Epigenetics and Flowering Any potentially stable and heritable change in gene expression that occurs without a change in DNA sequence
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1 Epigenetics and Flowering Any potentially stable and heritable change in gene expression that occurs without a change in DNA sequence
2 Epigenetics Usually this means information coded beyond the DNA sequence, such as in covalent modifications to the DNA or modifications to the chromatin structure. Transcription Epigenetic Silencing
3 Epigenetic programming in plants helps control developmental transitions Embryonic to vegetative transition Vegetative to reproductive transition Embryonic development Vegetative development Reproductive development
4 Function Epigenetic marks and their maintenance DNA methylation Histone modifications (acetylation etc.) Epigenetic genome regulation in plants Transposon silencing Control of flowering time Developmental switches and stress responses Gene silencing in trans; paramutation Resetting the epigenome
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7 The Histone Code Histones can be modified by Acetylation (Ac) Ubiquitination (Ub) Methylation (Me) Phosphorylation (P) Sumoylation (Su) Depending on their position, these can contribute to transcriptional activation or inactivation.
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9 The histone code The N-terminal tail of histone H3 has four lysine residues K4, K9, K27 and K36 that are capable of being methylated by histone methyltransferases (HMTases) histone acetyltransferase (HAT) and histone decatylases (HDAC) Henderson and Dean (2004). Development 131:
10 Modification
11 DNA methylation DNA can be covalently modified by cytosine methylation. cytosine 5-methylcytosine Methylcytosine TTCGCCGACTAA
12 For example: H3 modifications H3 Me Me P Ac Me Ac Ac Me Me P A R T K Q T A R K S T G G K A P R K Q L A T K A A R K S The amino terminus of H3 is often modified at one or more positions, which can contribute to an activation or inhibition of transcription.
13 Different histone modifications are associated with genes Gene mrna H3K4me H3K4me is associated with actively transcribed genes and mrna. H3K9me Me-C H3K9me is associated with methylated DNA (Me-C) and transposons. Red = high correlation Green = low correlation Lippman et al., (2004). Nature 430:
14 Epigenetic controls in whole-plant processes Transposon silencing Control of flowering time Developmental switches and stress responses
15 Epigenetic programming in plants helps control developmental transitions Embryonic development Embryonic to vegetative transition Vegetative to reproductive transition Vegetative development Reproductive development
16 Epigenetic control of flowering time Prolonged cold treatment Vegetative Development Autumn Winter Reproductive Development Spring Some plants require a prolonged cold period (vernalization) - as experienced during winter, before they will flower.
17 FLOWERING LOCUS C (FLC) mutants flower early flc mutant Autumn Winter Spring FLC is an inhibitor of flowering; removing FLC removes the vernalization requirement
18 FLC inhibits FT, an activator of flowering Wild-type plant FLC FT gene Transcription of FT gene repressed by FLC binding flc mutant plant FT gene
19 Florigen: Arabidopsis protein FLOWERING LOCUS T FT is a small, globular protein that exhibits the properties that would be expected of florigen FT protein moves via the phloem from the leaves to the shoot apical meristem under inductive photoperiods. In the meristem, FT forms a complex with the transcription factor FD to activate floral identity genes
20 Multiple developmental pathways for flowering in Arabidopsis
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22 (RNA binding protein) Activate and upregulate floral meristem identity genes that execute the floral transition Encodes a homeodomain protein epigenetically, regulate FLC The level of FLC mrna is down regulated by the autonomous pathway components, FCA, FY, FLK, FPA, LD, FLD and FVE. None of these factors regulate one another at the mrna level, but instead appear to regulate FLC through different mechanisms. FCA is an RNA-binding protein that interacts with the 30-end RNA-processing factor FY to control FLC. FPA and FLK are also RNA-binding proteins, but FPA at least regulates FLC independently of FCA.
23 FLC is silenced by vernalization After 40 days at 4 C, FLC is not expressed. Ten days after return to 22 C FLC expression is still off. Autumn FLC gene transcribed Winter Spring FLC gene silenced Reprinted by permission from Macmillan Publishers, Ltd: NATURE Sung, S., and Amasino, R.M. (2004) Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3. Nature 427: Copyright 2004.
