- Research article
- Open Access
Genome-wide identification and characterization of the NF-Y gene family in grape (vitis vinifera L.)
© The Author(s). 2016
- Received: 9 May 2016
- Accepted: 2 August 2016
- Published: 11 August 2016
Nuclear factor Y (NF-Y) transcription factor is composed of three distinct subunits: NF-YA, NF-YB and NF-YC. Many members of NF-Y family have been reported to be key regulators in plant development, phytohormone signaling and drought tolerance. However, the function of the NF-Y family is less known in grape (Vitis vinifera L.).
A total of 34 grape NF-Y genes that distributed unevenly on grape (V. vinifera) chromosomes were identified in this study. Phylogenetic analysis was performed to predict functional similarities between Arabidopsis thaliana and grape NF-Y genes. Comparison of the structures of grape NF-Y genes (VvNF-Ys) revealed their functional conservation and alteration. Furthermore, we investigated the expression profiles of VvNF-Ys in response to various stresses, phytohormone treatments, and in leaves and grape berries with various sugar contents at different developmental stages. The relationship between VvNF-Y transcript levels and sugar content was examined to select candidates for exogenous sugar treatments. Quantitative real-time PCR (qPCR) indicated that many VvNF-Ys responded to different sugar stimuli with variations in transcript abundance. qPCR and publicly available microarray data suggest that VvNF-Ys exhibit distinct expression patterns in different grape organs and developmental stages, and a number of VvNF-Ys may participate in responses to multiple abiotic and biotic stresses, phytohormone treatments and sugar accumulation or metabolism.
In this study, we characterized 34 VvNF-Ys based on their distributions on chromosomes, gene structures, phylogenetic relationship with Arabidopsis NF-Y genes, and their expression patterns. The potential roles of VvNF-Ys in sugar accumulation or metabolism were also investigated. Altogether, the data provide significant insights on VvNF-Ys, and lay foundations for further functional studies of NF-Y genes in grape.
- Grape (Vitis vinifera L.)
- NF-Y transcription factor
- Phylogenetic analysis
- Expression profiles
- Quantitative real-time PCR
NF-Y (for Nuclear factor Y) transcription factors (TFs) are almost found in all eukaryotes, and they are involved in regulation of gene expression by binding the CCAAT element [1, 2]. The NF-Y complex known as CCAAT binding factor (CBF) or heme activator protein (HAP) consists of three distinct subunits: NF-YA (also known as CBF-B or HAP2), NF-YB (CBF-A or HAP3) and NF-YC (CBF-C or HAP5) . All subunits contain evolutionarily-conserved DNA binding and subunit interaction domains to form heterotrimeric complexes [4–6]. Notably, the NF-YB proteins without a nuclear localization signal (NLS) have to interact with NF-YC in the cytoplasm to translocate into the nucleus, where the heterodimer is combined with NF-YA to form the final heterotrimer [7, 8]. Despite the ubiquity of NF-Y proteins in eukaryotes, there is only one or two genes encoding each NF-Y subunit in animals and yeast [9, 10]. In contrast, there are multiple genes encoding each subunit in plants [10, 11]. For example, 10 NF-YAs, 13 NF-YBs, and 13 NF-YCs are encoded by the Arabidopsis thaliana genome [1, 10]. This expansion is a common feature in the plant kingdom, and it helps plants form flexible, versatile TF systems to accommodate complex and diverse environment conditions .
As a kind of combinatorial TFs, NF-Ys have been reported to be involved in regulation of plant development and respond to various abiotic and biotic stresses [12–19]. The Arabidopsis LEAFY COTYLEDON 1 (LEC1, AtNF-YB9) is the first cloned and well-known plant NF-Y gene, and it has been proven that LEC1 is a pivotal regulator in embryogenesis [12, 13, 20, 21]. Recently, the NF-Y genes are also found to be involved in response to endoplasmic reticulum (ER) stress [22, 23]. Grape (Vitis spp.) is cultivated worldwide and has tremendous economic value, and a few reports have emerged revealing the role of VvL1L in grape [24, 25]. However, the function of the overwhelming majority of NF-Y genes in grape is still poorly understood, despite the conservation of functional amino acid residues across different species [26–28].
To explore and characterize the potential functions of grape NF-Y genes (VvNF-Ys), we adopted bioinformatics to analyze the 34 identified VvNF-Ys (8 NF-YAs, 18 NF-YBs, 8 NF-YCs) based on publicly available data. Furthermore, we investigated the expression patterns of VvNF-Ys in response to different biotic and abiotic stresses, exogenous phytohormone, and sugar treatments. In addition, the expression profiles of VvNF-Ys in grape berries were examined at different developmental stages. The phylogenetic analysis of NF-Ys from grape and Arabidopsis, investigation of protein motif and exon-intron structure patterns, and the experimental data provide insights on the function of VvNF-Ys. Taken together, our results provide a set of candidate NF-Y genes for future study and genetic modification in grape.
