Flower Development Pathways
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1 Developmental Leading to Flowering Flower Development s meristem Inflorescence meristem meristems organ identity genes Flower development s to Flowering Multiple pathways ensures flowering will take place Precisely regulate flowering Cross pollination Favorable environmental conditions External s to Flowering - Summary response to length of day or night. allows events to occur at a particular time of year promotion of flowering by cold temperature. Autonomous Flowering in response to strictly internal factors such as age or size. Autonomous Hormonal Repressor Internal Hormonal Induction of flowering by plant hormones. Gibberellic acid is a key hormone. Repressor Inhibition of flowering. s to Flowering Genes s to Flowering Leaf & Phloem Genes FD AP1 Ft from leaf FD FD gene produces FD leucine zipper transcription factor. Location meristem only Ft/FD Ft/FD complex in shoot meristem. Activates floral genes like Apetala1 and meristem identity gene Key floral meristem identity gene. Gene product = MADS box-containing transcription factor. Integrates signals from many pathways. transcription factor activates floral homeotic genes for floral organ development. Positive feedback loop with AP1. gene encodes a MADS domain that acts as a repressor of flowering. has a central role in regulating the response to vernalization. CO CONSTANS gene in phloem of leaves. produces a transcription factor stimulating downstream expression of FT. FT Flowering Locus T gene. Downstream target of CO gene product. Stimulates flowering Expressed in phloem of leaf or apical meristem. Phloem-mobile mrna = floral stimulus moves from leaf phloem shoot apex. RAF kinase inhibitor initiates kinase cascade in gene regulation. FD FD gene. Located in phloem at shoot apex. FD interacts with Ft in shoot meristem. FD = leucine-zipper transcription factor. Clock Genes allow plant to determine day length. 1
2 Outline Measuring days and seasons 1. Biological Clock & Clock Genes circadian rhythms measuring the time of day for events to occur Circadian Rhythms & Biological Clocks respiration photosynthesis leaf & petal movements spore production in fungi pupal emergence in fruit flies 2. detecting day length & seasonal responses 3. Phytochromes & photomorphogenesis Video Biological Clock Circadian rhythm rhythmic behavior every 24 hours. allows plants to determine time of day Characteristics of circadian rhythms rhythms continue to be expressed in darkness based on internal pacemaker endogenous oscillator Defined by period, phase & amplitude Circadian rhythm parameters Period time between max or min points. Phase any point recognized by its relationship to rest of the cycle. Amplitude distance from peak to trough. How do responses remain on time when daily durations of light and darkness change with seasons how does entrainment occur? Entrainment = synchronizing effect of light at daybreak. 24hr entrainment reverts to 26hr cycle in continuous darkness. ± 26hr cycle = free-running period characteristic of species. Rephased cycle with light pulse during darkness. Light pulse early in dark cycle light pulse interpreted as end of previous day. rhythm delayed Light pulse late in dark cycle light pulse interpreted as beginning of next day. rhythm accelerated Molecular basis of circadian endogenous oscillator Elements of the circadian endogenous oscillator 1) Circadian cycles 24 hours when entrained, otherwise 26 hrs ± 2) Endogenous because it persists in the absence of external factors. 3) Oscillator suggests an internal pacemaker 4) Temperature compensation unaffected by temperature 5) Gene Regulation several genes all regulatory s transcription translation positive & negative feedback loop transcription-translation products influence RNA synthesis positive feedback products turn on gene expression negative feedback products turn off gene expression loop positive & negative feedback cycles from day to night Genes Clock Genes all produce regulatory transcription factors (s) = CIRCADIAN CLOCK-ASSOCIATED 1 = LATE ELONGATED HYPOCOTYLS = TIMING OF CAB EXPRESSION 7) Entrainment synchronizes oscillator with morning light 8) Modulators factors that influence endogenous oscillators pigments phytochromes and cryptochromes Molecular basis of circadian endogenous oscillator Circadian Oscillator Model Light reinforcement of effect of is the underlying mechanism of entrainment. NIGHT pm DAY am & 6 gene 4 morning genes (e.g. LHCB) 5 pm 3 1 genes TIC 2 1. & accumulate at night. activates & gene expression. 