SNP-based high-density linkage map construction and QTL mapping of black spot disease resistance in Chinese sand pear.
Black spot disease
Linkage map
Marker-assisted breeding
Molecular makers
SLAF-seq
Sand pear
Ubiquitin
Journal
Journal of applied genetics
ISSN: 2190-3883
Titre abrégé: J Appl Genet
Pays: England
ID NLM: 9514582
Informations de publication
Date de publication:
Feb 2023
Feb 2023
Historique:
received:
04
06
2022
accepted:
16
09
2022
revised:
15
09
2022
pubmed:
20
10
2022
medline:
17
1
2023
entrez:
19
10
2022
Statut:
ppublish
Résumé
Black spot disease (PBS) caused by Alternaria alternata is an economic disease of pear (Pyrus pyrifolia Nakai). Developing cultivars with durable PBS resistance traits is an important research objective for improving pear germplasm. The Deshengxiang is a popular pear variety in China and resistant to PBS. This study aimed to detect quantitative trait loci (QTL) associated with PBS resistance trait in pear and determine closely linked molecular markers by specific locus amplified fragment sequencing (SLAF-seq). F1 population resulting from a cross between "Deshengxiang" (female) and "Guiguan," a susceptible (male) variety, was developed and evaluated in 2016 and 2017. SLAF technology was used to discover SNPs in the F1 individuals and subsequently a high-density genetic linkage map for PBS resistance was constructed which contained 17,604 SNP markers. Based on the linkage map, the markers were distributed into 17 linkage groups, spanning 1548.48 cM, with a mean marker distance of 0.09 cM, representing the densest genetic map of the genus Pyrus. QTL analysis of PBS resistance identified a locus strongly related to PBS resistance at 77.68 ~ 112.99 cM on linkage group 15, which was further narrowed down to 93.79 ~ 112.99 cM. Two markers, Marker94293 and Marker94206, located at 97.47 and 102.93 cM, were closely associated with PBS resistance, with a Δ (SNP index) value of 0.46. Co-localization of QTL interval, bioinformatics analysis, and functional annotation revealed PBS putative candidate genes. Overall, the high-density pear linkage map is a suitable reference for mapping PBS resistance trait, QTL, and genes identified in this study contribute information that could be useful for PBS improvement in pear.
Identifiants
pubmed: 36261770
doi: 10.1007/s13353-022-00726-8
pii: 10.1007/s13353-022-00726-8
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
23-36Subventions
Organisme : National Key Research and Development Program
ID : 2019YFD1001404
Organisme : National Science Foundation of China
ID : 31801819
Organisme : Transformation Project of Agricultural Scientific and technological achievements
ID : (2021ABC013
Informations de copyright
© 2022. The Author(s), under exclusive licence to Institute of Plant Genetics Polish Academy of Sciences.
Références
Abe A, Kosugi S, Yoshida K et al (2012) Genome sequencing reveals agronomically important loci in rice using mutmap. Nat Biotechnol 30:174–178
doi: 10.1038/nbt.2095
Arends D, Prins P, Jansen RC, Broman KW (2010) R/qtl: high-throughput multiple QTL mapping. Bioinformatics 26(23):2990–2992
doi: 10.1093/bioinformatics/btq565
Ashburner M, Ball CA, Blake JA et al (2000) Gene ontology: tool for the unification of biology. Nat Genet 25:25–29
doi: 10.1038/75556
Bairoch A, Apweiler R (2000) The SWISS-PROT Protein Sequence Database and Its Supplement TrEMBL in 2000. Nucleic Acids Res 28:45–48
doi: 10.1093/nar/28.1.45
Banno K, Ishikawa H, Hamauzu Y, Tabira H (1999) Identification of a RAPD marker linked to the susceptible gene of black spot disease in Japanese pear. J Japan Soc Hort Sci 68:476–481
doi: 10.2503/jjshs.68.476
Bassil N, Postman JD (2010) Identification of European and Asian pears using EST-SSRs from Pyrus. Genet Resour Crop Evol 57(3):357–370
