GmGBP1, a homolog of human ski interacting protein in soybean, regulates flowering and stress tolerance in Arabidopsis
© Zhang et al.; licensee BioMed Central Ltd. 2013
Received: 6 November 2012
Accepted: 28 January 2013
Published: 6 February 2013
SKIP is a transcription cofactor in many eukaryotes. It can regulate plant stress tolerance in rice and Arabidopsis. But the homolog of SKIP protein in soybean has been not reported up to now.
In this study, the expression patterns of soybean GAMYB binding protein gene (GmGBP1) encoding a homolog of SKIP protein were analyzed in soybean under abiotic stresses and different day lengths. The expression of GmGBP1 was induced by polyethyleneglycol 6000, NaCl, gibberellin, abscisic acid and heat stress. GmGBP1 had transcriptional activity in C-terminal. GmGBP1 could interact with R2R3 domain of GmGAMYB1 in SKIP domain to take part in gibberellin flowering pathway. In long-day (16 h-light) condition, transgenic Arabidopsis with the ectopic overexpression of GmGBP1 exhibited earlier flowering and less number of rosette leaves; Suppression of AtSKIP in Arabidopsis resulted in growth arrest, flowering delay and down-regulation of many flowering-related genes (CONSTANS, FLOWERING LOCUS T, LEAFY); Arabidopsis myb33 mutant plants with ectopic overexpression of GmGBP1 showed the same flowering phenotype with wild type. In short-day (8 h-light) condition, transgenic Arabidopsis plants with GmGBP1 flowered later and showed a higher level of FLOWERING LOCUS C compared with wild type. When treated with abiotic stresses, transgenic Arabidopsis with the ectopic overexpression of GmGBP1 enhanced the tolerances to heat and drought stresses but reduced the tolerance to high salinity, and affected the expressions of several stress-related genes.
In Arabidopsis, GmGBP1 might positively regulate the flowering time by affecting CONSTANS, FLOWERING LOCUS T, LEAFY and GAMYB directly or indirectly in photoperiodic and gibberellin pathways in LDs, but GmGBP1 might represse flowering by affecting FLOWERING LOCUS C and SHORT VEGETATIVE PHASE in autonomous pathway in SDs. GmGBP1 might regulate the activity of ROS-eliminating to improve the resistance to heat and drought but reduce the high-salinity tolerance.
KeywordsGmGBP1 Abiotic stress Flowering Day-length Gibberellin
Flowering time plays key roles in plant development, plant adaptation to growing regions , crop yield [2, 3] and disease resistance . Abiotic stress such as drought, high salinity and heat, is another major limiting factor for crop yield . Genetic and molecular analyses has revealed that several distinct but linked signaling pathways regulate the flowering-time in response to light and temperature signals or to internal signals such as vernalization, autonomous pathways and gibberellin signal pathway [1, 5–7]. Interaction of different signal transduction pathways before their convergence may allow a coordinated regulation of the activity of the respective pathways. The signals from these pathways are integrated through up-regulating the expression of one or more common target genes: FT, SOC1 and LFY to determine when flowering. The expressions of SOC1 and FT are negatively regulated by FLC but positively regulated by CO[8, 9]. FLC, a MADS-box transcription factor, is a negative regulator of floral initiation and an integrator of the autonomous and vernalization pathways. CO, encoding a B-box zinc-finger transcription factor, integrate circadian clock and light signals and up-regulate the expression of FT and SOC1 directly in the long-day pathway . CONSTANS and GAMYB (AtMYB33) regulate the expression of LFY by binding with different cis-acting elements in the promoter of LFY respectively [11–14]. SKIP is a transcription cofactor in many eukaryotes. All the SKIP homologs identified so far contained a SKIP domain with an S-N-W-K-N peptide signature and may have conserved basic functions, such as acting as a cofactor in transcription and splicing . However, the derived or additional functions of the SKIP homologs varied among species. SKIP was an essential protein for pre-mRNA splicing in Saccharomyces cerevisiae. In Drosophila melanogaster, SKIP was involved in ecdysone-stimulated transcription  and known to be a coactivator in Notch [18, 19]. In Caenorhabditis elegans, SKIP was an essential component of many RNA polymerase II transcription complexes and indispensable for C. elegans development . In Hordeum vulgare L., SKIP could interact with GAMYB. In Oryza sativa L., OsSKIPa could positively modulate cell viability and stress tolerance . AtSKIP functions as not only a positive regulator and putative potential transcription factor in the abiotic stress signaling pathway in Arabidopsis , but also a component of the spliceosome linking alternative splicing and the circadian clock in Arabidopsis . However, there has been no report on the identification of SKIP homologs in soybean and on their functions in the regulation of flowering time in any species so far.