2. Light activates clock genes & at dawn. Morning (red) light reinforces effect of. TIC gene modulates morning light to entrain gene to day length. 3. Clock gene & products activate morning genes (e.g. LHCB involved in chlorophyll activation) 4. Clock genes and repress gene. 5. repression causes gradual reduction in & expression. 6. Loss of & releases gene from inhibition. 2
3 DAY Molecular basis of circadian endogenous oscillator Circadian Oscillator Model NIGHT 6 4 morning genes (e.g. LHCB) TIC 2 What would happen with a loss of function mutation of or if these genes are involved in the circadian clock? What would happen with constitutive overexpression of & if these genes are involved in the circadian clock? What would happen with loss of function mutation in TIC gene? Answer: 1) Circadian rhythm abolished. Point is: Loss of function mutations or over-expression of & is strong evidence for their role in the circadian clock. & Flowering 1. Circadian clock keeps track of the time of day. 2. keeps track of day length. Plant response is to seasonal change in relative day length Short day plants Long day plants Day neutral plants 3. Photomorphogenesis light-regulated plant development 4. Phytochrome & photomorphogenesis - Effect of Latitude on Day Length & Flowering Short Day Plants Long Day Plants Light 24 hr Critical duration of darkness Dark gene DAWN Circadian Oscillation of Clock Genes gene DUSK Light-Dependent s Leading To Flowering Short-day plants Late-summer flowering Goldenrod Chrysanthemum Poinsettia Soybeans Long-day plants Early summer flowering Irises Clover Lettuce Spinach Hollyhocks Day-neutral plants Flower anytime Snapdragons Roses Tomatoes Tropical Plants & clock genes TIC gene & & genes Advantages of photoperiodic control Optimal environmental conditions Spring ephemerals flower before forest canopy develops Long day plants flower early spring and summer Short day plants flower late summer and early fall morning genes activated (e.g. LHCB) & 3
4 Photoperiodic Timekeeping Measures Duration of Darkness Short Day Plants Long Day Plants Clock Hypothesis for Photoperiodic Timekeeping 1. Photoperiodic timekeeping depends on an endogenous circadian oscillator. Oscillator is coupled to gene expression related to flowering. 2. Flowering occurs when light break (or morning light) coincides with a certain phase of an endogenous circadian oscillator. Percentage of Flowering 8hr light 64 hour Dark Period = 4 hr night break SDP soybean Night break reverses flowering Night break promotes flowering Time at which Night Break was given Flowering in SDP requires dark period of sufficient duration dawn signal at at appropriate time in the cycle Clock Hypothesis for Photoperiodic Timekeeping Circadian oscillator controls timing of light-sensitive & light-insensitive phases. FLOWERING IN SHORT DAY PLANTS Light signal given at light-sensitive phase Flowering inhibited Light signal given at light-insensitive phase Flowering promoted Maximum Flowering No Flowering Percentage of Flowering 8hr light 64 hour Dark Period = 4 hr night break SDP soybean Time at which Night Break was given Maximum Light Sensitivity since light interrupted night length & inhibited flowering of a short day plant Continued oscillation of sensitive & insensitive responsiveness to stimulus in absence of dawn or dusk light signals is characteristic of control by a circadian oscillator. What about flowering? Coincidence Model Coincidence Model Erwin Bunning (1936 & 1960) proposed control of flowering is achieved by an oscillation of phases with different sensitivities to light Circadian oscillator controls timing of light-sensitive and light-insensitive phases Promotion or inhibition of flowering depends of phase of the rhythm SDP light signal during light sensitive phase