Screening transcription factors of IbMYB1-4 by yeast one-hybrid assays in purple-fleshed sweet potato

doi:10.21203/rs.3.rs-2470336/v1

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Screening transcription factors of IbMYB1-4 by yeast one-hybrid assays in purple-fleshed sweet potato

https://doi.org/10.21203/rs.3.rs-2470336/v1

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The transcription factor IbMYB1 has been identified to be involved in anthocyanin biosynthesis in purple-fleshed sweet potato. However, the upstream transcription factors of PIbMYB1-4 involved in anthocyanin biosynthesis have rarely been studied. In this study, yeast one-hybrid screen was conducted in purple-fleshed sweet potato storage roots to identify upstream transcription factors of PIbMYB1-4. Three proteins, IbERF1, IbPGP19 and IbPDC, were screened as the upstream binding proteins of PIbMYB1-4. Yeast one-hybrid assays and luciferase reporter assays were used to verify that upstream binding proteins interacted with the promoters. The interaction between the promoters and upstream binding proteins was verified by yeast one-hybrid and luciferase reporter assays. The gene expression of upstream transcription factors, transcription factors and structural genes involved in anthocyanin biosynthesis in different root stages of purple-fleshed and white-fleshed sweet potato was analyzed by real-time PCR. IbERF1 has been identified as the upstream transcription factor of PIbMYB1 involved in anthocyanin biosynthesis in purple-fleshed sweet potato. It has been identified that IbERF1 plays an important role in anthocyanin biosynthesis in purple-fleshed sweet potato.

anthocyanin biosynthesis

IbERF1

IbPDC

IbPGP19

upstream transcription factors

Sweet potato is an important crop in China. It is mainly grown in tropical and subtropical regions. Purple sweet potato is rich in anthocyanins that have special physiological activities and functions. Anthocyanin has anticancer and antioxidation functions and plays a role in lowering blood pressure and preventing arteriosclerosis (Kano et al. 2005). Anthocyanin accumulation is regulated by the expression of several structural genes, such as CHS, CHI, F3H, DFR, ANS, and UF3GT. The expression of structural genes is regulated by transcription factors. Transcription factors are trans-acting factors that are a class of DNA-binding proteins that can specifically bind to cis-acting elements of eukaryotic genes and have a regulatory effect on the activation or inhibition of gene transcription (Lambert et al. 2018). The transcription factors forming the MYB–bHLH–WD40 (MBW) complex regulate anthocyanin biosynthesis in purple sweet potato (Xie et al. 2012; An et al. 2012). It was found that the expression of the IbMYB1 gene in purple heart sweet potato was significantly positively correlated with the expression of related structural genes in the anthocyanin synthesis pathway. However, the upstream transcription factors of PIbMYB1-4 involved in anthocyanin biosynthesis have rarely been reported in purple-fleshed sweet potato storage roots.

The ethylene response factors AP2/ERF families involved in multiple physiological processes in plant growth and responses to biological and nonbiological stress (Zhuang et al. 2011; Johni et al. 2019). The endogenous hormone ethylene is involved in the growth and development of roots, leaves, flowers, and fruits (Ueda and Kusaba 2015). In fruit, the endogenous hormone ethylene controls fruit color change (Xie et al. 2016). ERF has been reported to regulate fruit peel color change and anthocyanin biosynthesis in orange (Peng et al. 2013; Lia et al. 2019), banana (Xie et al. 2016), mango (Xie et al. 2016), pear (Yao et al. 2017; Ni et al. 2019), apple (Zhang et al. 2018; An et al. 2019) and others. In purple-fleshed sweet potato storage roots, ERFs have not been identified involved in anthocyanin biosynthesis. It has been found that IbERF1 regulates the biosynthesis of anthocyanin in purple-fleshed sweet potatoes by combining in the promoter of IbMYB1-4.

Plant materials

Purple-fleshed sweet potato cv. A5 and white-fleshed sweet potato cv. Yubeibai were cultivated in the biological garden at South China Normal University, Guangzhou, GuangDong, China. Arabidopsis (Arabidopsis thaliana) used for subcellular localization and dual luciferase assays were grown in a growth chamber with a day/night cycle of 16 h/8 h at 20 ± 2 °C. The light intensity was 100 μmol/m²/s.

