Anthocyanin Accumulation in Grape Berry Skin Promoted by Endophytic Microbacterium sp. che218 Isolated from Wine Grape Shoot Xylem
Abstract
:1. Introduction
2. Materials and Methods
2.1. Plant Materials
2.2. Identification of Anthocyanin Biosynthesis-Promoting Endophytic Bacteria from Grapevine Shoot Xylems
2.3. Field Experiments
2.4. Anthocyanin Measurement
2.5. Total RNA Isolation
2.6. cDNA Synthesis
2.7. Quantitative RT-PCR
2.8. Identification of che218 by Whole Genome Sequencing
2.9. Statistical Analysis
3. Results
3.1. Effect of che218 Treatment on Anthocyanin Accumulation in Grapevine Cultured Cells
3.2. Effect of che218 Treatment on Anthocyanin Accumulation in Berry Skins of Field-Grown Grapevines
3.3. Effect of che218 Treatment on the Transcription of Anthocyanin Biosynthesis-Related Genes in Berry Skins of Field-Grown Grapevines
3.4. che218 Is a Microbacterium sp.
4. Discussion
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Castellarin, S.D.; Gaspero, D.G. Transcriptional control of anthocyanin biosynthetic genes in extreme phenotypes for berry pigmentation of naturally occurring grapevines. BMC Plant Biol. 2007, 30, 46–55. [Google Scholar] [CrossRef] [PubMed]
- Ma, W.; Guo, A.; Zhang, Y.; Wang, H.; Liu, Y.; Li, H. A review on astringency and bitterness perception of tannins in wine. Trends Food Sci. Technol. 2014, 40, 6–19. [Google Scholar] [CrossRef]
- Rogiers, S.Y.; Greer, D.H.; Liu, Y.; Baby, T.; Xiao, Z. Impact of climate change on grape berry ripening: An assessment of adaptation strategies for the Australian vineyard. Front. Plant Sci. 2022, 13, 1094633. [Google Scholar] [CrossRef] [PubMed]
- Morales-Castilla, I.; de Cortázar-Atauri, I.G.; Cook, B.I.; Lacombe, T.; Parker, A.; van Leeuwen, C.; Nicholas, K.A.; Wolkovich, E.M. Diversity buffers winegrowing regions from climate change losses. Proc. Natl. Acad. Sci. USA 2020, 117, 2864–2869. [Google Scholar] [CrossRef]
- Brar, H.S.; Singh, Z.; Swinny, E.; Cameron, I. Girdling and grapevine leafroll associated viruses affect berry weight, colour development and accumulation of anthocyanins in ‘Crimson Seedless’ grapes during maturation and ripening. Plant Sci. 2008, 175, 885–897. [Google Scholar] [CrossRef]
- Matsuyama, S.; Tanzawa, F.; Kobayashi, H.; Suzuki, S.; Takata, R.; Saito, H. Leaf removal accelerated accumulation of delphinidin-based anthocyanins in ‘Muscat Bailey A’ (Vitis × labruscana (Bailey) and Vitis vinifera (Muscat Hamburg)) grape skin. J. Jpn. Soc. Hortic. Sci. 2014, 83, 17–22. [Google Scholar] [CrossRef]
- Guidoni, S.; Allara, P.; Schubert, A. Effect of cluster thinning on berry skin anthocyanin composition of Vitis vinifera cv. Nebbiolo. Am. J. Enol. Vitic. 2002, 53, 224–226. [Google Scholar] [CrossRef]
- Peppi, M.C.; Walker, M.A.; Fidelibus, M.W. Application of abscisic acid rapidly upregulated UFGT gene expression and improved color of grape berries. Vitis 2008, 47, 11–24. [Google Scholar] [CrossRef]
