Interactions of JAZ Repressors with Anthocyanin Biosynthesis-Related Transcription Factors of Fragaria × ananassa
Abstract
:1. Introduction
2. Materials and Methods
2.1. Identification of Ortholog Sequences
2.2. Isolation and Cloning of Encoding Sequences
2.3. Sequence Analysis
2.4. Yeast Two-Hybrid Assays
3. Results and Discussion
3.1. The JA-Signaling Pathway is Structurally and Functionally Conserved in Fragaria × ananassa
3.2. bHLH and MYB Transcription Factors Interact with of JAZ Repressors in Fragaria × ananassa
3.3. The Transcription Factor YAB1 Interacts with JAZ Repressors in Fragaria × ananassa
4. Conclusions
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Giampieri, F.; Alvarez-Suarez, J.M.; Mazzoni, L.; Forbes-Hernandez, T.Y.; Gasparrini, M.; Gonzàlez-Paramàs, A.M.; Santos-Buelga, C.; Quiles, J.L.; Bompadre, S.; Mezzetti, B.; et al. An anthocyanin-rich strawberry extract protects against oxidative stress damage and improves mitochondrial functionality in human dermal fibroblasts exposed to an oxidizing agent. Food Funct. 2014, 5, 1939–1948. [Google Scholar] [CrossRef] [PubMed]
- Carbone, F.; Preuss, A.; De Vos, R.C.H.; D’Amico, E.; Perrotta, G.; Bovy, A.G.; Martens, S.; Rosati, C. Developmental, genetic and environmental factors affect the expression of flavonoid genes, enzymes and metabolites in strawberry fruits. Plant Cell Environ. 2009, 32, 1117–1131. [Google Scholar] [CrossRef] [PubMed]
- Hébert, C.; Charles, M.T.; Gauthier, L.; Willemot, C.; Khanizadeh, S.; Cousineau, J. Strawberry proanthocyanidins: Biochemical markers for botrytis cinerea resistance and shelf-life predictability. Acta Hortic. 2002, 659–662. [Google Scholar] [CrossRef]
- Cerezo, A.B.; Cuevas, E.; Winterhalter, P.; Garcia-Parrilla, M.C.; Troncoso, A.M. Isolation, identification, and antioxidant activity of anthocyanin compounds in Camarosa strawberry. Food Chem. 2010, 123, 574–582. [Google Scholar] [CrossRef]
- Xu, W.; Dubos, C.; Lepiniec, L. Transcriptional control of flavonoid biosynthesis by MYB–bHLH–WDR complexes. Trends Plant Sci. 2015, 20, 176–185. [Google Scholar] [CrossRef]
- Schaart, J.G.; Dubos, C.; Romero De La Fuente, I.; van Houwelingen, A.M.M.L.; de Vos, R.C.H.; Jonker, H.H.; Xu, W.; Routaboul, J.-M.; Lepiniec, L.; Bovy, A.G. Identification and characterization of MYB-bHLH-WD40 regulatory complexes controlling proanthocyanidin biosynthesis in strawberry (Fragaria × ananassa) fruits. New Phytol. 2013, 197, 454–467. [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]
- Lin-Wang, K.; Bolitho, K.; Grafton, K.; Kortstee, A.; Karunairetnam, S.; McGhie, T.K.; Espley, R.V.; Hellens, R.P.; Allan, A.C. An R2R3 MYB transcription factor associated with regulation of the anthocyanin biosynthetic pathway in Rosaceae. BMC Plant Biol. 2010, 10, 50. [Google Scholar] [CrossRef] [Green Version]
- Lin-Wang, K.; McGhie, T.K.; Wang, M.; Liu, Y.; Warren, B.; Storey, R.; Espley, R.V.; Allan, A.C. Engineering the anthocyanin regulatory complex of strawberry (Fragaria vesca). Front Plant Sci. 2014, 5. [Google Scholar] [CrossRef] [Green Version]
- 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. MdMYB9 and MdMYB11 are Involved in the Regulation of the JA-Induced Biosynthesis of Anthocyanin and Proanthocyanidin in Apples. Plant Cell Physiol. 2015, 56, 650–662. [Google Scholar] [CrossRef] [Green Version]
