Multiomic investigation of sugarcane mosaic virus resistance in sugarcane (2024)

https://doi.org/10.1101/2022.08.18.504288

Видання: 2022

Видавець: Cold Spring Harbor Laboratory

Автори:

Анотація

AbstractSugarcane mosaic virus (SCMV) is the main etiological agent of sugarcane mosaic disease, which affects sugarcane, maize and other economically important grass species. Despite the extensive characterization of quantitative trait loci controlling resistance to SCMV in maize, the genetic basis of this trait is largely unexplored in sugarcane. Here, a genome-wide association study was performed and machine learning coupled to feature selection was used for the genomic prediction of resistance to SCMV in a diverse panel of sugarcane accessions. This ultimately led to the identification of nine single nucleotide polymorphisms (SNPs) explaining up to 29.9% of the phenotypic variance and a 73-SNP set that predicted resistance with high accuracy, precision, recall, and F1 scores. Both marker sets were validated in additional sugarcane genotypes, in which the SNPs explained up to 23.6% of the phenotypic variation and predicted resistance with a maximum accuracy of 69.1%. Synteny analyses showed that the gene responsible for the major SCMV resistance in maize is probably absent in sugarcane, explaining why such a major resistance source is thus far unknown in this crop. Lastly, using sugarcane RNA sequencing data, markers associated with the resistance to SCMV in sugarcane were annotated and a gene coexpression network was constructed to identify the predicted biological processes involved in SCMV resistance. This allowed the identification of candidate resistance genes and confirmed the involvement of stress responses, photosynthesis and regulation of transcription and translation in the resistance to this virus. These results provide a viable marker-assisted breeding approach for sugarcane and identify target genes for future molecular studies on resistance to SCMV.