doi: 10.1007/s10722-009-9474-7
Bateman A, Coin L, Durbin R et al (2004) The Pfam protein families database. Nucleic Acids Res 32:D138–D141
doi: 10.1093/nar/gkh121
Berrocal-Lobo M, Stone S, Yang X et al (2010) ATL9, a RING zinc finger protein with E3 ubiquitin ligase activity implicated in chitin- and NADPH oxidase-mediated defense responses. PLoS ONE 5:E14426
doi: 10.1371/journal.pone.0014426
Cao Y, Liu F, Hu H, Zhang B (2006) Pear germplasm resources described norms and standards (the first edition). China Agri Press 2006:86–87
Devoto A, Paul R, Muskett PR, Ken Shirasu K (2003) Role of ubiquitination in the regulation of plant defence against pathogens. Review Curr Opin Plant Biol 6(4):307–311. https://doi.org/10.1016/s1369-5266(03)00060-8
doi: 10.1016/s1369-5266(03)00060-8
Doligez A, Bertrand Y, Dias S et al (2010) QTLs for fertility in table grape (Vitis vinifera L). Tree Genet Genomes 6:413–422
doi: 10.1007/s11295-009-0259-0
Donald TM, Pelleroneb F, Adam-Blondon AF, Bouquet A, Tomas MR, Dry IB (2002) Identification of resistance gene analogs linked to a powdery mildew resistance locus in grapevine. Theor Appl Genet 104(4):610–618
doi: 10.1007/s00122-001-0768-1
Dondini L, Pierantoni L, Gaiotti F et al (2005) Identifying QTLs for fire-blight resistance via a European pear (Pyrus communis L) genetic linkage map. Mol Breed 14:407–418
doi: 10.1007/s11032-005-0505-6
Duplan V, Rivas S (2014) E3 ubiquitin-ligases and their target proteins during the regulation of plant innate immunity. Front Plant Sci 13(5):42. https://doi.org/10.3389/fpls.2014.00042
doi: 10.3389/fpls.2014.00042
Fan S, Bielenberg DG, Zhebentyayeva TN et al (2010) Mapping quantitative trait loci associated with chilling requirement, heat requirement and bloom date in peach (Prunus persica). New Phytol 185:917–930
doi: 10.1111/j.1469-8137.2009.03119.x
Finn RD, Mistry J, Tate J et al (2010) The Pfam protein families database. Nucleic Acids Res 38:D211–D222
doi: 10.1093/nar/gkp985
Furniss JJ, Spoel SH (2015) Cullin-RING ubiquitin ligases in salicylic acid-mediated plant immune signaling. Front Plant Sci 13(6):154. https://doi.org/10.3389/fpls.2015.00154
doi: 10.3389/fpls.2015.00154
Huang X, Zhao Y, Wei X et al (2012) Genome-wide association study of flowering time and grain yield traits in a worldwide collection of rice germplasm. Nat Genet 44:32–39
doi: 10.1038/ng.1018
Iketani H, Abe K, Yamamoto T et al (2001) Mapping of disease-related genes in Japanese pear using a molecular linkage map with RAPD markers. Breed Sci 51:179–184
doi: 10.1270/jsbbs.51.179
Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329
doi: 10.1038/nature05286
Kan J, Liu T, Ma N, Li H, Li X, Wang J et al (2017) Transcriptome analysis of Callery pear (Pyrus calleryana) reveals a comprehensive signalling network in response to Alternaria alternata. PLoS ONE 12(9):e0184988. https://doi.org/10.1371/journal.pone.0184988
doi: 10.1371/journal.pone.0184988
Kanehisa M, Goto S (2000) KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28:27–30
doi: 10.1093/nar/28.1.27
Khan MA, Duffy B, Gessler C, Patocchi A (2006) QTL mapping of fire blight resistance in apple. Mol Breed 17:299–306
doi: 10.1007/s11032-006-9000-y
Kozaki, I. (1973) Black spot disease resistance in Japanese pear. I. Heredity of the disease resistance. Bulletin. Series A.
Lauvergeat V, Lacomme C, Lacombe E, Lasserre E, Roby D, Grima-Pettenati J (2001) Two cinnamoyl-CoA reductase (CCR) genes from Arabidopsis thaliana are differentially expressed during development and in response to infection with pathogenic bacteria. Phytochemistry 57(7):1187–1195
doi: 10.1016/S0031-9422(01)00053-X
Lee DH, Choi HW, Hwang BK, (2011) The pepper E3 ubiquitin ligase RING1 gene, CaRING1, is required for cell death and the salicylic acid-dependent defense response. Plant Physiology, 156(4).
