Transcriptome Analysis of Berries of Spine Grape (Vitis davidii Föex) Infected by Colletotrichum viniferum during Symptom Development

Horticulturae - Tập 8 Số 9 - Trang 843
Lei Yan1,2, Xiaojian Yuan3, Ting Chen2, Yuan Yuan1, Xinming Liu2, Xinbiao Tang1,2, Qingxi Chen1
1College of Horticulture, Fujian Agriculture and Forestry University, Fuzhou 350002, China
2Fruit Research Institute, Fujian Academy of Agricultural Sciences, Fuzhou 350013, China
3College of Horticulture, Northwest A&F University, Yangling 712100, China

Tóm tắt

Grape ripe rot (Colletotrichum viniferum) causes huge losses in grape production in vineyards in southern China. However, the molecular mechanism against ripe rot in grape species and the responsive genes implicated in these processes are relatively unknown. Here, we present the transcriptome analysis of berries from a C. viniferum-resistant species (Vitis davidii Föex). Uninfected berries at day zero were used as control samples (CK), an inoculation was made at day zero, and the berries were subsequently analyzed at 1 day, 3 days, and 7 days post inoculation (dpi), which exhibited a sequential disease-progression stage. There were a total of 1810 differentially expressed genes, including 1315 up-regulated and 495 down-regulated transcripts. At 7 dpi, these differentially expressed genes (DEGs) were predominantly enriched in berries. In addition, in C. viniferum-infected grape fruits at 7 dpi, considerable changes in gene expression were induced, and those up-regulated genes involved in MAPK cascade, calcium ion binding, and serine/threonine kinase activity were enriched. According to our KEGG pathway analysis, numerous enriched biological processes, such as plant–pathogen interaction, phenylpropanoid biosynthesis, and metabolism, were implicated in grape–fungus interactions. Our research also revealed alterations in the expression pattern of phenylalanine-pathway-related transcription factors (TFs) and genes. We proposed a model in which C. viniferum invasion produces intracellular and extracellular Ca2+ deregulation to stimulate the MAPK pathway to activate TFs’ (WRKY, ERF, and MYB) up-regulation, thus initiating disease-resistant responses in the tolerant Vitis species. Our results offer comprehensive transcriptomic data about molecular responses in C. viniferum-infected grape, and these data will aid in understanding of processes underlying plant responses to C. viniferum.

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Tài liệu tham khảo

Welke, 2019, Fungal and mycotoxin problems in grape juice and wine industries, Curr. Opin. Food Sci., 29, 7, 10.1016/j.cofs.2019.06.009

Oo, 2017, Identification and characterization of new record of grape ripe rot disease caused by Colletotrichum viniferum in Korea, Mycobiology, 45, 421, 10.5941/MYCO.2017.45.4.421

Cosseboom, S.D., and Hu, M. (2022). Predicting Ripe Rot of Grape, Caused by Colletotrichum fioriniae, with Leaf Wetness, Temperature, and the Crop Growth. PhytoFrontiers.

Whitelawweckert, 2007, Phylogenetic relationships and pathogenicity of Colletotrichum acutatum isolates from grape in subtropical Australia, Plant Pathol., 56, 448, 10.1111/j.1365-3059.2007.01569.x

Dou, 2022, Genome Sequence Resource for Colletotrichum viniferum, the cause of grapevine ripe rot in China, Mol. Plant-Microbe Interact., 35, 90, 10.1094/MPMI-04-21-0077-A

Sadoughi, N. (2016). Effect of Ripe Rot of Grapes (Colletotrichum spp.) on the Chemical Composition and Off-Flavour Compounds in Grapes and Wine. [Ph.D. Dissertation, Charles Sturt University].

Ji, T., Salotti, I., Dong, C., Li, M., and Rossi, V. (2021). Modeling the effects of the environment and the host plant on the ripe rot of grapes, caused by the Colletotrichum species. Plants, 10.

Shiraishi, 2007, Screening for resistance to ripe rot caused by Colletotrichum acutatum in grape germplasm, Vitis, 46, 196

Fu, 2019, Cgr1, a ripe rot resistance QTL in Vitis amurensis ‘Shuang Hong’ grapevine, Hortic. Res., 6, 67, 10.1038/s41438-019-0148-0

Reid, K.E., Olsson, N., Schlosser, J., Peng, F.Y., and Lund, S.T. (2006). An optimized grapevine RNA isolation procedure and statistical determination of reference genes for real-time RT-PCR during berry development. BMC Plant Biol., 6.

