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1.  Memory of the vernalized state in plants including the model grass Brachypodium distachyon 
Plant species that have a vernalization requirement exhibit variation in the ability to “remember” winter – i.e., variation in the stability of the vernalized state. Studies in Arabidopsis have demonstrated that molecular memory involves changes in the chromatin state and expression of the flowering repressor FLOWERING LOCUS C, and have revealed that single-gene differences can have large effects on the stability of the vernalized state. In the perennial Arabidopsis relative Arabis alpina, the lack of memory of winter is critical for its perennial life history. Our studies of flowering behavior in the model grass Brachypodium distachyon reveal extensive variation in the vernalization requirement, and studies of a particular Brachypodium accession that has a qualitative requirement for both cold exposure and inductive day length to flower reveal that Brachypodium can exhibit a highly stable vernalized state.
PMCID: PMC3971174  PMID: 24723926
vernalization; flowering; Brachypodium; epigenetics; life history
2.  Two FLX family members are non-redundantly required to establish the vernalization requirement in Arabidopsis 
Nature communications  2013;4:2186.
Studies of natural genetic variation for the vernalization requirement in Arabidopsis have revealed two genes, FRIGIDA (FRI) and FLOWERING LOCUS C (FLC), that are determinants of the vernalization-requiring, winter-annual habit. In this study, we show that FLC EXPRESSOR LIKE 4 (FLL4) is essential for up-regulation of FLC in winter-annual Arabidopsis accessions and establishment of a vernalization requirement. FLL4 is part of the FLC EXPRESSOR (FLX) gene family and both are non-redundantly involved in flowering-time control. Epistasis analysis among FRI, FLL4, FLX and autonomous-pathway genes reveals that FRI fve exhibits an extreme delay of flowering compared to fri fve, but mutants in other autonomous-pathway genes do not, indicating that FVE acts most antagonistically to FRI. FLL4 may represent a new member of a FRI-containing complex that activates FLC.
PMCID: PMC3753012  PMID: 23864009
3.  ARABIDOPSIS TRITHORAX-RELATED3/SET DOMAIN GROUP2 is Required for the Winter-Annual Habit of Arabidopsis thaliana 
Plant and Cell Physiology  2012;53(5):834-846.
The winter-annual habit of Arabidopsis thaliana requires active alleles of FLOWERING LOCUS C (FLC), which encodes a potent flowering repressor, and FRIGIDA (FRI), an activator of FLC. FLC activation by FRI is accompanied by an increase in specific histone modifications, such as tri-methylation of histone H3 at lysine 4 (H3K4me3), and requires three H3K4 methyltransferases, the Drosophila Trithorax-class ARABIDOPSIS TRITHORAX1 (ATX1) and ATX2, and yeast Set1-class ATX-RELATED7/SET DOMAIN GROUP25 (ATXR7/SDG25). However, lesions in all of these genes failed to suppress the enhanced FLC expression caused by FRI completely, suggesting that another H3K4 methyltransferase may participate in the FLC activation. Here, we show that ATXR3/SDG2, which is a member of a novel class of H3K4 methyltransferases, also contributes to FLC activation. An ATXR3 lesion suppressed the enhanced FLC expression and delayed flowering caused by an active allele of FRI in non-vernalized plants. The decrease in FLC expression in atxr3 mutants was accompanied by reduced H3K4me3 levels at FLC chromatin. We also found that the rapid flowering of atxr3 was epistatic to that of atxr7, suggesting that ATXR3 functions in FLC activation in sequence with ATXR7. Our results indicate that the novel-class H3K4 methyltransferase, ATXR3, is a transcriptional activator that plays a role in the FLC activation and establishing the winter-annual habit. In addition, ATXR3 also contributes to the activation of other FLC clade members, such as FLOWERING LOCUS M/MADS AFFECTING FLOWERING1 (FLM/MAF1) and MAF5, at least partially explaining the ATXR3 function in delayed flowering caused by non-inductive photoperiods.
PMCID: PMC3345368  PMID: 22378382
ARABIDOPSIS TRITHORAX; Flowering; FLOWERING LOCUS C; Histone methylation; Winter-annual Arabidopsis
4.  A physical map of Brassica oleracea shows complexity of chromosomal changes following recursive paleopolyploidizations 
BMC Genomics  2011;12:470.
Evolution of the Brassica species has been recursively affected by polyploidy events, and comparison to their relative, Arabidopsis thaliana, provides means to explore their genomic complexity.
A genome-wide physical map of a rapid-cycling strain of B. oleracea was constructed by integrating high-information-content fingerprinting (HICF) of Bacterial Artificial Chromosome (BAC) clones with hybridization to sequence-tagged probes. Using 2907 contigs of two or more BACs, we performed several lines of comparative genomic analysis. Interspecific DNA synteny is much better preserved in euchromatin than heterochromatin, showing the qualitative difference in evolution of these respective genomic domains. About 67% of contigs can be aligned to the Arabidopsis genome, with 96.5% corresponding to euchromatic regions, and 3.5% (shown to contain repetitive sequences) to pericentromeric regions. Overgo probe hybridization data showed that contigs aligned to Arabidopsis euchromatin contain ~80% of low-copy-number genes, while genes with high copy number are much more frequently associated with pericentromeric regions. We identified 39 interchromosomal breakpoints during the diversification of B. oleracea and Arabidopsis thaliana, a relatively high level of genomic change since their divergence. Comparison of the B. oleracea physical map with Arabidopsis and other available eudicot genomes showed appreciable 'shadowing' produced by more ancient polyploidies, resulting in a web of relatedness among contigs which increased genomic complexity.
A high-resolution genetically-anchored physical map sheds light on Brassica genome organization and advances positional cloning of specific genes, and may help to validate genome sequence assembly and alignment to chromosomes.
