Identifying potential flavonoid biosynthesis regulator in Zanthoxylum bungeanum Maxim. by genome-wide characterization of the MYB transcription factor gene family

doi:10.1016/S2095-3119(21)63747-4

摘要/Abstract

摘要：

本研究在花椒中鉴定了270个MYB基因，并将其分为四个亚家族。 R2R3-MYB (ZbMYB) 包含251个基因，根据系统发育结果和序列相似性分为33个亚科。这些亚科中有24个同时包含花椒MYB和拟南芥AtMYB，9个仅包含花椒或拟南芥。具有相似功能的ZbMYB聚集在同一亚科中，表明功能保守。亚细胞定位分析预测大多数ZbMYB基因存在于细胞核中。转座复制在花椒MYB基因家族的扩展中起主要作用。通过系统发育分析和转录组分析，发现28个ZbMYB基因可能调控花椒中黄酮类化合物的生物合成，这些基因呈现出独特的时空表达模式。在花椒果实不同发育阶段，通过qRT-PCR分析得出EVM0042160和EVM0033809基因的表达模式与花椒中的黄酮类和花青素物质含量曲线非常相似。进一步相关性分析表明，不同发育阶段花椒果实的黄酮类物质含量与28个ZbMYB基因的转录本丰度具有不同程度的相关性。这些结果表明ZbMYB基因可能参与了花椒中黄酮类物质代谢途径。对为花椒中MYB基因家族全面系统分析以及进一步研究MYB转录因子的功能奠定了坚实的基础。

Abstract: Plant MYB transcription factors (TFs) play crucial roles in regulating the biosynthesis of flavonoids but current analysis on their role in Zanthoxylum bungeanum Maxim. (ZBM) is far from comprehensive. In this study, we identified 270 MYB genes in ZBM and divided them into four subfamilies. The R2R3-MYB (ZbMYB) category contained 251 genes and was classified into 33 subfamilies according to their phylogenetic results and sequence similarity. These subfamilies included 24 subgroups containing both MYBs of ZBM plants and AtMYBs, and nine subgroups containing only ZBM MYBs or AtMYBs. ZbMYBs with similar functions clustered into the same subgroup, indicating functional conservation. The subcellular localization analysis predicted that most ZbMYB genes were found in the nucleus. The transposed duplications appeared to play a major role in the expansion of the MYB gene family in ZBM. Through phylogenetic analysis and transcriptome profiling, it was found that 28 ZbMYB genes may regulate the biosynthesis of flavonoids in ZBM, and these genes expression presented distinct temporal and spatial expression patterns. In different fruit development stages of ZBM, the expression patterns of EVM0042160 and EVM0033809 genes obtained by qRT-PCR analysis are very similar to the flavonoid and anthocyanin content curves in ZBM. Further correlation analysis showed that the content of flavonoids in different fruit development stages and the transcript abundance levels of 28 ZbMYB genes have different degrees of correlation relationship. These results indicated that the ZbMYB genes might be involved in the flavonoid metabolic pathway. This comprehensive and systematic analysis of MYB family genes provided a solid foundation for further functional analysis of MYB TFs in ZBM.

Key words: Zanthoxylum bungeanum Maxim. , MYB transcription factor , expression pattern , regulation of flavonoid biosynthesis

. [J]. Journal of Integrative Agriculture, 2022, 21(7): 1997-2018.

WANG Xiang-yuan, TIAN Lu, FENG Shi-jing, WEI An-zhi. Identifying potential flavonoid biosynthesis regulator in Zanthoxylum bungeanum Maxim. by genome-wide characterization of the MYB transcription factor gene family[J]. Journal of Integrative Agriculture, 2022, 21(7): 1997-2018.

参考文献

van Aalten D M, Grotewold E, Joshua-Tor L. 1998. Essential dynamics from NMR clusters: Dynamic properties of the Myb DNA-binding domain and a hinge-bending enhancing variant. Methods, 14, 318–328.
Aharoni A, De Vos C H R, Wein M, Sun Z, Greco R, Kroon A, Mol J N M, O’Connell A P. 2001. The strawberry FaMYB1 transcription factor suppresses anthocyanin and flavonol accumulation in transgenic tobacco. The Plant Journal, 28, 319–332.
Altschul S F, Madden T L, Schäffer A A, Zhang J, Zhang Z, Miller W, Lipman D J. 1997. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Research, 25, 3389–3402.