In this study, the expression patterns of soybean GAMYB binding protein encoding a homolog of SKIP protein were analyzed under several abiotic stresses and light conditions. Yeast two-hybrid assay was performed to identify the interactions between GmGBP1 and GmGAMYB1. The phenotypes of transgenic Arabidopsis lines in different stress and day-length were analyzed to study the function of GmGBP1.
GmGBP1encodes a homolog of the human SKIP transcriptional coregulator
The SKIP homolog gene in soybean was obtained from subtracting long-day from short-day treated mRNA. The predicted gene, named as GmGBP1 (Glycine max GAMYB-binding protein gene, GenBank DQ112540), wasamplified from the cDNA of DongNong 42 using PCR. The full length cDNA of GmGBP1, containing 2253 bp with an open reading frame of 1,839 bp, was predicted to encode 612 amino acids. GmGBP1 protein had a predicted isoelectric point (pI) of 8.69 and a molecular weight (MW) of 69.10 kDa.
A yeast transformation was used to detect the transcriptional activity of GmGBP1. GmGBP1, GmGBP1a, GmGBP1b and GmGBP1c were fused to the GAL4 DNA-binding domain and transformed into yeast strain YRG-2 cells respectively. The proteins of GmGBP1 and GmGBP1c were both capable of inducing LacZ expression in yeast cells and could grow in the medium lacking His, indicating that GmGBP1 protein had transcriptional activity in its C-terminal domain (Figure 1C).
GmGBP1expression in soybean
GmGBP1 interacts with GmGAMYB1in yeast cells
The homozygous mutant atskip of Arabidopsiswas lethal at late stage
Considering the homozygous mutant of AtSKIP was lethal, RNAi was used to produce the atskip-i plant to suppress the expression of this gene. Although the expression of AtSKIP was only partially suppressed (Figure 4E), the plants showed abnormal phenotypes such as late flowering, small rosette leaves. According to RT-PCR analyses, the expressions of several key flowering-related genes were down-regulated (Figure 4E). The promotion and inhibitory factors of flowering were both down-regulated, which suggested that SKIP might be involved in more than two different flowering pathways.
Ectopic expression of GmGBP1alters stress tolerance in Arabidopsis
Heat tolerance experiment revealed that GmGBP1 might improve heat tolerance of Arabidopsis plants with ectopic expression of GmGBP1. 7days old plants of transgenic Arabidopsis, treated with 37°C for 5 days, exhibited symptom of flagged leaves, but WT and atskip-i plants showed more serious symptom with whitened leaves (Figure 5E: a, b and c). Furthermore, WT and atskip-i plants of 15days old showed more whitened leaves, even dead after treated with 37°C for 8 days, whereas GmGBP1-ox plants showed more vital (Figure 5E: d, e and f).
The GmGBP1-ox plants had a higher Superoxide dismutase (SOD) level than both atskip-i and WT plants under heat or drought conditions. The malondialdehyde (MDA) level of GmGBP1-ox plants was much lower than both atskip-i and WT plants, indicating that the ectopic expression of GmGBP1 in Arabidopsis might enhance the heat and drought tolerance. However, the highest MDA level and the lowest SOD level of GmGBP1-ox plants implied the reduced salt tolerance in GmGBP1-transgenic Arabidopsis (Figure 5F).
Stress resistance-related genes are affected by GmGBP1
Early flowering of GmGBP1-ox plants in long-day condition
However, in the short-day (SD) condition, the T3 plants of GmGBP1-ox Arabidopsis flowered latest and had the most rosette leaves (Figure 7A, Figure 7D). In contrast, atskip-i plants showed the earliest flowering and had the fewest rosette leaves. This result suggested that there might be some other ways to regulate flowering in SDs. The key flowering inhibitor gene, FLC, was significantly up-regulated in GmGBP1-ox plants (Figure 7B). All the results suggested autonomous pathway could account for the late flowering phenotype.
GAMYB genetically acts downstream of GBPto regulate flowering time
Previous reports showed that AtMYB33 influenced flowering by mediating GA responsiveness of the LFY promoter [12, 14], and was down-regulated in atskip-i plant in this study (Figure 4D). myb33 mutant plants (SALK058312) and myb33 mutant plants containing extra copies of GmGBP1 gene were introduced to investigate the impact of the interaction between GmGBP1 and GmGAMYB1 on flowering. In LDs, no effect on flowering time and leaf numbers was observed in GmGBP1-ox/myb33 plants (Figure 7A, Figure 7D), and the expression level of LFY in GmGBP1-ox/myb33 plants was same to the level of WT, but GmGBP1-ox plants had a high level of LFY (Figure 7C). GmGBP1 was directly located on the upstream of GAMYB, and regulate flowering in LDs.