Список літератури

Identification of genes differentially expressed in onion infected with Iris yellow spot virus, Phytopathol. Mediterr, № 57, с. 334
Gene expression profiling of reactive oxygen species (ROS) and antioxidant defense system following Sugarcane mosaic virus (SCMV) infection, BMC Plant Biol, № 20, с. 532
https://doi.org/10.1186/s12870-020-02737-1
Alexa, A. and Rahnenfuhrer, J . (2010) topGO: Enrichment Analysis for Gene Ontology. R Package Version.
Machine learning approaches reveal genomic regions associated with sugarcane brown rust resistance, Sci. Rep, № 10, с. 20057
https://doi.org/10.1038/s41598-020-77063-5
A joint learning approach for genomic prediction in polyploid grasses, Scientific Reports, № 12, с. 1
Bailey, R.A. and Fox, P.H . (1987) A preliminary report on the effect of sugarcane mosaic virus on the yield of sugarcane varieties NCo376 and N12. In Proceedings of the South African Sugar Technologists’ Association, pp. 1–4.
Comparing genotyping-by-sequencing and single nucleotide polymorphism chip genotyping for quantitative trait loci mapping in wheat, Crop Sci, № 56, с. 232
https://doi.org/10.2135/cropsci2015.06.0389
The identification of potential genetic markers in sugarcane varieties for the prediction of disease and pest resistance ratings, Proc. Annu. Congr. S. Afr. Sugar Technol. Assoc, № 71, с. 57
Brune, A.E. and Rutherford, R.S. (2005) Investigating the association of sugarcane kinase analogs and NBS-LRR resistance gene analogs with susceptibility and/or resistance to the pathogens Ustilago scitaminea (smut) and sugarcane mosaic virus (SCMV). In Proceedings of the 79th Annual Congress of South African Sugar Technologists’ Association. Kwa-Shukela, Mount Edgecombe, South Africa: South African Sugar Technologists’ Association, pp. 235–238.
Burbano, R.C.V. , da Silva, M.F. , Coutinho, A.E. , Gonçalves, M.C. , dos Anjos, I.A. , Anjos, L.O.S. , Perecin, D. and Pinto, L.R. (2022) Marker-trait association for resistance to sugarcane mosaic virus (SCMV) in a Sugarcane (Saccharum spp.) panel. Sugar Tech, 1–13. https://doi.org/10.1007/s12355-022-01131-5
https://doi.org/10.1007/s12355-022-01131-5
The potential of the energy cane as the main biomass crop for the cellulosic industry, Chem. Biol. Technol. Agric, № 1, с. 20
https://doi.org/10.1186/s40538-014-0020-2
Castillo, A.G. , Morilla, G. , Lozano, R. , Collinet, D. , Perez-Luna, A. , Kashoggi, A. and Bejarano, E. (2007) Identification of plant genes involved in TYLCV replication. In Tomato Yellow Leaf Curl Virus Disease: Management, Molecular Biology, Breeding for Resistance ( Czosnek, H. , ed). Dordrecht: Springer, pp. 207–221.
https://doi.org/10.1007/978-1-4020-4769-5_12
Detection of Sugarcane yellow leaf virus in quarantine and production of virus-free sugarcane by apical meristem culture, Plant Dis., № 85, с. 1177
https://doi.org/10.1094/PDIS.2001.85.11.1177
Identification of differentially regulated maize proteins conditioning Sugarcane mosaic virus systemic infection, New Phytol., № 215, с. 1156
https://doi.org/10.1111/nph.14645
Chen, T. and Guestrin, C. (2016) XGBoost: a scalable tree boosting system. In Proceedings of the 22nd ACM SIGKDD International Conference on Knowledge Discovery and Data Mining. San Francisco, California, USA: Association for Computing Machinery, pp. 785–794.
https://doi.org/10.1145/2939672.2939785
Costa, A.S. and Muller, G.W. (1982) General evaluation of the impacts of virus diseases of economic crops on the development of Latin American Countries. In Proc. Conf. Impact of Viral Diseases in Developing Latin American and Caribbean Countries. Rio de Janeiro, pp. 216–130.
Cristianini, N. and Shawe-Taylor, J. (2000) An Introduction to Support Vector Machines and Other Kernel-Based Learning Methods. Cambridge, UK: Cambridge University Press.
https://doi.org/10.1017/CBO9780511801389
Cronje, C.P.R. , Bechet, G.R. and Bailey, R.A. (1994) Symptom expression of sugarcane mosaic virus (SCMV) and associated effects on sugarcane yield. In Proceedings of the Annual Congress South African Sugar Technologists’ Association, pp. 8–11.