Identification and characterization of grape NF-Y genes
NF-Y transcription factors in grape
Best match in Arabidopsis
No. of aa
Characteristics of the 34 VvNF-Ys are shown in Table 1. Significant difference of the length of VvNF-Y sequences was observed, with a range from 351 to 51,220 bp, and the difference results in variability of predicted amino acid numbers. The exon-intron structures of VvNF-Ys were also analyzed (Additional file2: Figure S2). The exon-intron organization could indicate the evolutionary relationships within multi-gene families . Most of VvNF-YAs had five or six exons and four or five introns and their intron phases occurred in the same pattern except for VvNF-YA1 and VvNF-YA8. The structures of VvNF-YBs and VvNF-YCs were more variable and complicated, and the two families shared similar exon-intron organization (Additional file 2: Figure S2). The results were consistent with the previous report .
Phylogenetic analysis and multiple alignment of NF-Y protein sequences
Expression patterns of VvNF-Ys in response to abiotic, biotic stresses and phytohormones
Numerous reports have revealed the function of individual NF-Y genes in responses to various biotic and abiotic stresses [14, 18, 19, 34, 35]. To further investigate how NF-Y genes response to stresses, expression of VvNF-Y genes was measured under several stresses. Probe sets from Affymetrix GeneChip platform for 16 VvNF-Ys (Additional file 3: Table S1) were successfully obtained and corresponding genes were selected for further study.
Expression profiles of VvNF-Ys in grape leaves and berries at different development stages
Additionally, expression profiles of VvNF-Ys in different berry tissues were also detected . Five VvNF-Ys exhibited different expression patterns in different berry tissues (Fig. 6c). Two VvNF-YAs (VvNF-YA3 and VvNFF-YA8) and VvNF-YB13 were differentially expressed (>2-fold) in seed, and VvNF-YB9 as well as VvNF-YC2 was predominantly expressed (>1.5-fold) in pulp and skin (Fig. 6c). Notably, the expression of VvNF-YB9 in pulp and skin was affected (>1.5-fold) by water supply, suggesting its possible role in response to water deficiency.
Expression of VvNF-Ys in response to different sugar content and exogenous sugar treatment
NF-Y proteins have been revealed to be key factors in multiple physiological processes in plants [12, 13, 24, 25, 41, 42]. However, the function of most NF-Y proteins in grape are still unknown. Here we tried to take advantage of available data to explore and analyze the grape NF-Y family. Based on the results obtained from searching the Uniprot database by using PFAM and KOG IDs of conserved domains, we identified 32 previously predicted NF-Y proteins in PlantTFDB and two more members (Table 1). The two proteins, VvNF-YA1 and VvNF-YB13, consisted of more than 1000 amino acids, and their corresponding genes contained 13 and 11 exons, respectively (Additional file 2: Figure S2). Sequence analysis in InterPro revealed that VvNF-YA1 contained multiple functional domains, and the CBF signature (CBFB/NFYA, PFAM02045) was located between glutamic (E1510) and phenylalanine (F1572) next to the N-terminus. VvNF-YB13 contained only two domains, and the CBF domain (CBFD_NFYB_HMF, PF00808) was located between arginine (R914) and methionine (M979) close to the N-terminus as well. The phylogenetic analysis showed that VvNF-YA1 was homologous to VvNF-YA6, AtNF-YA4 and AtNF-YA7, while VvNF-YB13 was homologous to VvNF-YB14, AtNF-YB2 and AtNF-YB3 (Fig. 1). Altogether, VvNF-YA1 and VvNF-YB13 were regarded as the members of grape NF-Y family.
Evolutionary analysis could be used to predict potential functions of unknown members based on the known functions of those well-studied members of the same clade [3, 43, 44]. Therefore, an un-rooted phylogenetic tree based on sequences of NF-Y proteins from grape and Arabidopsis were constructed to explore the functions of VvNF-Ys (Fig. 1). For example, AtNF-YB2 and AtNF-YB3, the homologous genes of VvNF-YB13 and VvNF-YB14 in Arabidopsis, were reported to promote flowering in response to inductive long-day condition , so the two VvNF-YBs might play roles in regulation of flowering in grape. More importantly, the genes required for flowering time control were generally expressed in leaf vascular tissue [45, 46], and our data showed that VvNF-YB14 was differentially expressed in leaves (Fig. 6a). This result indicates that VvNF-YB14 should be the candidate gene of particular interest for further study of flowering time control in grape.
