Plants are sessile organisms and are, consequently, exposed to a wide variety of environmental stresses, both abiotic and biotic, exerted by their surroundings. The most common of these is temperature. Within the range of temperatures tolerable to plants, the response to low temperature, particularly near-freezing temperature, is well understood. Plants have evolved a number of adaptive mechanisms to meet the challenge of low temperature. In Arabidopsis, flowering is accelerated by prolonged exposure to cold, a process called vernalization. The epigenetic silencing of the FLOWERING LOCUS C (FLC) (Michaels and Amasino 1999;Sheldon et al. 1999) is central to the vernalization process (Sung and Amasino 2005), and this silencing has been attributed to the activities of the VERNALIZATION1 (VRN1), VERNAL-IZATION2 (VRN2), and VERNALIZATION INSENSI-TIVE3 (VIN3) genes (Gendall et al. 2001;Levy et al. 2002;Sung and Amasino 2004). Cold acclimation is another well-characterized response to low temperature (Guy 1990). Plants become tolerant to freezing temperatures by being previously exposed to short periods of low but nonfreezing temperatures. Analyses of mutant plants have identified C-Repeat-binding factor (CBF)-dependent and CBF-independent signaling pathways in cold acclimation (Sharma et al. 2005), suggesting that plants use distinct mechanisms to respond to low temperature.There is increasing concern about the potential impact of global temperature changes, which significantly affect ambient temperature, on plant development. Several lines of evidence suggest that the recently observed alterations in the flowering times of many plant species and the increase in plant respiration rates are closely associated with these changes in ambient temperature (Fitter and Fitter 2002;Atkin and Tjoelker 2003). Although a great deal of progress has been made in our understanding of the regulation of plant development by low temperature, less is currently known about the molecular mechanisms underlying the responses of plants to changes in ambient temperature (Coupland and Prat Monguio 2005;Samach and Wigge 2005). Here, we show that the SHORT VEGETATIVE PHASE (SVP) gene mediates ambient temperature signaling in Arabidopsis and that the SVP-mediated control of FLOWERING LOCUS T (FT) expression is one of the molecular mechanisms evolved by plants to modulate the timing of the developmental transition to flowering phase in response to changes in the ambient temperature. Results and DiscussionAs a first step to determining the mechanism underlying the perception and transduction of ambient temperature signaling in plants, we assessed mutants in known flowering time genes for their insensitivity to changes in ambient growth temperature. Of the flowering time mutants tested, one with a lesion in svp was indeed insensitive to such changes. The flowering of the majority of these flowering time mutants was noticeably delayed at 16°C, with flowering time ratios (16°C/23°C) ranging from 1.1 to 2.0 (Fig. 1A), the exception being ld-1. However,...
CONSTANS (CO) regulates flowering time by positively regulating expression of two floral integrators, FLOWERING LOCUS T (FT) and SUPPRESSOR OF OVEREXPRESSION OF CO 1 (SOC1), in Arabidopsis (Arabidopsis thaliana). FT and SOC1 have been proposed to act in parallel pathways downstream of CO based on genetic analysis using weak ft alleles, since ft soc1 double mutants showed an additive effect in suppressing the early flowering of CO overexpressor plants. However, this genetic analysis was inconsistent with the sequential induction pattern of FT and SOC1 found in inducible CO overexpressor plants. Hence, to identify genetic interactions of CO, FT, and SOC1, we carried out genetic and expression analyses with a newly isolated T-DNA allele of FT, ft-10. We found that ft-10 almost completely suppressed the early flowering phenotype of CO overexpressor plants, whereas soc1-2 partially suppressed the phenotype, suggesting that FT is the major output of CO. Expression of SOC1 was altered in gain-or loss-of-function mutants of FT, whereas expression of FT remained unchanged in gain-or loss-of-function mutants of SOC1, suggesting that FT positively regulates SOC1 to promote flowering. In addition, inactivation of FTcaused down-regulation of SOC1 even in plants overexpressing CO, indicating that FT is required for SOC1 induction by CO. Taken together, these data suggest that CO activates SOC1 through FT to promote flowering in Arabidopsis.The phase transition to flowering in plants is precisely controlled by environmental conditions and endogenous developmental cues so that plants produce their progeny under favorable conditions. The response to multiple factors suggests the existence of a complex network regulating this phase transition in plants ( Koornneef et al., 1998). To identify genes that control the transition, mutants that showed accelerated or delayed flowering under different conditions, commonly known as flowering-time mutants, have been isolated (Redei, 1975). These mutants were grouped according to their responses to various physiological conditions and then integrated into genetic pathways to explain the control of flowering time. Four floral promotion pathways have been genetically identified in Arabidopsis (Arabidopsis thaliana): the photoperiod, autonomous, vernalization, and GA pathways . Among these pathways, genes within the photoperiod pathway, or the long-day pathway, play an important role in controlling flowering time (Komeda, 2004), since Arabidopsis is a facultative long-day plant.One of the central regulators in the photoperiod pathway is CONSTANS (CO), which encodes a nuclear protein that contains a CCT motif and two B-box-type zinc-finger domains (Putterill et al., 1995). Loss of CO function delays the phase transition, whereas gain of function of CO accelerates it, suggesting that CO positively regulates flowering time in Arabidopsis. Furthermore, CO mRNA levels show a circadian rhythm under continuous light, such that CO mRNA levels peak at night and are reduced during the day (SuarezLopez et...