Extraction of genomic DNA and RNA, gene isolation and sequence analysis

An amount of root tissue (0.5g) was ground to a fine powder in the presence of liquid nitrogen using a mortar and pestle. A plant genomic DNA kit (Cat. No. 4992201, Tiangen, China) was used for DNA extraction and a Hipure Plant RNA Mide kit (Cat. No. R4152, Magen, China) was used for RNA extraction. In order to eliminate any possibility of DNA contamination, total RNA was treated with DNAse I digestion using an RNAse-free kit (TaKaRa, Japan). Utilizing a BioPhotometer plus (Eppendorf, Germany), DNA concentrations and purity were determined using absorbance measurements at 230, 260, and 280 nm. DNA samples had 1.8≤OD₂₆₀/OD₂₈₀≤1.9 and OD₂₆₀/OD₂₃₀≥2.0. RNA samples with 1.9≤OD₂₆₀/OD₂₈₀≤2.0, OD₂₆₀/OD₂₃₀≥2.0.

cDNA synthesis was performed using the GoScript^TM Reverse Transcription System (cat. no. A5001, Promega). The promoter and genomic fragments were cloned and sequenced. PCR products were analyzed on 1.2% agarose gels. The fragment was ligated into the plasmid, transformed into Escherichia coli DH5α competent cells (Weidi, China) and sequenced at Sangon Biotech.

Yeast one-hybrid screening

The Y1H screening assays were performed following the Matchmaker Gold Yeast One-Hybrid Library Screening System based on a previous report (Shim et al. 2013). Total RNA was isolated from the storage roots of cv. A5 to construct the prey cDNA library (TaKaRa). A cDNA pool were separately inserted into the the prey vector pGADT7-Rec. The promoter of IbMYB1-4 were inserted into pAbAi to construct the pAbAi-bait. The pAbAi-bait plasmids were linearized and transformed into Y1HGold. The colonies were selected on selective synthetic dextrose medium absence of uracil . After determining the minimal inhibitory concentrations of aureobasidin A (AbA) for the bait strains, the linear pGADT7-Rec vector was cotransformed into the bait yeast strains and selected on synthetic dextrose (SD)/-Leu/AbA plates. The primers used for the yeast one-hybrid screening are listed in Supplemental Table 1.

Yeast one-hybrid assay (Y1H)

Y1H were performed following the Matchmaker Gold Yeast One-Hybrid System based on a previous study (Vidal and Legrain, 1999). Y1H were performed to identify IbERF1, IbPGP19 and IbPDC interacted with the IbMYB1-4 promoter. The promoter of IbMYB1-4 were inserted into pAbAi to construct the pAbAi-bait. The complete CDSs of the IbERF1, IbPGP19 and IbPDC were separately inserted into the pGADT7 vector to construct the prey-AD vectors. The AD-prey vectors were transferred into the bait strain and grown on SD/-Leu/AbA plates. The primers used for Y1H are listed in Supplemental Table 1.

Yeast two-hybrid assay (Y2H)

The transcriptional activity of IbERF1, IbPGP19 and IbPDC was investigated using the Matchmaker^TMGold Yeast Two-Hybrid System (Clontech). The full-length coding sequences of IbERF1, IbPGP19 and IbPDC were cloned into the pGBKT7 vector to construct the bait-BD vectors. The PGBKT7-bait and PGADT7-empty vectors were co-transferred into the yeast strain Y2HGold and grown on the following plates: SD/-Trp medium, SD/-His-AbA medium and SD/-His-AbA X-a-Gal plus medium. The pGBKT7-53 vector co-transformed with pGADT7-53 vector acted as

positive control and pGBKT7 vector co-transformed with pGADT7-53 vector acted as negative control. The primers used for Y2H are listed in Supplemental Table 1.

Dual-luciferase assay

Dual-luciferase assays were carried out to measure the transactivation of activities of IbERF1, IbPGP19 and IbPDC on the promoter of IbMYB1-4. In brief, the full-length cDNAs of IbERF1, IbPGP19 and IbPDC were inserted into the pGreen II 0029 62-SK vector and the promoter of IbMYB1-4 was inserted into pGreen II 0800-LUC vector. Both constructs were transformed into arabidopsis protoplasts accordance with a previous publication (Fu et al. 2020). The ratio of enzyme activities of LUC and REN was measured with an E1910 Dual-Luciferase^® Reporter Assay System (Promega). For each interaction between transcription factors and promoters, three independent experiments were carried out, with three replicates in each experiment. A luciferase gene from Renilla driven by a 35S promoter in the luciferase vector acted as a positive control. The mixtures that contained each transcription factor and empty vector 62-SK were also tested on the promoter as a control. The primers used for the dual-luciferase assay are listed in Supplemental Table 1.

Subcellular localization analysis

For the subcellular localization analysis, the upstream transcription factor CDSs without the stop codon were amplified and cloned into the pCambia1300 vector with BamH Ⅰ and Hind Ⅱ, which contained the UBQ promoter and GFP gene. Both constructs were transformed into arabidopsis protoplasts accordance with a previous publication (Fu et al. 2020). GFP fluorescence was observed by a Zeiss confocal microscope LSM710. The primers used for subcellular localization analysis are listed in Supplemental Table 1.