Since GmGBP1 regulated flowering in autonomous pathway in SDs, a further study was performed to investigate the responsibility of MYB33 in the late flowering phenotype. The result revealed that GmGBP1-ox/myb33 plants also showed late flowering like GmGBP1-ox plants (Figure 7A and Figure 7D), suggesting that GmGBP1 was independent of MYB33 in delaying flowering time in SDs.
Essential roles of SKIPfor plant growth and stress tolerance
SKIP protein, as a spliceosome component, played a vital role in maintaining cell viability in yeast (PRP45), C. elegans (CeSKIP) and O. sativa (OsSKIPa) [16, 20, 22]. The homozygous mutant of AtSKIP in Arabidopsis resulted in death of plants, which was similar to the phenotype of severe growth arrest and even death of O. sativa with suppression of OsSKIPa and embryonic arrest of the CeSKIP mutant in C. elegans, which indicated that AtSKIP was also required for maintaining cell viability and normal growth in Arabidopsis. The indispensable role of SKIP homolog in keeping normal cell viability and growth might be conserved in plants, which was supported by that the plant SKIP homologs possessed the conserved SKIP domain for cell viability identified in PRP45. However, it needs further study to confirm whether the SKIP homologs in soybean could have the conserved function for cell viability.
Drought and high-salinity repressed plant growth and limited seed yield. SKIP homologs in Arabidopsis and rice could improve the tolerance to drought and high-salinity [22, 23]. In this study, the ectopic expression of GmGBP1 in Arabidopsis could enhance the tolerance to drought. However, GmGBP1-ox plants showed a salt-sensitive appearance, although atskip-i plants reduced the tolerance to salt as previous report . Thus, the tolerance of SKIP homologs to salt might be not conserved in plant. Heat, one of serious environmental stresses, affected the growth of plants and the productivity of crops. There was no report about heat tolerance of SKIP homologs previously. Our result showed that GmGBP1-ox plants increased the tolerance to heat whereas atskip-i plants reduced the tolerance to heat, indicating that AtSKIP has the ability of heat tolerance.
Reactive oxygen species (ROS) could be induced by abiotic stresses, and over-accumulation of ROS could lead to cell damage and even death. SOD was used to eliminate ROS, and MDA was the intermediate product during the elimination of ROS [29, 30]. In this study, the raised content of ROS in GmGBP1-ox plants treated with salinity and the decreased content of ROS in GmGBP1-ox plants treated with heat (or drought) indicated that the altered stress tolerance of GmGBP1-ox plants may be partially due to the regulation of the activity of ROS-eliminating.
GmGBP1regulates flowering time
Interestingly, in this study ectopic expression of GmGBP1 in Arabidopsis induced earlier flowering in LDs and late flowering in SDs. The finding of a flowering-regulation function from a SKIP homolog has not yet been reported in any plants so far. The specific function of GmGBP1 in regulating flowering time might be especially useful for developing soybean cultivars with the adaptability to broad grow regions.
Flowering time was controlled by several signaling pathways, such as the day-length, vernalization, autonomous pathways and gibberellin signal pathway [1, 5–7], and it could be measured by scoring the number of rosette leaves at flowering time and the number of days from germination to bolting in Arabidopsis . The number of rosette leaves at flowering time and the number of days from germination to bolting measured in GmGBP1-ox plants were both reduced in LDs, suggesting that ectopic expression of GmGBP1 induced early flowering. atskip-i plants delayed flowering in LDs supported the early flowering of GmGBP1-ox plants in another hand. However, when GmGBP1 ectopicly expressed in myb33 plants, no early flowering could be observed in LDs, indicating that the early flowering function of GmGBP1 might depend on the existence of MYB33. When the transgenic lines were transferred into SDs, the phenotypes of flowering were all changed. The flowering times of GmGBP1-ox and GmGBP1-ox/myb33 plants were both delayed significantly, and atskip-i displayed the early flowering phenotype in SDs.
The expression levels of numerous flowering-related genes could be induced by day-length or gibberellin. The expression level of GmGBP1 was regulated by both day-length and gibberellin, suggesting that GmGBP1 might participate in both day-length and gibberellin signal pathways. In atskip i plants of Arabidopsis, the expression levels of more than 10 flowering-related genes were affected. In particular, the mRNA levels of several flowering integrators (FT LFY and SOC1) were significantly lower. Our results showed that FT and LFY were both up-regulated in GmGBP1-ox plants in LDs, but LFY showed no change when GmGBP1 was ectopic expression in myb33 mutants. Considering the interaction between GmGBP1 and GmGAMYB1, and the conserved function on photoperiodic flowering of FT homologs in soybean [32–34], GmGBP1 might regulate flowering time in two ways by its function as a transcription factor and interaction in LDs. On one hand, GmGBP1 could regulate the expressions of flowering-related genes in day-length signal pathway, and on the other hand, GmGBP1 could bind with GmGAMYB1 in gibberellin signal pathway to control flowering time.
