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First published online April 16, 2008; 10.1104/pp.107.115634 Plant Physiology 147:707-718 (2008) © 2008 American Society of Plant Biologists OPEN ACCESS ARTICLE
Two GATA Transcription Factors Are Downstream Effectors of Floral Homeotic Gene Action in Arabidopsis1,[W],[OA]Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, Connecticut 06520–8104
Floral organogenesis is dependent on the combinatorial action of MADS-box transcription factors, which in turn control the expression of suites of genes required for growth, patterning, and differentiation. In Arabidopsis (Arabidopsis thaliana), the specification of petal and stamen identity depends on the action of two MADS-box gene products, APETALA3 (AP3) and PISTILLATA (PI). In a screen for genes whose expression was altered in response to the induction of AP3 activity, we identified GNC (GATA, nitrate-inducible, carbon-metabolism-involved) as being negatively regulated by AP3 and PI. The GNC gene encodes a member of the Arabidopsis GATA transcription factor family and has been implicated in the regulation of chlorophyll biosynthesis as well as carbon and nitrogen metabolism. In addition, we found that the GNC paralog, GNL (GNC-like), is also negatively regulated by AP3 and PI. Using chromatin immunoprecipitation, we showed that promoter sequences of both GNC and GNL are bound by PI protein, suggesting a direct regulatory interaction. Analyses of single and double gnc and gnl mutants indicated that the two genes share redundant roles in promoting chlorophyll biosynthesis, suggesting that in repressing GNC and GNL, AP3/PI have roles in negatively regulating this biosynthetic pathway in flowers. In addition, coexpression analyses of genes regulated by AP3, PI, GNC, and GNL indicate a complex regulatory interplay between these transcription factors in regulating a variety of light and nutrient responsive genes. Together, these results provide new insights into the transcriptional cascades controlling the specification of floral organ identities.
The floral homeotic APETALA3 (AP3) and PISTILLATA (PI) genes encode MADS-box transcription factors that are necessary for specifying petal and stamen identity in Arabidopsis (Arabidopsis thaliana; Bowman et al., 1989  ; Jack et al., 1992, 1994; Krizek and Meyerowitz, 1996). They have been shown to act as obligate heterodimers in binding to DNA, and likely act as components of higher order transcriptional complexes in conjunction with other MADS-box proteins (Goto and Meyerowitz, 1994; McGonigle et al., 1996; Riechmann et al., 1996a; Honma and Goto, 2001). Presumably each distinct MADS-box protein complex directs the development of a specific organ type through regulating the transcription of downstream target genes, although the exact mechanism by which this occurs is unknown (Jack, 2001).
A number of studies have been carried out to identify candidate downstream target genes regulated by MADS-box transcription factors. Global gene expression profiling methods have led to the identification of many genes whose transcription is regulated by AP3 or PI (Sablowski and Meyerowitz, 1998 In this study we have screened for genes that are targets of AP3/PI action using an inducible AP3 transgenic construct. One such gene is At5g56860, GNC (GATA, nitrate-inducible, carbon-metabolism involved), whose expression profile decreased 2.8-fold after AP3 induction. We also found that a paralog of GNC, GNL (At4g26150), is negatively regulated by AP3/PI. These data lend support to the idea that AP3/PI may have important roles in negative as well as positive regulation of downstream target genes.
GNC and GNL belong to a family of 29 genes encoding GATA transcription factors in Arabidopsis (Riechmann et al., 2000 Here we show that GNL is partially redundant with GNC in regulating chlorophyll biosynthesis and in the transcription of a number of GATA-motif-containing target genes. Furthermore, we show that GNC and GNL are both directly and negatively regulated by AP3/PI in petals and stamens. These observations suggest that AP3/PI function in part to repress GNC and GNL in these organs, resulting in the down-regulation of chlorophyll biosynthesis in petals and stamens. Furthermore, we examine the regulatory interplay between these MADS-box and GATA transcription factors, and reveal a complex network of regulatory interactions in the control of a variety of light- and nutrient-responsive genes.