Alterations in exon-intron structure or conserved domains would change the function of the gene or protein [1, 47]. Analysis of exon-intron structures revealed that most of VvNF-YAs had similar exon-intron organization pattern whereas VvNF-YBs and VvNF-YCs exhibited more variable and complicated structures (Additional file 2: Figure S2). Multiple alignments of NF-Y protein sequences among different species revealed the conservation of functional domains in VvNF-YAs (Fig. 2a). VvNF-YBs and VvNF-YCs, however, exhibit alterations in their functional domains, yet most of functionality required residues are conserved (Fig. 2b, c). The conservation of functional residues indicates the conserved functions of VvNF-Ys as their orthologs function in other plant lineages [47–52], whereas changes in protein sequences may imply the alterations of function. A good example is that VvL1L, the homolog of AtL1L in grape, has been reported to play a role in grape somatic embryogenesis [24, 25].
Expression patterns of VvNF-Ys in response to specific stresses
Fructose (2.0 %)
Fructose (0.5 %)
Recovery process after heat stress
Plasmopara viticola infection (with plant bearing Rpv2)
Plasmopara viticola infection (with plant bearing Rpv2)
Salt, PEG, cold (5 °C)
Plasmopara viticola infection (with plant bearing Rpv1 or Rpv2)
Fructose (2.0 %)
A common response of plants to abiotic stresses such as drought and salinity is the accumulation of sugars and other compatible solutes [55, 56]. The study of relationship between expression levels of VvNF-Ys and sugar contents showed that the changes of fructose contents and expression levels of the tested VvNF-Ys were highly consistent in at least four individual grape varieties (Fig. 7). Exogenous sugar treatments showed that expression of most VvNF-Ys were down-regulated in response to exogenous glucose and sucrose treatments (Fig. 8), except that VvNF-YB7 was up-regulated by glucose (the peak was around 2.0-fold, p < 0.01) and sucrose (the peak was over 3.0-fold, p < 0.01). This suggested that VvNF-YB7 could be involved in carbohydrate anabolism in grape. Notably, almost all the VvNF-Ys responded strongly to exogenous fructose treatment at the concentration of 0.5 % (Fig. 8). Among these genes, VvNF-YC2 and VvNF-YA6 responded to a higher concentration (2.0 %) of fructose likewise (Table 2), implying that they might play roles in fructose accumulation in grape berries ripening. Nevertheless, the expression of VvNF-YA6 was suppressed by exogenous glucose and sucrose. All the results revealed that the regulatory networks of sugar accumulation or metabolism in grape are complicated, and the involvement of VvNF-Ys in grape berry sugar signaling still need more experimental evidence.
In the present study, 34 VvNF-Ys were identified, and evolutionary, structural and expression analyses were conducted to reveal their possible biological roles in stress responses, development, and sugar metabolism. Comparison of NF-Ys from grape and Arabidopsis provided rudimentary insight on the function of less-studied VvNF-Ys in relation to their well-understood homologs. Furthermore, investigation of expression profiles showed that VvNF-Ys responded to various abiotic and biotic stresses as well as hormone treatments. Moreover, analysis of VvNF-Ys expression during grape berry development revealed that VvNF-Ys might play roles in fruit set, ripening and sugar accumulation in grape berry. Based on prediction and experimental data, the VvNF-Ys might be involved in responses to salt, drought, cold and pathogens and may also play significant roles in grape berry development as well as sugar accumulation. More significantly, VvNF-Ys probably function as regulators to mediate cross-talk between different signaling pathways. All these results may contribute to further functional investigation of grape NF-Y family.
Identification of VvNF-Y genes
The sequences of grape NF-Y proteins were obtained from the UniProt (http://www.uniprot.org/), using PFAM ID PF02045, PF00808 and KOG ID KOG0869, KOG0871, KOG1561 for NF-YA (HAP2), NF-YB (HAP3) and NF-YC (HAP5), as queries . The obtained sequences were then compared with those from the PlantTFDB database v3.0 (http://planttfdb.cbi.pku.edu.cn/) . All putative NF-Y proteins were further verified with the tool of InterProScan (http://www.ebi.ac.uk/Tools/pfa/iprscan/) to confirm the existence of the core domains. The corresponding sequences of NF-Y genes were acquired from the Grape Genome Browser (12×) (http://www.genoscope.cns.fr/externe/GenomeBrowser/Vitis/). The incomplete and redundant sequences were omitted.
Structure and chromosomal localization
The locations of NF-Y genes on grape chromosomes were obtained from the Grape Genome Browser (12×) (http://www.genoscope.cns.fr/externe/GenomeBrowser/Vitis/). Gene structures (exon-intron structures) were visualized by alignment of cDNA sequences with corresponding genomic DNA sequences with the online tool of GSDS 2.0 (http://gsds.cbi.pku.edu.cn/).
Alignments and phylogenetic analysis of NF-Y genes
Multiple sequence alignments of identified grape and Arabidopsis NF-Y proteins were conducted using ClustalX 2.0 . Then the results were used to construct Neighbor-Joining tree using MEGA5.0 with the number of bootstrap replications being set at 1000 . The sequences of Arabidopsis NF-Y proteins used for analyses were obtained from the PlantTFDB database v3.0 (http://planttfdb.cbi.pku.edu.cn/) and the Arabidopsis Information Resource (TAIR, https://www.arabidopsis.org/).
