Identification of MYB Transcription Factors Involving in Fruit Quality Regulation of Fragaria × ananassa Duch.
Abstract
:1. Introduction
2. Materials and Methods
2.1. Identification and Phylogenetic Analyses of FaMYB Family
2.2. Synteny Analysis and Alleles Identification of FaMYBs
2.3. Gene Structure, Motif and Cis-Acting Elements Analyses of FaMYB Family
2.4. Expression Analysis
3. Results
3.1. Identification and Lineages of FaMYB Family
3.2. Gene Duplications and Alleles of FaMYBs
3.3. The Gene Structures, Motifs, and Cis-Elements of FaMYBs
3.4. Expression Analysis of FaMYBs
4. Discussion
4.1. The Expansion and Naming of FaMYB
4.2. FaMYB Candidates Involved in Fruit Quality
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Stracke, R.; Werber, M.; Weisshaar, B. The R2R3-MYB gene family in Arabidopsis thaliana. Curr. Opin. Plant Biol. 2001, 4, 447–456. [Google Scholar] [CrossRef] [PubMed]
- Martin, C.; Paz-Ares, J. MYB transcription factors in plants. Trends Genet. 1997, 13, 67–73. [Google Scholar] [CrossRef] [PubMed]
- Dubos, C.; Stracke, R.; Grotewold, E.; Weisshaar, B.; Martin, C.; Lepiniec, L. MYB transcription factors in Arabidopsis. Trends Plant Sci. 2010, 15, 573–581. [Google Scholar] [CrossRef] [PubMed]
- Ma, D.; Constabel, C.P. MYB Repressors as Regulators of Phenylpropanoid Metabolism in Plants. Trends Plant Sci. 2019, 24, 275–289. [Google Scholar] [CrossRef] [PubMed]
- Bai, Q.; Huang, Y.; Shen, Y. The Physiological and Molecular Mechanism of Abscisic Acid in Regulation of Fleshy Fruit Ripening. Front. Plant Sci. 2020, 11, 619953. [Google Scholar] [CrossRef] [PubMed]
- Chen, L.; Hu, B.; Qin, Y.; Hu, G.; Zhao, J. Advance of the negative regulation of anthocyanin biosynthesis by MYB transcription factors. Plant Physiol. Biochem. 2019, 136, 178–187. [Google Scholar] [CrossRef]
- Naing, A.H.; Kim, C.K. Roles of R2R3-MYB transcription factors in transcriptional regulation of anthocyanin biosynthesis in horticultural plants. Plant Mol. Biol. 2018, 98, 1–18. [Google Scholar] [CrossRef]
- Yan, J.W.; Ban, Z.J.; Lu, H.Y.; Li, D.; Poverenov, E.; Luo, Z.S.; Li, L. The aroma volatile repertoire in strawberry fruit: A review. J. Sci. Food Agric. 2018, 98, 4395–4402. [Google Scholar] [CrossRef]
- Capocasa, F.; Diamanti, J.; Tulipani, S.; Battino, M.; Mezzetti, B. Breeding strawberry (Fragaria X ananassa Duch) to increase fruit nutritional quality. Biofactors 2008, 34, 67–72. [Google Scholar] [CrossRef]
- Basu, A.; Schell, J.; Scofield, R.H. Dietary fruits and arthritis. Food Funct. 2018, 9, 70–77. [Google Scholar] [CrossRef]
- Montefiori, M.; Brendolise, C.; Dare, A.P.; Lin-Wang, K.; Davies, K.M.; Hellens, R.P.; Allan, A.C. In the Solanaceae, a hierarchy of bHLHs confer distinct target specificity to the anthocyanin regulatory complex. J. Exp. Bot. 2015, 66, 1427–1436. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bustamante, L.; Sáez, V.; Hinrichsen, P.; Castro, M.H.; Vergara, C.; von Baer, D.; Mardones, C. Differences in Vvufgt and VvmybA1 Gene Expression Levels and Phenolic Composition in Table Grape (Vitis vinifera L.) ‘Red Globe’ and Its Somaclonal Variant ‘Pink Globe’. J. Agric. Food Chem. 2017, 65, 2793–2804. [Google Scholar] [CrossRef] [PubMed]