Identification of GNC and GNL as Targets of AP3 and PI
To identify genes regulated by AP3/PI, we carried out microarray experiments using an Arabidopsis whole genome GeneChip array (ATH1 GeneChip; Affymetrix) in conjunction with an inducible AP3-GR system. In this system, the AP3 protein is translationally fused to the rat glucocorticoid receptor; the fusion protein is rendered inactive because it is trapped in the cytoplasm through binding to heat shock protein hsp90 (Sablowski and Meyerowitz, 1998 RNA was extracted from inflorescences at 0 and 4 h after dex or a mock treatment and used as probes for our microarray experiments. Three biological replicates of each were hybridized to Affymetrix ATH1 arrays. We used the Affymetrix Microarray Suite software (MAS 5.0) to identify genes whose expression profiles changed only after dex treatment and are likely targets of AP3/PI. Thus, we eliminated genes whose expression profiles changed in the same direction after both dex and mock treatments and retained 283 genes that changed only in 0-h versus 4-h dex-treated samples and are potential targets of AP3/PI (Supplemental Tables S1–S3). Of these 283 genes, 100 genes were up or down-regulated at least 2-fold in two out of three replicates (Supplemental Table S4). To verify our microarray data, we chose 34 candidate genes that had a significant P value (<0.05), changed at least 2-fold in all three replicates, and/or belonged to a small gene family (Supplemental Table S4).
For all 34 genes, reverse transcription (RT)-PCR analyses corroborated the direction of fold change in 0-h versus 4-h dex and 0-h versus 4-h mock microarray experiments (data not shown). Because dex treatment should induce AP3 activity, genes that are up-regulated after dex treatment should be positively regulated by AP3/PI and genes that are down-regulated should be repressed. To determine if these 34 genes were potential targets of AP3/PI, we monitored their expression patterns in ap3-3 and pi-1 mutant plants compared to wild type by RT-PCR (data not shown). We confirmed 18 genes as putative targets of AP3/PI (Supplemental Table S5). One such gene was At5g56860 (GNC). GNC encodes a member of the GATA transcription factor family that has been implicated in regulating carbon and nitrogen metabolism and in promoting chlorophyll biosynthesis (Bi et al., 2005
Our microarray data indicated that GNC expression was down-regulated 2.8-fold after AP3 induction, suggesting that AP3/PI may negatively regulate GNC. RT-PCR data corroborate the microarray data such that GNC expression decreases 4 h after dex treatment of AP3-GR plants and increases in ap3-3 and pi-1 mutant flowers as compared to wild type (Fig. 1
). The most closely related paralog of GNC is At4g26150 (Reyes et al., 2004
We used ChIP to determine if GNC and GNL are direct targets of AP3/PI. It has been shown that the AP3/PI heterodimer can bind to a 10-bp conserved DNA region called the CArG box (CC(A/T)6GG; Schwarz-Sommer et al., 1992 ; Riechmann et al., 1996b; Hill et al., 1998). Using RSA tools software we identified a CArG-like box present in each of the promoter regions of GNC and GNL (Fig. 2A
). As a positive control, we assayed for binding to CArG box 3, a known autoregulatory region in the AP3 promoter (Fig. 2A; Hill et al., 1998). We extracted nuclei from wild-type and 35S::PI-HA epitope tagged transgenic plants and immunoprecipitated with either anti-HA antibody or normal mouse serum. For ChIP PCR, we used primers designed around each CArG-like box to monitor enrichment. We detected a 3.1-fold enrichment of a 354-bp fragment in the GNC promoter region that contains the CArG-like box in 35S::PI-HA extracts precipitated with anti-HA antibodies as compared to normal serum controls (Fig. 2, B and C). Thus, GNC is bound by PI protein, suggesting that GNC is a direct target of AP3/PI. We also detected a specific 2.0-fold enrichment of a 216-bp region spanning the CArG-like box present in the GNL promoter, suggesting that GNL may also be a direct target of AP3/PI (Fig. 2, B and C). As expected, we detected significant enrichment of the CArG box 3 region of the AP3 promoter in anti-HA immunoprecipitated DNA from 35S::PI-HA plants while no enrichment was detected for the promoter regions of our negative controls, PI (an indirect target of AP3/PI) or AST101 (a root-specific gene not regulated by AP3/PI; Fig. 2, B and C).