- Cherian, S.; Figueroa, C.R.; Nair, H. “Movers and shakers” in the regulation of fruit ripening: A cross-dissection of climacteric versus non-climacteric fruit. J. Exp. Bot. 2014, 65, 4705–4722. [Google Scholar] [CrossRef] [Green Version]
- Fuentes, L.; Figueroa, C.R.; Valdenegro, M. Recent Advances in Hormonal Regulation and Cross-Talk during Non-Climacteric Fruit Development and Ripening. Horticulturae 2019, 5, 45. [Google Scholar] [CrossRef] [Green Version]
- Jia, H.-F.; Chai, Y.-M.; Li, C.-L.; Lu, D.; Luo, J.-J.; Qin, L.; Shen, Y.-Y. Abscisic acid plays an important role in the regulation of strawberry fruit ripening. Plant Physiol. 2011, 157, 188–199. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Garrido-Bigotes, A.; Figueroa, P.M.; Figueroa, C.R. Jasmonate Metabolism and Its Relationship with Abscisic Acid During Strawberry Fruit Development and Ripening. J. Plant Growth Regul. 2018, 37, 101–113. [Google Scholar] [CrossRef]
- Delgado, L.D.; Zúñiga, P.E.; Figueroa, N.E.; Pastene, E.; Escobar-Sepúlveda, H.F.; Figueroa, P.M.; Garrido-Bigotes, A.; Figueroa, C.R. Application of a JA-Ile Biosynthesis Inhibitor to Methyl Jasmonate-Treated Strawberry Fruit Induces Upregulation of Specific MBW Complex-Related Genes and Accumulation of Proanthocyanidins. Molecules 2018, 23, 1433. [Google Scholar] [CrossRef] [Green Version]
- Valenzuela-Riffo, F.; Zúñiga, P.E.; Morales-Quintana, L.; Lolas, M.; Cáceres, M.; Figueroa, C.R. Priming of Defense Systems and Upregulation of MYC2 and JAZ1 Genes after Botrytis cinerea Inoculation in Methyl Jasmonate-Treated Strawberry Fruits. Plants 2020, 9, 447. [Google Scholar] [CrossRef] [Green Version]
- Zuñiga, P.E.; Castañeda, Y.; Arrey-Salas, O.; Fuentes, L.; Aburto, F.; Figueroa, C.R. Methyl Jasmonate Applications From Flowering to Ripe Fruit Stages of Strawberry (Fragaria × ananassa ‘Camarosa’) Reinforce the Fruit Antioxidant Response at Post-harvest. Front. Plant Sci. 2020, 11. [Google Scholar] [CrossRef]
- Jaakola, L. New insights into the regulation of anthocyanin biosynthesis in fruits. Trends Plant Sci. 2013, 18, 477–483. [Google Scholar] [CrossRef] [Green Version]
- Lin, Y.; Jiang, L.; Chen, Q.; Li, Y.; Zhang, Y.; Luo, Y.; Zhang, Y.; Sun, B.; Wang, X.; Tang, H. Comparative Transcriptome Profiling Analysis of Red- and White-Fleshed Strawberry (Fragaria × ananassa) Provides New Insight into the Regulation of the Anthocyanin Pathway. Plant Cell Physiol. 2018, 59, 1844–1859. [Google Scholar] [CrossRef]
- Boter, M.; Golz, J.F.; Giménez-Ibañez, S.; Fernandez-Barbero, G.; Franco-Zorrilla, J.M.; Solano, R. FILAMENTOUS FLOWER Is a Direct Target of JAZ3 and Modulates Responses to Jasmonate. Plant Cell 2015, 27, 3160–3174. [Google Scholar] [CrossRef] [Green Version]
- Shan, X.; Zhang, Y.; Peng, W.; Wang, Z.; Xie, D. Molecular mechanism for jasmonate-induction of anthocyanin accumulation in Arabidopsis. J. Exp. Bot. 2009, 60, 3849–3860. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Qi, T.; Song, S.; Ren, Q.; Wu, D.; Huang, H.; Chen, Y.; Fan, M.; Peng, W.; Ren, C.; Xie, D. The Jasmonate-ZIM-domain proteins interact with the WD-Repeat/bHLH/MYB complexes to regulate Jasmonate-mediated anthocyanin accumulation and trichome initiation in Arabidopsis thaliana. Plant Cell 2011, 23, 1795–1814. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fonseca, S.; Chini, A.; Hamberg, M.; Adie, B.; Porzel, A.; Kramell, R.; Miersch, O.; Wasternack, C.; Solano, R. (+)-7-iso-Jasmonoyl-L-isoleucine is the endogenous bioactive jasmonate. Nat. Chem. Biol. 2009, 5, 344–350. [Google Scholar] [CrossRef] [PubMed]