Many reports had revealed that GA pathway played a key role in flowering under SD condition when other regulatory pathways that promoted flowering were not active [1, 7, 35–37]. However, the late flowering of GmGBP1-ox plants indicated that there might be another way to control flowering in SDs. FLC was a negative regulator of floral initiation and an integrator of the autonomous and vernalization pathways. FLC could directly down-regulated FT and SOC1 to repress the flowering in these pathways [8, 9, 38]. SVP, a MADS box transcription factor, could interact with FLC and acted as partially redundant repressors of flowering time with FLC. The negative action on the phenotypes of the down-regulated FLC and SVP in atskip-i plants in LDs suggested that flowering time was regulated crossly by several signal pathways and SKIP might take part in more than two ways. In SDs, the expression of FLC was up-regulated in GmGBP1-ox plants, and was down-regulated in atskip-i plants as that in LDs. The late flowering of GmGBP1-ox plants in SDs elucidated that GmGBP1 might delay flowering time in SDs through autonomous pathway by improving the expression level of FLC, a key flowering inhibitor factor.
In general, GmGBP1 might regulate flowering time by three signal pathways. GmGBP1 positively controlled the flowering time by regulating CO, FT, LFY and GAMYB directly or indirectly in photoperiodic and gibberellin pathways in LDs, GmGBP1 repressed flowering by regulating FLC and SVP in autonomous pathway in SDs.
Diverse functions of SKIPhomologs in plant
SKIP had a conserved SKIP domain with an S-N-W-K-N peptide signature, and was considered as a cofactor for transcription regulation in all eukaryotes so far. However, the derived or additional functions of the SKIP homologs varied among species. Transgenic rice that overexpressed OsSKIPa exhibited stress tolerances (abscisic acid, salt, mannitol) at both seedling and reproductive stages . Overexpression of the AtSKIP gene in Arabidopsis modulated the induction of salt tolerance, dehydration resistance and insensitivity towards abscisic acid under stress conditions ; However, ectopic expression of GmGBP1 in Arabidopsis reduced tolerance to NaCl, but increased tolerance to drought and heat in this study.
Suppression of OsSKIP resulted in growth arrest of rice due to the reduced cell viability in the active growth regions . A decrease in AtSKIP expression led to altered plant development with the phenotype of reduced inflorescence stems and smaller rosette leaves . In this study, the homozygous atskip mutant was lethal to the growth, and the knockdown of AtSKIP showed late flowering and increased number of rosette leaves. The ectopic expression of GmGBP1 induced premature flowering of Arabidopsis in LDs. All the study on SKIP homologs in plant revealed that SKIPs might play a vital role in the growth and development of plant, but have different function on the stress tolerance and flowering in plant.
Plant SKIPs were divided into four groups based on the SKIP sequences by phylogenetic tree (Figure 1D). The different groups among OsSKIP, AtSKIP and GmGBP1 indicated the diversity of their functions. SKIP could be induced by various abiotic stresses, phytohormones treatments and day-length, but the expression patterns of SKIP varied among rice, Arabidopsis and soybean [22, 23]. The transcriptional levels of OsSKIP, AtSKIP and GmGBP1 were all up-regulated by ABA, NaCl and drought (PEG6000 or mannitol), but had different scales. GmGBP1 could be induced by day-length and heat, but no related report for OsSKIP and AtSKIP in rice and Arabidopsis. The various functions of SKIP homologs might be also owing to the diversification of SKIP-interacting proteins SIPs. Previous studies showed that the SKIP homologs, PRP45 (yeast), BX42 (Drosophila), CeSKIP (C. elegans), HvSKIP (barely) and OsSKIP (rice) had 34, 13, 5, 1 and 35 interacted proteins, respectively [16, 20–22, 40, 41]. Nevertheless, few SIPs could match each other among species. For example, both HvSKIP and GmGBP1 interacted with GAMYB but OsGAMYB was not included in the 35 OsSIPs [21, 22]. All the data indicated that SKIP might participate in distinct functions through the interaction with diverse proteins.