GNC and GNL Have Roles in the Leaves and Flowers GNC and GNL are both expressed most strongly in the cauline and rosette leaves of wild-type plants and to a lesser extent in the flowers, siliques, and stems (Fig. 3A ). To further characterize these expression patterns in the flower, we carried out in situ hybridizations. These data indicated that in young stage 3 flowers, GNC expression is detected throughout the floral bud (Fig. 3B). By stage 6, GNC expression is largely restricted to the inner whorls of the flower, specifically the petals, stamens, and carpels (Fig. 3C). In older flowers, from stage 8 onward, GNC expression is detectable in the petals, stamen filaments, and carpels with weaker expression in the anthers of the stamens (Fig. 3, D and E). Thus, AP3/PI may repress strong GNC expression in the anthers at later stages. The expression pattern of GNL overlaps with that of GNC, suggesting that the two genes may share redundant functions. GNL expression is first detected in at stage 3 throughout the entire floral bud (Fig. 3F). By stage 6, strongest expression is restricted to the inner three whorls (Fig. 3G). As the flower matures, GNL expression in the stamens decreases compared to the expression in the petals and carpels, suggesting that AP3/PI may repress GNL in the stamens (Fig. 3, H and I).
To explicitly test whether AP3/PI repress GNC and GNL expression in a spatially limited manner, we examined the expression domains of these genes in ap3-3 and pi-1 mutant flowers. The ap3-3 and pi-1 mutants display similar homeotic phenotypes, in which petals are transformed into sepalloid organs and stamens are transformed into carpeloid organs. Consistent with a role in modulating the overall levels of expression of GNC and GNL, expression of each gene was detectable in the inner three whorls, including third-whorl tissues, of ap3-3 and pi-1 flowers (Fig. 3, J–M).
Analyses of T-DNA insertional mutations in both GNC and GNL indicated that they have partially redundant roles in chlorophyll biosynthesis. T-DNA insertional mutations for each gene were obtained from the SALK collection (Alonso et al., 2003
Regulation of Sugar-Sensing Genes
Based on transcriptional profiling, it has been proposed that GNC regulates genes involved in carbon metabolism and sugar sensitivity (Bi et al., 2005
Surprisingly, the expression pattern of AtSTP13 in gnc and gnl mutants varied in the leaves compared to the flowers. In the leaves, AtSTP13 expression decreased significantly in the leaves of gnc and gnl single and double mutants (Fig. 5, A and B). However, AtSTP13 expression increased in the flowers of gnc and gnl single and double mutants, suggesting that GNC and GNL differentially regulate AtSTP13 in different parts of the plant (Fig. 5, A and C; Supplemental Fig. S1, B and E). Based on AtSTP13 promoter::reporter gene fusions that show expression in multiple senescing tissues as well as specifically in the vasculature of young petals, AtSTP13 has been suggested to have a role in regulating petal development (Norholm et al., 2006 ). In situ hybridizations indicate that AtSTP13 is highly expressed in the anthers at later stages of flower development (Supplemental Fig. S1, A and D). Together, these results suggest that the differential expression of AtSTP13 in petals and stamens may reflect flower-specific AP3/PI dependent regulation. To further define the AP3/PI pathway, we tested if HXK1, HXK2, AtSTP13, and AtPLT6 expression was altered in either ap3-3 and pi-1 or 35S::AP3 and 35S::PI mutant flowers as compared to wild type. Our data indicate that in the flower, AP3/PI negatively regulate GNC and GNL and that GNC and GNL negatively regulate HXK1 and AtSTP13 in flowers and positively regulate AtPLT6 expression. Thus, we would expect HXK1 and AtSTP13 expression to decrease while AtPLT6 expression should increase in ap3-3 and pi-1 mutant flowers. HXK2 expression should remain unchanged because it is not regulated by GNC or GNL. In agreement with our predictions, we found that HXK1 and AtSTP13 expression decreased significantly in ap3-3 and pi-1 mutants while HXK2 expression remained unchanged (Fig. 6, A and C ). However, we found AtPLT6 expression also decreased significantly in the mutants (Fig. 6, A and C). In 35S::AP3 and 35S::PI plants, HXK1 and AtSTP13 expression increased as predicted, while HXK2 expression remained unchanged (Fig. 6, A and B). AtPLT6 expression, however, also increased in 35S::AP3 and 35S::PI plants (Fig. 6, A and B). Although the expression pattern of AtPLT6 differs from our predictions, these results could indicate that there exists a more complicated regulatory pathway controlling the expression of this sugar-transporter gene, such as input from regulatory factors independent of AP3/PI. Thus, it appears that AP3/PI have roles in regulating genes involved in sugar metabolism and sensing through the direct regulation of GNC and GNL, but that other unidentified regulatory factors are also likely to be involved.