Aya K, Ueguchi-Tanaka M, Kondo M, Hamada K, Yano K, Nishimura M, Matsuoka M. 2009. Gibberellin modulates anther development in rice via the transcriptional regulation of GAMYB. The Plant Cell, 21, 1453–1472.
Bailey T L, Boden M, Buske F A, Frith M, Grant C E, Clementi L, Ren J, Li W W, Noble W S. 2009. MEME SUITE: Tools for motif discovery and searching. Nucleic Acids Research, 37, W202–W208.
Bateman A, Coin L, Durbin R, Finn R D, Hollich V, Griffiths-Jones S, Khanna A, Marshall M, Moxon S, Sonnhammer E L, Studholme D J, Yeats C, Eddy S R. 2004. The Pfam protein families database. Nucleic Acids Research, 32, D138–D141.
Buer C S, Imin N, Djordjevic M A. 2010. Flavonoids: New roles for old molecules. Journal of Integrative Plant Biology, 52, 98–111.
Butelli E, Licciardello C, Zhang Y, Liu J, Mackay S, Bailey P, Reforgiato-Recupero G, Martin C. 2012. Retrotransposons control fruit-specific, cold-dependent accumulation of anthocyanins in blood oranges. The Plant Cell, 24, 1242–1255.
Cannon S B, Mitra A, Baumgarten A, Young N D, May G. 2004. The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biology, 4, 10.
Cao Z H, Zhang S Z, Wang R K, Zhang R F, Hao Y J. 2013. Genome wide analysis of the apple MYB transcription factor family allows the identification of MdoMYB121 gene confering abiotic stress tolerance in plants. PLoS ONE, 8, e69955.
de Castro E, Sigrist C J, Gattiker A, Bulliard V, Langendijk-Genevaux P S, Gasteiger E, Bairoch A, Hulo N. 2006. ScanProsite: Detection of PROSITE signature matches and ProRule-associated functional and structural residues in proteins. Nucleic Acids Research, 34, W362–W365.
Chagné D, Lin-Wang K, Espley R V, Volz R K, How N M, Rouse S, Brendolise C, Carlisle C M, Kumar S, De Silva N, Micheletti D, McGhie T, Crowhurst R N, Storey R D, Velasco R, Hellens R P, Gardiner S E, Allan A C. 2013. An ancient duplication of apple MYB transcription factors is responsible for novel red fruit-flesh phenotypes. Plant Physiollgy, 161, 225–239.
Chen H, Ouyang K, Jiang Y, Yang Z, Hu W, Xiong L, Wang N, Liu X, Wang W. 2017. Constituent analysis of the ethanol extracts of Chimonanthus nitens Oliv. leaves and their inhibitory effect on α-glucosidase activity. International Journal of Biological Macromolecules, 98, 829–836.
Chen S, Li X, Liu X, Wang N, An Q, Ye X M, Zhao Z T, Zhao M, Han Y, Ouyang K H, Wang W J. 2020. Investigation of chemical composition, antioxidant activity, and the effects of alfalfa flavonoids on growth performance. Oxidative Medicine and Cellular Longevity, 10, 8569237.
Chen Y, Yang X, Kun H, Liu M, Li J, Gao Z, Lin Z, Zhang Y, Wang X, Qiu X, Shen Y, Zhang L, Deng X, Luo J, Deng X, Chen Z, Gu H, Qu L. 2006. The MYB transcription factor superfamily of Arabidopsis: expression analysis and phylogenetic comparison with the rice MYB family. Plant Molecular Biology, 60, 107–124.
Cheynier V, Comte G, Davies K M, Lattanzio V, Martens S. 2013. Plant phenolics: Recent advances on their biosynthesis, genetics, and ecophysiology. Plant Physiology and Biochemistry, 72, 1–20.
Conant G C, Wolfe K H. 2008. Turning a hobby into a job: How duplicated genes find new functions. Nature Reviews Genetics, 9, 938–950.
Crooks G E, Hon G, Chandonia J M, Brenner S E. 2004. WebLogo: A sequence logo generator. Genome Research, 14, 1188–1190.
Dai X, Wang Y, Yang A, Zhang W H. 2012. OsMYB2P-1, an R2R3 MYB transcription factor, is involved in the regulation of phosphate-starvation responses and root architecture in rice. Plant Physiology, 159, 169–183.
Dassanayake M, Oh D H, Haas J S, Hernandez A, Hong H, Ali S, Yun D J, Bressan R A, Zhu J K, Bohnert H J, Cheeseman J M. 2011. The genome of the extremophile crucifer Thellungiella parvula. Nature Genetics, 43, 913–918.