In this study, GmGBP1,as a homolog of SKIP in soybean, not only regulates plant flowering time but also alters plant resistance to abiotic stress in Arabidopsis. Such a flowering study about SKIP homolog in plant has no report so far. Although both OsSKIP and AtSKIP could improve plant tolerance to high salinity and drought [22, 23], GmGBP1 might improve plant tolerance to heat and drought, but reduce the resistance to high salinity. The flowering and stress related functions of GmGBP1 might be used to develop soybean cultivars with the adaptability to broad grow regions and environment.
Plant material, growth conditions and chemical treatments
Pure seeds of soybean cultivar ‘DongNong 42’ (photoperiod-sensitive) were obtained from Soybean Research Institute of Northeast Agricultural University (Harbin, China). To analysis the tissue-specific expression of GmGBP1,the root, stem, leaf, trifoliate leaves, flower bud, pod and immature seed from soybean under both LDs and SDs were sampled. To analysis the expression of GmGBP1 under abiotic stress conditions, the soybean plants, with the first fully expanding trifoliate leaves, were transplanted into 1/4 Murashige and Skoog (MS)  liquid medium (no agar supplement) supplemented with 100 μmol gibberellin, 100 μmol ABA, 200 mM NaCl or 8% PEG6000. The plants that were transplanted into 1/4 MS liquid medium without the supplements of agar, gibberellin, ABA or NaCl were used as the control. The plants were sampled at 0, 0.5, 1, 2, 4 and 12 hours after transfer.
Arabidopsis thaliana ecotype Columbia (Col-0) was used in this study. Seeds of atmyb33 T-DNA insertion line (Salk_058312) and atskip T-DNA insertion line (SAIL_681_H11) were obtained from The Arabidopsis Information Resource (TAIR).
Identification of mutant
PCR with the gene-specific primer pair and T-DNA-specific primer were used for genotyping to identify homozygous T-DNA inserted plants. The left genomic primer (LP), right genomic primer (RP) and the left T-DNA border primer (LB) for atskip were as follows: LP: 5′ CAAGCACAAGAGAGTCCCAAG 3′ RP: 5′ CGCCACTTGCTCTCATAGTTC 3′ LB: 5′ GCCTTTTCAGAAATGGATAAATAGCCTTGCTTCC 3′. The LP, RP and LB primers for myb33 were as follows: LP: 5’ ATCCAGAACTGTCAGACGCTG 3′ RP: 5′ AATTGCGTATTTGGTTGGATG 3′ LB: 5′ ATTTTGCCGATTTCGGAAC 3′. After confirmation of homozygous T-DNA insertion, gene knock-out was confirmed by RT-PCR with gene-specific primer.
Gene expression analyses
Primers used in this study
Primer sequences (5’–3’)
Semi-quantitative RT-PCR was used to analyze the expression of flowering-related genes. Arabidopsis 18S rRNA gene was used as the endogenous control. The PCR products were analyzed through agarose gel electrophoresis and stained with ethidium bromide. All RT-PCR analyses were repeated three times, and one representative was shown.
Yeast two-hybrid assay
PCR-amplified cDNA fragments of GmGBP1, GmGBP1a (amino acids 1–189), GmGBP1b (amino acids 190–356) and GmGBP1c (amino acids 357–612) were cloned into EcoRI and PstI site of pBD-GAL4 as the bait constructs; PCR-amplified cDNA fragments of GmGAMYB1, GmGAMYB1a (amino acids 1–141) and GmGAMYB1b (amino acids 142–538) were cloned into BamHI and PstI site of pAD-GAL4 as the prey constructs. The primers used were: yGmGBP1-F and yGmGBP1-R; yGmGBP1a-F and yGmGBP1a-R; yGmGBP1b-F and yGmGBP1b-R; yGmGBP1c-F and yGmGBP1c-R; yGmGAMYB1-F and yGmGAMYB1-R; yGmGAMYB1a-F and yGmGAMYB1a-R; yGmGAMYB1b-F and yGmGAMYB1b-R (Table 1). All the bait constructs were transformed into the yeast strain YRG-2 respectively to detect the transcriptional activities.
The yeast two-hybrid assay was performed using the GAL4 Two-Hybrid phagemid vector System (Stratagene, USA). The yeast strain YRG-2 was transformed with the bait plasmid, and the cells containing the bait constructs that have no self-activation activity were transformed with the prey plasmid according to the manufacturer’s instruction manual. The co-transformants were selected on synthetic complete selection medium lacking Leu, Trp and His. Large yeast clones appearing within 7 days were picked out to test the LacZ reporter gene. Positive clones were identified by the restriction digest analyses.