Lee JH, Kim WT (2011) Regulation of abiotic stress signal transduction by E3 ubiquitin ligases in Arabidopsis. Mol Cells 31:201–208
doi: 10.1007/s10059-011-0031-9
Li R, Li Y, Kristiansen K, Wang J (2008) SOAP: short oligonucleotide alignment program. Bioinformatics 24:713–714
doi: 10.1093/bioinformatics/btn025
Liebhard R, Koller B, Patocchi A et al (2003) Mapping quantitative field resistance against apple scab in a ‘fiesta’ x ‘discovery’ progeny. Phytopathology 93:493–501
doi: 10.1094/PHYTO.2003.93.4.493
Liu D, Ma C, Hong W et al (2014) Construction and analysis of high-density linkage map using high-throughput sequencing data. PLoS ONE 9:E98855
doi: 10.1371/journal.pone.0098855
Luo C, Shu B, Yao Q, Wu H, Xu W, Wang S (2016) Construction of a high-density genetic map based on large-scale marker development in mango using specific-locus amplified fragment sequencing (SLAF-seq). Front Plant Sci 7:1310
doi: 10.3389/fpls.2016.01310
Marino D, Peeters N, Rivas S, (2012). Ubiquitination during plant immune signaling. Plant Physiology. 160, (1)15–27. https://www.jstor.org/stable/23274670
Martínez-García PJ, Parfitt DE, Ogundiwin EA et al (2013) High density SNP mapping and QTL analysis for fruit quality characteristics in peach (Prunus persica L). Tree Genet Genomes 9:19–36
doi: 10.1007/s11295-012-0522-7
Mi H, Muruganujan A, Casagrande JT, Thomas PD (2013) Large-scale gene function analysis with the PANTHER classification system. Nat Protoc 8:1551–1566
doi: 10.1038/nprot.2013.092
Miao Y, Zentgraf U (2010) A HECT E3 ubiquitin ligase negatively regulates Arabidopsis leaf senescence through degradation of the transcription factor WRKY53. Plant J 63:179–188
doi: 10.1111/j.1365-313X.2010.04233.x
Miao Y, Zentgraf U (2007) The antagonist function of Arabidopsis WRKY53 and ESR/ESP in leaf senescence is modulated by the jasmonic and salicylic acid equilibrium. Plant Cell 19:819–830
doi: 10.1105/tpc.106.042705
Montanari S, Saeed M, Knabel M et al (2013) Identification of Pyrus single nucleotide polymorphisms (SNPs) and evaluation for genetic mapping in European pear and interspecific Pyrus hybrids. PLoS ONE 8:E77022
doi: 10.1371/journal.pone.0077022
Pierantoni L, Dondini L, Cho KH, Shin IS, Gennari F, Chiodini R, Sansavini S (2007) Pear scab resistance QTLs via a European pear (Pyrus communis) linkage map. Tree Genet Genomes 3(4):311
doi: 10.1007/s11295-006-0070-0
Pruitt KD, Tatusova T, Maglott DR (2007) NCBI reference sequences (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res 35:D61–D65
doi: 10.1093/nar/gkl842
Reis RF, De Almeida TF, Stuchi ES, De Goes A (2007) Susceptibility of citrus species to Alternaria alternata, the causal agent of the Alternaria brown spot. Sci Hortic 113(4):336–342
doi: 10.1016/j.scienta.2007.04.005
Sugiyama A, Omura M, Matsumoto H et al (2011) Quantitative trait loci (QTL) analysis of carotenoid content in Citrus fruit. Journal of the Japanese Society for Horticultural Science 80:136–144
doi: 10.2503/jjshs1.80.136
Sun X, Liu D, Zhang X et al (2013) SLAF-seq: an efficient method of large-scale de novo SNP discovery and genotyping using high-throughput sequencing. PLoS ONE 8:e58700
doi: 10.1371/journal.pone.0058700
Takizawa M, Goto A, Watanabe Y (2005) The tobacco ubiquitin-activating enzymes NtE1A and NtE1B are induced by tobacco mosaic virus, wounding and stress hormones. Mol Cells 19:228–231
Tatusov RL, Galperin MY, Natale DA, Koonin EV (2000) The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res 28:33–36
doi: 10.1093/nar/28.1.33
Teng Y (2011). The pear industry and research in China. Proc. 11th International Pear Symposium Eds.: E. Sánchez et al. Acta Hort. 909, ISHS.