- Pilati, S.; Bagagli, G.; Sonego, P.; Moretto, M.; Brazzale, D.; Castorina, G.; Simoni, L.; Tonelli, C.; Guella, G.; Engelen, K.; et al. Abscisic acid is a major regulator of grape berry ripening onset: New insights into ABA signaling network. Front. Plant Sci. 2017, 8, 1093. [Google Scholar] [CrossRef]
- Ferrara, G.; Mazzeo, A.; Matarrese, A.M.S.; Pacucci, C.; Pacifico, A.; Gambacorta, G.; Faccia, M.; Trani, A.; Gallo, V.; Cafagna, I.; et al. Application of abscisic acid (S-ABA) to ‘Crimson Seedless’ grape berries in a mediterranean climate: Effects on color, chemical characteristics, metabolic profile, and S-ABA concentration. J. Plant Growth Regul. 2013, 32, 491–505. [Google Scholar] [CrossRef]
- Koyama, R.; Roberto, S.R.; de Souza, R.T.; Borges, W.F.S.; Anderson, M.; Waterhouse, A.L.; Cantu, D.; Fidelibus, M.W.; Blanco-Ulate, B. Exogenous abscisic acid promotes anthocyanin biosynthesis and increased expression of flavonoid synthesis genes in Vitis vinifera × Vitis labrusca table grapes in a subtropical region. Front. Plant Sci. 2018, 9, 323. [Google Scholar] [CrossRef] [PubMed]
- Enoki, S.; Hattori, T.; Ishiai, S.; Tanaka, S.; Mikami, M.; Arita, K.; Nagasaka, S.; Suzuki, S. Vanillylacetone up-regulates expression of genes leading to anthocyanin accumulation by inducing endogenous abscisic acid in grape cell cultures. J. Plant Physiol. 2017, 219, 22–27. [Google Scholar] [CrossRef] [PubMed]
- Pan, X.-X.; Chen, C.-X.; Wang, Y.-T.; Zhu, Y.-Y.; Yang, M.-Z. Exposure to the endophytic fungi regulates the anthocyanin profiles in the post-veraison grape berries of ‘Cabernet Sauvignon’. Horticulturae 2023, 9, 237. [Google Scholar] [CrossRef]
- Kottb, M.; Gigolashvili, T.; Großkinsky, D.K.; Piechulla, B. Trichoderma volatiles effecting Arabidopsis: From inhibition to protection against phytopathogenic fungi. Front. Microbiol. 2015, 6, 995. [Google Scholar] [CrossRef] [PubMed]
- Cohen, A.C.; Travaglia, C.N.; Bottini, R.; Piccoli, P.N. Participation of abscisic acid and gibberellins produced by endophytic Azospirillum in the alleviation of drought effects in maize. Botany 2009, 87, 455–462. [Google Scholar] [CrossRef]
- Yamakawa, T.; Kato, S.; Ishida, K.; Kodama, T.; Minoda, Y. Production of anthocyanins by Vitis cells in suspension culture. Agric. Biol. Chem. 1983, 47, 2185–2191. [Google Scholar] [CrossRef]
- Reuther, G. Die Vermehrung von Pelargonienmutterpflanzen. Gb+Gw 1982, 32, 727–734. [Google Scholar]
- Hamaoka, K.; Aoki, Y.; Suzuki, S. Isolation and characterization of endophyte Bacillus velezensis KOF112 from grapevine shoot xylem as biological control agent for fungal diseases. Plants 2021, 10, 1815. [Google Scholar] [CrossRef]
- Bakker, J.; Preston, N.W.; Timberlake, C.F. The determination of anthocyanins in aging red wines comparison of HPLC and spectral methods. Am. J. Enol. Vitic. 1986, 37, 121–126. [Google Scholar] [CrossRef]
- Yokotsuka, K.; Nagao, A.; Nakazawa, K.; Sato, M. Changes in anthocyanins in berry skins of Merlot and Cabernet Sauvignon grapes grown in two soils modified with limestone or oyster shell versus a native soil over two years. Am. J. Enol. Vitic. 1999, 50, 1–12. [Google Scholar] [CrossRef]