Real-time quantitative PCR

The expression of upstream transcription factors (IbERF1), transcription factors (IbMYB1, IbbHLH2, IbWD40) and structure genes (IbCHI, IbCHS, IbF3H, IbF3’H, IbDFR, IbANS, IbUF3GT) in fibrous roots, thick roots and storage roots of purple-fleshed sweet potato cv. A5 and white-fleshed sweet potato cv. Yubeibai were analyzed using real-time quantitative PCR. First-strand cDNA was synthesized from total RNA using Prime Script™ RT Master Mix (Takara). RT‒qPCR was conducted using SYBR^® Premix Ex Taq™ II (Takara) in a total reaction volume of 20 μL consisting of 100 ng of template cDNA, each primer at 0.5 μM and 10 μl of SYBR^® Premix Ex Taq™ II, and the amplification program was as follows: 1 cycle of 95 °C for 10 s followed by 40 cycles of 95 °C for 5 s and 60 °C for 30 s with a Bio-Rad CFX96 Real-Time PCR system (BIO-RAD, USA) according to the manufacturers’ instructions. IbG14 was used as an internal control and calculated using the comparative Ct analysis method. The primers used for RT‒qPCR are listed in Supplemental Table 1.

Statistical analysis

Three biological replicates of each sample were subjected to one-way analysis of variance (ANOVA). Significant differences were calculated using SPSS 21.0 Statistics (SPSS Inc., Chicago, II, USA) by Tukey’s honest test (P<0.05) . Figures were drawn with Sigmaplot 12.3.

Screening the upstream transcription factors on the promoter of IbMYB1

The minimum inhibitory concentration of AbA for the PAbAi-PIbMYB1-4 strains was 400 ng/mL. The positive colonies of PIbMYB1-4 screened were 519. The binding protein on the promoter of IbMYB1-4 by yeast one-hybrid screened were 130. The analysis of the gene sequences on PIbMYB1-4 is shown in Supplemental Table 2. The proteins IbERF1, IbPGP19 and IbPDC interacted with the promoter of IbMYB1-4 involved in anthocyanin biosynthesis.

The transcriptional activity of IbERF1, IbPGP19 and IbPDC

Y2H assays were performed to identify the transcriptional activity of IbERF1, IbPGP19 and IbPDC. The results revealed that pGADT7-53+pGBKT7-53 and pGBKT7-IbERF1/IbPGP19/IbPDC+pGADT7-empty transformed strains can grow on SD/-Trp, SD/-His-AbA plus and SD/-His-AbA X-a-Gal plus plates, and the color of emerging yeast colony was blue. The pGADT7-53+PGBKT7 transformed strains could not grow on SD/-Trp, SD/-His-AbA plus and SD/-His-AbA X-a-Gal plus plates (Fig. 1). The results indicated that IbERF1 owned transcriptional activity.

The interaction between IbERF1, IbPGP19 and IbPDC with PIbMYB1-4

Y1H were performed to identify whether IbERF1, IbPGP19 and IbPDC interacted with PIbMYB1-4. The yeast one-hybrid assay results indicated that the positive control can grow on SD/-Leu/AbA plates and that the negative control cannot grow on SD/-Leu/AbA plates. All of the transformed strains grew on SD/-Leu/AbA plates (Fig. 2). The results identified the interaction between IbERF1, IbPGP19 and IbPDC with PIbMYB1-4.

Dual-luciferase assays were carried out to further confirm the interaction between IbERF1, IbPGP19 and IbPDC with PIbMYB1-4. As illustrated in Fig. 3, IbERF1, IbPGP19 and IbPDC showed a significant activation effect on PIbMYB1-4. The results identified the interaction between IbERF1, IbPGP19 and IbPDC with PIbMYB1-4.

Subcellular localization of IbERF1, IbPGP19 and IbPDC

Subcellular localization prediction showed that IbERF1, IbPGP19 and IbPDC were localized in the nuclei. To confirm this prediction, green fluorescent protein (GFP) was fused to the C-terminus of IbERF1, IbPGP19, and IbPDC and transiently expressed in arabidopsis protoplasts under the control of the UBQ promoter. The green fluorescence of the GFP control was observed in the nucleus and cytoplasm. Green fluorescence from IbERF1/IbPGP19/IbPDC-GFP fusions was only detected in the nucleus (Fig. 4), suggesting that IbERF1, IbPGP19 and IbPDC were nuclear proteins and functioned as TFs to regulate the expression of downstream genes.