Plant development is highly responsive to ambient temperature, and this trait has been linked to the ability of plants to adapt to climate change. The mechanisms by which natural populations modulate their thermoresponsiveness are not known. To address this, we surveyed Arabidopsis accessions for variation in thermal responsiveness of elongation growth and mapped the corresponding loci. We find that the transcriptional regulator EARLY FLOWERING3 (ELF3) controls elongation growth in response to temperature. Through a combination of modeling and experiments, we show that high temperature relieves the gating of growth at night, highlighting the importance of temperature-dependent repressors of growth. ELF3 gating of transcriptional targets responds rapidly and reversibly to changes in temperature. We show that the binding of ELF3 to target promoters is temperature dependent, suggesting a mechanism where temperature directly controls ELF3 activity.
Flowering is the primary trait affected by ambient temperature changes. Plant microRNAs (miRNAs) are small non-coding RNAs playing an important regulatory role in plant development. In this study, to elucidate the mechanism of flowering-time regulation by small RNAs, we identified six ambient temperature-responsive miRNAs (miR156, miR163, miR169, miR172, miR398 and miR399) in Arabidopsis via miRNA microarray and northern hybridization analyses. We also determined the expression profile of 120 unique miRNA loci in response to ambient temperature changes by miRNA northern hybridization analysis. The expression of the ambient temperature-responsive miRNAs and their target genes was largely anticorrelated at two different temperatures (16 and 23°C). Interestingly, a lesion in short vegetative phase (SVP), a key regulator within the thermosensory pathway, caused alteration in the expression of miR172 and a subset of its target genes, providing a link between a thermosensory pathway gene and miR172. The miR172-overexpressing plants showed a temperature-independent early flowering phenotype, suggesting that modulation of miR172 expression leads to temperature insensitivity. Taken together, our results suggest a genetic framework for flowering-time regulation by ambient temperature-responsive miRNAs under non-stress temperature conditions.
MicroRNA (miRNA)-guided cleavage initiates entry of primary transcripts into the transacting siRNA (tasiRNA) biogenesis pathway involving RNA-DEPENDENT RNA POLYMERASE6, DICER-LIKE4, and SUPPRESSOR OF GENE SILENCING3. Arabidopsis thaliana TAS1 and TAS2 families yield tasiRNA that form through miR173-guided initiation-cleavage of primary transcripts and target several transcripts encoding pentatricopeptide repeat proteins and proteins of unknown function. Here, the TAS1c locus was modified to produce synthetic (syn) tasiRNA to target an endogenous transcript encoding PHY-TOENE DESATURASE and used to analyze the role of miR173 in routing of transcripts through the tasiRNA pathway. miR173 was unique from other miRNAs in its ability to initiate TAS1c-based syn-tasiRNA formation. A single miR173 target site was sufficient to route non-TAS transcripts into the pathway to yield phased siRNA. We also show that miR173 functions in association with ARGONAUTE 1 (AGO1) during TAS1 and TAS2 tasiRNA formation, and we provide data indicating that the miR173-AGO1 complex possesses unique functionality that many other miRNA-AGO1 complexes lack.Arabidopsis ͉ ARGONAUTE ͉ microRNA ͉ transacting siRNA M icroRNA (miRNA) and transacting siRNA (tasiRNA) form through distinct biogenesis pathways, but both function to guide endonucleolytic cleavage or translational modulation of target RNA transcripts (1). For miRNA, self-complementary foldback structures within primary transcripts are processed into Ϸ21-to 22-nt miRNA/miRNA* duplexes. For tasiRNA in plants, primary transcripts are first processed by miRNA-guided cleavage. One product of the cleaved transcript is stabilized, possibly by SUPPRESSOR OF GENE SILENCING3 (SGS3), and converted to dsRNA by RNA-DEPENDENT RNA POLYMERASE6 (RDR6) (2-5). The resulting dsRNA is processed sequentially by DICER-LIKE4 (DCL4) into 21-nt siRNA duplexes in register with the miRNA-guided cleavage site (2, 6, 7). One strand of each miRNA or tasiRNA duplex is selectively sorted to one or more ARGONAUTE (AGO) proteins according to the 5Ј nucleotide or other sequence/structural elements of the small RNA (8-10). AGO proteins, which contain a 3Ј RNA binding domain (PAZ), a mid domain that confers small RNA recognition or binding function, and an RNaseH-like domain (PIWI) (11), provide the effector component for silencing complexes.Arabidopsis thaliana has eight characterized tasiRNA-generating (TAS) loci belonging to four families. TAS1 and TAS2 tasiRNA target multiple different mRNAs, including several encoding pentatricopeptide repeat (PPR) proteins (3)(4)(5)(12)(13)(14). TAS4 tasiRNA target mRNA encoding several MYB transcription factors (15). TAS3 tasiRNA target AUXIN RESPONSE FACTORs (ARF3 and ARF4) mRNA, regulation of which is important for proper patterning and developmental timing (4,(16)(17)(18)(19)(20). In addition to tasiRNA-based regulation, the RDR6/SGS3/DCL4 silencing pathway contributes to antiviral and transgene silencing (21-25).It is not clear how transcripts are routed into the RDR6/SGS3/ DCL4 s...