- Aoki, Y.; Asada, T.; Nojiri, M.; Suzuki, S. Complete genome sequence of Microbacterium sp. che218, an endophyte isolated from Vitis vinifera cv. Chardonnay shoot xylem. Microbiol. Resour. Announc. 2024. manuscript in revision. [Google Scholar]
- Nishimura, Y.; Yamada, K.; Okazaki, Y.; Ogata, H. DiGAlign: Versatile and interactive visualization of sequence alignment for comparative genomics. Microbes Environ. 2024, 39, ME23061. [Google Scholar] [CrossRef] [PubMed]
- Kobayashi, S.; Goto-Yamamoto, N.; Hirokawa, H. Retrotransposon-induced mutations in grape skin color. Science 2004, 304, 982. [Google Scholar] [CrossRef]
- Tanizawa, Y.; Fujisawa, T.; Nakamura, Y. DFAST: A flexible prokaryotic genome annotation pipeline for faster genome publication. Bioinformatics 2018, 34, 1037–1039. [Google Scholar] [CrossRef]
- Takino, J.; Kozaki, T.; Sato, Y.; Liu, C.; Ozaki, T.; Minami, A.; Oikawa, H. Unveiling biosynthesis of the phytohormone abscisic acid in fungi: Unprecedented mechanism of core scaffold formation catalyzed by an unusual sesquiterpene synthase. J. Am. Chem. Soc. 2018, 140, 12392–12395. [Google Scholar] [CrossRef]
- Yoon, S.H.; Ha, S.M.; Lim, J.; Kwon, S.; Chun, J. A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie Leeuwenhoek 2017, 110, 1281–1286. [Google Scholar] [CrossRef]
- Wang, L.; Brouard, E.; Prodhomme, D.; Hilbert, G.; Renaud, C.; Petit, J.P.; Edwards, E.; Betts, A.; Delrot, S.; Ollat, N.; et al. Regulation of anthocyanin and sugar accumulation in grape berry through carbon limitation and exogenous ABA application. Food Res. Int. 2022, 160, 111478. [Google Scholar] [CrossRef]
- Gagné, S.; Estève, K.; Deytieux, C.; Saucier, C.; Gény, L. Influence of abscisic acid in triggering “véraison” in grape berry skins of Vitis vinifera L. cv. Cabernet Sauvignon. J. Int. Sci. Vigne Vin 2006, 40, 7–14. [Google Scholar] [CrossRef]
- Cohen, A.C.; Bottini, R.; Piccoli, P. Azospirillum brasilense sp. 245 produces ABA in chemically-defined culture medium and increases ABA content in arabidopsis plants. Plant Growth Regul. 2008, 54, 97–103. [Google Scholar] [CrossRef]
- Gowtham, H.G.; Duraivadivel, P.; Ayusman, S.; Sayani, D.; Gholap, S.L.; Niranjana, S.R.; Hariprasad, P. ABA analogue produced by Bacillus marisflavi modulates the physiological response of Brassica juncea L. under drought stress. Appl. Soil Ecol. 2021, 159, 103845. [Google Scholar] [CrossRef]
- Yamazaki, M.; Ishida, A.; Suzuki, Y.; Aoki, Y.; Suzuki, S.; Enoki, S. Ethylene induced by sound stimulation enhances anthocyanin accumulation in grape berry skin through direct upregulation of UDP-glucose: Flavonoid 3-O-glucosyltransferase. Cells 2021, 10, 2799. [Google Scholar] [CrossRef] [PubMed]
- Corretto, E.; Antonielli, L.; Sessitsch, A.; Höfer, C.; Puschenreiter, M.; Widhalm, S.; Swarnalakshmi, K.; Brader, G. Comparative genomics of Microbacterium species to reveal diversity, potential for secondary metabolites and heavy metal resistance. Front. Microbiol. 2020, 11, 1869. [Google Scholar] [CrossRef] [PubMed]