Trapnell, 2009, TopHat: Discovering splice junctions with RNA-Seq, Bioinformatics, 25, 1105, 10.1093/bioinformatics/btp120

Jaillon, 2007, The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla, Nature, 449, 463, 10.1038/nature06148

Mortazavi, 2008, Mapping and quantifying mammalian transcriptomes by RNA-Seq, Nat. Methods, 5, 621, 10.1038/nmeth.1226

Conesa, 2008, Blast2GO: A comprehensive suite for functional analysis in plant genomics, Int. J. Plant Genom., 2008, 619832

Robinson, 2010, edgeR: A Bioconductor package for differential expression analysis of digital gene expression data, Bioinformatics, 26, 139, 10.1093/bioinformatics/btp616

Anders, 2010, Differential expression analysis for sequence count data, Genome Biol., 11, 1, 10.1186/gb-2010-11-10-r106

Benjamini, 1995, Controlling the false discovery rate: A practical and powerful approach to multiple testing, J. R. Stat. Soc. B, 57, 289, 10.1111/j.2517-6161.1995.tb02031.x

Du, 2010, agriGO: A GO analysis toolkit for the agricultural community, Nucleic Acids Res., 38, W64, 10.1093/nar/gkq310

Kotera, 2012, The KEGG databases and tools facilitating omics analysis: Latest developments involving human diseases and pharmaceuticals, Methods Mol. Biol., 802, 19, 10.1007/978-1-61779-400-1_2

Langfelder, P., and Horvath, S. (2008). WGCNA: An R package for weighted correlation network analysis. BMC Bioinform., 9.

Shannon, 2003, Cytoscape: A software environment for integrated models of biomolecular interaction networks, Genome Res., 13, 2498, 10.1101/gr.1239303

Livak, 2001, Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method, Methods, 25, 402, 10.1006/meth.2001.1262

Sudheeran, 2021, Induced defense response in red mango fruit against Colletotrichum gloeosporioides, Hortic. Res., 8, 17, 10.1038/s41438-020-00452-4

Li, 2015, Comparative transcriptome analysis reveals defense-related genes and pathways against downy mildew in Vitis amurensis grapevine, Plant Physiol. Biochem., 95, 1, 10.1016/j.plaphy.2015.06.016

Xu, 2014, Transcriptome profiling of Vitis amurensis, an extremely cold-tolerant Chinese wild Vitis species, reveals candidate genes and events that potentially connected to cold stress, Plant Mol. Biol., 86, 527, 10.1007/s11103-014-0245-2

Marzin, S., Hanemann, A., Sharma, S., Hensel, G., Kumlehn, J., Schweizer, G., and Roder, M.S. (2016). Are PECTIN ESTERASE INHIBITOR genes involved in mediating resistance to rhynchosporium commune in barley. PLoS ONE, 11.

Baker, 1997, Signaling in plant-microbe interactions, Science, 276, 726, 10.1126/science.276.5313.726

Freeman, 1998, Characterization of Colletotrichum species responsible for anthracnose diseases of various fruits, Plant Dis., 82, 596, 10.1094/PDIS.1998.82.6.596

Jayawardena, 2016, Notes on currently accepted species of Colletotrichum, Mycosphere, 7, 1192, 10.5943/mycosphere/si/2c/9

Hong, 2008, Morphological variations, genetic diversity and pathogenicity of Colletotrichum species causing grape ripe rot in Korea, Plant Pathol. J., 24, 269, 10.5423/PPJ.2008.24.3.269

Echeverrigaray, 2020, Colletotrichum species causing grape ripe rot disease in Vitis labrusca and V. vinifera varieties in the highlands of southern Brazil, Plant Pathol., 69, 1504, 10.1111/ppa.13240

Yan, 2014, Diverse species of Colletotrichum associated with grapevine anthracnose in China, Fungal Divers., 71, 233, 10.1007/s13225-014-0310-9

Kim, 2021, First report of Colletotrichum aenigma causing anthracnose of grape in Korea, Plant Dis., 105, 2729, 10.1094/PDIS-11-20-2458-PDN

Sawant, 2016, Biocontrol potential of two novel grapevine associated Bacillus strains for management of anthracnose disease caused by Colletotrichum gloeosporioides, Biocontrol. Sci. Technol., 26, 964, 10.1080/09583157.2016.1174770