D’Hont, A. and Glaszmann, J.C. (2001) Sugarcane genome analysis with molecular markers: a first decade of research. In International Society of Sugar Cane Technologists. Proceedings of the XXIV Congress. Mackay, Australia: Australian Society of Sugar Cane Technologists, pp. 556–559.
Sugarcane mosaic virus mediated changes in cytosine methylation pattern and differentially transcribed fragments in resistance-contrasting sugarcane genotypes, PLoS One, № 15, с. e0241493
https://doi.org/10.1371/journal.pone.0241493
Screening sugarcane wild accessions for resistance to Sugarcane mosaic virus (SCMV), Sugar Tech, № 17, с. 252
https://doi.org/10.1007/s12355-014-0323-4
Evaluation of Brazilian sugarcane genotypes for resistance to Sugarcane mosaic virus under greenhouse and field conditions, Crop Prot., № 70, с. 15
https://doi.org/10.1016/j.cropro.2015.01.002
Elimination of SCMV (Sugarcane Mozaik Virus) and rapid propagation of virus-free sugarcane (Saccharum officinarum L.) using somatic embryogenesis, Procedia Chem., № 18, с. 96
https://doi.org/10.1016/j.proche.2016.01.016
Fine mapping of Rscmv2, a major gene for resistance to sugarcane mosaic virus in maize, Mol. Breed., № 30, с. 1593
https://doi.org/10.1007/s11032-012-9741-8
Saturation of two chromosome regions conferring resistance to SCMV with SSR and AFLP markers by targeted BSA, Theor. Appl. Genet., № 106, с. 485
https://doi.org/10.1007/s00122-002-1107-x
Molecular mapping and gene action of Scm1 and Scm2, two major QTL contributing to SCMV resistance in maize, Plant Breed., № 119, с. 299
https://doi.org/10.1046/j.1439-0523.2000.00509.x
FAO (2022) FAOSTAT: Production Sheet. Rome: FAO.
Genome-wide association mapping identifies markers associated with cane yield components and sucrose traits in the Louisiana sugarcane core collection, Genomics, № 111, с. 1794
https://doi.org/10.1016/j.ygeno.2018.12.002
Haplotype-based variant detection from short-read sequencing, arXiv preprint arXiv, № 1207, с. 3907
A mosaic monoploid reference sequence for the highly complex genome of sugarcane, Nat. Commun., № 9, с. 2638
https://doi.org/10.1038/s41467-018-05051-5
Genetic variability of Sugarcane mosaic virus causing maize mosaic in Brazil, Pesqui. Agropecu. Bras., № 46, с. 362
https://doi.org/10.1590/S0100-204X2011000400004
Identificação e caracterização de isolados pertencentes ao subgrupo do Sugarcane mosaic virus no estado de São Paulo, Fitopatol. Bras., № 29, с. 129
Virus diseases of sugarcane. A constant challenge to sugarcane breeding in Brazil, Funct. Plant Sci. Biotechnol., № 6, с. 108
Caracterização de um isolado do Sugarcane mosaic virus que quebra a resistência de variedades comerciais de cana-de-açúcar, Fitopatol. Bras, № 32, с. 32
https://doi.org/10.1590/S0100-41582007000100004
Genome wide association mapping of agro-morphological and disease resistance traits in sugarcane, Euphytica, № 202, с. 269
https://doi.org/10.1007/s10681-014-1294-y
Genetic analysis of Sugarcane mosaic virus resistance in the wisconsin diversity panel of maize, Crop Sci., № 58, с. 1853
https://doi.org/10.2135/cropsci2017.11.0675
Molecular cloning, sequencing, and phylogenetic relationships of a new potyvirus: sugarcane streak mosaic virus, and a reevaluation of the classification of the Potyviridae, Mol. Phylogenetics Evol., № 10, с. 323
https://doi.org/10.1006/mpev.1998.0535
Aphid transmission of Sugarcane mosaic virus (SCMV), Pak. J. Agric. Sci, № 40, с. 74
Accuracy of genomic prediction of complex traits in sugarcane, Theor. Appl. Genet., № 134, с. 1455
https://doi.org/10.1007/s00122-021-03782-6
Photosynthesis in sugarcane varieties infected with strains of sugarcane mosaic virus, Physiol. Plant., № 24, с. 51
https://doi.org/10.1111/j.1399-3054.1971.tb06714.x
ISO (2022) International Sugar Organization. London: ISO.
DsRNA molecules from the Tobacco mosaic virus p126 gene counteract TMV-induced proteome changes at an early stage of infection, Front. Plant Sci., № 12, с. 663707