- Howe, G.A.; Major, I.T.; Koo, A.J. Modularity in Jasmonate Signaling for Multistress Resilience. Ann. Rev. Plant Biol. 2018, 69, 387–415. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ueda, M.; Kaji, T.; Kozaki, W. Recent Advances in Plant Chemical Biology of Jasmonates. Int. J. Mol. Sci. 2020, 21, 1124. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sheard, L.B.; Tan, X.; Mao, H.; Withers, J.; Ben-Nissan, G.; Hinds, T.R.; Kobayashi, Y.; Hsu, F.-F.; Sharon, M.; Browse, J.; et al. Jasmonate perception by inositol-phosphate-potentiated COI1-JAZ co-receptor. Nature 2010, 468, 400–405. [Google Scholar] [CrossRef]
- Valenzuela-Riffo, F.; Garrido-Bigotes, A.; Figueroa, P.M.; Morales-Quintana, L.; Figueroa, C.R. Structural analysis of the woodland strawberry COI1-JAZ1 co-receptor for the plant hormone jasmonoyl-isoleucine. J. Mol. Graph. Model. 2018, 85, 250–261. [Google Scholar] [CrossRef]
- Garrido-Bigotes, A.; Valenzuela-Riffo, F.; Torrejón, M.; Solano, R.; Morales-Quintana, L.; Figueroa, C.R. A new functional JAZ degron sequence in strawberry JAZ1 revealed by structural and interaction studies on the COI1–JA-Ile/COR–JAZs complexes. Sci. Rep. 2020, 10. [Google Scholar] [CrossRef]
- Chini, A.; Fonseca, S.; Fernández, G.; Adie, B.; Chico, J.M.; Lorenzo, O.; García-Casado, G.; López-Vidriero, I.; Lozano, F.M.; Ponce, M.R.; et al. The JAZ family of repressors is the missing link in jasmonate signalling. Nature 2007, 448, 666–671. [Google Scholar] [CrossRef]
- Thines, B.; Katsir, L.; Melotto, M.; Niu, Y.; Mandaokar, A.; Liu, G.; Nomura, K.; He, S.Y.; Howe, G.A.; Browse, J. JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling. Nature 2007, 448, 661–665. [Google Scholar] [CrossRef]
- Fernández-Calvo, P.; Chini, A.; Fernández-Barbero, G.; Chico, J.-M.; Gimenez-Ibanez, S.; Geerinck, J.; Eeckhout, D.; Schweizer, F.; Godoy, M.; Franco-Zorrilla, J.M.; et al. The Arabidopsis bHLH transcription factors MYC3 and MYC4 are targets of JAZ repressors and act additively with MYC2 in the activation of jasmonate responses. Plant Cell 2011, 23, 701–715. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Figueroa, P.; Browse, J. Male sterility in Arabidopsis induced by overexpression of a MYC5-SRDX chimeric repressor. Plant J. 2015, 81, 849–860. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pauwels, L.; Barbero, G.F.; Geerinck, J.; Tilleman, S.; Grunewald, W.; Pérez, A.C.; Chico, J.M.; Bossche, R.V.; Sewell, J.; Gil, E.; et al. NINJA connects the co-repressor TOPLESS to jasmonate signalling. Nature 2010, 464, 788–791. [Google Scholar] [CrossRef] [Green Version]
- Fonseca, S.; Fernández-Calvo, P.; Fernández, G.M.; Díez-Díaz, M.; Gimenez-Ibanez, S.; López-Vidriero, I.; Godoy, M.; Fernández-Barbero, G.; Van Leene, J.; De Jaeger, G.; et al. bHLH003, bHLH013 and bHLH017 Are New Targets of JAZ Repressors Negatively Regulating JA Responses. PLoS ONE 2014, 9, e86182. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vanholme, B.; Grunewald, W.; Bateman, A.; Kohchi, T.; Gheysen, G. The tify family previously known as ZIM. Trends Plant Sci. 2007, 12, 239–244. [Google Scholar] [CrossRef]
