 and FT (Searle et al., 2006). Allelic variation at FLC has been found to contribute to natural variation in vernalization requirement between different Arabidopsis accessions (Gazzani et al., 2003; Michaels et al., 2003; Werner et al., 2005) with some of the naturally occurring weak FLC alleles being caused by changes in expression rather than alterations of protein function. Landsberg erecta (Ler) contains a Mutator-like transposon at the 3' end of the large FLC intron 1 (Gazzani et al., 2003; Michaels et al., 2003). This induces an RNAi-mediated suppression of at least some of the FLC transcripts so reducing overall FLC levels (Liu et al., 2004).
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Repression of FLC by genes of the autonomous promotion pathway |
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TopAbstractIntroductionThe floral repressor, FLCRepression of FLC by...FCA interaction with FY...Additional roles for the...ConclusionReferences |
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Analysis of mutants (initially Ler but also recently Col) that flower very late in both long and short day photoperiods defined the autonomous promotion pathway (Koornneef et al., 1991). They have subsequently all been shown to regulate the common target, FLC. Their late-flowering phenotype is overcome by vernalization, so vernalization and the autonomous promotion pathway are considered to function in parallel. In the absence of FRI, this pathway is the major activity regulating FLC levels and vernalization requirement (Fig. 1). There are currently seven members of the autonomous promotion pathway; FCA, FY, FPA, FVE, LUMINIDEPENDENS (LD), FLOWERING LATE KH MOTIF (FLK), and FLOWERING LOCUS D (FLD) (Table 1). Some mutations (in LD, FLD, and possibly FLK) cause a late-flowering phenotype in a Columbia background but are not late or only slightly late-flowering in a Ler background (Lee et al., 1994b; Sanda and Amasino, 1996b).
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FVE encodes an MSI1 homologue (Ausin et al., 2004; Kim et al., 2004) and FLD a putative homologue of the lysine-specific histone demethylase LSD1 (Sanda and Amasino, 1996a; He et al., 2003; Shi et al., 2004, 2005; Metzger et al., 2005). Both FVE and FLD have been implicated in histone deacetylation complexes (He et al., 2003; Ausin et al., 2004). FCA, FPA and FLK all contain putative RNA-binding proteins; the otherwise unrelated FCA and FPA proteins contain RRM-domains (Macknight et al., 1997; Schomburg et al., 2001), while FLK contains three KH domains (Lim et al., 2004; Mockler et al., 2004). FY is homologous to Pfs2p, an essential polyadenylation and 3'-end processing factor from yeast (Simpson et al., 2003). LD is a homeodomain protein with unknown function (Lee et al., 1994a). Genetic and biochemical analysis indicates that FCA, FY form one sub-pathway, while FPA and FVE might form another (Koornneef et al., 1998; Simpson et al., 2003). Since the ld and fld mutations are strongly suppressed by Ler-FLC the interaction of these mutations with other autonomous promotion pathway mutations has not been reported so far. Thus the autonomous promotion pathway consists of a diverse set of biochemical functions, some of which play generic roles in other organisms.
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FCA interaction with FY mediates changes in FCA transcript processing |
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TopAbstractIntroductionThe floral repressor, FLCRepression of FLC by...FCA interaction with FY...Additional roles for the...ConclusionReferences |
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FCA physically interacts with FY through a WW domain in the C-terminal part of FCA and PPLPP residues in the C-terminal part of FY (Simpson et al., 2003) (Fig. 2A, B). The C-terminal part of FY is an additional domain of the protein not present in the yeast Pfs2p and so may have evolved to play a regulatory role. The FY homologues in humans and mouse also have an unrelated 3' extension relative to the yeast protein so this could be quite a general phenomenon. Functional evidence to show that the homology of FY to yeast poly A/3' processing factor is meaningful and was found through analysis of FCA regulation. Four FCA transcripts are present in cells, in one of which polyadenylation occurs within the third intron (Fig. 2C). Over-expression of FCA promotes the use of this proximal polyadenylation site so reducing the abundance of the full-length FCA transcript (FCA
), the only transcript that produces a functional FCA protein. The FCA/FY interaction is required for the use of this proximal poly A site and so for the negative autoregulation of FCA. Thus, this negative feedback is missing in fy-1 (Macknight et al., 2002; Quesada et al., 2003), Fig. 2C. The phenotype of fy-1, the only fy allele available for many years, is a slight delay in flowering. When a second allele was identified from the Salk T-DNA collection it was also found to be late-flowering with increased FLC levels. However, both these alleles were still found to express the N-terminal part of the FY protein containing the seven WD repeats, which constitutes the whole protein in yeast (Henderson et al., 2005). To assess the phenotype of a true fy null mutant, alleles from the NSF TILLING population (McCallum et al., 2000) were characterized. fy-4 was found to carry a premature stop codon at the end of the first WD repeat and this prevented any FY protein being made. fy-4 mutants are embryo lethal suggesting that, as in yeast, FY has a general role in Arabidopsis and FCA might recruit specific transcripts to the canonical polyadenylation machinery (Henderson et al., 2005).
