The WKRY transcription factor MdWRKY75 regulates anthocyanins accumulation in apples (Malus domestica)
Mengyu Su A B , Weifang Zuo A B , Yicheng Wang A B , Wenjun Liu A B , Zongying Zhang A B , Nan Wang A B and Xuesen Chen A B *A State Key Laboratory of Crop Biology, College of Horticulture Science and Engineering, Shandong Agricultural University, Tai-An, Shandong, China.
B Collaborative Innovation Center of Fruit and Vegetable Quality and Efficient Production in Shandong, Tai-An, China.
Functional Plant Biology 49(9) 799-809 https://doi.org/10.1071/FP21146
Submitted: 10 May 2021 Accepted: 25 April 2022 Published: 17 May 2022
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
Anthocyanins play important roles in plant secondary metabolism. Although previous studies have identified many transcription factors (TFs) that participate in the synthetic pathway of anthocyanins, the regulation mechanism of the pathway remain poorly understood. In this study, we identified a WRKY Group IIc TF, MdWRKY75, which contained a typical WRKYGQK heptapeptide sequence and a C2H2-zinc finger structure. Subcellular localisation assays found that MdWRKY75 was located in the nucleus. Overexpression of MdWRKY75 promoted the accumulation of anthocyanins in apple (Malus domestica L.) ‘Orin’ calli. MdWRKY75 mainly stimulated the accumulation of anthocyanins by binding to the promoter of MYB transcription factor, MdMYB1. Our research could provide new insights into how WRKY TFs regulate the accumulation of anthocyanins in apples.
Keywords: anthocyanin, apple, expression analysis, interaction, MdMYB1, MdWKRY75, MYB transcription factor, WRKY transcription factor.
References
Amato A, Cavallini E, Zenoni S, Finezzo L, Begheldo M, Ruperti B, Tornielli GB (2017) A grapevine TTG2-like WRKY transcription factor is involved in regulating vacuolar transport and flavonoid biosynthesis. Frontiers in Plant Science 7, 1979| A grapevine TTG2-like WRKY transcription factor is involved in regulating vacuolar transport and flavonoid biosynthesis.Crossref | GoogleScholarGoogle Scholar | 28105033PubMed |
An X-H, Tian Y, Chen K-Q, Wang X-F, Hao Y-J (2012) The apple WD40 protein MdTTG1 interacts with bHLH but not MYB proteins to regulate anthocyanin accumulation. Journal of Plant Physiology 169, 710–717.
| The apple WD40 protein MdTTG1 interacts with bHLH but not MYB proteins to regulate anthocyanin accumulation.Crossref | GoogleScholarGoogle Scholar | 22405592PubMed |
An X-H, Tian Y, Chen K-Q, Liu X-J, Liu D-D, Xie X-B, Cheng C-G, Cong P-H, Hao Y-J (2015) MdMYB9 and MdMYB11 are involved in the regulation of the JA-induced biosynthesis of anthocyanin and proanthocyanidin in apples. Plant and Cell Physiology 56, 650–662.
| MdMYB9 and MdMYB11 are involved in the regulation of the JA-induced biosynthesis of anthocyanin and proanthocyanidin in apples.Crossref | GoogleScholarGoogle Scholar | 25527830PubMed |
An J-P, Zhang X-W, You C-X, Bi S-Q, Wang X-F, Hao Y-J (2019a) MdWRKY40 promotes wounding-induced anthocyanin biosynthesis in association with MdMYB1 and undergoes MdBT2-mediated degradation. New Phytologist 224, 380–395.
| MdWRKY40 promotes wounding-induced anthocyanin biosynthesis in association with MdMYB1 and undergoes MdBT2-mediated degradation.Crossref | GoogleScholarGoogle Scholar | 31225908PubMed |
An J-P, Wang X-F, Zhang X-W, Bi S-Q, You C-X, Hao Y-J (2019b) MdBBX22 regulates UV-B-induced anthocyanin biosynthesis through regulating the function of MdHY5 and is targeted by MdBT2 for 26S proteasome-mediated degradation. Plant Biotechnology Journal 17, 2231–2233.