Dias A P, Braun E L, McMullen M D, Grotewold E. 2003. Recently duplicated maize R2R3 Myb genes provide evidence for distinct mechanisms of evolutionary divergence after duplication. Plant Physiology, 131, 610–620.
Du H, Feng B R, Yang S S, Huang Y B, Tang Y X. 2012a. The R2R3-MYB transcription factor gene family in maize. PLoS ONE, 7, e37463.
Du H, Yang S S, Liang Z, Feng B R, Liu L, Huang Y B, Tang Y X. 2012b. Genome-wide analysis of the MYB transcription factor superfamily in soybean. BMC Plant Biology, 12, 106.
Dubos C, Stracke R, Grotewold E, Weisshaar B, Martin C, Lepiniec L. 2010. MYB transcription factors in Arabidopsis. Trends in Plant Science, 15, 573–581.
Falcone Ferreyra M L, Rius S P, Casati P. 2012. Flavonoids: Biosynthesis, biological functions, and biotechnological applications. Frontiers in Plant Science, 3, 222.
Feng S, Liu Z, Cheng J, Li Zi, Tian L, Liu M, Yang T, Liu Y, Liu Y, Dai H, Yang Z, Zhang Q, Wang G, Zhang J, Jiang H, Wei A. 2021. Zanthoxylum-specific whole genome duplication and recent activity of transposable elements in the highly repetitive paleotetraploid Z. bungeanum genome. Horticulture Research, 8, 205.
Finn R D, Clements J, Eddy S R. 2011. HMMER web server: Interactive sequence similarity searching. Nucleic Acids Research, 39, W29–W37.
Flagel L E, Wendel J F. 2009. Gene duplication and evolutionary novelty in plants. New Phytologist, 183, 557–564.
Fu L, Xie H, Shi S. 2018. Multielement analysis of Zanthoxylum bungeanum Maxim. essential oil using ICP-MS/MS. Analytical and Bioanalytical Chemistry, 410, 3769–3778.
Gonzalez A, Zhao M, Leavitt J M, Lloyd A M. 2008. Regulation of the anthocyanin biosynthetic pathway by the TTG1/bHLH/Myb transcriptional complex in Arabidopsis seedlings. The Plant Journal, 53, 814–827.
Grotewold E, Athma P, Peterson T. 1991. Alternatively spliced products of the maize P gene encode proteins with homology to the DNA-binding domain of myb-like transcription factors. Proceedings of the National Academy of Sciences of the United States of America, 88, 4587–4591.
Guo L, Ma X, Li Y, Wang P J I C. 2021. The impact of polysaccharides and flavonoids in black fungus on resistance to oxidative stress and X-ray environmental radiation. IOP Conference Series (Earth and Environmental Science), 631, 012010.
Ha M, Li W H, Chen Z J. 2007. External factors accelerate expression divergence between duplicate genes. Trends in Genetics, 23, 162–166.
Hajiebrahimi A, Owji H, Hemmati S. 2017. Genome-wide identification, functional prediction, and evolutionary analysis of the R2R3-MYB superfamily in Brassica napus. Genome, 60, 797–814.
Heine G F, Hernandez J M, Grotewold E. 2004. Two cysteines in plant R2R3 MYB domains participate in REDOX-dependent DNA binding. Journal of Biochemistry and Molecular Biology, 279, 37878–37885.
Hou X J, Li S B, Liu S R, Hu C G, Zhang J Z. 2014. Genome-wide classification and evolutionary and expression analyses of citrus MYB transcription factor families in sweet orange. PLoS ONE, 9, e112375.
Huang D, Tang Z, Fu J, Yuan Y, Deng X, Xu Q. 2020. CsMYB3 and CsRuby1 form an ‘Activator-and-Repressor’ loop for the regulation of anthocyanin biosynthesis in citrus. Plant Cell Physiology, 61, 318–330.
Jiang C, Gu X, Peterson T. 2004. Identification of conserved gene structures and carboxy-terminal motifs in the Myb gene family of Arabidopsis and Oryza sativa L. ssp. indica. Genome Biology, 5, R46.
Jiang C K, Rao G Y. 2020. Insights into the diversification and evolution of R2R3-MYB transcription factors in plants. Plant Physiology, 183, 637–655.
Jin H, Cominelli E, Bailey P, Parr A, Mehrtens F, Jones J, Tonelli C, Weisshaar B, Martin C. 2000. Transcriptional repression by AtMYB4 controls production of UV-protecting sunscreens in Arabidopsis. EMBO Journal, 19, 6150–6161.
Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones S J, Marra M A J G R. 2009. Circos: An information aesthetic for comparative genomics. Genome Research, 19, 1639–1645.
Larkin M A, Blackshields G, Brown N P, Chenna R, McGettigan P A, McWilliam H, Valentin F, Wallace I M, Wilm A, Lopez R, Thompson J D, Gibson T J, Higgins D G. 2007. Clustal W and clustal X version 2.0. Bioinformatics, 23, 2947–2948.
Lei H, Niu T, Song H, Bai B, Liu A J I C, Products. 2021. Comparative transcriptome profiling reveals differentially expressed genes involved in flavonoid biosynthesis between biennial and triennial Sophora flavescens. Industrial Crops and Products, 161, 113217.
Letunic I, Copley R R, Schmidt S, Ciccarelli F D, Doerks T, Schultz J, Ponting C P, Bork P. 2004. SMART 4.0: towards genomic data integration. Nucleic Acids Research, 32, D142–D144.
Li C, Lu S. 2014. Genome-wide characterization and comparative analysis of R2R3-MYB transcription factors shows the complexity of MYB-associated regulatory networks in Salvia miltiorrhiza. BMC Genomics, 15, 277.
Li X, Guo C, Ahmad S, Wang Q, Guo Y J B. 2019. Systematic analysis of MYB family genes in potato and their multiple roles in development and stress responses. Biomolecules, 9, 317.
Li X, Xue C, Li J, Qiao X, Li L, Yu L, Huang Y, Wu J. 2016. Genome-wide identification, evolution and functional divergence of MYB transcription factors in Chinese white pear (Pyrus bretschneideri). Plant Cell Physiology, 57, 824–847.
Lipsick J S. 1996. One billion years of Myb. Oncogene, 13, 223–235.
Liu C, Xie T, Chen C, Luan A, Long J, Li C, Ding Y, He Y. 2017. Genome-wide organization and expression profiling of the R2R3-MYB transcription factor family in pineapple (Ananas comosus). BMC Genomics, 18, 503–503.
Liu Y, Shi Z, Maximova S N, Payne M J, Guiltinan M J. 2015. Tc-MYBPA an Arabidopsis TT2-like transcription factor and functions in the regulation of proanthocyanidin synthesis in Theobroma cacao. BMC Plant Biology, 15, 160.
Livak K J, Schmittgen T D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods, 25, 402–408.
Ma D, Constabel C P. 2019. MYB repressors as regulators of phenylpropanoid metabolism in plants. Trends in Plant Science, 24, 275–289.
Ma Y, Wang Y, Li X, Hou L, Wei A. 2019. Sensory characteristics and antioxidant activity of Zanthoxylum bungeanum Maxim. pericarps. Chemistry & Biodiversity, 16, e1800238.
Matus J T, Aquea F, Arce-Johnson P. 2008. Analysis of the grape MYB R2R3 subfamily reveals expanded wine quality-related clades and conserved gene structure organization across Vitis and Arabidopsis genomes. BMC Plant Biology, 8, 83.
Medina-Puche L, Cumplido-Laso G, Amil-Ruiz F, Hoffmann T, Ring L, Rodríguez-Franco A, Caballero J L, Schwab W, Muñoz-Blanco J, Blanco-Portales R. 2014. MYB10 plays a major role in the regulation of flavonoid/phenylpropanoid metabolism during ripening of Fragaria×ananassa fruits. Journal of Experimental Botany, 65, 401–417.
Mol J, Grotewold E, Koes R. 1998. How genes paint flowers and seeds. Trends in Plant Science, 3, 212–217.
Morita Y, Saitoh M, Hoshino A, Nitasaka E, Iida S. 2006. Isolation of cDNAs for R2R3-MYB, bHLH and WDR transcriptional regulators and identification of c and ca mutations conferring white flowers in the Japanese morning glory. Plant and Cell Physiology, 47, 457–470.
Nakatsuka T, Saito M, Yamada E, Fujita K, Kakizaki Y, Nishihara M. 2012. Isolation and characterization of GtMYBP3 and GtMYBP4, orthologues of R2R3-MYB transcription factors that regulate early flavonoid biosynthesis, in gentian flowers. Journal of Experimental Botany, 63, 6505–6517.
Neff M M, Chory J. 1998. Genetic interactions between phytochrome A, phytochrome B, and cryptochrome 1 during Arabidopsis development. Plant Physiology, 118, 27–35.