The expression characteristics of IbERF1

The gene expression of upstream transcription factors, transcription factors and structural genes involved in anthocyanin biosynthesis in different root stages of purple-fleshed and white-fleshed sweet potato was analyzed by real-time PCR (Fig. 5). The results showed that the expression of transcription factors and structural genes in different root stages of purple-fleshed was higher than that in white-fleshed sweet potato.

Anthocyanin biosynthesis is regulated by the MYB-bHLH-WD40 complex in plants. Other TFs, including WRKYs, NACs, ERFs, COP1, SPL9 and DELLA proteins, have been identified to directly or indirectly affect the activity of the MBW complex in determining anthocyanin biosynthesis (Morishita et al. 2009; Gou et al. 2011; Maier et al. 2013; Zhou et al. 2015; Xie et al. 2016; Yao et al. 2017; Li et al. 2020). IbMYB1 has been identified to be involved in anthocyanin biosynthesis in purple-fleshed sweet potato. In this study, the upstream transcription factors of PIbMYB1 involved in anthocyanin biosynthesis were screened by yeast one-hybrid screening in purple-fleshed sweet potato storage roots. The results revealed that IbERF1 was the upstream transcription factor of PIbMYB1-4 involved in anthocyanin biosynthesis. The interaction between IbERF1 and PIbMYB1-4 was confirmed by a dual-luciferase assay and yeast one-hybrid assay. Subcellular localization analysis showed that IbERF1 was localized in the nucleus. Subcellular localization analysis indicated that IbERF1 was a nuclear protein and functioned as a TF to regulate the expression of downstream genes.

The ethylene response factors AP2/ERF are one of the largest transcription factor families involved in multiple physiological processes in plant growth and responses to biological and nonbiological stress (Zhuang et al. 2011; Johni et al. 2019). Studies have shown that transcription factor ERFs regulate anthocyanin biosynthesis in plants. In suspension-cultured carrot cells, DcERF1 can upregulate DcPAL3 promoter activity, and DcERF2 functions in different ways in anthocyanin biosynthesis (Kimura et al. 2008). In Salvia miltiorrhiza flowers, the transcription factors AP2/ERFs may regulate anthocyanin biosynthesis due to their significantly different expression levels between purple and white flowers in transcriptome data (Jiang et al. 2020). Transcription factor ERFs have been identified to regulate ethylene-induced and light-induced anthocyanin biosynthesis in different species. In plum, seven PsERFs were positively correlated with PsMYB10 and most of the structural genes involved in anthocyanin biosynthesis (Cheng et al. 2016). In arabidopsis, a double mutant (aterf4 and aterf8) reduced light-induced anthocyanin accumulation, indicating that AtERF4 and AtERF8 positively regulate anthocyanin biosynthesis (Koyama and Sato 2018). In pear, transcription factor ERFs are involved in light-induced anthocyanin biosynthesis (Bai et al. 2017).

ERF interacts with MYB proteins and binds to the promoters of MYB to regulate anthocyanin biosynthesis in plants. In apple, MdERF1B interacted with MdMYB9, MdMYB1 and MdMYB11 proteins to regulate anthocyanin biosynthesis. Furthermore, MdERF1B also bound to the promoters of MdMYB9, MdMYB1, and MdMYB11 to regulate anthocyanin biosynthesis (Zhang et al. 2018). MdERF38 bound to the promoters of MdMYB1 to regulate drought stress-induced anthocyanin biosynthesis at the posttranslational level (An et al. 2019). In pear, PpERF3 interacted with PpMYB114 and PpbHLH3 from the ERF3-MYB114-bHLH3 complex to regulate the coloration of red pear fruit (Yao et al. 2017), and Pp4ERF24 and Pp12ERF96 regulated light-induced anthocyanin biosynthesis (Ni et al. 2019). In strawberry, FaERF9 and FaMYB98 form the ERF-MYB complex and activate the FaQR promoter and increase the furaneol content in cultivated strawberry (Zhang et al. 2018b). In this study, IbERF1 interacted with the promotor of IbMYB1-4 to regulate anthocyanin biosynthesis in purple-fleshed sweet potato. The results provide a possible underlying mechanism of anthocyanin biosynthesis and a potential understanding of the regulatory network in purple-fleshed sweet potato.

IbERF1 has been screened as the transcription factor of IbMYB1-4 to regulates anthocyanin biosynthesis in purple-fleshed sweet potato.

Author contributions

Feng Gao designed the research. ShaoHua Yang and Riu Liu interpreted the results. DanWen Fu performed experiments, wrote the manuscript, analysed the results and conceived the study. All authors read and approved the manuscript.

Acknowledgments

This work were funded by the Key-Area Research and Development Program of Guangdong Province (2020B020219001).

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No competing interests reported.

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Screening transcription factors of IbMYB1-4 by yeast one-hybrid assays in purple-fleshed sweet potato

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