Plant materials and sugar treatment
Grape (V. vinifera) seedlings were grown in the Vitis germplasm resources garden of Institute of Botany, the Chinese Academy of Sciences, Beijing, under natural conditions. For qPCR analysis of NF-Ys expression, grape berries and leaves at fruit set, veraison and fully ripe stages were sampled and ground into powder in liquid nitrogen before RNA extraction.
Grape suspension cells derived from embryogenic callus that was induced from whole flowers of ‘Chardonnay’ grape were used for exogenous sugar treatment. The suspension cells were cultured in 250 mL flasks filled with 50 mL of liquid CSM medium (MS basal medium supplemented with 0.5 g/L glutamic acid, 1 mg/L NOA, 5.0 mL/L glycerol and 20 g/L maltose), and shaken at 117 rpm at 27 ± 1 °C in the dark. All the suspension cells were sub-cultured every 7 days. For exogenous sugar treatment, glucose, sucrose and fructose were added to the media for final concentrations of 0.5, 1, and 2 % (w/v), respectively, at the time of 5 ~ 6 days (logarithmic growth phase of cells) after subculture. Then, the suspension cultures were centrifuged at 5000 rpm for 5 min, and the liquid media was removed. The collected cells were washed 3 ~ 4 times with sterile deionized water and subsequently ground in liquid nitrogen for RNA extraction. Each treatment replicated three times.
RNA isolation and quantitative real-time PCR
Total RNA was extracted using the RNAprep Pure Plant Kit (TianGen, Beijing, China) according to the manufacturer’s instructions. RNA integrity was confirmed by electrophoresis on 1 % agarose gels, and concentration as well as quality of RNA were detected by NanoDrop 2000 Spectrophotometer (Thermo Scientific, MA, USA). The removal of genomic DNA and synthesis of the first strand cDNA was performed using HiScript Q RT SuperMix for qPCR (+ gDNA wiper) Kit (Vazyme, Nanjing, China). Quantitative real-time PCR (qPCR) was carried out using AceQ qPCR SYBR Green Master Mix (Vazyme, Nanjing, China) with the CFX96 System (Bio-Rad, CA, USA). The qPCR reactions consisted of a hold at 95 °C for 5 min, followed by 40 cycles at 95 °C for 10 s and 60 °C for 30 s. Melting curve was included to verify the specificity of each primer pair. Grape Actin1 (accession no. AY680701) and UBC (accession no. EC922622)  were used as internal controls. The results were evaluated by the method of the 2-ΔΔCt . The data were obtained from three technological and biological replicates and are shown as mean values ± SD. The significance of differential expression between controls and treatments was examined by Student’s t-test with P < 0.05 and P < 0.01 indicating statistically significant and highly significant, respectively. Primers used for qPCR are listed in Additional file 5: Table S2.
Microarray and transcriptome data analysis
Two databases, the ViTis Co-expression DataBase (VTCdb, http://vtcdb.adelaide.edu.au/Home.aspx)  and the Plant Expression Database (PLEXdb, http://www.plexdb.org/index.php), were searched for the probe sets of grape NF-Y genes. Finally, 16 probe sets, which were designed for Affymetrix GeneChip 16 K Vitis vinifera (Grape) Genome Array and Affymetrix GrapeGen Vitis vinifera Array, were found in both two databases and successfully matched to the 16 sequences of the 34 identified NF-Y genes (Additional file 3: Table S1).
Microarray data of grape NF-Y genes were obtained from PLEXdb (http://www.plexdb.org/index.php). Probe IDs of NF-Y genes were used as query items to search the Affymetrix GeneChip platform. The expression data for selected NF-Y genes were obtained and shown as heatmaps with a color scale indicating log2 expression values.
Sugar extraction and HPLC analysis
Grape berries were collected and ground into powder in liquid nitrogen. The extraction of soluble sugars was conducted as previously described . Around 100 mg of powder was fitted with 10 mL of methanol:chloroform:water (12/5/3; v/v/v), then sonicated for 30 s, and subsequently centrifuged at 1200 × g for 10 min. The supernatants were collected and diluted with water (5/3; v/v). Finally, 2 mL of the aqueous phase was evaporated and then dissolved in 0.8 mL of deionized water. The prepared samples were analyzed by HPLC with water as eluent (0.6 mL min−1).
ABA, abscisic acid; CBF, CCAAT binding factor; CD, cyclodextrin elicitor; Dav, day after veraison; HAP, heme activator protein; MJ, methyl jasmonate; NF-Y, nuclear factor Y; PI, Plasmopara viticola inoculation; PM, powdery mildew; qPCR, quantitative real-time polymerase chain reaction; TF, transcription factor
We would particularly wish to thank Prof. Douglas D. Archbold for the revise and feedback on the manuscript.