| MdBBX22 regulates UV-B-induced anthocyanin biosynthesis through regulating the function of MdHY5 and is targeted by MdBT2 for 26S proteasome-mediated degradation.Crossref | GoogleScholarGoogle Scholar | 31222855PubMed |
Ban Y, Honda C, Hatsuyama Y, Igarashi M, Bessho H, Moriguchi T (2007) Isolation and functional analysis of a MYB transcription factor gene that is a key regulator for the development of red coloration in apple skin. Plant and Cell Physiology 48, 958–970.
| Isolation and functional analysis of a MYB transcription factor gene that is a key regulator for the development of red coloration in apple skin.Crossref | GoogleScholarGoogle Scholar | 17526919PubMed |
Baudry A, Heim MA, Dubreucq B, Caboche M, Weisshaar B, Lepiniec L (2004) TT2, TT8, and TTG1 synergistically specify the expression of BANYULS and proanthocyanidin biosynthesis in Arabidopsis thaliana. The Plant Journal 39, 366–380.
| TT2, TT8, and TTG1 synergistically specify the expression of BANYULS and proanthocyanidin biosynthesis in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 15255866PubMed |
Bogs J, Jaffé FW, Takos AM, Walker AR, Robinson SP (2007) The grapevine transcription factor VvMYBPA1 regulates proanthocyanidin synthesis during fruit development. Plant Physiology 143, 1347–1361.
| The grapevine transcription factor VvMYBPA1 regulates proanthocyanidin synthesis during fruit development.Crossref | GoogleScholarGoogle Scholar | 17208963PubMed |
Boss PK, Davies C, Robinson SP (1996) Analysis of the expression of anthocyanin pathway genes in developing Vitis vinifera L. cv Shiraz grape berries and the implications for pathway regulation. Plant Physiology 111, 1059–1066.
| Analysis of the expression of anthocyanin pathway genes in developing Vitis vinifera L. cv Shiraz grape berries and the implications for pathway regulation.Crossref | GoogleScholarGoogle Scholar | 12226348PubMed |
Britsch L, Grisebach H (1986) Purification and characterization of (2S)-flavanone 3-hydroxylase from Petunia hybrida. European Journal of Biochemistry 156, 569–577.
| Purification and characterization of (2S)-flavanone 3-hydroxylase from Petunia hybrida.Crossref | GoogleScholarGoogle Scholar | 3699024PubMed |
Chen L, Song Y, Li S, Zhang L, Zou C, Yu D (2012) The role of WRKY transcription factors in plant abiotic stresses. Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms 1819, 120–128.
| The role of WRKY transcription factors in plant abiotic stresses.Crossref | GoogleScholarGoogle Scholar |
Chen L, Xiang S, Chen Y, Li D, Yu D (2017) Arabidopsis WRKY45 interacts with the DELLA protein RGL1 to positively regulate age-triggered leaf senescence. Molecular Plant 10, 1174–1189.
| Arabidopsis WRKY45 interacts with the DELLA protein RGL1 to positively regulate age-triggered leaf senescence.Crossref | GoogleScholarGoogle Scholar | 28735023PubMed |
Devaiah BN, Karthikeyan AS, Raghothama KG (2007) WRKY75 transcription factor is a modulator of phosphate acquisition and root development in Arabidopsis. Plant Physiology 143, 1789–1801.
| WRKY75 transcription factor is a modulator of phosphate acquisition and root development in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 17322336PubMed |
Dixon RA, Paiva NL (1995) Stress-induced phenylpropanoid metabolism. The Plant Cell 7, 1085–1097.
| Stress-induced phenylpropanoid metabolism.Crossref | GoogleScholarGoogle Scholar | 12242399PubMed |
Duan S, Wang J, Gao C, Jin C, Li D, Peng D, Du G, Li Y, Chen M (2018) Functional characterization of a heterologously expressed Brassica napus WRKY41-1 transcription factor in regulating anthocyanin biosynthesis in Arabidopsis thaliana. Plant Science 268, 47–53.
