The availability of a complete peach genome assembly and three different peach genome sequences created by our group provide new opportunities for application of genomic data and can improve the power of the classical Quantitative Trait Loci (QTL) approaches to identify candidate genes for peach disease resistance. Brown rot caused by Monilinia spp., is the most important fungal disease of stone fruits worldwide. Improved levels of peach fruit rot resistance have been identified in some cultivars and advanced selections developed in the UC Davis and USDA breeding programs. Whole genome sequencing of the Pop-DF parents lead to discovery of high-quality SNP markers for QTL genome scanning in this experimental population. Pop-DF created by crossing a brown rot moderately resistant cultivar ‘Dr. Davis’ and a brown rot resistant introgression line, ‘F8,1–42’, derived from an initial almond × peach interspecific hybrid, was evaluated for brown rot resistance in fruit of harvest maturity over three seasons. Using the SNP linkage map of Pop-DF and phenotypic data collected with inoculated fruit, a genome scan for QTL identified several SNP markers associated with brown rot resistance. Two of these QTLs were placed on linkage group 1, covering a large (physical) region on chromosome 1. The genome scan for QTL and SNP effects predicted several candidate genes associated with disease resistance responses in other host-pathogen systems. Two potential candidate genes, ppa011763m and ppa026453m, may be the genes primarily responsible for M. fructicola recognition in peach, activating both PAMP-triggered immunity (PTI) and effector-triggered immunity (ETI) responses. Our results provide a foundation for further genetic dissection, marker assisted breeding for brown rot resistance, and development of peach cultivars resistant to brown rot.
References
[1]
Ogawa JM, English M (1991) Fungal diseases of stone fruit. In: Publication University of California Division of Agriculture, Natural Resources, editor. Disease of temperate zone tree fruit and nut crops. Oakland, CA. 3345: 461.
[2]
Adaskaveg JE, Kanetis L, Forster H (2005) Ensuring the future of postharvest disease control with new reduced-risk fungicides and resistance management strategies. Phytopathology 95: S140–S140.
[3]
Janisiewicz WJ, Korsten L (2002) Biological control of postharvest diseases of fruits. Annu Rev Phytopathology 40: 411–441.
[4]
Ma ZH, Michailides TJ (2005) Advances in understanding molecular mechanisms of fungicide resistance and molecular detection of resistant genotypes in phytopathogenic fungi. Crop Prot 24: 853–863.
[5]
Cantoni L, Bassi D, Tacconi M (1996) Brown rot in stone fruits: aspects of biology and techniques of selection for resistance. Rivista di Frutticoltura e di Ortofloricoltura 58: 59–65.
[6]
Ogawa JM, Manji BT, Sonoda RM (1985) Management of the brown rot disease on stone fruits and almonds in California. In: Burr TJ, editor. New York State. Agr. Expt. Geneva. 5–8.
[7]
Bostock RM, Adaskaveg JE, Madden S (1994) Role of cutinase in pathogenicity of the brown rot fungus, Monilinia fructicola. Central Valler Postharvest News 3: 16–17.
[8]
Feliciano A, Feliciano AJ, Ogawa JM (1987) Monilinia fructicola resistance in the peach cultivar Bolinha. Phytopathology 77: 776–780.
[9]
Gradziel TM (2003) Interspecific hybridizations and subsequent gene introgression within Prunus subgenus Amygdalus. Acta Hort 622: 249–255.
[10]
Gradziel TM, Wang DC (1993) Evaluation of brown-rot resistance and its relation to enzymatic browning in clingstone peach germplasm. J Am Soc Hortic Sci 118: 675–679.
[11]
Ogundiwin EA, Bostock RM, Gradziel TM, Michailides T, Parfitt DE, et al. (2008) Genetic analysis of host resistance to postharvest brown rot and sour rot in Prunus persica. 4th International Rosaceae Genomics Conference. Pucon, Chile, 15–19 March, 2008.
[12]
Gradziel TM, Wang D (1994) Susceptibility of california almond cultivars to aflatoxigenic Aspergillus flavus. HortScience 29: 33–35.
[13]
Bostock RM, Wilcox SM, Wang G, Adaskaveg JE (1999) Suppression of Monilinia fructicola cutinase production by peach fruit surface phenolic acids. Physiol Mol Plant P 54: 37–50.
[14]
Lee MH, Chiu CM, Roubtsova T, Chou CM, Bostock RM (2010) Overexpression of a redox-regulated cutinase gene, MfCUT1, increases virulence of the brown rot pathogen Monilinia fructicola on Prunus spp. Mol Plant Microbe In 23: 176–186.
[15]
Lee MH, Bostock RM (2007) Fruit exocarp phenols in relation to quiescence and development of Monilinia fructicola infections in Prunus spp.: A role for cellular redox? Phytopathology 97: 269–277.
[16]
Prusky D, Lichter A (2007) Activation of quiescent infections by postharvest pathogens during transition from the biotrophic to the necrotrophic stage. FEMS Microbiol Lett 268: 1–8.
[17]
International Peach Genome Initiative, Verde I, Abbott AG, Scalabrin S, Jung S, et al. (2013) The high-quality draft genome of peach (Prunus persica) identifies unique patterns of genetic diversity, domestication and genome evolution. Nat Genet 45: 487–494.
[18]
Ahmad R, Parfitt DE, Fass J, Ogundiwin E, Dhingra A, et al. (2011) Whole genome sequencing of peach (Prunus persica L.) for SNP identification and selection. BMC Genomics 12: 569.