- Lai, B.; Du, L.N.; Liu, R.; Hu, B.; Su, W.B.; Qin, Y.H.; Zhao, J.T.; Wang, H.C.; Hu, G.B. Two LcbHLH Transcription Factors Interacting with LcMYB1 in Regulating Late Structural Genes of Anthocyanin Biosynthesis in Nicotiana and Litchi chinensis During Anthocyanin Accumulation. Front. Plant Sci. 2016, 7, 166. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kadomura-Ishikawa, Y.; Miyawaki, K.; Takahashi, A.; Noji, S. RNAi-mediated silencing and overexpression of the FaMYB1 gene and its effect on anthocyanin accumulation in strawberry fruit. Biol. Plant. 2015, 59, 677–685. [Google Scholar] [CrossRef]
- 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. MYB10 plays a major role in the regulation of flavonoid/phenylpropanoid metabolism during ripening of Fragaria × ananassa fruits. J. Exp. Bot. 2014, 65, 401–417. [Google Scholar] [CrossRef] [Green Version]
- Castillejo, C.; Waurich, V.; Wagner, H.; Ramos, R.; Oiza, N.; Muñoz, P.; Triviño, J.C.; Caruana, J.; Liu, Z.; Cobo, N.; et al. Allelic Variation of MYB10 Is the Major Force Controlling Natural Variation in Skin and Flesh Color in Strawberry (Fragaria spp.) Fruit. Plant Cell 2020, 32, 3723–3749. [Google Scholar] [CrossRef]
- Yuan, H.; Cai, W.; Chen, X.; Pang, F.; Wang, J.; Zhao, M. Heterozygous frameshift mutation in FaMYB10 is responsible for the natural formation of red and white-fleshed strawberry (Fragaria × ananassa Duch). Front. Plant Sci. 2022, 13, 1027567. [Google Scholar] [CrossRef]
- Wei, L.; Mao, W.; Jia, M.; Xing, S.; Usman, A.; Zhao, Y.; Chen, Y.; Cao, M.; Dai, Z.; Zhang, K. FaMYB44.2, a transcriptional repressor, negatively regulates sucrose accumulation in strawberry receptacles through interplay with FaMYB10. J. Exp. Bot. 2018, 69, 4805–4820. [Google Scholar] [CrossRef] [Green Version]
- Rao, M.J.; Zuo, H.; Xu, Q. Genomic insights into citrus domestication and its important agronomic traits. Plant Commun. 2021, 2, 100138. [Google Scholar] [CrossRef]
- Strazzer, P.; Spelt, C.E.; Li, S.; Bliek, M.; Federici, C.T.; Roose, M.L.; Koes, R.; Quattrocchio, F.M. Hyperacidification of Citrus fruits by a vacuolar proton-pumping P-ATPase complex. Nat. Commun. 2019, 10, 744. [Google Scholar] [CrossRef]
- Quattrocchio, F.; Verweij, W.; Kroon, A.; Spelt, C.; Mol, J.; Koes, R. 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. Plant Cell 2006, 18, 1274–1291. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liu, Y.; Zhu, L.; Yang, M.; Xie, X.; Sun, P.; Fang, C.; Zhao, J. R2R3-MYB transcription factor FaMYB5 is involved in citric acid metabolism in strawberry fruits. J. Plant Physiol. 2022, 277, 153789. [Google Scholar] [CrossRef] [PubMed]
- Liu, J.; Osbourn, A.; Ma, P. MYB Transcription Factors as Regulators of Phenylpropanoid Metabolism in Plants. Mol. Plant 2015, 8, 689–708. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sater, H.M.; Bizzio, L.N.; Tieman, D.M.; Muñoz, P.D. A Review of the Fruit Volatiles Found in Blueberry and Other Vaccinium Species. J. Agric. Food Chem. 2020, 68, 5777–5786. [Google Scholar] [CrossRef] [PubMed]