| Functional characterization of a heterologously expressed Brassica napus WRKY41-1 transcription factor in regulating anthocyanin biosynthesis in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 29362083PubMed |
Espley RV, Hellens RP, Putterill J, Stevenson DE, Kutty-Amma S, Allan AC (2007) Red colouration in apple fruit is due to the activity of the MYB transcription factor, MdMYB10. The Plant Journal 49, 414–427.
| Red colouration in apple fruit is due to the activity of the MYB transcription factor, MdMYB10.Crossref | GoogleScholarGoogle Scholar | 17181777PubMed |
Espley RV, Brendolise C, Chagné D, Kutty-Amma S, Green S, Volz R, Putterill J, Schouten HJ, Gardiner SE, Hellens RP, Allan AC (2009) Multiple repeats of a promoter segment causes transcription factor autoregulation in red apples. The Plant Cell 21, 168–183.
| Multiple repeats of a promoter segment causes transcription factor autoregulation in red apples.Crossref | GoogleScholarGoogle Scholar | 19151225PubMed |
Fang H, Dong Y, Yue X, Hu J, Jiang S, Xu H, Wang Y, Su M, Zhang J, Zhang Z, Wang N, Chen X (2019) The B-box zinc finger protein MdBBX20 integrates anthocyanin accumulation in response to ultraviolet radiation and low temperature. Plant, Cell & Environment 42, 2090–2104.
| The B-box zinc finger protein MdBBX20 integrates anthocyanin accumulation in response to ultraviolet radiation and low temperature.Crossref | GoogleScholarGoogle Scholar |
Gangappa SN, Botto JF (2016) The multifaceted roles of HY5 in plant growth and development. Molecular Plant 9, 1353–1365.
| The multifaceted roles of HY5 in plant growth and development.Crossref | GoogleScholarGoogle Scholar | 27435853PubMed |
Gonzalez A, Brown M, Hatlestad G, Akhavan N, Smith T, Hembd A, Moore J, Montes D, Mosley T, Resendez J, Nguyen H, Wilson L, Campbell A, Sudarshan D, Lloyd A (2016) TTG2 controls the developmental regulation of seed coat tannins in Arabidopsis by regulating vacuolar transport steps in the proanthocyanidin pathway. Developmental Biology 419, 54–63.
| TTG2 controls the developmental regulation of seed coat tannins in Arabidopsis by regulating vacuolar transport steps in the proanthocyanidin pathway.Crossref | GoogleScholarGoogle Scholar | 27046632PubMed |
Hahlbrock K, Scheel D (1989) Physiology and molecular biology of phenylpropanoid metabolism. Annual Review of Plant Biology and Plant Molecular Biology 40, 347–369.
| Physiology and molecular biology of phenylpropanoid metabolism.Crossref | GoogleScholarGoogle Scholar |
Harborne JB, Williams CA (2000) Advances in flavonoid research since 1992. Phytochemistry 55, 481–504.
| Advances in flavonoid research since 1992.Crossref | GoogleScholarGoogle Scholar | 11130659PubMed |
Hichri I, Barrieu F, Bogs J, Kappel C, Delrot S, Lauvergeat V (2011) Recent advances in the transcriptional regulation of the flavonoid biosynthetic pathway. Journal of Experimental Botany 62, 2465–2483.
| Recent advances in the transcriptional regulation of the flavonoid biosynthetic pathway.Crossref | GoogleScholarGoogle Scholar | 21278228PubMed |
Hu J, Fang H, Wang J, Yue X, Su M, Mao Z, Zou Q, Jiang H, Guo Z, Yu L, Feng T, Lu L, Peng Z, Zhang Z, Wang N, Chen X (2020) Ultraviolet B-induced MdWRKY72 expression promotes anthocyanin synthesis in apple. Plant Science 292, 110377
| Ultraviolet B-induced MdWRKY72 expression promotes anthocyanin synthesis in apple.Crossref | GoogleScholarGoogle Scholar | 32005382PubMed |
Jaakola L (2013) New insights into the regulation of anthocyanin biosynthesis in fruits. Trends in Plant Science 18, 477–483.