[19]
Martínez-García PJ, Fresnedo-Ramírez J, Parfitt DE, Gradziel TM, Crisosto CH (2013) Effect prediction of identified SNPs linked to fruit quality and chilling injury in peach [Prunus persica (L.) Batsch]. Plant Mol Biol 81: 161–174.
[20]
Martínez-García PJ, Parfitt DE, Ogundiwin EA, Fass J, Chan HM, 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.
[21]
SAS Institute Inc. (1989–2007) JMP, Version 7. Cary, NC: SAS Institute Inc.
[22]
Van Ooijen JW, Maliepaard C (1997) MapQTL version 3.0: software for the calculation of QTL positions on genetic maps. Advances in biometrical genetics Proceedings of the tenth meeting of the EUCARPIA Section Biometrics in Plant Breeding, Poznan, Poland.
[23]
Cingolani P, Platts A, Wang LL, Coon M, Nguyen T, et al. (2012) A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w (1118) ; iso-2; iso-3. Fly (Austin) 6: 80–92.
[24]
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406–425.
[25]
Felsenstein J (1985) Confidence-Limits on Phylogenies – an approach using the bootstrap. evolution 39: 783–791.
[26]
Zuckerkandl E, Pauling L (1965) Evolutionary divergence and convergence in proteins. In: Bryson V, Vogel HJ, editors. Evolving Genes and Proteins. New York.: Academic Press. 97–166.
[27]
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, et al. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731–2739.
[28]
Aranzana MJ, Abbassi E-K, Howad W, Arus P (2010) Genetic variation, population structure and linkage disequilibrium in peach commercial varieties. BMC Genet 11: 69.
[29]
Whitham S, Dinesh-Kumar SP, Choi D, Hehl R, Corr C, et al. (1994) The product of the tobacco mosaic virus resistance gene N: similarity to toll and the interleukin-1 receptor. Cell 78: 1101–1115.
[30]
Jones JD, Dangl JL (2006) The plant immune system. Nature 444: 323–329.
[31]
Padmanabhan MS, Ma S, Burch-Smith TM, Czymmek K, Huijser P, et al. (2013) Novel positive regulatory role for the SPL6 transcription factor in the N TIR-NB-LRR receptor-mediated plant innate immunity. PLoS Pathog 9: e1003235.
[32]
Burch-Smith TM, Schiff M, Caplan JL, Tsao J, Czymmek K, et al. (2007) A novel role for the TIR domain in association with pathogen-derived elicitors. PLoS Biol 5: e68.
[33]
Miyazaki S, Murata T, Sakurai-Ozato N, Kubo M, Demura T, et al. (2009) ANXUR1 and 2, sister genes to FERONIA/SIRENE, are male factors for coordinated fertilization. Curr Biol 19: 1327–1331.
[34]
Dardick C, Schwessinger B, Ronald P (2012) Non-arginine-aspartate (non-RD) kinases are associated with innate immune receptors that recognize conserved microbial signatures. Curr Opin Plant Biol 15: 358–366.
[35]
Zipfel C, Kunze G, Chinchilla D, Caniard A, Jones JD, et al. (2006) Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125: 749–760.
[36]
Zimaro T, Gottig N, Garavaglia BS, Gehring C, Ottado J (2011) Unraveling plant responses to bacterial pathogens through proteomics. J Biomed Biotechnol 2011: 354801.
[37]
He C, Fong SH, Yang D, Wang GL (1999) BWMK1, a novel MAP kinase induced by fungal infection and mechanical wounding in rice. Mol Plant Microbe In 12: 1064–1073.
[38]
Chen LQ, Hou BH, Lalonde S, Takanaga H, Hartung ML, et al. (2010) Sugar transporters for intercellular exchange and nutrition of pathogens. Nature 468: 527–532.
[39]
Nessler CL, Allen RD, Galewsky S (1985) Identification and characterization of latex-specific proteins in opium poppy. Plant Physiol 79: 499–504.
[40]
Lytle BL, Song J, de la Cruz NB, Peterson FC, Johnson KA, et al. (2009) Structures of two Arabidopsis thaliana major latex proteins represent novel helix-grip folds. Proteins 76: 237–243.
[41]
Wietholter N, Graessner B, Mierau M, Mort AJ, Moerschbacher BM (2003) Differences in the methyl ester distribution of homogalacturonans from near-isogenic wheat lines resistant and susceptible to the wheat stem rust fungus. Mol Plant Microbe In 16: 945–952.
[42]
Giovane A, Servillo L, Balestrieri C, Raiola A, D'Avino R, et al. (2004) Pectin methylesterase inhibitor. Biochim Biophys Acta 1696: 245–252.
[43]
Di Matteo A, Giovane A, Raiola A, Camardella L, Bonivento D, et al. (2005) Structural basis for the interaction between pectin methylesterase and a specific inhibitor protein. Plant Cell 17: 849–858.
[44]
Hasunuma T, Fukusaki E, Kobayashi A (2004) Expression of fungal pectin methylesterase in transgenic tobacco leads to alteration in cell wall metabolism and a dwarf phenotype. J Biotechnol 111: 241–251.
[45]
de Vries RP, Visser J (2001) Aspergillus enzymes involved in degradation of plant cell wall polysaccharides. Microbiol Mol Biol Rev 65: 497–522.
[46]
Lazar EE, Wills RB, Ho BT, Harris AM, Spohr LJ (2008) Antifungal effect of gaseous nitric oxide on mycelium growth, sporulation and spore germination of the postharvest horticulture pathogens, Aspergillus niger, Monilinia fructicola and Penicillium italicum. Lett Appl Microbiol 46: 688–692.