- Verdonk, J.C.; Haring, M.A.; van Tunen, A.J.; Schuurink, R.C. ODORANT1 regulates fragrance biosynthesis in petunia flowers. Plant Cell 2005, 17, 1612–1624. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bandeira Reidel, R.V.; Melai, B.; Cioni, P.; Flamini, G.; Pistelli, L. Aroma Profile of Rubus ulmifolius Flowers and Fruits During Different Ontogenetic Phases. Chem. Biodivers. 2016, 13, 1776–1784. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Y.; Yin, X.; Xiao, Y.; Zhang, Z.; Li, S.; Liu, X.; Zhang, B.; Yang, X.; Grierson, D.; Jiang, G.; et al. An ETHYLENE RESPONSE FACTOR-MYB Transcription Complex Regulates Furaneol Biosynthesis by Activating QUINONE OXIDOREDUCTASE Expression in Strawberry. Plant Physiol. 2018, 178, 189–201. [Google Scholar] [CrossRef] [Green Version]
- Lu, H.; Luo, Z.; Wang, L.; Liu, W.; Li, D.; Belwal, T.; Xu, Y.; Li, L. FaMYB9 is involved in the regulation of C6 volatile biosynthesis in strawberry. Plant Sci. 2020, 293, 110422. [Google Scholar] [CrossRef]
- Wang, S.; Shi, M.; Zhang, Y.; Pan, Z.; Xie, X.; Zhang, L.; Sun, P.; Feng, H.; Xue, H.; Fang, C.; et al. The R2R3-MYB transcription factor FaMYB63 participates in regulation of eugenol production in strawberry. Plant Physiol. 2022, 188, 2146–2165. [Google Scholar] [CrossRef]
- Medina-Puche, L.; Molina-Hidalgo, F.J.; Boersma, M.; Schuurink, R.C.; López-Vidriero, I.; Solano, R.; Franco-Zorrilla, J.M.; Caballero, J.L.; Blanco-Portales, R.; Muñoz-Blanco, J. An R2R3-MYB Transcription Factor Regulates Eugenol Production in Ripe Strawberry Fruit Receptacles. Plant Physiol. 2015, 168, 598–614. [Google Scholar] [CrossRef]
- Fan, Z.; Hasing, T.; Johnson, T.S.; Garner, D.M.; Schwieterman, M.L.; Barbey, C.R.; Colquhoun, T.A.; Sims, C.A.; Resende, M.F.R.; Whitaker, V.M. Strawberry sweetness and consumer preference are enhanced by specific volatile compounds. Hortic. Res. 2021, 8, 66. [Google Scholar] [CrossRef] [PubMed]
- Staudt, G. Strawberry Biogeography, Genetics and Systematics. Acta Hortic. 2009, 842, 71–84. [Google Scholar] [CrossRef]
- Edger, P.P.; Poorten, T.J.; VanBuren, R.; Hardigan, M.A.; Colle, M.; McKain, M.R.; Smith, R.D.; Teresi, S.J.; Nelson, A.D.L.; Wai, C.M.; et al. Origin and evolution of the octoploid strawberry genome. Nat. Genet. 2019, 51, 541–547. [Google Scholar] [CrossRef] [Green Version]
- Feng, C.; Wang, J.; Harris, A.J.; Folta, K.M.; Zhao, M.; Kang, M. Tracing the Diploid Ancestry of the Cultivated Octoploid Strawberry. Mol. Biol. Evol. 2021, 38, 478–485. [Google Scholar] [CrossRef] [PubMed]
- Edger, P.P.; McKain, M.R.; Yocca, A.E.; Knapp, S.J.; Qiao, Q.; Zhang, T. Reply to: Revisiting the origin of octoploid strawberry. Nat. Genet. 2020, 52, 5–7. [Google Scholar] [CrossRef] [PubMed]