| New insights into the regulation of anthocyanin biosynthesis in fruits.Crossref | GoogleScholarGoogle Scholar | 23870661PubMed |
Jaakola L, Poole M, Jones MO, Kämäräinen-Karppinen T, Koskimäki JJ, Hohtola A, Häggman H, Fraser PD, Manning K, King GJ, Thomson H, Seymour GB (2010) A SQUAMOSA MADS box gene involved in the regulation of anthocyanin accumulation in bilberry fruits. Plant Physiology 153, 1619–1629.
| A SQUAMOSA MADS box gene involved in the regulation of anthocyanin accumulation in bilberry fruits.Crossref | GoogleScholarGoogle Scholar | 20566708PubMed |
Jiang Y, Liang G, Yang S, Yu D (2014) Arabidopsis WRKY57 functions as a node of convergence for jasmonic acid- and auxin-mediated signaling in jasmonic acid-induced leaf senescence. The Plant Cell 26, 230–245.
| Arabidopsis WRKY57 functions as a node of convergence for jasmonic acid- and auxin-mediated signaling in jasmonic acid-induced leaf senescence.Crossref | GoogleScholarGoogle Scholar | 24424094PubMed |
Johnson CS, Kolevski B, Smyth DR (2002) TRANSPARENT TESTA GLABRA2, a trichome and seed coat development gene of Arabidopsis, encodes a WRKY transcription factor. The Plant Cell 14, 1359–1375.
| TRANSPARENT TESTA GLABRA2, a trichome and seed coat development gene of Arabidopsis, encodes a WRKY transcription factor.Crossref | GoogleScholarGoogle Scholar | 12084832PubMed |
Koes R, Verweij W, Quattrocchio F (2005) Flavonoids: a colorful model for the regulation and evolution of biochemical pathways. Trends in Plant Science 10, 236–242.
| Flavonoids: a colorful model for the regulation and evolution of biochemical pathways.Crossref | GoogleScholarGoogle Scholar | 15882656PubMed |
Kubasek WL, Shirley BW, McKillop A, Goodman HM, Briggs W, Ausubel FM (1992) Regulation of flavonoid biosynthetic genes in germinating Arabidopsis seedlings. The Plant Cell 4, 1229–1236.
| Regulation of flavonoid biosynthetic genes in germinating Arabidopsis seedlings.Crossref | GoogleScholarGoogle Scholar | 12297632PubMed |
Li Y-Y, Mao K, Zhao C, Zhao X-Y, Zhang H-L, Shu H-R, Hao Y-J (2012) MdCOP1 ubiquitin E3 ligases interact with MdMYB1 to regulate light-induced anthocyanin biosynthesis and red fruit coloration in apple. Plant Physiology 160, 1011–1022.
| MdCOP1 ubiquitin E3 ligases interact with MdMYB1 to regulate light-induced anthocyanin biosynthesis and red fruit coloration in apple.Crossref | GoogleScholarGoogle Scholar | 22855936PubMed |
Li W, Wang H, Yu D (2016) Arabidopsis WRKY transcription factors WRKY12 and WRKY13 oppositely regulate flowering under short-day conditions. Molecular Plant 9, 1492–1503.
| Arabidopsis WRKY transcription factors WRKY12 and WRKY13 oppositely regulate flowering under short-day conditions.Crossref | GoogleScholarGoogle Scholar | 27592586PubMed |
Liu W, Wang Y, Yu L, Jiang H, Guo Z, Xu H, Jiang S, Fang H, Zhang J, Su M, Zhang Z, Chen X, Chen X, Wang N (2019) MdWRKY11 participates in anthocyanin accumulation in red-fleshed apples by affecting MYB transcription factors and the photoresponse factor MdHY5. Journal of Agricultural and Food Chemistry 67, 8783–8793.
| MdWRKY11 participates in anthocyanin accumulation in red-fleshed apples by affecting MYB transcription factors and the photoresponse factor MdHY5.Crossref | GoogleScholarGoogle Scholar | 31310107PubMed |
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25, 402–408.
| Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method.Crossref | GoogleScholarGoogle Scholar | 11846609PubMed |
Martens S, Teeri T, Forkmann G (2002) Heterologous expression of dihydroflavonol 4-reductases from various plants. FEBS Letters 531, 453–458.
| Heterologous expression of dihydroflavonol 4-reductases from various plants.Crossref | GoogleScholarGoogle Scholar | 12435592PubMed |
Miao Y, Zentgraf U (2007) The antagonist function of Arabidopsis WRKY53 and ESR/ESP in leaf senescence is modulated by the jasmonic and salicylic acid equilibrium. The Plant Cell 19, 819–830.
| The antagonist function of Arabidopsis WRKY53 and ESR/ESP in leaf senescence is modulated by the jasmonic and salicylic acid equilibrium.Crossref | GoogleScholarGoogle Scholar | 17369373PubMed |
Nesi N, Debeaujon I, Jond C, Pelletier G, Caboche M, Lepiniec L (2000) The TT8 gene encodes a basic helix-loop-helix domain protein required for expression of DFR and BAN genes in Arabidopsis siliques. The Plant Cell 12, 1863–1878.
| The TT8 gene encodes a basic helix-loop-helix domain protein required for expression of DFR and BAN genes in Arabidopsis siliques.Crossref | GoogleScholarGoogle Scholar | 11041882PubMed |
Quattrocchio F, Verweij W, Kroon A, Spelt C, Mol J, Koes R (2006) PH4 of Petunia Is an R2R3 MYB protein that activates vacuolar acidification through interactions with basic-helix-loop-helix transcription factors of the anthocyanin pathway. The Plant Cell 18, 1274–1291.
| PH4 of Petunia Is an R2R3 MYB protein that activates vacuolar acidification through interactions with basic-helix-loop-helix transcription factors of the anthocyanin pathway.Crossref | GoogleScholarGoogle Scholar | 16603655PubMed |
Rinerson CI, Rabara RC, Tripathi P, Shen QJ, Rushton PJ (2015) The evolution of WRKY transcription factors. BMC Plant Biology 15, 66
| The evolution of WRKY transcription factors.Crossref | GoogleScholarGoogle Scholar | 25849216PubMed |
Ross JA, Kasum CM (2002) DIETARY FLAVONOIDS: bioavailability, metabolic effects, and safety. Annual Review of Nutrition 22, 19–34.
| DIETARY FLAVONOIDS: bioavailability, metabolic effects, and safety.Crossref | GoogleScholarGoogle Scholar | 12055336PubMed |
Rushton PJ, Somssich IE, Ringler P, Shen QJ (2010) WRKY transcription factors. Trends in Plant Science 15, 247–258.
| WRKY transcription factors.Crossref | GoogleScholarGoogle Scholar | 20304701PubMed |
Schaart JG, Dubos C, Romero De La Fuente I, van Houwelingen AMML, de Vos RCH, Jonker HH, Xu W, Routaboul J-M, Lepinice L, Bovy AG (2013) Identification and characterization of MYB-bHLH-WD40 regulatory complexes controlling proanthocyanidin biosynthesis in strawberry (Fragaria × ananassa) fruits. New Phytologist 197, 454–467.
| Identification and characterization of MYB-bHLH-WD40 regulatory complexes controlling proanthocyanidin biosynthesis in strawberry (Fragaria × ananassa) fruits.Crossref | GoogleScholarGoogle Scholar | 23157553PubMed |
Song Y, Chen L, Zhang L, Yu D (2010) Overexpression of OsWRKY72 gene interferes in the abscisic acid signal and auxin transport pathway of Arabidopsis. Journal of Biosciences 35, 459–471.