- Bai, Y.; Meng, Y.; Huang, D.; Qi, Y.; Chen, M. Origin and evolutionary analysis of the plant-specific TIFY transcription factor family. Genomics 2011, 98, 128–136. [Google Scholar] [CrossRef] [Green Version]
- Garrido-Bigotes, A.; Valenzuela-Riffo, F.; Figueroa, C.R. Evolutionary Analysis of JAZ Proteins in Plants: An Approach in Search of the Ancestral Sequence. Int. J. Mol. Sci. 2019, 20, 5060. [Google Scholar] [CrossRef] [Green Version]
- Monte, I.; Franco-Zorrilla, J.M.; García-Casado, G.; Zamarreño, A.M.; García-Mina, J.M.; Nishihama, R.; Kohchi, T.; Solano, R. A Single JAZ Repressor Controls the Jasmonate Pathway in Marchantia polymorpha. Mol. Plant 2019, 12, 185–198. [Google Scholar] [CrossRef] [Green Version]
- Garrido-Bigotes, A.; Figueroa, N.E.; Figueroa, P.M.; Figueroa, C.R. Jasmonate signalling pathway in strawberry: Genome-wide identification, molecular characterization and expression of JAZs and MYCs during fruit development and ripening. PLoS ONE 2018, 13. [Google Scholar] [CrossRef] [Green Version]
- Chini, A.; Gimenez-Ibanez, S.; Goossens, A.; Solano, R. Redundancy and specificity in jasmonate signalling. Curr. Opin. Plant Biol. 2016, 33, 147–156. [Google Scholar] [CrossRef]
- Pauwels, L.; Goossens, A. The JAZ Proteins: A Crucial Interface in the Jasmonate Signaling Cascade. Plant Cell 2011, 23, 3089–3100. [Google Scholar] [CrossRef] [Green Version]
- Goossens, J.; Mertens, J.; Goossens, A. Role and functioning of bHLH transcription factors in jasmonate signalling. J. Exp. Bot. 2017, 68, 1333–1347. [Google Scholar] [CrossRef] [PubMed]
- Sievers, F.; Higgins, D.G. Clustal Omega, Accurate Alignment of Very Large Numbers of Sequences. In Multiple Sequence Alignment Methods; Russell, D.J., Ed.; Methods in Molecular Biology; Humana Press: Totowa, NJ, USA, 2014; pp. 105–116. [Google Scholar]
- Waterhouse, A.M.; Procter, J.B.; Martin, D.M.A.; Clamp, M.; Barton, G.J. Jalview Version 2--a multiple sequence alignment editor and analysis workbench. Bioinformatics 2009, 25, 1189–1191. [Google Scholar] [CrossRef] [Green Version]
- Kumar, S.; Stecher, G.; Li, M.; Knyaz, C.; Tamura, K. MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. Mol. Biol. Evol. 2018, 35, 1547–1549. [Google Scholar] [CrossRef]
- He, Z.; Zhang, H.; Gao, S.; Lercher, M.J.; Chen, W.-H.; Hu, S. Evolview v2: An online visualization and management tool for customized and annotated phylogenetic trees. Nucleic Acids Res. 2016, 44, 236–241. [Google Scholar] [CrossRef] [PubMed]
- Shyu, C.; Figueroa, P.; DePew, C.L.; Cooke, T.F.; Sheard, L.B.; Moreno, J.E.; Katsir, L.; Zheng, N.; Browse, J.; Howe, G.A. JAZ8 Lacks a Canonical Degron and Has an EAR Motif That Mediates Transcriptional Repression of Jasmonate Responses in Arabidopsis[C][W]. Plant Cell 2012, 24, 536–550. [Google Scholar] [CrossRef] [Green Version]
- Wang, L.; Wu, S.-M.; Zhu, Y.; Fan, Q.; Zhang, Z.-N.; Hu, G.; Peng, Q.-Z.; Wu, J.-H. Functional characterization of a novel jasmonate ZIM-domain interactor (NINJA) from upland cotton (Gossypium hirsutum). Plant Physiol. Biochem. 2017, 112, 152–160. [Google Scholar] [CrossRef] [PubMed]
- Figueroa, P.; Browse, J. The Arabidopsis JAZ2 promoter contains a G-Box and thymidine-rich module that are necessary and sufficient for jasmonate-dependent activation by MYC transcription factors and repression by JAZ proteins. Plant Cell Physiol. 2012, 53, 330–343. [Google Scholar] [CrossRef] [Green Version]