flowering inhibited LDP light signal during light sensitive phase flowering promoted Originally published in Science Express on 11 August 2005 Science 9 September 2005: Vol no. 5741, pp DOI: /science Prev Table of Contents Next RESEARCH ARTICLES This article has been retracted CONSTANS GENE (CO) key component in flowering pathway promotes flowering in Arabidopsis in long days zinc finger transcription factor co mutant was incapable of photoperiodic response CO expression controlled by a circadian clock accumulation of CO will induce flowering through activation of Flowering Locus T (FT) gene The mrna of the Arabidopsis Gene FT Moves from Leaf to Shoot Apex and Induces Flowering Tao Huang,1 Henrik Böhlenius,1 Sven Eriksson,1 François Parcy,2 Ove Nilsson1* Day length controls flowering time in many plants. The day-length signal is perceived in the leaf, but how this signal is transduced to the shoot apex, where floral initiation occurs, is not known. In Arabidopsis, the day-length response depends on the induction of the FLOWERING LOCUS T (FT) gene. We show here that local induction of FT in a single Arabidopsis leaf is sufficient to trigger flowering. The FT messenger RNA is transported to the shoot apex, where downstream genes are activated. These data suggest that the FT mrna is an important component of the elusive "florigen" signal that moves from leaf to shoot apex. 4
5 How are flowering genes related to circadian control? CO CONSTANS GENE - in phloem of leaves. produces a transcription factor stimulating downstream expression of FT. CO promotes flowering CO mrna has a circadian oscillation CO mrna & accumulates to induce flowering only during a long day. Light enhances stability of CO. Dark CO tagged with ubiquitin and degraded by proteasome. Arabidopsis -LDP CO mrna Light Alternative Consequences of Circadian Rhythm Entrainment TIC Gene Light receptor Clock Genes Circadian Rhythm Repetitive 24 hr Entrained Physiological Response e.g. epinasty Single response e.g. flowering CO FT mrna Transmissible floral stimulus Photoreceptors Phytochrome & photoreversibility Three classes of photoreceptors Photoreceptor Light sensed Functions Phytochrome Red and Far Red Seed germination Flowering Cryptochrome Blue and UVA Seedling development Flowering Phototropin Blue and UVA Differential growth Phytochrome - Photoreversibility Photoreversible control of germination Lettuce seed germination experiment imbibed for 3 hr prior to irradiation with red or far red light R = Red light 660nm for 1 minute FR = Far red light 700nm for 3 minutes Score % germination after 48h in darkness Irradiations Germination (%) R 88 R, FR 22 R, FR, R 84 R, FR, R, FR 18 R, FR, R, FR, R 72 R, FR, R, FR, R, FR 22 Explanation Pr Photochromic receptor system Two state equilibrium model Red light Far Red light Pfr Effect of Phytochrome on Internode Elongation Chenopodium album lambsquarters pigweed Chenopodium album seedling growth More Red Red:Far Red Ratio More Far Red 5
6 Phytochrome Pr & Pfr connections Phytochrome is the photoreceptor in photoperiodism Phytochrome Monitoring Changes in Natural Light Environments Phytochrome & Light Quality in the Environment Relative response LFR = Low Fluence Response FR-reversible VLFR HIR umoles light 1 umol 0.1 second under plant canopy 1000 umol 1 second full daylight Log Fluence (umol m -2 ) 1. Phytochrome enables plant adaptation to changes in light quality Red light 660nm Far red light 730nm photonfluence@660nm 2. Red:Far Red ratio = photonfluence@730nm Photon flux density required for a phytochrome response could be as low as 10-6 umol m -2 s -1 or approximately 1. 2 billionths daylight for 1 second second daylight Phytochrome Absorption Spectrum Phytochrome Structure 665nm Chromophor e 730nm Apo Chromophore open chain tetrapyrrole covalently linked to through a cysteine aa 6