Terakami S, Iketani AY, H., et al (2007) Genetic mapping of genes for susceptibility to black spot disease in Japanese pears. Genome 50:735–741
doi: 10.1139/G07-053
Terakami S, Moriya S, Adachi Y et al (2016) Fine mapping of the gene for susceptibility to black spot disease in Japanese pear (Pyrus pyrifolia Nakai). Breed Res 66(2):271–280
doi: 10.1270/jsbbs.66.271
Terakami S, Adachi Y, Yamane H, Wu J, Matsumoto T, Kunihisa M, Nishitani C, Saito T, Yamamoto T (2012) Fine mapping and BAC contigs construction of the susceptible gene to black spot disease in Japanese pear (Pyrus pyrifolia Nakai). Breed Res 14(1):272
Terakami S, Kimura T, Nishitani C et al (2009) Genetic linkage map of the Japanese pear ‘Housui’identifying three homozygous genomic regions. J Japanese Soc Horticultural Sci 78:417–424
doi: 10.2503/jjshs1.78.417
Terakami S, Shoda M, Adachi Y et al (2006) Genetic mapping of the pear scab resistance gene Vnk of Japanese pear cultivar kinchaku. Theor Appl Genet 113:743–752
doi: 10.1007/s00122-006-0344-9
Van Ooijen JW (2011) Multipoint maximum likelihood mapping in a full-sib family of an outbreeding species. Genetics Res 93(5):343–349
doi: 10.1017/S0016672311000279
Van Os H, Stam P, Visser RG, Van Eck HJ (2005) SMOOTH: a statistical method for successful removal of genotyping errors from high-density genetic linkage data. Theor Appl Genet 112:187–194
doi: 10.1007/s00122-005-0124-y
Wang L, Li X, Wang L et al (2017) Construction of a high-density genetic linkage map in pear (Pyrus communis × Pyrus pyrifolia Nakai) using SSRs and SNPs developed by SLAF-seq. Sci Hortic 218:198–204
doi: 10.1016/j.scienta.2017.02.015
Wei Q, Wang Y, Qin X et al (2014) An SNP-based saturated genetic map and QTL analysis of fruit-related traits in cucumber using specific-length amplified fragment (SLAF) sequencing. BMC Genomics 15:1158
doi: 10.1186/1471-2164-15-1158
Wu J, Li LT, Li M et al (2014) High-density genetic linkage map construction and identification of fruit-related QTLs in pear using SNP and SSR markers. J Exp Bot 65:5771–5781
doi: 10.1093/jxb/eru311
Wu J, Wang Z, Shi Z et al (2013) The genome of the pear (Pyrus bretschneideri Rehd). Genome Res 23:396–408
doi: 10.1101/gr.144311.112
Xu S, Hu Z (2010) Mapping quantitative trait loci using distorted markers. Int J Plant Genomics 2009:11
Yamamoto M, Terakami S, Takada N, Yamamoto T (2016) Physical mapping of black spot disease resistance/susceptibility-related genome regions in Japanese pear (Pyrus pyrifolia) by BAC-FISH. Breed Sci 66:444–449
doi: 10.1270/jsbbs.15085
Yamamoto T, Kimura T, Shoda M et al (2002) Genetic linkage maps constructed by using an interspecific cross between Japanese and European pears. Theor Appl Genet 106:9–18
doi: 10.1007/s00122-002-0966-5
Yamamoto T, Kimura T, Terakami S et al (2007) Integrated reference genetic linkage maps of pear based on SSR and AFLP markers. Breed Sci 57:321–329
doi: 10.1270/jsbbs.57.321
Yang X, Hu H, Yu D, Sun Z, He X, Zhang J et al (2015) Candidate resistant genes of sand pear (Pyrus pyrifolia Nakai) to Alternaria alternata revealed by transcriptome sequencing. PLoS ONE 10(8):e0135046
doi: 10.1371/journal.pone.0135046
Zeng LR, Vega-Sánchez ME, Zhu T, Wang GL (2006) Ubiquitination-mediated protein degradation and modification: an emerging theme in plant-microbe interactions. Cell Res 16(5):413
doi: 10.1038/sj.cr.7310053
Zhang HL, Wang YJ, Zhang CH, Wang XP, Li HE, XR X (2011) Isolation, characterization and expression analysis of resistance gene candidates in pear (Pyrus spp). Scientia Horticulturae 127(3):282–289
doi: 10.1016/j.scienta.2010.10.016
Zhang J, Zhang Q, Cheng T et al (2015) High-density genetic map construction and identification of a locus controlling weeping trait in an ornamental woody plant (Prunus mume Sieb. et Zucc). DNA Res 22:183–191
doi: 10.1093/dnares/dsv003
Zhang Y, Wang L, Xin H et al (2013) Construction of a high-density genetic map for sesame based on large scale marker development by specific length amplified fragment (SLAF) sequencing. BMC Plant Biol 13:141
doi: 10.1186/1471-2229-13-141