This work was supported by the National Natural Science Foundation of China (NO. 31572090).
Availability of data and materials
The data (sequence alignment and phylogenetic tree) used for phylogenetic analysis have been deposited in TreeBASE repository under the URL http://purl.org/phylo/treebase/phylows/study/TB2:S19620. The microarray data used in this article are available in the Gene.
Expression Omnibus (GEO) repository under accession numbers of GSE31594 (http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE31594), GSE6404 (http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE6404), GSE31664 (http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE31664),GSE11406 (http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE11406),GSE42312 (http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE42312),GSE11857 (http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE11857), and GSE41423 (http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE41423), or are available at the PLEXdb (http://www.plexdb.org/modules/PD_browse/experiment_browser.php).
CR, SL and ZL designed the study. CR and YW performed bioinformatics analyses. ZZ carried out the treatments and HPLC analysis. CR performed qPCR tests and statistical analysis. CR draft the manuscript and ZL revised it. All authors read and approved the final manuscript.
The authors declare that they have no competing interests.
Consent for publication
Ethics approval and consent to participate
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- Siefers N, Dang KK, Kumimoto RW, Bynum IV WE, Tayrose G, Holt III BF. Tissue-specific expression patterns of Arabidopsis NF-Y transcription factors suggest potential for extensive combinatorial complexity. Plant Physiol. 2009;149:625–41.View ArticlePubMedPubMed CentralGoogle Scholar
- Quach TN, Nguyen HTM, Valliyodan B, Joshi T, Xu D, Nguyen HT. Genome-wide expression analysis of soybean NF-Y genes reveals potential function in development and drought response. Mol Genet Genomics. 2015;290:1095–115.View ArticlePubMedGoogle Scholar
- Li S, Li K, Ju Z, Cao DY, Fu DQ, Zhu HL, et al. Genome-wide analysis of tomato NF-Y factors and their role in fruit ripening. BMC Genomics. 2016;17:36.View ArticlePubMedPubMed CentralGoogle Scholar
- Sinha S, Maity SN, Lu J, de Crombrugghe B. Recombinant rat CBF-C, the third subunit of CBF/NFY, allows formation of a protein-DNA complex with CBF-A and CBF-B and with yeast HAP2 and HAP3. Proc Natl Acad Sci U S A. 1995;92:1624–8.View ArticlePubMedPubMed CentralGoogle Scholar
- Sinha S, Kim IS, Sohn KY, de Crombrugghe B, Maity SN. Three classes of mutations in the A subunit of the CCAAT-binding factor CBF delineate functional domains involved in the three-step assembly of the CBF-DNA complex. Mol Cell Biol. 1996;16:328–37.View ArticlePubMedPubMed CentralGoogle Scholar
- Calvenzani V, Testoni B, Gusmaroli G, Lorenzo M, Gnesutta N, Petroni K, et al. Interactions and CCAAT-binding of Arabidopsis thaliana NF-Y subunits. PLoS One. 2012;7, e42902.View ArticlePubMedPubMed CentralGoogle Scholar
- Frontini M, Imbriano C, Manni I, Mantovani R. Cell cycle regulation of NF-YC nuclear localization. Cell Cycle. 2004;3:217–22.View ArticlePubMedGoogle Scholar
- Kahle J, Baake M, Doenecke D, Albig W. Subunits of the heterotrimeric transcription factor NF-Y are imported into the nucleus by distinct pathways involving importin beta and importin 13. Mol Cell Biol. 2005;25:5339–54.View ArticlePubMedPubMed CentralGoogle Scholar
- Mantovani R. The molecular biology of the CCAAT-binding factor NF-Y. Gene. 1999;239:15–27.View ArticlePubMedGoogle Scholar
- Riechmann JL, Heard J, Martin G, Reuber L, Jiang C, Keddie J, et al. Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science. 2000;290:2105–10.View ArticlePubMedGoogle Scholar
- Petroni K, Kumimoto RW, Gnesutta N, Calvenzani V, Fornari M, Tonelli C, et al. The promiscuous life of plant NUCLEAR FACTOR Y transcription factors. Plant Cell. 2012;24:4777–92.View ArticlePubMedPubMed CentralGoogle Scholar