| Overexpression of OsWRKY72 gene interferes in the abscisic acid signal and auxin transport pathway of Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Sun Q, Jiang S, Zhang T, Xu H, Fang H, Zhang J, Su M, Wang Y, Zhang Z, Wang N, Chen X (2019) Apple NAC transcription factor MdNAC52 regulates biosynthesis of anthocyanin and proanthocyanidin through MdMYB9 and MdMYB11. Plant Science 289, 110286
| Apple NAC transcription factor MdNAC52 regulates biosynthesis of anthocyanin and proanthocyanidin through MdMYB9 and MdMYB11.Crossref | GoogleScholarGoogle Scholar | 31623786PubMed |
Takos AM, Jaffé FW, Jacob SR, Bogs J, Robinson SP, Walker AR (2006) Light-induced expression of a MYB gene regulates anthocyanin biosynthesis in red apples. Plant Physiology 142, 1216–1232.
| Light-induced expression of a MYB gene regulates anthocyanin biosynthesis in red apples.Crossref | GoogleScholarGoogle Scholar | 17012405PubMed |
Ülker B, Somssich IE (2004) WRKY transcription factors: from DNA binding towards biological function. Current Opinion in Plant Biology 7, 491–498.
| WRKY transcription factors: from DNA binding towards biological function.Crossref | GoogleScholarGoogle Scholar | 15337090PubMed |
Umemura H, Otagaki S, Wada M, Kondo S, Matsumoto S (2013) Expression and functional analysis of a novel MYB gene, MdMYB110a_JP, responsible for red flesh, not skin color in apple fruit. Planta 238, 65–76.
| Expression and functional analysis of a novel MYB gene, MdMYB110a_JP, responsible for red flesh, not skin color in apple fruit.Crossref | GoogleScholarGoogle Scholar | 23568403PubMed |
Verweij W, Spelt CE, Bliek M, de Vries M, Wit N, Faraco M, Koes R, Quattrocchio FM (2016) Functionally similar WRKY proteins regulate vacuolar acidification in petunia and hair development in Arabidopsis. The Plant Cell 28, 786–803.
| Functionally similar WRKY proteins regulate vacuolar acidification in petunia and hair development in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 26977085PubMed |
Wang L, Lee I-M, Zhang SM, Blumberg JB, Buring JE, Sesso HD (2009) Dietary intake of selected flavonols, flavones, and flavonoid-rich foods and risk of cancer in middle-aged and older women. The American Journal of Clinical Nutrition 89, 905–912.
| Dietary intake of selected flavonols, flavones, and flavonoid-rich foods and risk of cancer in middle-aged and older women.Crossref | GoogleScholarGoogle Scholar | 19158208PubMed |
Wang N, Xu H, Jiang S, Zhang Z, Lu N, Qiu H, Qu C, Wang Y, Wu S, Chen X (2017) MYB12 and MYB22 play essential roles in proanthocyanidin and flavonol synthesis in red-fleshed apple (Malus sieversii f. niedzwetzkyana). The Plant Journal 90, 276–292.
| MYB12 and MYB22 play essential roles in proanthocyanidin and flavonol synthesis in red-fleshed apple (Malus sieversii f. niedzwetzkyana).Crossref | GoogleScholarGoogle Scholar | 28107780PubMed |
Williams CA, Grayer RJ (2004) Anthocyanins and other flavonoids. Natural Product Reports 21, 539–573.
| Anthocyanins and other flavonoids.Crossref | GoogleScholarGoogle Scholar | 15282635PubMed |
Wu J, Zhao G, Yang Y-N, Le W-Q, Khan MA, Zhang S-L, Gu C, Huang W-J (2013) Identification of differentially expressed genes related to coloration in red/green mutant pear (Pyrus communis L.). Tree Genetics & Genomes 9, 75–83.
| Identification of differentially expressed genes related to coloration in red/green mutant pear (Pyrus communis L.).Crossref | GoogleScholarGoogle Scholar |
Xie D-Y, Sharma SB, Paiva NL, Ferreira D, Dixon RA (2003) Role of anthocyanidin reductase, encoded by BANYULS in plant flavonoid biosynthesis. Science 299, 396–399.
| Role of anthocyanidin reductase, encoded by BANYULS in plant flavonoid biosynthesis.Crossref | GoogleScholarGoogle Scholar | 12532018PubMed |
Xie X-B, Li S, Zhang R-F, Zhao J, Chen Y-C, Zhao Q, Yao Y-X, You C-X, Zhang X-S, Hao Y-J (2012) The bHLH transcription factor MdbHLH3 promotes anthocyanin accumulation and fruit colouration in response to low temperature in apples. Plant, Cell & Environment 35, 1884–1897.