- Hardigan, M.A.; Feldmann, M.J.; Lorant, A.; Bird, K.A.; Famula, R.; Acharya, C.; Cole, G.; Edger, P.P.; Knapp, S.J. Genome Synteny Has Been Conserved Among the Octoploid Progenitors of Cultivated Strawberry Over Millions of Years of Evolution. Front. Plant Sci. 2019, 10, 1789. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Whitaker, V.M.; Knapp, S.J.; Hardigan, M.A.; Edger, P.P.; Slovin, J.P.; Bassil, N.V.; Hytönen, T.; Mackenzie, K.K.; Lee, S.; Jung, S.; et al. A roadmap for research in octoploid strawberry. Hortic. Res. 2020, 7, 33. [Google Scholar] [CrossRef] [Green Version]
- Sheng, L.; Ni, Y.; Wang, J.; Chen, Y.; Gao, H. Characteristic-Aroma-Component-Based Evaluation and Classification of Strawberry Varieties by Aroma Type. Molecules 2021, 26, 6219. [Google Scholar] [CrossRef]
- Noguchi, Y.; Muro, T.; Morishita, M. The possibility of using decaploid interspecific hybrids (Fragaria × Ananassa × F. nilgerrensis) as a parent for a new strawberry. Acta Hortic. 2009, 842, 447–450. [Google Scholar] [CrossRef]
- Sheng, L.; Ma, C.; Chen, Y.; Gao, H.; Wang, J. Genome-Wide Screening of AP2 Transcription Factors Involving in Fruit Color and Aroma Regulation of Cultivated Strawberry. Genes 2021, 12, 530. [Google Scholar] [CrossRef]
- Urün, I.; Attar, S.H.; Sönmez, D.A.; Gündeşli, M.A.; Ercişli, S.; Kafkas, N.E.; Bandić, L.M.; Duralija, B. Comparison of Polyphenol, Sugar, Organic Acid, Volatile Compounds, and Antioxidant Capacity of Commercially Grown Strawberry Cultivars in Turkey. Plants 2021, 10, 1654. [Google Scholar] [CrossRef] [PubMed]
- Liu, J.; Wang, J.; Wang, M.; Zhao, J.; Zheng, Y.; Zhang, T.; Xue, L.; Lei, J. Genome-Wide Analysis of the R2R3-MYB Gene Family in Fragaria × ananassa and Its Function Identification During Anthocyanins Biosynthesis in Pink-Flowered Strawberry. Front. Plant Sci. 2021, 12, 702160. [Google Scholar] [CrossRef] [PubMed]
- Potter, S.C.; Luciani, A.; Eddy, S.R.; Park, Y.; Lopez, R.; Finn, R.D. HMMER web server: 2018 update. Nucleic Acids Res. 2018, 46, W200–W204. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, Y.; Tang, H.; Debarry, J.D.; Tan, X.; Li, J.; Wang, X.; Lee, T.H.; Jin, H.; Marler, B.; Guo, H.; et al. MCScanX: A toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res. 2012, 40, e49. [Google Scholar] [CrossRef] [Green Version]
- Chen, C.; Chen, H.; Zhang, Y.; Thomas, H.R.; Frank, M.H.; He, Y.; Xia, R. TBtools: An Integrative Toolkit Developed for Interactive Analyses of Big Biological Data. Mol. Plant 2020, 13, 1194–1202. [Google Scholar] [CrossRef]
- Emms, D.M.; Kelly, S. OrthoFinder: Phylogenetic orthology inference for comparative genomics. Genome Biol. 2019, 20, 238. [Google Scholar] [CrossRef] [Green Version]
- Kumar, S.; Stecher, G.; Tamura, K. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol. Biol. Evol. 2016, 33, 1870–1874. [Google Scholar] [CrossRef] [Green Version]
- Stracke, R.; Jahns, O.; Keck, M.; Tohge, T.; Niehaus, K.; Fernie, A.R.; Weisshaar, B. Analysis of Production of Flavonol Glycosides-dependent flavonol glycoside accumulation in Arabidopsis thaliana plants reveals MYB11-, MYB12- and MYB111-independent flavonol glycoside accumulation. New Phytol. 2010, 188, 985–1000. [Google Scholar] [CrossRef]