- Braybrook SA, Harada JJ. LECs go crazy in embryo development. Trends Plant Sci. 2008;13:624–30.View ArticlePubMedGoogle Scholar
- Gaj MD, Zhang S, Harada JJ, Lemaux PG. Leafy cotyledon genes are essential for induction of somatic embryogenesis of Arabidopsis. Planta. 2005;222:977–88.View ArticlePubMedGoogle Scholar
- Laloum T, De Mita S, Gamas P, Baudin M, Niebel A. CCAAT-box binding transcription factors in plants: Y so many? Trends Plant Sci. 2013;18:157–66.View ArticlePubMedGoogle Scholar
- Wenkel S, Turck F, Singer K, Gissot L, Gourrierec JL, Samach A, et al. CONSTANS and the CCAAT box binding complex share a functionally important domain and interact to regulate flowering of Arabidopsis. Plant Cell. 2006;18:2971–84.View ArticlePubMedPubMed CentralGoogle Scholar
- Cao SH, Kumimoto RW, Gnesutta N, Calogero AM, Mantovani R, Holt III BF. A distal CCAAT/NUCLEARFACTORY complex promotes chromatin looping at the FLOWERINGLOCUST promoter and regulates the timing of flowering in Arabidopsis. Plant Cell. 2014;26:1009–17.View ArticlePubMedPubMed CentralGoogle Scholar
- Combier JP, Frugier F, de Billy F, Boualem A, El-Yahyaoui F, Moreau S, et al. MtHAP2-1 is a key transcriptional regulator of symbiotic nodule development regulated by microRNA169 in Medicago truncatula. Genes Dev. 2006;20:3084–88.View ArticlePubMedPubMed CentralGoogle Scholar
- Nelson DE, Repetti PP, Adams TR, Creelman RA, Wu JR, Warner DC, et al. Plant nuclear factor Y (NF-Y) B subunits confer drought tolerance and lead to improved corn yields on water-limited acres. Proc Natl Acad Sci U S A. 2007;104:16450–5.View ArticlePubMedPubMed CentralGoogle Scholar
- Li WX, Oono Y, Zhu J, He XJ, Wu JM, Iida K, et al. The Arabidopsis NFYA5 transcription factor is regulated transcriptionally and posttranscriptionally to promote drought resistance. Plant Cell. 2008;20:2238–51.View ArticlePubMedPubMed CentralGoogle Scholar
- West M, Yee KM, Danao J, Zimmerman JL, Fischer RL, Goldberg RB, et al. LEAFY COTYLEDON1 is an essential regulator of late embryogenesis and cotyledon identity in Arabidopsis. Plant Cell. 1994;6:1731–45.View ArticlePubMedPubMed CentralGoogle Scholar
- Lotan T, Ohto M, Yee MK, West MA, Lo R, Kwong RW, et al. Arabidopsis LEAFY COTILEDON1 is sufficient to induce embryo development in vegetative cells. Cell. 1998;93:1195–205.View ArticlePubMedGoogle Scholar
- Liu JX, Srivastava R, Che P, Howell SH. An endoplasmic reticulum stress response in Arabidopsis is mediated by proteolytic processing and nuclear relocation of a membrane-associated transcription factor, bZIP28. Plant Cell. 2007;19:4111–99.View ArticlePubMedPubMed CentralGoogle Scholar
- Liu JX, Howell SH. bZIP28 and NF-Y transcription factors are activated by ER stress and assemble into a transcriptional complex to regulate stress response genes in Arabidopsis. Plant Cell. 2010;22:782–96.View ArticlePubMedPubMed CentralGoogle Scholar
- Schellenbaum P, Jacques A, Maillot P, Bertsch C, Mazet F, Farine S, et al. Characterization of VvSERK1, VvSERK2, VvSERK3 and VvL1L genes and their expression during somatic embryogenesis of grapevine (Vitis vinifera L.). Plant Cell Rep. 2008;27:1799–809.View ArticlePubMedGoogle Scholar
- Maillot P, Lebel S, Schellenbaum P, Jacques A, Walter B. Differential regulation of SERK, LEC1-Like and pathogenesis-related genes during indirect secondary somatic embryogenesis in grapevine. Plant Physiol Biochem. 2009;47:743–52.View ArticlePubMedGoogle Scholar
- Coustry F, Maity SN, Sinha S, de Crombrugghe B. The transcriptional activity of the CCAAT-binding factor CBF is mediated by two distinct activation domains, one in the CBF-B subunit and the other in the CBF-C subunit. J Biol Chem. 1996;271:14485–91.View ArticlePubMedGoogle Scholar
- Kim IS, Sinha S, de Crombrugghe B, Maity SN. Determination offunctional domains in the C subunit of the CCAAT- binding factor (CBF)necessary for formation of a CBF-DNA complex: CBF- B interactssimultaneously with both the CBF-A and CBF-C subunits to form aheterotrimeric CBF molecule. Mol Cell Biol. 1996;16:4003–13.View ArticlePubMedPubMed CentralGoogle Scholar