GNC and GNL Regulate Genes Previously Identified as AP3/PI Targets
Because our data indicate that GNC and GNL are regulated by AP3/PI in flowers, genes downstream of GNC and GNL should also be part of the AP3/PI pathway. Using microarray analyses, Bi et al. (2005) To determine the regulatory hierarchies controlling the expression of these five genes, we assayed their expression in various mutant combinations. First we tested if the expression of these five genes is altered in the leaves and flowers of gnc and gnl single and double mutants (Fig. 7, A–C ). Using RT-PCR, we found that the expression of At2g29350 in the leaves and flowers decreased significantly in both gnc and gnl mutants and was nearly undetectable in gnc;gnl double mutants. At4g35770 expression decreased significantly in the leaves and flowers of gnc mutants and was nearly abolished in gnl single and gnc;gnl double mutants (Fig. 7, A–C; Supplemental Fig. S1, C and F). At1g57990 expression decreased significantly in the leaves and flowers of gnc and gnc;gnl double mutants but to a lesser extent in the leaves and flowers of gnl single mutants. At4g30270 expression was significantly decreased in the leaves and flowers of gnc and gnl single and double mutants. In the leaves, At2g15890 expression decreased significantly, while in the flowers At1g15890 expression increased in the gnc, gnl, and gnc;gnl double mutants. Thus, GNC and GNL share partially redundant roles in regulating At2g29350, At4g35770, At4g30270, At1g57990, and At2g15890 expression in the leaves and flowers. Furthermore, GNC and GNL differentially regulate At2g15890 in the leaves versus the flowers.
Next we wanted to confirm that At2g29350, At4g35770, At1g57990, At4g30270, and At2g15890 expression is regulated by AP3/PI. Microarray data suggests that in the flower, At2g29350, At4g35770, At4g30270, and At2g15890 expression is positively regulated by AP3/PI (Zik and Irish, 2003 ; data not shown). Thus, expression of these genes should decrease in ap3-3 and pi-1 mutants compared to wild type. We found that expression of all four genes did decrease significantly in these mutants (Fig. 8, A and C
). On the other hand, if these genes are positively regulated by AP3/PI we would expect their expression to increase in 35S::AP3 and 35S::PI transgenic plants compared to wild type. We found that the expression of all five genes did increase in the transgenic flowers, further supporting the idea that these genes are positively regulated by AP3/PI (Fig. 8, A and B).
The RT-PCR data described above support the idea that these five genes are regulated by AP3/PI as well as by GNC and GNL. However, we found that in the flower AP3/PI negatively regulate GNC and GNL, which in turn positively regulate At2g29350, At4g35770, At1g57990, and At4g30270, and negatively regulate At2g15890 expression. In this simple scenario, AP3/PI should negatively regulate At2g29350, At4g35770, At1g57990, and At4g30270, and positively regulate At2g15890 expression. As expected, we found that At2g15890 expression was positively regulated by AP3/PI (Fig. 8). However, we also found that At2g29350, At4g35770, At1g57990, and At4g30270 expression was positively regulated by AP3/PI. This inconsistency was also found for AtPLT6 expression as described earlier. Thus, the AP3/PI regulatory pathway controlling At2g29350, At4g35770, At1g57990, and At4g30270 expression must involve input from additional unidentified factors or be independent of GNC and GNL.