Lei, 2016, Identification and characterization of Colletotrichum species causing grape ripe rot in southern China, Mycosphere, 7, 1177, 10.5943/mycosphere/si/2c/8

Fung, 2007, Powdery mildew induces defense-oriented reprogramming of the transcriptome in a susceptible but not in a resistant grapevine, Plant Physiol., 146, 236, 10.1104/pp.107.108712

Bhadauria, V., Bett, K.E., Zhou, T., Vandenberg, A., Wei, Y., and Banniza, S. (2013). Identification of Lens culinaris defense genes responsive to the anthracnose pathogen Colletotrichum truncatum. BMC Genet., 14.

Padder, B.A., Kamfwa, K., Awale, H., and Kelly, J.D. (2016). Transcriptome profiling of the phaseolus vulgaris-Colletotrichum lindemuthianum pathosystem. PLoS ONE, 11.

Wang, L., Wang, Y., Cao, H., Hao, X., Zeng, J., Yang, Y., and Wang, X. (2016). Transcriptome analysis of an anthracnose-resistant tea plant cultivar reveals genes associated with resistance to Colletotrichum camelliae. PLoS ONE, 11.

Mishra, 2017, Differential expression of defense-related genes in chilli pepper infected with anthracnose pathogen Colletotrichum truncatum, Physiol. Mol. Plant Pathol., 97, 1, 10.1016/j.pmpp.2016.11.001

Wang, 2018, Transcriptional analysis and histochemistry reveal that hypersensitive cell death and H2O2 have crucial roles in the resistance of tea plant (Camellia sinensis (L.) O. Kuntze) to anthracnose, Hortic. Res., 5, 18, 10.1038/s41438-018-0025-2

Trouvelot, 2014, Carbohydrates in plant immunity and plant protection: Roles and potential application as foliar sprays, Front. Plant Sci., 5, 592, 10.3389/fpls.2014.00592

Jiang, 2017, Plants transfer lipids to sustain colonization by mutualistic mycorrhizal and parasitic fungi, Science, 356, 1172, 10.1126/science.aam9970

Lionetti, 2012, Methyl esterification of pectin plays a role during plant–pathogen interactions and affects plant resistance to diseases, J. Plant Physiol., 169, 1623, 10.1016/j.jplph.2012.05.006

Mao, 2018, Transcriptome analysis revealed glucose application affects plant hormone signal transduction pathway in “Red Globe” grape plantlets, Plant Growth Regul., 84, 45, 10.1007/s10725-017-0320-1

Dixon, 1995, Stress-induced phenylpropanoid metabolism, Plant Cell, 7, 1085, 10.2307/3870059

Patel, 2021, Induction of pre-chorismate, jasmonate and salicylate pathways by Burkholderia sp. RR18 in peanut seedlings, J. Appl. Microbiol., 131, 1417, 10.1111/jam.15019

Dixon, 2001, Natural products and plant disease resistance, Nature, 411, 843, 10.1038/35081178

Ahuja, 2012, Phytoalexins in defense against pathogens, Trends Plant Sci., 17, 73, 10.1016/j.tplants.2011.11.002

Ciaffi, M., Paolacci, A.R., Paolocci, M., Alicandri, E., Bigini, V., Badiani, M., and Muganu, M. (2019). Transcriptional regulation of stilbene synthases in grapevine germplasm differentially susceptible to downy mildew. BMC Plant Biol., 19.

Meng, 2013, MAPK cascades in plant disease resistance signaling, Annu. Rev. Phytopathol., 51, 245, 10.1146/annurev-phyto-082712-102314

Guo, 2016, An ethylene response-related factor, GbERF1-like, from Gossypium barbadense improves resistance to Verticillium dahliae via activating lignin synthesis, Plant Mol. Biol., 91, 305, 10.1007/s11103-016-0467-6

Wong, 2017, Constructing integrated networks for identifying new secondary metabolic pathway regulators in grapevine: Recent applications and future opportunities, Front. Plant Sci., 8, 1, 10.3389/fpls.2017.00505

Vannozzi, 2018, Combinatorial regulation of stilbene synthase genes by WRKY and MYB transcription factors in grapevine (Vitis vinifera L.), Plant Cell Physiol., 59, 1043, 10.1093/pcp/pcy045