7 Phytochrome Pr and Pfr are cis-trans isomers Chromophore Apo Pfr Flowering Phytochrome Mechanism of Action Pfr (phosphorylated) moves to nucleus Pfr PIF3 transcription factor G-box promoter of myb gene myb gene (clock gene) RNAs myb gene myb gene = clock gene transcription factors and & transcription factors Developmental response genes (e.g. CO) Bind to promoter regions of light-stimulated genes DNA Phytochrome response to red and far red light 665nm 730nm 1 Phytochrome synthesis 2. Conversion of Pr to Pfr in red light 3. Fates of Pfr Pfr Plant response Pfr Enzymatic destruction Pfr Slow conversion in darkness to Pr Pfr Far-red light conversion to Pr Multiple Phytochromes Exist in Plants Antagonistic Roles of Phytochrome A & B Types of Phytochrome Encoding gene phya PHYA phyb PHYB phyc PHYC and phyd PHYD phye PHYE 1. Chromophore Same in all phytochromes 2. Sources of Variation in Phytochromes Protein amino acid sequence Expressed in different tissues Expressed at different times of development Mediate different light responses 7
8 Antagonistic Roles of Phytochrome A & B s to Flowering Genes External Long-day pathway Phytochromes Cryptochrome Leaf PhyB PhyA Open Sunlight Canopy shade (Far red-rich) CO Clock genes Phychrome B mediates deetiolation Phychrome A mediates de-etiolation. Phychrome A is labile.. Plant switches to PhyB for increased stem elongation. FT mrna Ft/FD Summary: s Leading to Flowering s to Flowering External Autonomous Hormonal Repressor Internal Temperature-Dependent = promotion of flowering with a cold treatment to a fully hydrated seed/seedling. Arabidopsis - vernalization + vernalization (40 days at 4C as a seedling) Temperature-Dependent Characteristics of vernalization 1. Temperature range = 1 to 7C (temps <0C are ineffective) 2. Requires several weeks of exposure to low temperature 3. High temperature can de-vernalize up to a point 4. Active metabolism required (sugars + oxygen + DNA replication) 4. Location of receptor is the shoot apical meristem applies to seedlings and embryos 5. Developmentally vernalization means competence of vegetative meristem to transition to floral meristem 6. Usually linked to photoperiod + long days = flowering in early summer. 7. Response to chilling is epigenetic = stable change in pattern of gene expression which can be passed on to descendant cells. 8
9 Temperature-Dependent Gene related to epigenetic changes during vernalization Flowering Locus C = Wild type without vernalization Temperature-Dependent Flowering Locus C () gene is a flowering repressor highly expressed in non-vernalized SAM switched off following vernalization loss of histone modifications in euchromatin & conversion to heterochromatin (inactive DNA) is a MADS box + vernalization (40 days cold) gene expressed No vernalization mutation Ft/FD Temperature-Dependent Ft/FD MADS-box transcription factor Protein = SUPPRESSOR OF CONSTANS OVEREXPRESSION 1 Probable transcription factor active in flowering time control Integrates signals from three pathways 1) photoperiod long days in long day plants upregulate 2) vernalization cold treatments upregulate 3) autonomous floral induction gradual increase during vegetative growth. Rapidly up-regulated in apical meristems during transition to flowering. Loss-of-function mutants (T-DNA insertion) are late-flowering. Up-regulated by gibberellins s to Flowering External Autonomous Hormonal Repressor Internal Hormonal Gibberellic Acid Hormone involved in flowering required for flowering under noninductive days transported from leaves to SAM gene GAMYB influenced by GA to promote and MYB characteristics 1) large group (>120) of transcription factors regulating metabolism 2) MYB synthesis is stimulated by absence of a DELLA repressor 3) GA signals degradation of DELLA repressor GAMYB GA Activation of Gene Expression Ft/FD MYB Activated MYB promotes & expression FLOWERING 9
10 s to Flowering External Autonomous 1. No external cues 2. Plants count number of leaves Autonomous Hormonal Repressor Internal 1. No external cues 2. Plants remember Autonomous Autonomous 1. No external cues 2. Plants count number of leaves 3. Plants remember once florally determined 4. All genes expressed in meristem 5. Acts by reducing expressing of FLOWERING LOCUS Ft/FD Autonomous s to Flowering Gene Interaction in the Leaf External Gibberellic Acid and FT mrna Autonomous Hormonal Repressor Internal Hormonal 10
11 Gene Interaction at the SAM Hormonal Autonomous (Temperature) END Development 11
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