https://doi.org/10.3389/fpls.2021.663707
Langfelder, P. and Horvath, S. (2017) WGCNA package: frequently asked questions.
Association mapping resolving the major loci Scmv2 conferring resistance to sugarcane mosaic virus in maize, Eur. J. Plant Pathol., № 145, с. 385
https://doi.org/10.1007/s10658-015-0852-z
Molecular mapping of a major QTL conferring resistance to SCMV based on immortal RIL population in maize, Euphytica, № 167, с. 229
https://doi.org/10.1007/s10681-008-9874-3
Molecular characterization of NBS–LRR genes in the soybean Rsv3 locus reveals several divergent alleles that likely confer resistance to the soybean mosaic virus, Theor. Appl. Genet., № 131, с. 253
https://doi.org/10.1007/s00122-017-2999-9
Midrib sucrose accumulation and sugar transporter gene expression in YCS-affected sugarcane leaves, Trop. Plant Biol., № 12, с. 186
https://doi.org/10.1007/s12042-019-09221-7
Identifying markers for resistance to sugarcane orange rust (Puccinia kuehnii) via selective genotyping and capture sequencing, Euphytica, № 215, с. 150
https://doi.org/10.1007/s10681-019-2340-6
Munoz, F. and Rodriguez, L.S. (2014) breedR: statistical methods for forest genetic resources analysis. In Trees for the Future: Plant Material in a Changing Climate. Tulln, Austria, pp. 13.
Transcriptomic analysis of cultivated cotton Gossypium hirsutum provides insights into host responses upon whitefly-mediated transmission of cotton leaf curl disease, PLoS One, № 14, с. e0210011
https://doi.org/10.1371/journal.pone.0210011
Peterson, R. (2017) Estimating normalization transformations with bestNormalize. https://github.com/petersonR/bestNormalize. [Accessed February 23, 2021].
Genome-wide approaches for the identification of markers and genes associated with sugarcane yellow leaf virus resistance, Sci. Rep., № 11, с. 15730
https://doi.org/10.1038/s41598-021-95116-1
Pinto, L.R. , Gonçalves, M.C. , Galdeano, D.M. , Perecin, D. , Medeiros, C.N.F. , Gonçalves, B.S. , Mancini, M.C. and Landell, M.G.D.A. (2013) Preliminary investigation of sugarcane mosaic virus resistance and marker association in a sugarcane family sample derived from a bi-parental cross. In Proceedings of International Society of Sugar Cane Technologists. Brisbane: International Society of Sugar Cane Technologists.
Multilayer perceptron and neural networks, WSEAS Trans. Circuits Syst., № 8, с. 579
Potyviral gene-silencing suppressor HCPro interacts with salicylic acid (SA)-binding protein 3 to weaken SA-mediated defense responses, Mol. Plant Microbe Interact., № 31, с. 86
https://doi.org/10.1094/MPMI-06-17-0128-FI
R Core Team (2011) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.
Rasmussen, C.E. (2003) Gaussian processes in machine learning. In Advanced Lectures on Machine Learning. ML 2003. Lecture Notes in Computer Science ( Bousquet, O. , von Luxburg, U. and Rätsch, G. , eds). Berlin, Heidelberg: Springer, pp. 63–71.
Rosyara, U.R. , De Jong, W.S. , Douches, D.S. and Endelman, J.B. (2016) Software for genome-wide association studies in autopolyploids and its application to potato. Plant Genome, 9 https://doi.org/10.3835/plantgenome2015.08.0073
https://doi.org/10.3835/plantgenome2015.08.0073
Genome-wide association study reveals new loci involved in Arabidopsis thaliana and Turnip mosaic virus (TuMV) interactions in the field, New Phytol., № 221, с. 2026
https://doi.org/10.1111/nph.15507
Identification and expression analysis of genes induced in response to tomato chlorosis virus infection in tomato, Plant Pathol. J., № 35, с. 257
https://doi.org/10.5423/PPJ.OA.12.2018.0287
Fine mapping of the RSC9 gene and preliminary functional analysis of candidate resistance genes in soybean (Glycine max), Plant Breed, № 141, с. 49
Effect of sugarcane mosaic potyvirus infection on metabolic activity, yield and juice quality, Sugar Cane, № 5, с. 19
Progressive decline in yield and quality of sugarcane due to sugarcane mosaic virus, Indian Phytopathol., № 56, с. 500
