Abstract
Previously, specific interactions in morphology were observed between grape cells and endophytic fungal strains during a dual culture experiment. However, the biochemical impacts of these fungal endophytes on grape cells is also expected due to their potential application in grape quality management. After assessed multiple physiochemical traits to those grape cells which have co-cultured with different endophytic fungal strains in this study, and found the presence of fungal endophytes obviously triggered ROS stress responses in grape cells, and the biochemical status in grape cells were differentially modified by different fungal strains. In those tested endophytic fungal strains, RH37 (Epicoccum sp.), RH6 (Alternaria sp.), RH32 (Alternaria sp.) and RH34 (Trichothecium sp.) conferred greater metabolic impacts on grape cells. And soluble protein (SPr), total flavonoids (TF), total phenols (TPh) and malondialdehyde (MDA) on the other hand, were sensitive biochemical parameters which can be influenced in greater ranges than other detected parameters. Most interestedly, fungal endophytes shaped metabolites patterns in grape cells during the dual culture appeared fungal genus/species/strain-specificity. The work confirmed the significance of fungal endophytes in grape metabolic regulation and elucidated the possibility to purposely manage grape quality using tool of fungal endophytes.
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Aly AH, Debbab A, Kjer J, Proksch P (2010) Fungal endophytes from higher plants: a prolific source of phytochemicals and other bioactive natural products. Fungal Divers 41:1–16
Arnold AE (2007) Understanding the diversity of foliar endophytic fungi: progress, challenges, and frontiers. Fungal Biol Rev 21:51–66
Asami DK, Hong Y-J, Barrett DM, Mitchell AE (2003) Comparison of the total phenolic and ascorbic acid content of freeze-dried and air-dried marionberry, strawberry, and corn grown using conventional, organic, and sustainable agricultural practices. J Agr Food Chem 51:1237–1241
Bergmeyer H-U (2012) Methods of enzymatic analysis: Elsevier
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Carolyn E, Jane E, John R (1996) Developmental changes in enzymes of flavonoid biosynthesis in the skins of red and green apple cultivators. J Sci Food Agr 71:313–320
Dhindsa R, Plumb-Dhindsa P, Thorpe T (1981) Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase. J Exp Bot 32:93–101
Doty SL (2015) Increasing Biomass Production with Reduced Inputs in Non-Legume Crops Using N-Fixing Endophytes of Poplar (Poster). In: Plant and Animal Genome XXIII Conference, January 10–14, 2015. Plant and Animal Genome, San Diego, CA, USA
Heath RL, Packer L (1965) Effect of light on lipid peroxidation in chloroplasts. Biochem Bioph Res Co 19:716–720
Huang L-h, Ao X-J, Shan h, Li h-X, Yang W-X, Zhang h-Bm Yang M-Z (2017) In vitro specific interactions revealed the infective characteristics of fungal endophytes to grapevine. Vitis 56:71–77
Kaul S, Gupta S, Ahmed M, Dhar MK (2012) Endophytic fungi from medicinal plants: a treasure hunt for bioactive metabolites. Phytochem Rev 11:487–505
Khan AL, Hamayun M, Kang S-M, Kim Y-H, Jung H-Y, Lee J-H, Lee I-J (2012) Endophytic fungal association via gibberellins and indole acetic acid can improve plant growth under abiotic stress: an example of Paecilomyces formosus LHL10. BMC Microbiol 12:3
Kuldau G, Bacon C (2008) Clavicipitaceous endophytes: their ability to enhance resistance of grasses to multiple stresses. Biol Control 46:57–71
Kusari S, Spiteller M (2012) Metabolomics of endophytic fungi producing associated plant secondary metabolites; Progress, Challenges and Opportunities, in U Roessner, ed, Metabolomics, InTech, Rijeka, Croatia, pp 241–266
Lu H, Zou WX, Meng JC, Hu J, Tan RX (2000) New bioactive metabolites produced by Colletotrichum sp., an endophytic fungus in Artemisia annua. Plant Sci 151:67–73
Ludwig-Müller J (2015) Plants and endophytes: equal partners in secondary metabolite production? Biotechnol Lett 37:1325–1334
Ma MD, Huang ZY, Zhang XY, Liu JQ, Yang MZ (2014) Diversity of endophytic fungi in leaves of different variety grape. Chinese Agr Sci Bull 30:118–125
Ma MD, Zhang XY, Cheng Y, Huang ZY, Zhang HB, Yang MZ (2014) Impacts on foliar endophytic fungi community structures after exogenous endophytic fungi re-inoculation. Microbiol China 12:009
Marks S, Clay K (1996) Physiological responses of Festuca arundinacea to fungal endophyte infection. New Phytol 727–733
Ownley BH, Griffin MR, Klingeman WE, Gwinn KD, Moulton JK, Pereira RM (2008) Beauveria bassiana: endophytic colonization and plant disease control. J Invertebr Pathol 98:267–270
Ramirez-Suero M, Bénard-Gellon M, Chong J, Laloue H, Stempien E, Abou-Mansour E, Fontaine F, Larignon P, Mazet-Kieffer F, Farine S (2014) Extracellular compounds produced by fungi associated with Botryosphaeria dieback induce differential defence gene expression patterns and necrosis in Vitis vinifera cv. Chardonnay cells. Protoplasma 251:1417–1426
Ren C-G, Chen Y, Fang F, Dai C-C (2012) Time and dosage effects of an endophytic fungal elicitor on the volatile oil production and physiology of Atractylodes lancea suspension cells. J Med Plants Res 6:5369–5376
Rodriguez R, White Jr J, Arnold A, Redman R (2009) Fungal endophytes: diversity and functional roles. New Phytol 182:314–330
Stone JK, Bacon CW, White J (2000) An overview of endophytic microbes: endophytism defined. Microbial Endophytes 3:29–33
Sudha G, Ravishankar GA (2002) Involvement and interaction of various signaling compounds on the plant metabolic events during defense response, resistance to stress factors, formation of secondary metabolites and their molecular aspects. Plant Cell Tiss Org 71:181–212
Tan R, Zou W (2001) Endophytes: a rich source of functional metabolites. Nat Prod Rep 18:448–459
Willett WC (2002) Balancing life-style and genomics research for disease prevention. Science 296:695–698
Xi Z-m, Zhang Z-w, Huo S-s, Luan L-y, Gao X, Ma L-n, Fang Y-l (2013) Regulating the secondary metabolism in grape berry using exogenous 24-epibrassinolide for enhanced phenolics content and antioxidant capacity. Food Chem 141:3056–3065
Yang M-Z, Ma M-D, Yuan M-Q, Huang Z-Y, Yang W-X, Zhang H-B, Huang L-H, Ren A-Y, Shan H (2016) Fungal Endophytes as a Metabolic Fine-Tuning Regulator for Wine Grape. PloS one, 11:e0163186
Zhao J, Zhou L, Wang J, Shan T, Zhong L, Liu X, Gao X (2010) Endophytic fungi for producing bioactive compounds originally from their host plants. Curr Res Technol Educ Trop Appl Microbiol Microbial Biotechnol 1:567–576
Zoecklein BW, Fugelsang KC, Gump BH, Nury FS (1995) Wine Analysis and Production. Food Qual Prefer 9:VII–VIII
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Yang, MZ., Huang, LH., Ao, XJ. et al. Endophytic Fungal strains Specifically Modified the Biochemical Status of Grape Cells. J. Plant Biol. 61, 210–216 (2018). https://doi.org/10.1007/s12374-017-0413-4
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DOI: https://doi.org/10.1007/s12374-017-0413-4