| The bHLH transcription factor MdbHLH3 promotes anthocyanin accumulation and fruit colouration in response to low temperature in apples.Crossref | GoogleScholarGoogle Scholar |
Xu Y-H, Wang J-W, Wang S, Wang J-Y, Chen X-Y (2004) Characterization of GaWRKY1, a cotton transcription factor that regulates the sesquiterpene synthase gene (+)-δ-cadinene synthase-A. Plant Physiology 135, 507–515.
| Characterization of GaWRKY1, a cotton transcription factor that regulates the sesquiterpene synthase gene (+)-δ-cadinene synthase-A.Crossref | GoogleScholarGoogle Scholar | 15133151PubMed |
Xu H, Wang N, Liu J, Qu C, Wang Y, Jiang S, Lu N, Wang D, Zhang Z, Chen X (2017) The molecular mechanism underlying anthocyanin metabolism in apple using the MdMYB16 and MdbHLH33 genes. Plant Molecular Biology 94, 149–165.
| The molecular mechanism underlying anthocyanin metabolism in apple using the MdMYB16 and MdbHLH33 genes.Crossref | GoogleScholarGoogle Scholar | 28286910PubMed |
Yao G, Ming M, Allan AC, Gu C, Li L, Wu X, Wang R, Chang Y, Qi K, Zhang S, Wu J (2017) Map-based cloning of the pear gene MYB114 identifies an interaction with other transcription factors to coordinately regulate fruit anthocyanin biosynthesis. The Plant Journal 92, 437–451.
| Map-based cloning of the pear gene MYB114 identifies an interaction with other transcription factors to coordinately regulate fruit anthocyanin biosynthesis.Crossref | GoogleScholarGoogle Scholar | 28845529PubMed |
Zhang Z-L, Xie Z, Zou X, Casaretto J, David Ho T-h, Shen QJ (2004) A rice WRKY gene encodes a transcriptional repressor of the gibberellin signaling pathway in aleurone cells. Plant Physiology 134, 1500–1513.
| A rice WRKY gene encodes a transcriptional repressor of the gibberellin signaling pathway in aleurone cells.Crossref | GoogleScholarGoogle Scholar | 15047897PubMed |
Zhang J, Xu H, Wang N, Jiang S, Fang H, Zhang Z, Yang G, Wang Y, Su M, Xu L, Chen X (2018) The ethylene response factor MdERF1B regulates anthocyanin and proanthocyanidin biosynthesis in apple. Plant Molecular Biology 98, 205–218.
| The ethylene response factor MdERF1B regulates anthocyanin and proanthocyanidin biosynthesis in apple.Crossref | GoogleScholarGoogle Scholar | 30182194PubMed |
Zhou X, Jiang Y, Yu D (2011) WRKY22 transcription factor mediates dark-induced leaf senescence in Arabidopsis. Molecules and Cells 31, 303–313.
| WRKY22 transcription factor mediates dark-induced leaf senescence in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 21359674PubMed |
Zhou H, Lin-Wang K, Wang H, Gu C, Dare AP, Espley RV, He H, Allan AC, Han Y (2015) Molecular genetics of blood-fleshed peach reveals activation of anthocyanin biosynthesis by NAC transcription factors. The Plant Journal 82, 105–121.
| Molecular genetics of blood-fleshed peach reveals activation of anthocyanin biosynthesis by NAC transcription factors.Crossref | GoogleScholarGoogle Scholar | 25688923PubMed |
Zou XL, Seemann JR, Neuman D, Shen QJ (2004) A WRKY gene from creosote bush encodes an activator of the abscisic acid signaling pathway. Journal of Biological Chemistry 279, 55770–55779.
| A WRKY gene from creosote bush encodes an activator of the abscisic acid signaling pathway.Crossref | GoogleScholarGoogle Scholar |