Transient expression of the coat protein of sugarcane mosaic virus in sugarcane protoplasts and expression inEscherichia coli, Arch. Virol., № 125, с. 15
https://doi.org/10.1007/BF01309625
Molecular mapping of quantitative trait loci (QTLs) determining resistance to Sugarcane mosaic virus in maize using simple sequence repeat (SSR) markers, Afr. J. Biotechnol., № 11, с. 3496
Song, P. , Chen, X. , Wu, B. , Gao, L. , Zhi, H. and Cui, X. (2016) Identification for soybean host factors interacting with P3N-PIPO protein of Soybean mosaic virus. Acta Physiol. Plant., 38 https://doi.org/10.1007/s11738-016-2126-6
https://doi.org/10.1007/s11738-016-2126-6
Combined linkage and association mapping reveals candidates for Scmv1, a major locus involved in resistance to sugarcane mosaic virus (SCMV) in maize, BMC Plant Biol., № 13, с. 162
https://doi.org/10.1186/1471-2229-13-162
The challenge of analyzing the sugarcane genome, Front. Plant Sci., № 9, с. 616
https://doi.org/10.3389/fpls.2018.00616
Unraveling the genome of a high yielding colombian sugarcane hybrid, Front. Plant Sci., № 12, с. 694859
https://doi.org/10.3389/fpls.2021.694859
Gel-free/label-free proteomic, photosynthetic, and biochemical analysis of cowpea (Vigna unguiculata [L.] Walp.) resistance against Cowpea severe mosaic virus (CPSMV), J. Proteom, № 163, с. 76
https://doi.org/10.1016/j.jprot.2017.05.003
Impact of mosaic infection on growth and yield of sugarcane, Sugar Tech, № 7, с. 61
https://doi.org/10.1007/BF02942419
Genetic analysis and molecular mapping of two dominant complementary genes determining resistance to sugarcane mosaic virus in maize, Euphytica, № 156, с. 355
https://doi.org/10.1007/s10681-007-9384-8
Comparative proteomic analysis of the plant–virus interaction in resistant and susceptible ecotypes of maize infected with sugarcane mosaic virus, J. Proteom., № 89, с. 124
https://doi.org/10.1016/j.jprot.2013.06.005
Sugarcane mosaic virus – long history but still a threat to industry, Crop Prot., № 42, с. 74
https://doi.org/10.1016/j.cropro.2012.07.005
Xavier, M. , Silva, M. , Gonçalves, M. , Pinto, L. , Perecin, D. and Landell, M. (2013) Family selection for detection of promising crosses of sugarcane varieties for resistance to SCMV in Ribeirão Preto and Jaú. In International Society of Sugar Cane Technologists: Proceedings of the XXVIIIth Congress. São Paulo, Brazil: International Society of Sugar Cane Technologists.
Quantitative trait loci mapping of resistance to sugarcane mosaic virus in maize, Phytopathology, № 89, с. 660
https://doi.org/10.1094/PHYTO.1999.89.8.660
High-resolution mapping of loci conferring resistance to sugarcane mosaic virus in maize using RFLP, SSR, and AFLP markers, Mol. Gen. Genet., № 261, с. 574
https://doi.org/10.1007/s004380051003
Identifying quantitative trait loci (QTLs) and developing diagnostic markers linked to orange rust resistance in sugarcane (Saccharum spp.), Front. Plant Sci, № 9, с. 350
https://doi.org/10.3389/fpls.2018.00350
Target enrichment sequencing of 307 germplasm accessions identified ancestry of ancient and modern hybrids and signatures of adaptation and selection in sugarcane (Saccharum spp.), a ‘sweet’ crop with ‘bitter’ genomes, Plant Biotechnol. J., № 17, с. 488
https://doi.org/10.1111/pbi.12992
QTL mapping for resistance to SCMV in Chinese maize germplasm, Maydica, № 48, с. 307
Zhou, W. , Bellis, E.S. , Stubblefield, J. , Causey, J. , Qualls, J. , Walker, K. and Huang, X. (2019) Minor QTLs mining through the combination of GWAS and machine learning feature selection. BioRxiv, 712190. https://doi.org/10.1101/712190
https://doi.org/10.1101/702761
A DnaJ protein that interacts with soybean mosaic virus coat protein serves as a key susceptibility factor for viral infection, Virus Res, № 281, с. 197870
https://doi.org/10.1016/j.virusres.2020.197870

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Multiomic investigation of sugarcane mosaic virus resistance in sugarcane (2024)

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