Nesi N, Jond C, Debeaujon I, Caboche M, Lepiniec L. 2001. The Arabidopsis TT2 gene encodes an R2R3 MYB domain protein that acts as a key determinant for proanthocyanidin accumulation in developing seed. The Plant Cell, 13, 2099–2114.
Owens D K, Alerding A B, Crosby K C, Bandara A B, Westwood J H, Winkel B S. 2008. Functional analysis of a predicted flavonol synthase gene family in Arabidopsis. Plant Physiology, 147, 1046–1061.
Petroni K, Tonelli C. 2011. Recent advances on the regulation of anthocyanin synthesis in reproductive organs. Plant Science, 181, 219–229.
Pollastri S, Tattini M. 2011. Flavonols: Old compounds for old roles. Annals of Botany, 108, 1225–1233.
Preston J, Wheeler J, Heazlewood J, Li S F, Parish R W. 2004. AtMYB32 is required for normal pollen development in Arabidopsis thaliana. The Plant Journal, 40, 979–995.
Qiao X, Li Q, Yin H, Qi K, Li L, Wang R, Zhang S, Paterson A H. 2019. Gene duplication and evolution in recurring polyploidization–diploidization cycles in plants. Genome Biology, 20, 38.
Ross J A, Kasum C M. 2002. Dietary flavonoids: Bioavailability, metabolic effects, and safety. Annual Review of Nutrition, 22, 19–34.
Routaboul J M, Kerhoas L, Debeaujon I, Pourcel L, Caboche M, Einhorn J, Lepiniec L. 2006. Flavonoid diversity and biosynthesis in seed of Arabidopsis thaliana. Planta, 224, 96–107.
Sampath P, Lee S C, Lee J, Izzah N K, Choi B S, Jin M, Park B S, Yang T J. 2013. Characterization of a new high copy Stowaway family MITE, BRAMI-1 in Brassica genome. BMC Plant Biology, 13, 56.
Seifert E. 2014. OriginPro 9.1: Scientific data analysis and graphing software - software review. Journal of Chemical Information and Modeling, 54, 1552.
Solomon A, Golubowicz S, Yablowicz Z, Grossman S, Bergman M, Gottlieb H E, Altman A, Kerem Z, Flaishman M A. 2006. Antioxidant activities and anthocyanin content of fresh fruits of common fig (Ficus carica L.). Journal of Agricultural and Food Chemistry, 54, 7717–7723.
Stracke R, Holtgräwe D, Schneider J, Pucker B, Sörensen T R, Weisshaar B. 2014. Genome-wide identification and characterisation of R2R3-MYB genes in sugar beet (Beta vulgaris). BMC Plant Biology, 14, 249.
Stracke R, Ishihara H, Huep G, Barsch A, Mehrtens F, Niehaus K, Weisshaar B. 2007. Differential regulation of closely related R2R3-MYB transcription factors controls flavonol accumulation in different parts of the Arabidopsis thaliana seedling. The Plant Journal, 50, 660–677.
Stracke R, Werber M, Weisshaar B. 2001. The R2R3-MYB gene family in Arabidopsis thaliana. Current Opinion in Plant Biology, 4, 447–456.
Sutharut J, Sudarat J. 2012. Total anthocyanin content and antioxidant activity of germinated colored rice. International Food Research Journal, 19, 215–221.
Tamate S C, Kawata M, Makino T. 2014. Contribution of nonohnologous duplicated genes to high habitat variability in mammals. Molecular Biology and Evolution, 31, 1779–1786.
Thompson J D, Gibson T J, Plewniak F, Jeanmougin F, Higgins D G. 1997. The CLUSTAL_X windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research, 25, 4876–4882.
Trapnell C, Williams B A, Pertea G, Mortazavi A, Kwan G, van Baren M J, Salzberg S L, Wold B J, Pachter L. 2010. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nature Biotechnology, 28, 511–515.
Walker A R, Lee E, Bogs J, McDavid D A, Thomas M R, Robinson S P. 2007. White grapes arose through the mutation of two similar and adjacent regulatory genes. The Plant Journal, 49, 772–785.
Wang X, Niu Q W, Teng C, Li C, Mu J, Chua N H, Zuo J. 2009. Overexpression of PGA37/MYB118 and MYB115 promotes vegetative-to-embryonic transition in Arabidopsis. Cell Research, 19, 224–235.
Wang Y, Tang H, Debarry D J, Tan X, Li J, Wang X, Lee T H, Jin H, Marler B, Guo H, Kissinger J C, Paterson A H. 2012a. MCScanX: A toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Research, 40, e49–e49.