- Romier C, Cocchiarella F, Mantovani R, Moras D. The NF-YB/NF-YC structure gives insight into DNA binding and transcription regulation by CCAAT factor NF-Y. J Biol Chem. 2003;278:1336–45.View ArticlePubMedGoogle Scholar
- Rípodas C, Castaingts M, Clúa J, Blanco F, Zanetti ME. Annotation, phylogeny and expression analysis of the nuclear factor Y families in common bean (Phaseolus vulgaris). Front Plant Sci. 2015;14:761.Google Scholar
- Maity SN, de Crombrugghe B. Role of the CCAAT-binding protein CBF/NF-Y in transcription. Trends Biochem Sci. 1998;23:174–8.View ArticlePubMedGoogle Scholar
- Maity SN, de Crombrugghe B. Biochemical analysis of the B subunit of the heteromeric CCAAT-binding factor. A DNA-binding domain and a subunit interaction domain are specified by two separate segments. J Biol Chem. 1992;267:8286–92.PubMedGoogle Scholar
- Xing Y, Fikes JD, Guarente L. Mutations in yeast HAP2/HAP3 define a hybrid CCAAT box binding domain. EMBO J. 1993;12:4647.PubMedPubMed CentralGoogle Scholar
- Hackenberg D, Wu Y, Voigt A, Adams R, Schramm P, Grimm B. Studies on differential nuclear translocation mechanism and assembly of the three subunits of the Arabidopsis thaliana transcription factor NF-Y. Mol Plant. 2012;5:876–88.View ArticlePubMedGoogle Scholar
- Shen B, Allen WB, Zheng P, Li C, Glassman K, Ranch J, et al. Expression of ZmLEC1 and ZmWRI1 increases seed oil production in maize. Plant Physiol. 2010;153:980–7.View ArticlePubMedPubMed CentralGoogle Scholar
- Alam MM, Tanaka T, Nakamura H, Ichikawa H, Kobayashi K, Yaeno T, et al. Overexpression of a rice heme activator protein gene (OsHAP2E) confers resistance to pathogens, salinity and drought, and increases photosynthesis and tiller number. Plant Biotechnol J. 2014;13:85–96.View ArticlePubMedGoogle Scholar
- Liu GT, Wang JF, Cramer G, Dai ZW, Duan W, Xu HG, et al. Transcriptomic analysis of grape (Vitis vinifera L.) leaves during and after recovery from heat stress. BMC Plant Biol. 2012;12:174.View ArticlePubMedPubMed CentralGoogle Scholar
- Fung RWM, Gonzalo M, Fekete C, Kovacs LG, He Y, Marsh E, et al. Powdery mildew induces defense-oriented reprogramming of the transcriptome in a susceptible but not in a resistant grapevine. Plant Physiol. 2008;146:236–49.View ArticlePubMedPubMed CentralGoogle Scholar
- Wolters H, Jurgens G. Survival of the flexible: hormonal growth control and adaptation in plant development. Nat Rev Genet. 2009;10:305–17.View ArticlePubMedGoogle Scholar
- Grimplet J, Deluc LG, Tillett RL, Wheatley MD, Schlauch KA, Cramer GR, et al. Tissue-specific mRNA expression profiling in grape berry tissues. BMC Genomics. 2007;8:187.View ArticlePubMedPubMed CentralGoogle Scholar
- Coombe BG, McCarthy MG. Dynamics of grape berry growth and physiology of ripening. Aust J Grape Wine Res. 2000;6:131–5.View ArticleGoogle Scholar
- Laporte P, Lepage A, Fournier J, Catrice O, Moreau S, Jardinaud MF, et al. The CCAAT box-binding transcription factor NF-YA1 controls rhizobial infection. J Exp Bot. 2013;65:481–94.View ArticlePubMedPubMed CentralGoogle Scholar
- Soyano T, Kouchi H, Hirota A, Hayashi M. Nodule inception directly targets NF-Y subunit genes to regulate essential processes of root nodule development in Lotus japonicus. PLoS Genet. 2013;9, e1003352.View ArticlePubMedPubMed CentralGoogle Scholar
- Li DY, Fu FY, Zhang HJ, Song FM. Genome-wide systematic characterization of the bZIP transcriptional factor family in tomato (Solanum lycopersicum L.). BMC Genomics. 2015;16:771.View ArticlePubMedPubMed CentralGoogle Scholar
- Peng XJ, Liu H, Wang D, Shen SH. Genome-wide identification of the Jatropha curcas MYB family and functional analysis of the abiotic stress responsive gene JcMYB2. BMC Genomics. 2016;17:251.View ArticlePubMedPubMed CentralGoogle Scholar
- Kumimoto RW, Zhang Y, Siefers N, Holt 3rd BF. NF-YC3, NF-YC4 and NF-YC9 are required for CONSTANS-mediated, photoperiod-dependent flowering in Arabidopsis thaliana. Plant J. 2010;63:379–91.View ArticlePubMedGoogle Scholar