Gene constructs and Arabidopsis transformation
The GmGBP1-overexpression construct was constructed by directionally inserting the full cDNA into the cloned vector pMD18T and then into the binary vector pCAMBIA3300. To make a dsRNAi construct of GmGBP1, a 505 bp fragment of GmGBP1, 73% of nucleotide homology to AtSKIP, was generated by PCR with primers GmGBP1-i-F and GmGBP1-i-R (Table 1) and cloned into pJawoh18 vector through attB × attP (BP) recombination cloning. The attB1 and attB2 were the two sequences for the BP recombination reaction (Invitrogen, USA). The constructs were transformed into the Agrobacterium tumefaciens strain LBA4404 and used to transform Arabidopsis ecotype Columbia using the floral dip method (Clough and Bent 1998).
Seedlings were germinated on MS medium, and then transferred to 1:1 of vermiculite and turfy-soil and grown under LDs or SDs conditions. The flowering time of Arabidopsis was measured by scoring the number of rosette leaves at the flowering time and the number of days from germination to bolting . At least 20 plants were analyzed each time, and the experiments were repeated for three times.
Reactive oxygen species
Murashige and skoog
This work was supported by National Core Soybean Genetic Engineering Project (Contract No. 2011ZX08004-005), Chinese National Natural Science Foundation (31101169, 31271748), Soybean Research & Development Center, CARS and National education Ministry for the teams of soybean molecular design.
- Putterill J, Laurie R, Macknight R: It’s time to flower: the genetic control of flowering time. Bioessays. 2004, 26 (4): 363-373. 10.1002/bies.20021.PubMedView ArticleGoogle Scholar
- Atkinson NJ, Urwin PE: The interaction of plant biotic and abiotic stresses: from genes to the field. J Exp Bot. 2012, 63 (10): 3523-3543. 10.1093/jxb/ers100.PubMedView ArticleGoogle Scholar
- Yuan J, Njiti VN, Meksem K, Iqbal MJ, Triwitayakorn K, Kassem MA, Davis GT, Schmidt ME, Lightfoot DA: Quantitative trait loci in two soybean recombinant Inbred line populations segregating for yield and disease resistance. Crop Sci. 2002, 42 (1): 271-277. 10.2135/cropsci2002.0271.PubMedView ArticleGoogle Scholar
- Njiti VN, Lightfoot DA: Genetic analysis infers Dt loci underlie resistance to Fusarium solani f. sp. glycines in indeterminate soybeans. Can J Plant Sci. 2006, 86 (1): 83-90. 10.4141/P05-046.View ArticleGoogle Scholar
- Cerdan PD, Chory J: Regulation of flowering time by light quality. Nature. 2003, 423 (6942): 881-885. 10.1038/nature01636.PubMedView ArticleGoogle Scholar
- Moon J, Suh SS, Lee H, Choi KR, Hong CB, Paek NC, Kim SG, Lee I: The SOC1 MADS-box gene integrates vernalization and gibberellin signals for flowering in Arabidopsis. Plant J. 2003, 35 (5): 613-623. 10.1046/j.1365-313X.2003.01833.x.PubMedView ArticleGoogle Scholar
- Mouradov A, Cremer F, Coupland G: Control of flowering time: interacting pathways as a basis for diversity. The Plant Cell. 2002, 14 (1): 111-130.Google Scholar
- Hepworth SR, Valverde F, Ravenscroft D, Mouradov A, Coupland G: Antagonistic regulation of flowering-time gene SOC1 by CONSTANS and FLC via separate promoter motifs. EMBO J. 2002, 21 (16): 4327-4337. 10.1093/emboj/cdf432.PubMedPubMed CentralView ArticleGoogle Scholar
- Samach A, Onouchi H, Gold SE, Ditta GS, Schwarz-Sommer Z, Yanofsky MF, Coupland G: Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science. 2000, 288 (5471): 1613-1616. 10.1126/science.288.5471.1613.PubMedView ArticleGoogle Scholar
- Hayama R, Coupland G: Shedding light on the circadian clock and the photoperiodic control of flowering. Curr Opin Plant Biol. 2003, 6 (1): 13-19. 10.1016/S1369-5266(02)00011-0.PubMedView ArticleGoogle Scholar
- Blazquez MA, Weigel D: Integration of floral inductive signals in Arabidopsis. Nature. 2000, 404 (6780): 889-892. 10.1038/35009125.PubMedView ArticleGoogle Scholar