A Gene Regulatory Network Controlled by AP3/PI
Through a microarray-based screen for downstream targets of AP3/PI, we identified GNC as a gene that is negatively regulated by AP3/PI. We also found that AP3/PI negatively regulate the paralog of GNC, GNL, suggesting that AP3/PI may have important roles in down-regulating many genes to ensure the proper development of petals and stamens. We have also shown by ChIP that AP3/PI can bind to CArG-like boxes present in the GNC and GNL promoters, suggesting that AP3/PI act to directly regulate the transcription of these targets. AP3/PI could be acting as transcriptional repressors through recruiting specific corepressors to transcriptional complexes at these promoters, or through affecting histone modifications of the promoter regions. The MADS domain proteins AP1 and SEPALLATA3 have been shown to act as components of transcriptional repression complexes through interactions with specific corepressor proteins (Sridhar et al., 2006
Microarray-based expression analyses have been informative in identifying targets of AP3/PI (Zik and Irish, 2003 Surprisingly, the characterization of the expression patterns of these genes in various mutant and transgenic backgrounds revealed that their regulation was more complex than would be expected. Three genes, HXK1, AtSTP13, and At2g15890, are negatively regulated by GNC and GNL, and positively regulated by AP3 and PI; these observations can be explained by a simple linear pathway of negative regulation (Fig. 9 ). However, it is clear that AtSTP13 and At2g15890 are differentially regulated in vegetative tissues because their expression is dependent on GNC and GNL activity in leaves. The other five genes, AtPLT6, At1g57990, At2g29350, At4g30270, and At4g35770, are positively regulated by GNC and GNL in flowers as well as leaves. However, their expression in flowers is also positively regulated by AP3/PI. This points to the possibility that additional factors play a role, either through modulating GNC and GNL activity, or independently thereof, in regulating the expression of these genes in floral tissues.
AP3/PI Regulate Pathways Required for Nitrogen Metabolism, Sugar Sensing, and Photosynthesis
We have shown that GNC and GNL expression levels are negatively regulated by AP3/PI in flowers, likely through direct transcriptional repression. GNC and GNL are the only two out of 30 GATA transcription factors that were found to be nitrate inducible (Wang et al., 2003 The negative regulation of GNC and GNL by AP3/PI implies that chlorophyll levels are regulated in part by these floral homeotic MADS-box gene products. Our in situ data indicates that GNC and GNL are expressed strongly in the petals, stamen filaments, and the carpels, and to a lesser extent in the anthers of the stamens. GNC and GNL expression appears to be regulated by AP3/PI because ap3 and pi mutants show higher levels of expression of GNC and GNL. This is consistent with a model whereby AP3/PI, presumably in conjunction with tissue-specific factors, regulates expression of these GATA transcription factors in particular floral tissues, including the stamens.
AP3/PI, GNC, and GNL all positively regulate the expression of At4g30270, which encodes a putative endoxyloglucan transferase, an enzyme that modifies xyloglucan, which is a major structural component of the plant cell wall (Campbell and Braam, 1999
Additionally, AP3/PI may have roles in regulating senescence because senescence is delayed in ap3-3 and pi-1 mutants compared to wild type (Zik and Irish, 2003 Together, these results indicate that AP3/PI can act to regulate transcriptional cascades that in turn are necessary for integrating energy requirements with developmental and environmental signals to promote appropriate floral organ type differentiation.