- Cao S, Kumimoto RW, Siriwardana CL, Risinger JR, Holt 3rd BF. Identification and characterization of NF-Y transcription factor families in the monocot model plant Brachypodium distachyon. PLoS One. 2011;6, e21805.View ArticlePubMedPubMed CentralGoogle Scholar
- Xu GX, Guo CC, Shan HY, Kong HZ. Divergence of duplicate genes in exon-intron structure. Proc Natl Acad Sci U S A. 2012;109:1187–92.View ArticlePubMedPubMed CentralGoogle Scholar
- Paradkar PN, Roth JA. Expression of the 1B isoforms of divalent metal transporter (DMT1) is regulated by interaction of NF-Y with a CCAAT-box element near the transcription start site. J Cell Physiol. 2007;211:183–8.View ArticlePubMedGoogle Scholar
- Ni Z, Hu Z, Jiang Q, Zhang H. GmNFYA3, a target gene of miR169, is a positive regulator of plant tolerance to drought stress. Plant Mol Biol. 2013;82:113–29.View ArticlePubMedGoogle Scholar
- Tan H, Yang X, Zhang X, Qu C, Mu J, Fu F, et al. Enhanced seed oil production in canola by conditional expression of Brassica napus LEAFY COTYLEDON1 and LEC1-LIKE in developing seeds. Plant Physiol. 2011;156:1577–88.View ArticlePubMedPubMed CentralGoogle Scholar
- Mendes A, Kelly AA, van Erp H, Shaw E, Powers SJ, Kurup S, et al. bZIP67 regulates the omega-3 fatty acid content of Arabidopsis seed oil by activating fatty acid desaturase3. Plant Cell. 2013;25:3104–16.View ArticlePubMedPubMed CentralGoogle Scholar
- Kwong RW, Bui AQ, Lee H, Kwong LW, Fischer RL, Goldberg RB, et al. LEAFY COTYLEDON1-LIKE defines a class of regulators essential for embryo development. Plant Cell. 2003;15:5–18.View ArticlePubMedPubMed CentralGoogle Scholar
- Mu J, Tan H, Hong S, Liang Y, Zuo J. Arabidopsis transcription factor genes NF-YA1, 5, 6, and 9 play redundant roles in male gametogenesis, embryogenesis, and seed development. Mol Plant. 2013;6:188–201.View ArticlePubMedGoogle Scholar
- Fujita M, Fujita Y, Noutoshi Y, Takahashi F, Narusaka Y, Yamaguchi-Shinozaki K, et al. Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Curr Opin Plant Biol. 2006;9:436–42.View ArticlePubMedGoogle Scholar
- de Silva JM, Arrabaca MC. Contributions of soluble carbohydrates to the osmotic adjustment in the C4 grass Setaria sphacelata: a comparison between rapidly and slowly imposed water stress. J Plant Physiol. 2004;161:551–5.View ArticlePubMedGoogle Scholar
- Garg AK, Kim JK, Owens TG, Ranwala AP, Choi YD, Kochian LV, et al. Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses. Proc Natl Acad Sci U S A. 2002;99:15898–903.View ArticlePubMedPubMed CentralGoogle Scholar
- Jin J, Zhang H, Kong L, Gao G, Luo J. PlantTFDB 3.0: a portal for the functional and evolutionary study of plant transcription factors. Nucleic Acids Res. 2014;42:D1182–7.View ArticlePubMedGoogle Scholar
- Larkin MA, Blackshields G, Brown NP, Chenna R, Mcgettigan PA, Mcwilliam H, et al. Clustal W and Clustal X version 2.0. Bioinformatics. 2007;23:2947–8.View ArticlePubMedGoogle Scholar
- Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: Molecular Evolutionary Genetics Analysis using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Mol Biol Evol. 2011;28:2731–9.View ArticlePubMedPubMed CentralGoogle Scholar
- Reid KE, Olsson N, Schlosser J, Peng F, Lund ST. An optimized grapevine RNA isolation procedure and statistical determination of reference genes for real-time RT-PCR during berry development. BMC Plant Biol. 2006;6:27.View ArticlePubMedPubMed CentralGoogle Scholar
- Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) Method. Methods. 2001;25:402–8.View ArticlePubMedGoogle Scholar
- Wong DCJ, Sweetman C, Drew DP, Ford CM. VTCdb: a gene co-expression database for the crop species Vitis vinifera (grapevine). BMC Genomics. 2013;14:882.View ArticlePubMedPubMed CentralGoogle Scholar
- Anna M, Maryse L, Rossitza A. Profiling of sugar transporter genes in grapevine coping with water deficit. FEBS Lett. 2014;588:3989–97.View ArticleGoogle Scholar
- Peng WT, Lee YW, Nester EW. The phenolic recognition profiles of the Agrobacterium tumefaciens VirA protein are broadened by a high level of the sugar binding protein ChvE. J Bacteriol. 1998;180:5632–8.PubMedPubMed CentralGoogle Scholar