SUMMARYThe FLOWERING LOCUS T (FT)/TERMINAL FLOWER 1 (TFL1) family is a small gene family that encodes important regulators that control flower development in Arabidopsis. Here, we investigated the biological role of the product of BROTHER OF FT AND TFL1 (BFT), a member of this family, whose function remains unknown.Comparison of the critical residues that play a role in distinguishing FT-or TFL1-like activity revealed that BFT is more similar to FT. Similar to FT expression, BFT expression showed a diurnal oscillation pattern, peaking in the evening. In situ hybridization revealed BFT expression in the shoot apical meristem, young leaf and axillary inflorescence meristem. Transgenic plants over-expressing BFT exhibited delayed flowering and severe floral defects (floral indeterminacy and compact inflorescences surrounded by serrate leaves), similar to 35S::TFL1 plants. LEAFY (LFY) and APETALA1 (AP1) expression was significantly reduced in 35S::BFT plants. BFT overexpression failed to rescue the terminal flower phenotype of tfl1 mutants; however, it delayed both terminal flower formation in the primary inflorescence and axillary inflorescence development in the tfl1 mutant background. Consistent with this, the loss-of-function BFT alleles, bft-2 and an BFT RNAi line, accelerated termination of the primary inflorescence and formation of axillary inflorescences in the tfl1 mutant background. Taken together, our results suggest that, despite similarities in the critical residues of BFT and FT, BFT possesses a TFL1-like activity and functions redundantly with TFL1 in inflorescence meristem development, and possibly contributes to the regulation of plant architecture.
SummaryTemperature is a key environmental variable influencing plant growth and survival. Protection against high temperature stress in eukaryotes is coordinated by heat shock factors (HSFs), transcription factors that activate the expression of protective chaperones such as HEAT SHOCK PROTEIN 70 (HSP70); however, the pathway by which temperature is sensed and integrated with other environmental signals into adaptive responses is not well understood. Plants are exposed to considerable diurnal variation in temperature, and we have found that there is diurnal variation in thermotolerance in Arabidopsis thaliana, with maximal thermotolerance coinciding with higher HSP70 expression during the day. In a forward genetic screen, we identified a key role for the chloroplast in controlling this response, suggesting that light-induced chloroplast signaling plays a key role. Consistent with this, we are able to globally activate binding of HSFA1a to its targets by altering redox status in planta independently of a heat shock.
In Arabidopsis, long-distance movement of FLOWERING LOCUS T (FT) protein from the leaf to the shoot apex triggers flower development. In wild-type Arabidopsis plants under long-day conditions, FT is mainly expressed in the cotyledon but is weakly expressed in the first true leaf prior to floral induction. To test the importance of the cotyledon in floral induction, we developed a cotyledon micrografting (Cot-grafting) method that, unlike other grafting methods, allows the FT protein from the graft to be transported via its native route from leaves to the shoot apex. By using Cot-grafting, we found that grafting a single wild-type cotyledon onto an ft-10 mutant strongly suppressed the ft-10 late flowering phenotype. Neither Y-grafting wild-type shoots nor butt-grafting wild-type roots to ft-10 plants resulted in comparably accelerated flowering in the ft-10 recipient plants. ft-10 mutants grafted with a 35S::FT cotyledon flowered as early as wild-type plants. When phloem-specific tracers were applied to a donor cotyledon, the tracers were detected in the vein of the true leaf of recipient plants 6 d after Cot-grafting. Also, macromolecule trafficking of an FT:yellow fluorescent protein:hemagglutinin fusion occurred across the graft junction 6 d after Cot-grafting. These results suggest that Cot-grafting, which allows protein movement in a manner consistent with the natural flow of FT protein from the leaf to the shoot apex, can efficiently suppress the late flowering of ft-10 mutants. Our results further suggest that in Arabidopsis, the cotyledon is an important organ for producing FT protein to induce flowering.
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