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, ß, and Pleiotropic functions for FY in development had been previously suggested by the genetic analysis of the autonomous promotion pathway mutants (Koornneef et al., 1998). An fy-1, fpa double mutant had never been recovered, suggesting that it may cause embryo lethality. By contrast, fca fy-1 and fca fpa double mutants are viable. Analysis of plants heterozygous for fy-1 but homozygous for fpa led to a high incidence of aborted seed and when these plants were crossed reciprocally with Ler it became clear that both fy and fpa cause weak gametophytic defects which, when combined together, cause synergistic lethality (Henderson et al., 2005).
A likely model for how FCA and FY regulate FLC is through a similar mode of action to that by which they regulate FCA. However, only one FLC transcript accumulates to significant levels in Arabidopsis seedlings. So if FCA/FY promote polyadenylation at a proximal site the resultant transcript is rapidly degraded. The mode of action of FCA/FY on FLC is being investigated using a suppressor mutagenesis approach where the FCA cDNA has been over-expressed from a 35S promoter. The resultant early-flowering line was mutagenized and late-flowering individuals identified (V Quesada, F Liu, C Dean, unpublished data). Analysis of the genes identified, together with molecular analysis of low abundance FLC transcripts, should reveal the molecular mechanism involved.
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Additional roles for the autonomous promotion pathway |
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TopAbstractIntroductionThe floral repressor, FLCRepression of FLC by...FCA interaction with FY...Additional roles for the...ConclusionReferences |
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The current view of the autonomous promotion pathway is a series of semi-redundant sub-pathways which, based on the embryo lethality phenotype of null fy mutants and the observation that mutations in FVE have also been identified in screens for cold stress signalling (Kim et al., 2004), are unlikely to be floral specific. In order to define the activities of this pathway further, a microarray analysis was undertaken comparing wild-type and fca mutant seedling gene expression. A previous microarray analysis had used a custom array of 13 000 genes (Wilson et al., 2005). This analysis examined all the mutants of the autonomous pathway plus members of the vernalization and photoperiod pathways. The overall conclusion was that there were very few changes in gene expression in the mutants and the genes that did change were involved in defence and metabolism. It was decided to repeat some of the array experiments using the commercially available and widely used Affymetrix Arabidopsis 8k microarrays. These provide an excellent opportunity to examine a large fraction of the Arabidopsis transcriptome simultaneously and compare experiments between many laboratories (Schmid et al., 2005; Zimmerman et al., 2005). However, data created in microarray experiments are susceptible to influences from plant growth conditions, RNA handling, and hybridization. A commonly implemented method to ensure generation of reliable data is to use duplicates or triplicates of the same but independently obtained samples. To test which of the observed changes are shared by the replicates, the data can be subjected to a principal component analysis or a condition tree analysis, both features in Genespring software. The results were compared from eight arrays: duplicates of Columbia, fca-9 (a Col fca allele), Ler, and fca-1 (the strongest Ler allele). Using the tests to study the comparability of the microarrays analysed, a batch effect became obvious. Instead of grouping as expected according to their genotypes, the similarity of the datasets was mostly determined by the experiment date. This led to the formation of four major correlation groups (CGs) in the condition tree analysis. The observation that there was a wild-type control and an fca mutant microarray within each of the CGs gave the potential to improve the data and circumvent the batch effect problem. It was reasoned that if the batch effect superimposes the expression differences caused by the genotype and leads to the observed grouping by date, it might be possible to extract the interesting, overlaid genotypic differences using a three step mechanism. First, the comparison between fca and wild-type within each separate CG was regarded as a way to subtract a vast amount of the superimposed changes and to deliver the first two subsets of 1.5-fold up- and down-regulated gene lists. This was followed with the identification of those genes which were shared within the two 1.5-fold up- and down-regulated gene lists obtained for each of the two ecotypes examined (CG 1 and 3 are in Ler, CG 2 and 4 are in Col-0). This produced four gene-lists; 1.5-fold up- and down-regulated for each ecotype, comprising each between 400 and 600 genes. Since an fca mutation shows a similar phenotype in both Col-0 and Ler, it was reasoned that it would be appropriate to assume similar transcript changes across the accessions. Therefore it was decided to check the gene-lists obtained in step two for shared up- and down-regulated genes across the accessions as the third step. In theory, the analysis of accession-independent transcriptome changes is a strength of the research because a more general regulatory network can be identified. Confidence was gained in the approach because two genes known to be affected by fca, FLC and SOC1, were consistently found in their respective gene lists after each step. Our final gene lists comprised 31 up- and 37 down-regulated genes in fca mutant versus wild-type plants (Tables 2, 3).