- Gocal GF, Sheldon CC, Gubler F, Moritz T, Bagnall DJ, MacMillan CP, Li SF, Parish RW, Dennis ES, Weigel D, et al: GAMYB-like genes, flowering, and gibberellin signaling in Arabidopsis. Plant Physiol. 2001, 127 (4): 1682-1693. 10.1104/pp.010442.PubMedPubMed CentralView ArticleGoogle Scholar
- Gubler F, Raventos D, Keys M, Watts R, Mundy J, Jacobsen JV: Target genes and regulatory domains of the GAMYB transcriptional activator in cereal aleurone. Plant J. 1999, 17 (1): 1-9. 10.1046/j.1365-313X.1999.00346.x.PubMedView ArticleGoogle Scholar
- Millar AA, Gubler F: The Arabidopsis GAMYB-like genes, MYB33 and MYB65, are microRNA-regulated genes that redundantly facilitate anther development. Plant Cell. 2005, 17 (3): 705-721. 10.1105/tpc.104.027920.PubMedPubMed CentralView ArticleGoogle Scholar
- Folk P, Puta F, Skruzny M: Transcriptional coregulator SNW/SKIP: the concealed tie of dissimilar pathways. Cellular and molecular life sciences: CMLS. 2004, 61 (6): 629-640. 10.1007/s00018-003-3215-4.PubMedView ArticleGoogle Scholar
- Albers M, Diment A, Muraru M, Russell CS, Beggs JD: Identification and characterization of Prp45p and Prp46p, essential pre-mRNA splicing factors. RNA. 2003, 9 (1): 138-150. 10.1261/rna.2119903.PubMedPubMed CentralView ArticleGoogle Scholar
- Wieland C, Mann S, Von Besser H, Saumweber H: The Drosophila nuclear protein Bx42, which is found in many puffs on polytene chromosomes, is highly charged. Chromosoma. 1992, 101 (8): 517-525. 10.1007/BF00352475.PubMedView ArticleGoogle Scholar
- Negeri D, Eggert H, Gienapp R, Saumweber H: Inducible RNA interference uncovers the Drosophila protein Bx42 as an essential nuclear cofactor involved in Notch signal transduction. Mech Dev. 2002, 117 (1–2): 151-162.PubMedView ArticleGoogle Scholar
- Ivanov AI, Rovescalli AC, Pozzi P, Yoo S, Mozer B, Li HP, Yu SH, Higashida H, Guo V, Spencer M, et al: Genes required for Drosophila nervous system development identified by RNA interference. Proc Natl Acad Sci USA. 2004, 101 (46): 16216-16221. 10.1073/pnas.0407188101.PubMedPubMed CentralView ArticleGoogle Scholar
- Kostrouchova M, Housa D, Kostrouch Z, Saudek V, Rall JE: SKIP is an indispensable factor for Caenorhabditis elegans development. Proc Natl Acad Sci USA. 2002, 99 (14): 9254-9259. 10.1073/pnas.112213799.PubMedPubMed CentralView ArticleGoogle Scholar
- Woodger FJ, Millar A, Murray F, Jacobsen JV, Gubler F: The Role of GAMYB Transcription Factors in GA-Regulated Gene Expression. Journal of Plant Growth Regulation. 2003, 22 (2): 176-184. 10.1007/s00344-003-0025-8.View ArticleGoogle Scholar
- Hou X, Xie K, Yao J, Qi Z, Xiong L: A homolog of human ski-interacting protein in rice positively regulates cell viability and stress tolerance. Proc Natl Acad Sci USA. 2009, 106 (15): 6410-6415. 10.1073/pnas.0901940106.PubMedPubMed CentralView ArticleGoogle Scholar
- Lim GH, Zhang X, Chung MS, Lee DJ, Woo YM, Cheong HS, Kim CS: A putative novel transcription factor, AtSKIP, is involved in abscisic acid signalling and confers salt and osmotic tolerance in Arabidopsis. New Phytol. 2010, 185 (1): 103-113. 10.1111/j.1469-8137.2009.03032.x.PubMedView ArticleGoogle Scholar
- Wang X, Wu F, Xie Q, Wang H, Wang Y, Yue Y, Gahura O, Ma S, Liu L, Cao Y, et al: SKIP Is a Component of the Spliceosome Linking Alternative Splicing and the Circadian Clock in Arabidopsis. Plant Cell. 2012, 24 (8): 3278-3295. 10.1105/tpc.112.100081.PubMedPubMed CentralView ArticleGoogle Scholar
- Zhai H, Bai X, Zhu Y, Li Y, Cai H, Ji W, Ji Z, Liu X, Li J: A single-repeat R3-MYB transcription factor MYBC1 negatively regulates freezing tolerance in Arabidopsis. Biochem Biophys Res Commun. 2010, 394 (4): 1018-1023. 10.1016/j.bbrc.2010.03.114.PubMedView ArticleGoogle Scholar
- Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K: Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell. 2003, 15 (1): 63-78. 10.1105/tpc.006130.PubMedPubMed CentralView ArticleGoogle Scholar
- Seo PJ, Lee SB, Suh MC, Park MJ, Go YS, Park CM: The MYB96 transcription factor regulates cuticular wax biosynthesis under drought conditions in Arabidopsis. Plant Cell. 2011, 23 (3): 1138-1152. 10.1105/tpc.111.083485.PubMedPubMed CentralView ArticleGoogle Scholar
- Chico JM, Chini A, Fonseca S, Solano R: JAZ repressors set the rhythm in jasmonate signaling. Curr Opin Plant Biol. 2008, 11 (5): 486-494. 10.1016/j.pbi.2008.06.003.PubMedView ArticleGoogle Scholar
- Apel K, Hirt H: Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol. 2004, 55: 373-399. 10.1146/annurev.arplant.55.031903.141701.PubMedView ArticleGoogle Scholar
- Mittler R: Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci. 2002, 7 (9): 405-410. 10.1016/S1360-1385(02)02312-9.PubMedView ArticleGoogle Scholar
- Liu LJ, Zhang YC, Li QH, Sang Y, Mao J, Lian HL, Wang L, Yang HQ: COP1-mediated ubiquitination of CONSTANS is implicated in cryptochrome regulation of flowering in Arabidopsis. Plant Cell. 2008, 20 (2): 292-306. 10.1105/tpc.107.057281.PubMedPubMed CentralView ArticleGoogle Scholar
- Kong F, Liu B, Xia Z, Sato S, Kim BM, Watanabe S, Yamada T, Tabata S, Kanazawa A, Harada K, et al: Two coordinately regulated homologs of FLOWERING LOCUS T are involved in the control of photoperiodic flowering in soybean. Plant Physiol. 2010, 154 (3): 1220-1231. 10.1104/pp.110.160796.PubMedPubMed CentralView ArticleGoogle Scholar
- Thakare D, Kumudini S, Dinkins RD: The alleles at the E1 locus impact the expression pattern of two soybean FT-like genes shown to induce flowering in Arabidopsis. Planta. 2011, 234 (5): 933-943. 10.1007/s00425-011-1450-8.PubMedView ArticleGoogle Scholar
- Yamagishi N, Yoshikawa N: Expression of FLOWERING LOCUS T from Arabidopsis thaliana induces precocious flowering in soybean irrespective of maturity group and stem growth habit. Planta. 2011, 233 (3): 561-568. 10.1007/s00425-010-1318-3.PubMedView ArticleGoogle Scholar
- Eriksson S, Bohlenius H, Moritz T, Nilsson O: GA4 is the active gibberellin in the regulation of LEAFY transcription and Arabidopsis floral initiation. Plant Cell. 2006, 18 (9): 2172-2181. 10.1105/tpc.106.042317.PubMedPubMed CentralView ArticleGoogle Scholar
- Hisamatsu T, King RW: The nature of floral signals in Arabidopsis. II. Roles for FLOWERING LOCUS T (FT) and gibberellin. J Exp Bot. 2008, 59 (14): 3821-3829. 10.1093/jxb/ern232.PubMedPubMed CentralView ArticleGoogle Scholar
- Mutasa-Gottgens E, Hedden P: Gibberellin as a factor in floral regulatory networks. J Exp Bot. 2009, 60 (7): 1979-1989. 10.1093/jxb/erp040.PubMedView ArticleGoogle Scholar
- Lee J, Lee I: Regulation and function of SOC1, a flowering pathway integrator. J Exp Bot. 2010, 61 (9): 2247-2254. 10.1093/jxb/erq098.PubMedView ArticleGoogle Scholar
- Fujiwara S, Oda A, Yoshida R, Niinuma K, Miyata K, Tomozoe Y, Tajima T, Nakagawa M, Hayashi K, Coupland G, et al: Circadian clock proteins LHY and CCA1 regulate SVP protein accumulation to control flowering in Arabidopsis. Plant Cell. 2008, 20 (11): 2960-2971. 10.1105/tpc.108.061531.PubMedPubMed CentralView ArticleGoogle Scholar
- Dahl R, Wani B, Hayman MJ: The Ski oncoprotein interacts with Skip, the human homolog of Drosophila Bx42. Oncogene. 1998, 16 (12): 1579-1586. 10.1038/sj.onc.1201687.PubMedView ArticleGoogle Scholar
- Martinkova K, Lebduska P, Skruzny M, Folk P, Puta F: Functional mapping of Saccharomyces cerevisiae Prp45 identifies the SNW domain as essential for viability. J Biochem. 2002, 132 (4): 557-563. 10.1093/oxfordjournals.jbchem.a003257.PubMedView ArticleGoogle Scholar
- Murashige T, Skoog F: A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant. 1962, 15 (3): 473-497. 10.1111/j.1399-3054.1962.tb08052.x.View ArticleGoogle Scholar