24 FLC is regulated by epigenetic modifications H2A.Z incorporation H3K4me, H3K36me H3K9Ac, H3K14Ac cold H3K9me2, H3K27me2 Autumn FLC gene transcribed Winter Spring FLC gene silenced
25 The FLC gene is epigenetically modified during vernalization P V U The FLC gene promoter (P), intron (V) and 3 UTR (U) were examined for histone modifications. Before vernalization, P and V showed activating modifications (H3Ac), and after vernalization they showed inhibitory modifications (H3K27me, H3K9me). NV = no vernalization VT0 = 40 days at 4 VT7 = 40 days at 4 followed by 7 days at 22 Sung and Amasino (2004). Nature 427:
26 The FLC gene is epigenetically modified during vernalization P V U Quantification at intron H NV = no vernalization VT0 = 40 days at 4 VT7 = 40 days at 4 followed by 7 days at 22 H3Ac H3K27me H3K9me Sung and Amasino (2004). Nature 427:
27 VIN3 is induced by vernalization Autumn VIN3 gene silent Winter VIN3 gene transcribed Spring Sung and Amasino (2004). Nature 427:
28 Holec and Berger (2012). Plant Physiol. 158: Many developmental genes and switches are epigenetically regulated
29 Resetting the epigenome FLC ON Autumn Winter FLC OFF Spring When does FLC switch on again between generations?
30 Overview on flowering pathways in Arabidopsis FLC and other FLC-related proteins repress floral integrator genes, including FT, FD and SOC1, in Arabidopsis. Upon the activation of floral integrators, the floral transition ensues. FT is induced by the photoperiod pathway through the activation of CO. FT protein is a mobile flowering signal that physically interacts with FD protein at meristem to activate SOC1 and other floral activators. Therefore, FLC and CO antagonistically determine proper timing of flowering in Arabidopsis. Two genetically independent pathways, vernalization and autonomous pathways, repress the transcription of FLC. The autonomous pathway is required for repression of FLC regardless of environment stimuli. The vernalization pathway triggers stable repression of FLC. Gibberellin, a phytohormone, independently promotes flowering through the activation of SOC1 and other floral activator genes. Arabidopsis Book (2012)
31 Vernalization-mediated acceleration of flowering Winter-annual strains of Arabidopsis flower late without vernalization (Left). Flowering of winter-annual strains of Arabidopsis is accelerated by vernalization (Right) Arabidopsis Book (2012)
32 Models of flowering time regulation by vernalization in various flowering plants Green: floral activator, Pink: floral repressor, Violet: upstream repressor of floral repressor. Arabidopsis Book (2012)
33 Pathways controlling flowering-time in Arabidopsis Henderson and Dean (2004). Development 131:
34 The flowering-time pathways control the expression of the floral pathway integrators SUPPRESSOR OF OVEREXPRESSION OF CONSTANS1 (SOC1), FT and LEAFY (LFY). These genes encode proteins that activate the floral meristem identity (FMI) genes APETALA1 (AP1), APETALA2 (AP2), FRUITFULL (FUL), CAULIFLOWER (CAL) and LFY, which convert the vegetative meristem to a floral fate. FUL may also act as a floral integrator (Schmid et al., 2004). The photoperiod, gibberellin, lightquality and ambient-temperature pathways activate floral pathway integrators. The CONSTANS (CO) transcription factor functions in the photoperiod pathway; long-day photoperiods promote flowering by circadian clock (CLOCK) dependent and independent mechanisms, which control the activity of CO. Activation of flowering is antagonised by the floral repressors encoded by (shown in green) FLOWERING LOCUS C (FLC), FLOWERING LOCUS M (FLM), TERMINAL FLOWER1 (TFL1), TERMINAL FLOWER2 (TFL2), SHORT VEGETATIVE PHASE (SVP), TARGET OF EAT1 (TOE1), TARGET OF EAT2 (TOE2), SCHNARCHZAPFEN (SNZ), SCHLAFMUTZE (SMZ) and EMBRYONIC FLOWER1/2 (EMF1, EMF2). TFL1 may also be downstream of CO, as it is