Wang Y, Wang X, Paterson A H. 2012b. Genome and gene duplications and gene expression divergence: a view from plants. Annals of the New York Academy of Sciences, 1256, 1–14.
Waqas M, Azhar M T, Rana I A, Azeem F, Ali M A, Nawaz M A, Chung G, Atif R M. 2019. Genome-wide identification and expression analyses of WRKY transcription factor family members from chickpea (Cicer arietinum L.) reveal their role in abiotic stress-responses. Genes Genomics, 41, 467–481.
Wei Y, Shi H, Xia Z, Tie W, Ding Z, Yan Y, Wang W, Hu W, Li K. 2016. Genome-wide identification and expression analysis of the WRKY gene family in Cassava. Frontiers in Plant Science, 7, 25.
Wilkins O, Nahal H, Foong J, Provart N J, Campbell M M. 2009. Expansion and diversification of the Populus R2R3-MYB family of transcription factors. Plant Physiology, 149, 981–993.
Williams C E, Grotewold E. 1997. Differences between plant and animal Myb domains are fundamental for DNA binding activity, and chimeric Myb domains have novel DNA binding specificities. Journal of Biological Chemistry, 272, 563–571.
Xu G, Ma H, Nei M, Kong H. 2009. Evolution of F-box genes in plants: Different modes of sequence divergence and their relationships with functional diversification. Proceedings of the National Academy of Sciences of the United States of America, 106, 835–840.
Xu W, Dubos C, Lepiniec L. 2015. Transcriptional control of flavonoid biosynthesis by MYB-bHLH-WDR complexes. Trends in Plant Science, 20, 176–185.
Yang F X, Su Y Q, Li X H, Zhang Q, Sun R C. 2008. Studies on the preparation of biodiesel from Zanthoxylum bungeanum Maxim seed oil. Journal of Agricultural and Food Chemistry, 56, 7891–7896.
Yang L, Rong L, Jiang Z. 2012. Microwave-assisted extraction of flavonoids from Zanthoxylum bungeanum and its antioxidant activities. Food Science and Technology, 37, 214–222. (in Chinese)
Yang L C, Li R, Tan J, Jiang Z T. 2013. Polyphenolics composition of the leaves of Zanthoxylum bungeanum Maxim. grown in Hebei, China, and their radical scavenging activities. Journal of Agricultural and Food Chemistry, 61, 1772–1778.
Yang X, Zhou T, Wang M, Li T, Wang G, Fu F, Cao F. 2021. Systematic investigation and expression profiles of the GbR2R3-MYB transcription factor family in ginkgo (Ginkgo biloba L.). International Journal of Biological Macromolecules, 172, 250–262.
Zhang C, Ma R, Xu J, Yan J, Guo L, Song J, Feng R, Yu M. 2018. Genome-wide identification and classification of MYB superfamily genes in peach. PLoS ONE, 13, e0199192.
Zhang L, Zhao G, Jia J, Liu X, Kong X. 2012. Molecular characterization of 60 isolated wheat MYB genes and analysis of their expression during abiotic stress. Journal of Experimental Botany, 63, 203–214.
Zhang M, Wang J, Zhu L, Li T, Jiang W, Zhou J, Peng W, Wu C. 2017. Zanthoxylum bungeanum Maxim. (Rutaceae): A systematic review of its traditional uses, botany, phytochemistry, pharmacology, pharmacokinetics, and toxicology. International Journal of Molecular Sciences, 18, 2172.
Zhao Y, Dong W, Wang K, Zhang B, Allan A C, Lin-Wang K, Chen K, Xu C. 2017. Differential sensitivity of fruit pigmentation to ultraviolet light between two peach cultivars. Frontiers Plant Science, 8, 1552–1552.
Zhong R, Lee C, Zhou J, McCarthy R L, Ye Z H. 2008. A battery of transcription factors involved in the regulation of secondary cell wall biosynthesis in Arabidopsis. The Plant Cell, 20, 2763–2782.
Zhou J, Lee C, Zhong R, Ye Z H. 2009. MYB58 and MYB63 are transcriptional activators of the lignin biosynthetic pathway during secondary cell wall formation in Arabidopsis. The Plant Cell, 21, 248–266.
Zimmermann I M, Heim M A, Weisshaar B, Uhrig J F. 2004. Comprehensive identification of Arabidopsis thaliana MYB transcription factors interacting with R/B-like BHLH proteins. The Plant Journal, 40, 22–34.