Plant Material and Growth Condition
Arabidopsis (Arabidopsis thaliana) plants were grown on 12:3:1 mix of vermiculite:soil:sand at 22°C under long-day conditions (16-h-light/8-h-dark cycle). The mutant lines (ap3-3 and pi-1) and transgenic lines (ap3-3; 35S::PI; 35S::AP3-GR [AP3-GR]; 35S::AP3; and 35S::PI-HA) are in the Landsberg erecta background. The SALK T-DNA insertion lines (SALK 001778 and SALK 21362C) are in the Columbia background. The AP3-GR line was a gift from Robert W.M. Sablowski (John Innes Centre, Norwich, UK; Sablowski and Meyerowitz, 1998
Floral buds from 35S::AP3-GR, 35S::PI, ap3-3 plants were treated with dex (0.015% silwet, 0.1% ethanol, and 5 µM dex) or mock (0.015% silwet and 0.1% ethanol), collected at 0 and 4 h, and snap frozen in liquid nitrogen. Total RNA was extracted using Trizol (GibcoBRL) according to the manufacturer's instructions and purified using the Qiagen Rneasy kit (QIAGEN). Labeled complementary RNA was hybridized to the Affymetrix ATH1 GeneChip arrays (Affymetrix). Hybridization signals were detected using the Agilent GeneArray scanner and quantified by the Microarray suite software (MAS 5.0; Affymetrix). For comparisons, the overall intensity of each probe set on the array was scaled to a target intensity value of 500.
Total RNA was extracted from plant tissue using Trizol (GibcoBRL) according to the manufacturer's instructions. Complementary DNA was synthesized using Superscript III Rnase reverse transcriptase (Invitrogen) according to the manufacturer's instructions. RT-PCR quantification was done using the ImageJ software (rsb.info.nih.gov/ij/) and RT-PCR products were normalized to an actin control. The gene-specific primers used to analyze expression are listed in Supplemental Table SVI.
Nuclear extracts were prepared using MC, M1, M2, and M3 buffers as described in Ito et al. (1997)
In situ probes were generated by PCR amplification of complementary DNA using gene-specific primers containing T7 RNA polymerase-binding sites. T7 RNA polymerase (New England Biolabs) was used to transcribe digoxygenin-labeled UTP (Roche) probes. Tissue was fixed in 4% paraformaldehyde (Sigma) and embedded in Paraplast X-tra (Monoject Scientific). Sections (8 µm) were fixed to Probe-on-Plus slides at 42°C (Fisher Scientific). Procedures for in situ prehybridization, hybridization, and detection were performed as described previously (Carr and Irish, 1997
Homozygous SALK lines were identified by PCR genotyping for the presence of the T-DNA insertion. RNA was extracted from homozygous plants using the Trizol reagent (GibcoBRL) according to the manufacturer's instructions. RT-PCR analysis, as described above, was used to check for abolishment of the transcript. The primers used to verify SALK 001778 (GNC) and SALK 21362C (GNL) lines are listed in Supplemental Table S5.
Tissue was snap frozen in liquid nitrogen and then chlorophyll was extracted using 80% acetone as described in Lichtenthaler, 1987. Absorbance was measured at 645 and 657 nm and chlorophyll content was calculated using: (20.2 x A645 + 8.02 x A657)/g fresh weight. Microarray data from this article have been deposited with the NCBI Gene Expression Omnibus data repository (http://www.ncbi.nlm.nih.gov/geo/) under accession number GSE9702.
The following materials are available in the online version of this article.
Received December 28, 2007; accepted April 11, 2008; published April 16, 2008.
1 This work was supported by the National Science Foundation (grant no. IOS–0516789 to V.F.I.).  The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Vivian F. Irish (vivian.irish{at}yale.edu).
[W] The online version of this article contains Web-only data.
[OA] Open Access articles can be viewed online without a subscription. www.plantphysiol.org/cgi/doi/10.1104/pp.107.115634 * Corresponding author; e-mail vivian.irish{at}yale.edu.
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-HA antibody (HA) or normal serum (N). C, Quantified enrichment levels in the GNC, GNL, AP3, PI, and AST101 promoters. Black bars represent 35S::PI-HA samples immunoprecipitated with 