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The expression profile of these genes was validated by RNA gel blots. Primers were designed against the known Col-0 cDNA sequence to obtain specific DNA probes for 21 of the 68 differentially regulated genes. Twelve were successfully analysed and despite the strategy aimed at identifying genes mis-expressed in both Ler and Col-0 the only changes in gene expression that could be confirmed in both Ler and Col-0 were FLC and SOC1. The observed pattern of bands obtained with the SOC1 specific probe inversely correlates with the FLC abundance and is highest in flc mutants and in the 35S::FCA
overexpressing line (Fig. 3).
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Several other changes in gene expression could be confirmed, but only in an accession-specific manner. The genes encoding subtilase, PPR, DNA repair, and the RING-finger protein (Table 2) showed the expected RNA abundance patterns in Col-0 and fca-9 (Fig. 2), whereas changed SAC1 expression was confirmed in a Ler/fca-1 comparison (Table 3, data not shown). For the other probes analysed, RAD50, expressed Protein (At4g19970), PAP1, similar to FAR1, and ATRPAC14 (Tables 2, 3) the pattern of expression predicted from the arrays was not verified (data not shown). The observed accession-specific differences were unexpected given the analysis designed to identify regulatory patterns shared by both accessions. It is possible that the observed batch effect was too large to be overcome with the methods used or that differences in the genomic sequence between the two accessions interfered with the comparison both during hybridization of the microarray and validation on the northern blots.
The aim of the microarray experiments was to identify FCA targets that are required for FLC regulation or are direct targets independent of FLC. Therefore the expression of the Col-0 verified genes was compared in fca-9 and fca-9 flc-3. If the expression was the same in both, it was reasoned that the gene was a candidate we were interested in and was not dependent on FLC function. The genes encoding subtilase, PPR, DNA repair, and RING-finger proteins were equally down-regulated in fca-9 and the fca-9 flc-3 and this misregulation was not observed in flc-2 (Fig. 3). These genes may function downstream of FCA, but upstream of FLC or they may be FCA targets that do not play a role in flowering time regulation. Analysis of the phenotypes of knock-outs of these genes will help elucidate this. The four genes were down-regulated in the fca mutant suggesting that, unlike the situation for FLC, FCA may promote their expression. However, it was not known if these effects are direct.
Transcript levels of the four validated genes were examined in a Col-0 fy mutant background (fy-2) (Fig. 3). The down-regulation in fy-2 of all four FCA targets is consistent with FCA and FY functioning together in vivo to regulate these transcripts, but again, these effects may not be direct. Taken together, these findings point towards a model in which FCA and FY share multiple targets in vivo and play a more general role in gene expression than just regulating FLC.
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Conclusion |
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TopAbstractIntroductionThe floral repressor, FLCRepression of FLC by...FCA interaction with FY...Additional roles for the...ConclusionReferences |
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Mutants of Arabidopsis thaliana that flower late in long and short day photoperiods and whose phenotype can be corrected by vernalization, have led to the identification of genes functioning in the autonomous promotion pathway. The pathway functions to repress expression of the floral repressor FLC. However, during the cloning and biochemical analysis of some of the autonomous promotion pathway components a more general cellular role for some of the components has emerged. It is possible that, since FLC acts as a quantitative repressor, any changes in its expression would have phenotypic consequences, so general regulators would be identified as specific flowering time regulators. The microarray analysis described here has provided insight into the additional targets of the autonomous promotion pathway. Their analysis will further define the functional relationship of some of the autonomous promotion pathway mutants and continue to test the notion that the pathway has more general functions than flowering time control alone.
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Acknowledgements |
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We thank Mervyn Smith for looking after the Arabidopsis plants so beautifully, Professor Maarten Koornneef for providing so many mutants, Dr Clare Lister for help in the laboratory and Amelia Green for helpful comments on the manuscript. This work was supported by BBSRC grant 208/D14003 and an EC Marie Curie Training Fellowship programme to JIC.
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Footnotes |
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* Present address: CSIRO Plant Industry, PO Box 350, Glen Osmond, SA 5064, Australia.
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TopAbstractIntroductionThe floral repressor, FLCRepression of FLC by...FCA interaction with FY...Additional roles for the...ConclusionReferences |
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