induced after CO activation (Simon et al., 1996). FLC expression is controlled by a number of different pathways. The genes shown in purple, FRIGIDA (FRI), FRIGIDA-LIKE1 (FRL1), FRIGIDA-LIKE2 (FRL2), PHOTOPERIOD INSENSITIVE EARLY FLOWERING1 (PIE1), AERIAL ROSETTE1 (ART1), EARLY UNDER SHORT DAYS4 (ESD4), VERNALIZATION INDEPENDENCE3 (VIP3) and VERNALIZATION INDEPENDENCE4 (VIP4), encode proteins that promote FLC expression and delay flowering. FLC expression is downregulated in response to prolonged cold by proteins encoded by the genes (shown in blue) VERNALIZATION INSENSITIVE3 (VIN3), VERNALIZATION1 (VRN1) and VERNALIZATION2 (VRN2), and also by proteins encoded by the genes of the autonomous pathway (red): FCA, FY, LUMINIDEPENDENS (LD), FLOWERING LOCUS D (FLD), FVE, FLOWERING LOCUS K (FLK) and FPA.
35 Schematic representations of Arabidopsis plants summarizing the genetic control of vernalization requirement and response. The flowering phenotype of Arabidopsis is represented as either a rapid cycler (e.g. top right), which produces a flowering inflorescence, or as a winter annual accession (e.g. top left), which continues to produce rosette leaves. Rapid-cycling accessions do not require a vernalization treatment to flower early and are commonly used as laboratory backgrounds. By contrast, the majority of Arabidopsis accessions are winter annuals, which flower late unless they have been exposed to a prior vernalization treatment. Typically, 6 weeks of growth at 4 C produces a saturated vernalization response in Arabidopsis. Growth habit is indicated either with (+VRN) or without ( VRN) a vernalization treatment. When both FRI and FLC are active, the plant is vernalization responsive, as is found in many winter annual accessions. Mutations in either fri or flc can lead to rapid cycling. A vernalization-responsive FRI FLC accession is rendered insensitive to vernalization by a vrn mutation. Finally, a rapidcycling fri FLC genotype becomes a winter annual background in the presence of an autonomous pathway mutation such as fca. Henderson and Dean (2004). Development 131:
36 Model for the regulation of the floral repressor FLC throughout the Arabidopsis life cycle. During seedling growth, a group of genes encode proteins that function as activators of FLC expression (shown in purple); these genes include FRI, FRL1, FRL2, ESD4, ART1, PIE1, VIP3 and VIP4. These proteins may maintain FLC chromatin in an active state (indicated by an open structure and the presence of active histone tail modifications shown in green). The autonomous pathway functions antagonistically to the activators to repress FLC expression. The RNAbinding proteins FCA, FPA and FLK, and the polyadenylation factor FY, may function posttranscriptionally to achieve this and are shown in red. The FVE/FLD proteins act with a putative histone deacetylase (HDAC; all shown in orange) to promote an inactive FLC chromatin state, represented by a closed structure with inactive histone tail modifications (red). Henderson and Dean (2004). Development 131: FLC is also repressed by exposure to long periods of cold (vernalization). The proteins acting in the vernalization pathway are shown in pink. Prolonged cold induces VIN3 expression, which promotes an inactive FLC chromatin state. Subsequently, the VRN1 and VRN2 proteins are recruited to FLC, and are required for the methylation of FLC histones and the maintenance of silencing. These marks may promote the association of silencing factors with FLC chromatin that reinforce its repression. During meiosis, gametogenesis or early embryogenesis, FLC repression is overcome, thus resetting its expression in the next generation.
37 Henderson and Dean (2004). Development 131: Floral promotive genes
38 Henderson and Dean (2004). Development 131: Floral repressive genes
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