- Gao, J.L.; Sun, P.; Wang, X.M.; Lv, F.Y.; Sun, J.G. Microbacterium zeae sp. nov., an endophytic bacterium isolated from maize stem. Antonie Leeuwenhoek 2017, 110, 697–704. [Google Scholar] [CrossRef] [PubMed]
- Alves, A.; Correia, A.; Igual, J.M.; Trujillo, M.E. Microbacterium endophyticum sp. nov. and Microbacterium halimionae sp. nov., endophytes isolated from the salt-marsh plant Halimione portulacoides and emended description of the genus Microbacterium. Syst. Appl. Microbiol. 2014, 37, 474–479. [Google Scholar] [CrossRef]
- Tsavkelova, E.A.; Volynchikova, E.A.; Potekhina, N.V.; Lavrov, K.V.; Avtukh, A.N. Auxin production and plant growth promotion by Microbacterium albopurpureum sp. nov. from the rhizoplane of leafless Chiloschista parishii Seidenf. orchid. Front. Plant Sci. 2024, 15, 1360828. [Google Scholar] [CrossRef]
- Jones, G.V.; Edwards, E.J.; Bonada, M.; Sadras, V.O.; Krstic, M.P.; Herderich, M.J. Climate change and its consequences for viticulture. In Woodhead Publishing Series in Food Science, Technology and Nutrition, Managing Wine Quality, 2nd ed.; Reynolds, A.G., Ed.; Woodhead Publishing: Sawston, UK, 2022; pp. 727–778. [Google Scholar] [CrossRef]
- Shimizu, M.; Yazawa, S.; Ushijima, Y. A promising strain of endophytic Streptomyces sp. for biological control of cucumber anthracnose. J. Gen. Plant Pathol. 2009, 75, 27–36. [Google Scholar] [CrossRef]
- Liu, H.; Carvalhais, L.C.; Crawford, M.; Singh, E.; Dennis, P.G.; Pieterse, C.M.J.; Schenk, P.M. Inner plant values: Diversity, colonization, and benefits from endophytic bacteria. Front. Microbiol. 2017, 8, 2552. [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. |
© 2024 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
Teshigawara, Y.; Sato, S.; Asada, T.; Nojiri, M.; Suzuki, S.; Aoki, Y. Anthocyanin Accumulation in Grape Berry Skin Promoted by Endophytic Microbacterium sp. che218 Isolated from Wine Grape Shoot Xylem. Microorganisms 2024, 12, 1906. https://doi.org/10.3390/microorganisms12091906
Teshigawara Y, Sato S, Asada T, Nojiri M, Suzuki S, Aoki Y. Anthocyanin Accumulation in Grape Berry Skin Promoted by Endophytic Microbacterium sp. che218 Isolated from Wine Grape Shoot Xylem. Microorganisms. 2024; 12(9):1906. https://doi.org/10.3390/microorganisms12091906
Chicago/Turabian StyleTeshigawara, Yuka, Shiori Sato, Takayuki Asada, Masutoshi Nojiri, Shunji Suzuki, and Yoshinao Aoki. 2024. "Anthocyanin Accumulation in Grape Berry Skin Promoted by Endophytic Microbacterium sp. che218 Isolated from Wine Grape Shoot Xylem" Microorganisms 12, no. 9: 1906. https://doi.org/10.3390/microorganisms12091906
APA StyleTeshigawara, Y., Sato, S., Asada, T., Nojiri, M., Suzuki, S., & Aoki, Y. (2024). Anthocyanin Accumulation in Grape Berry Skin Promoted by Endophytic Microbacterium sp. che218 Isolated from Wine Grape Shoot Xylem. Microorganisms, 12(9), 1906. https://doi.org/10.3390/microorganisms12091906