- Zhao, F.; Li, G.; Hu, P.; Zhao, X.; Li, L.; Wei, W.; Feng, J.; Zhou, H. Identification of basic/helix-loop-helix transcription factors reveals candidate genes involved in anthocyanin biosynthesis from the strawberry white-flesh mutant. Sci. Rep. 2018, 8, 2721. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sasaki-Sekimoto, Y.; Jikumaru, Y.; Obayashi, T.; Saito, H.; Masuda, S.; Kamiya, Y.; Ohta, H.; Shirasu, K. Basic Helix-Loop-Helix Transcription Factors JASMONATE-ASSOCIATED MYC2-LIKE1 (JAM1), JAM2, and JAM3 Are Negative Regulators of Jasmonate Responses in Arabidopsis1[W][OPEN]. Plant Physiol. 2013, 163, 291–304. [Google Scholar] [CrossRef] [Green Version]
- Aharoni, A.; Vos, C.H.R.D.; Wein, M.; Sun, Z.; Greco, R.; Kroon, A.; Mol, J.N.M.; O’Connell, A.P. The strawberry FaMYB1 transcription factor suppresses anthocyanin and flavonol accumulation in transgenic tobacco. Plant J. 2001, 28, 319–332. [Google Scholar] [CrossRef] [PubMed]
- 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]
- Song, S.; Qi, T.; Huang, H.; Ren, Q.; Wu, D.; Chang, C.; Peng, W.; Liu, Y.; Peng, J.; Xie, D. The Jasmonate-ZIM domain proteins interact with the R2R3-MYB transcription factors MYB21 and MYB24 to affect Jasmonate-regulated stamen development in Arabidopsis. Plant Cell 2011, 23, 1000–1013. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- 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]
- Siegfried, K.R.; Eshed, Y.; Baum, S.F.; Otsuga, D.; Drews, G.N.; Bowman, J.L. Members of the YABBY gene family specify abaxial cell fate in Arabidopsis. Development 1999, 126, 4117–4128. [Google Scholar]
- Bowman, J.L. The YABBY gene family and abaxial cell fate. Curr. Opin. Plant Biol. 2000, 3, 17–22. [Google Scholar] [CrossRef]
- Zhang, S.; Wang, L.; Sun, X.; Li, Y.; Yao, J.; van Nocker, S.; Wang, X. Genome-Wide Analysis of the YABBY Gene Family in Grapevine and Functional Characterization of VvYABBY4. Front. Plant Sci. 2019, 10. [Google Scholar] [CrossRef]
- Huang, Z.; Van Houten, J.; Gonzalez, G.; Xiao, H.; van der Knaap, E. Genome-wide identification, phylogeny and expression analysis of SUN, OFP and YABBY gene family in tomato. Mol. Genet. Genomics 2013, 288, 111–129. [Google Scholar] [CrossRef]
- Xiang, Y.; Huang, C.-H.; Hu, Y.; Wen, J.; Li, S.; Yi, T.; Chen, H.; Xiang, J.; Ma, H. Evolution of Rosaceae Fruit Types Based on Nuclear Phylogeny in the Context of Geological Times and Genome Duplication. Mol. Biol. Evol. 2017, 34, 262–281. [Google Scholar] [CrossRef] [Green Version]
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Garrido-Bigotes, A.; Torrejón, M.; Solano, R.; Figueroa, C.R. Interactions of JAZ Repressors with Anthocyanin Biosynthesis-Related Transcription Factors of Fragaria × ananassa. Agronomy 2020, 10, 1586. https://doi.org/10.3390/agronomy10101586
Garrido-Bigotes A, Torrejón M, Solano R, Figueroa CR. Interactions of JAZ Repressors with Anthocyanin Biosynthesis-Related Transcription Factors of Fragaria × ananassa. Agronomy. 2020; 10(10):1586. https://doi.org/10.3390/agronomy10101586
Chicago/Turabian StyleGarrido-Bigotes, Adrián, Marcela Torrejón, Roberto Solano, and Carlos R. Figueroa. 2020. "Interactions of JAZ Repressors with Anthocyanin Biosynthesis-Related Transcription Factors of Fragaria × ananassa" Agronomy 10, no. 10: 1586. https://doi.org/10.3390/agronomy10101586