- Duan, S.; Wang, J.; Gao, C.; Jin, C.; Li, D.; Peng, D.; Du, G.; Li, Y.; Chen, M. Functional characterization of a heterologously expressed Brassica napus WRKY41-1 transcription factor in regulating anthocyanin biosynthesis in Arabidopsis thaliana. Plant Sci. 2018, 268, 47–53. [Google Scholar] [CrossRef]
- Panchy, N.; Lehti-Shiu, M.; Shiu, S.H. Evolution of Gene Duplication in Plants. Plant Physiol. 2016, 171, 2294–2316. [Google Scholar] [CrossRef]
- Hong, S.; Lim, Y.P.; Kwon, S.Y.; Shin, A.Y.; Kim, Y.M. Genome-Wide Comparative Analysis of Flowering-Time Genes; Insights on the Gene Family Expansion and Evolutionary Perspective. Front. Plant Sci. 2021, 12, 702243. [Google Scholar] [CrossRef] [PubMed]
- Reams, A.B.; Neidle, E.L. Selection for gene clustering by tandem duplication. Annu. Rev. Microbiol. 2004, 58, 119–142. [Google Scholar] [CrossRef] [PubMed]
- Cannon, S.B.; Mitra, A.; Baumgarten, A.; Young, N.D.; May, G. The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol. 2004, 4, 10. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hirakawa, H.; Shirasawa, K.; Kosugi, S.; Tashiro, K.; Nakayama, S.; Yamada, M.; Kohara, M.; Watanabe, A.; Kishida, Y.; Fujishiro, T.; et al. Dissection of the octoploid strawberry genome by deep sequencing of the genomes of Fragaria species. DNA Res. 2014, 21, 169–181. [Google Scholar] [CrossRef]
- Wei, Q.; Chen, R.; Wei, X.; Liu, Y.; Zhao, S.; Yin, X.; Xie, T. Genome-wide identification of R2R3-MYB family in wheat and functional characteristics of the abiotic stress responsive gene TaMYB344. BMC Genom. 2020, 21, 792. [Google Scholar] [CrossRef]
- Wang, H.; Zhang, H.; Yang, Y.; Li, M.; Zhang, Y.; Liu, J.; Dong, J.; Li, J.; Butelli, E.; Xue, Z.; et al. The control of red colour by a family of MYB transcription factors in octoploid strawberry (Fragaria × ananassa) fruits. Plant Biotechnol. J. 2020, 18, 1169–1184. [Google Scholar] [CrossRef] [Green Version]
- Lotkowska, M.E.; Tohge, T.; Fernie, A.R.; Xue, G.P.; Balazadeh, S.; Mueller-Roeber, B. The Arabidopsis Transcription Factor MYB112 Promotes Anthocyanin Formation during Salinity and under High Light Stress. Plant Physiol. 2015, 169, 1862–1880. [Google Scholar] [CrossRef]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Wang, J.; Yin, Y.; Gao, H.; Sheng, L. Identification of MYB Transcription Factors Involving in Fruit Quality Regulation of Fragaria × ananassa Duch. Genes 2023, 14, 68. https://doi.org/10.3390/genes14010068
Wang J, Yin Y, Gao H, Sheng L. Identification of MYB Transcription Factors Involving in Fruit Quality Regulation of Fragaria × ananassa Duch. Genes. 2023; 14(1):68. https://doi.org/10.3390/genes14010068
Chicago/Turabian StyleWang, Jianwen, Yujia Yin, Hongsheng Gao, and Lixia Sheng. 2023. "Identification of MYB Transcription Factors Involving in Fruit Quality Regulation of Fragaria × ananassa Duch." Genes 14, no. 1: 68. https://doi.org/10.3390/genes14010068
APA StyleWang, J., Yin, Y., Gao, H., & Sheng, L. (2023). Identification of MYB Transcription Factors Involving in Fruit Quality Regulation of Fragaria × ananassa Duch. Genes, 14(1), 68. https://doi.org/10.3390/genes14010068