All the physical mapping data is freely shared at a WebFPC site (; Temporarily password-protected: account: pgml; password: 123qwe123.
PMCID: PMC3193055  PMID: 21955929
Comparative genomics; polyploidy; Arabidopsis thaliana
5.  Brahma Is Required for Proper Expression of the Floral Repressor FLC in Arabidopsis 
PLoS ONE  2011;6(3):e17997.
BRAHMA (BRM) is a member of a family of ATPases of the SWI/SNF chromatin remodeling complexes from Arabidopsis. BRM has been previously shown to be crucial for vegetative and reproductive development.
Methodology/Principal Findings
Here we carry out a detailed analysis of the flowering phenotype of brm mutant plants which reveals that, in addition to repressing the flowering promoting genes CONSTANS (CO), FLOWERING LOCUS T (FT) and SUPPRESSOR OF OVEREXPRESSION OF CO1 (SOC1), BRM also represses expression of the general flowering repressor FLOWERING LOCUS C (FLC). Thus, in brm mutant plants FLC expression is elevated, and FLC chromatin exhibits increased levels of histone H3 lysine 4 tri-methylation and decreased levels of H3 lysine 27 tri-methylation, indicating that BRM imposes a repressive chromatin configuration at the FLC locus. However, brm mutants display a normal vernalization response, indicating that BRM is not involved in vernalization-mediated FLC repression. Analysis of double mutants suggests that BRM is partially redundant with the autonomous pathway. Analysis of genetic interactions between BRM and the histone H2A.Z deposition machinery demonstrates that brm mutations overcome a requirement of H2A.Z for FLC activation suggesting that in the absence of BRM, a constitutively open chromatin conformation renders H2A.Z dispensable.
BRM is critical for phase transition in Arabidopsis. Thus, BRM represses expression of the flowering promoting genes CO, FT and SOC1 and of the flowering repressor FLC. Our results indicate that BRM controls expression of FLC by creating a repressive chromatin configuration of the locus.
PMCID: PMC3061888  PMID: 21445315
6.  Repression of FLOWERING LOCUS T Chromatin by Functionally Redundant Histone H3 Lysine 4 Demethylases in Arabidopsis 
PLoS ONE  2009;4(11):e8033.
FLOWERING LOCUS T (FT) plays a key role as a mobile floral induction signal that initiates the floral transition. Therefore, precise control of FT expression is critical for the reproductive success of flowering plants. Coexistence of bivalent histone H3 lysine 27 trimethylation (H3K27me3) and H3K4me3 marks at the FT locus and the role of H3K27me3 as a strong FT repression mechanism in Arabidopsis have been reported. However, the role of an active mark, H3K4me3, in FT regulation has not been addressed, nor have the components affecting this mark been identified. Mutations in Arabidopsis thaliana Jumonji4 (AtJmj4) and EARLY FLOWERING6 (ELF6), two Arabidopsis genes encoding Jumonji (Jmj) family proteins, caused FT-dependent, additive early flowering correlated with increased expression of FT mRNA and increased H3K4me3 levels within FT chromatin. Purified recombinant AtJmj4 protein possesses specific demethylase activity for mono-, di-, and trimethylated H3K4. Tagged AtJmj4 and ELF6 proteins associate directly with the FT transcription initiation region, a region where the H3K4me3 levels were increased most significantly in the mutants. Thus, our study demonstrates the roles of AtJmj4 and ELF6 as H3K4 demethylases directly repressing FT chromatin and preventing precocious flowering in Arabidopsis.
PMCID: PMC2777508  PMID: 19946624
7.  FLOWERING LOCUS C -dependent and -independent regulation of the circadian clock by the autonomous and vernalization pathways 
BMC Plant Biology  2006;6:10.
The circadian system drives pervasive biological rhythms in plants. Circadian clocks integrate endogenous timing information with environmental signals, in order to match rhythmic outputs to the local day/night cycle. Multiple signaling pathways affect the circadian system, in ways that are likely to be adaptively significant. Our previous studies of natural genetic variation in Arabidopsis thaliana accessions implicated FLOWERING LOCUS C (FLC) as a circadian-clock regulator. The MADS-box transcription factor FLC is best known as a regulator of flowering time. Its activity is regulated by many regulatory genes in the "autonomous" and vernalization-dependent flowering pathways. We tested whether these same pathways affect the circadian system.
Genes in the autonomous flowering pathway, including FLC, were found to regulate circadian period in Arabidopsis. The mechanisms involved are similar, but not identical, to the control of flowering time. By mutant analyses, we demonstrate a graded effect of FLC expression upon circadian period. Related MADS-box genes had less effect on clock function. We also reveal an unexpected vernalization-dependent alteration of periodicity.
This study has aided in the understanding of FLC's role in the clock, as it reveals that the network affecting circadian timing is partially overlapping with the floral-regulatory network. We also show a link between vernalization and circadian period. This finding may be of ecological relevance for developmental programing in other plant species.
PMCID: PMC1525167  PMID: 16737527
8.  Defending science education against intelligent design: a call to action 
Journal of Clinical Investigation  2006;116(5):1134-1138.
We review here the current political landscape and our own efforts to address the attempts to undermine science education in Wisconsin. To mount an effective response, expertise in evolutionary biology and in the history of the public controversy is useful but not essential. However, entering the fray requires a minimal tool kit of information. Here, we summarize some of the scientific and legal history of this issue and list a series of actions that scientists can take to help facilitate good science education and an improved atmosphere for the scientific enterprise nationally. Finally, we provide some model legislation that has been introduced in Wisconsin to strengthen the teaching of science.
PMCID: PMC1451210  PMID: 16670753

Results 1-8 (8)