Abstract
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Six QTLs were associated with affected leaf area in response to inoculation with Acidovorax citrulli in a recombinant inbred line population of Citrullus amarus.
Abstract
Acidovorax citrulli, the causal agent of bacterial fruit blotch (BFB) of cucurbits, has the potential to devastate production of watermelon and other cucurbits. Despite decades of research on host-plant resistance to A. citrulli, no germplasm has been found with immunity and only a few sources with various levels of BFB resistance have been identified, but the genetic basis of resistance in these watermelon sources are not known. Most sources of resistance are plant introductions of Citrullus amarus (citron melon), a closely related species that crosses readily with cultivated watermelon (Citrullus lanatus L.). In this study, we evaluated a recombinant inbred line population (N = 200), derived from a cross between BFB-resistant (USVL246-FR2) and BFB-susceptible (USVL114) C. amarus lines, for foliar resistance to A. citrulli in three replicated greenhouse trials. We found the genetics of BFB resistance to be complicated by strong environmental influence, low heritability and significant genotype-by-environment interactions. QTL mapping of affected leaf area identified six QTL that each explained between 5 and 15% of the variation in BFB resistance in the population. This study represents the first identification of QTL associated with resistance to A. citrulli in any cucurbit.
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References
Amadi JE, Adebola MO, Eze CS (2009) Isolation and identification of a bacterial blotch organism from watermelon (Citrullus lanatus (Thunb.) Matsum. And Nakai). Afr J Agric Res 4:1291–1294
Bent AF, Kunkel BN, Dahlbeck D et al (1994) RPS2 of Arabidopsis thaliana: a leucine-rich repeat class of plant disease resistance genes. Science 265:1856–1860
Black MC, Isakeit T, Barnes LW, Kucharek TA, Hoover RJ, Hodge NC (1994) First report of bacterial fruit blotch of watermelon in Texas. Plant Dis 78:831
Block CC, Shepherd LM (2008) Long-term survival and seed transmission of Acidovorax avenae subsp citrulli in melon and watermelon seed. Plant Health Progress 10:1094. https://doi.org/10.1094/php-2008-1219-01-br
Branham SE, Levi A, Wechter WP (2017) A GBS-SNP-based linkage map and quantitative trait loci (QTL) associated with resistance to Fusarium oxysporum f. sp. niveum race 2 identified in Citrullus lanatus var. citroides. Theor Appl Genet 130:319–330. https://doi.org/10.1007/s00122-016-2813-0
Branham SE, Levi A, Wechter WP (2018) QTL mapping identifies novel source of resistance to Fusarium wilt race 1 in Citrullus amarus. Plant Dis. https://doi.org/10.1094/pdis-09-18-1677-re
Broman KW, Sen S (2009) A guide to QTL mapping with R/qtl, vol 46. Springer, New York
Broman KW, Wu H, Sen S, Churchill GA (2003) R/qtl: QTL mapping in experimental crosses. Bioinformatics 19:889–890. https://doi.org/10.1093/bioinformatics/btg112
Burdman S, Kots N, Kritzman G, Kopelowitz J (2005) Molecular, physiological, and host-range characterization of Acidovorax avenae subsp. citrulli isolates from watermelon and melon in Israel. Plant Dis 89:1339–1347
Carvalho FCQ, Santos LA, Dias RCS, Mariano RLR, Souza EB (2013) Selection of watermelon genotypes for resistance to bacterial fruit blotch. Euphytica 190:169–180
Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host–microbe interactions: shaping the evolution of the plant immune response. Cell 124:803–814. https://doi.org/10.1016/j.cell.2006.02.008
Chomicki G, Renner SS (2015) Watermelon origin solved with molecular phylogenetics including Linnaean material: another example of museomics. New Phytol 205:526–532. https://doi.org/10.1111/nph.13163
Core Team R (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Crall JM, Schenck NC (1969) Bacterial fruit rot of watermelon in Florida. Plant Dis Report 53:74–75
Demir G (1996) A new bacterial disease of watermelon in Türkiye: bacterial fruit blotch of watermelon (Acidovorax avenae subsp. citrulli (Schaad et al.) Willems et al.). J Turk Phytopathol 25:43–49
Dutta B, Avci U, Hahn MG, Walcott RR (2012) Location of Acidovorax citrulli in infested watermelon seeds is influenced by the pathway of bacterial invasion. Phytopathology 102:461–468
Elshire RJ, Glaubitz JC, Sun Q et al (2011) A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS ONE 6:e19379. https://doi.org/10.1371/journal.pone.0019379
Gilmour AR, Gogel BJ, Cullis BR et al (2009) ASReml user guide release 3.0. VSN International Ltd, Hemel Hemp-Stead
Gitaitis R, Walcott RR (2007) The epidemiology and management of seedborne bacterial diseases. Annu Rev Phytopathol 45:371–397
Godiard L, Sauviac L, Torii KU et al (2003) ERECTA, an LRR receptor-like kinase protein controlling development pleiotropically affects resistance to bacterial wilt. Plant J 36:353–365. https://doi.org/10.1046/j.1365-313X.2003.01877.x
Grant MR, Godiard L, Straube E et al (1995) Structure of the Arabidopsis RPM1 gene enabling dual specificity disease resistance. Science 269:843–846
Guo S, Zhang J, Sun H et al (2013) The draft genome of watermelon (Citrullus lanatus) and resequencing of 20 diverse accessions. Nat Genet 45:51–58. https://doi.org/10.1038/ng.2470
Gusmini G, Song R, Wehner TC (2005) Inheritance of resistance to gummy stem blight in watermelon. Crop Sci 45:582–588. https://doi.org/10.21273/HORTSCI12123-17
Haley CS, Knott SA (1992) A simple regression method for mapping quantitative trait loci in line crosses using flanking markers. Heredity 69:315–324. https://doi.org/10.1038/hdy.1992.131
Holeva MC, Karafla CD, Glynos PE (2010) Acidovorax avenae subsp. citrulli newly reported to cause bacterial fruit blotch of watermelon in Greece. Plant Pathol 59:797
Hopkins DL (1995) Copper-containing fungicides reduce the spread of bacterial fruit blotch of watermelon in the greenhouse. Phytopathology 85:510
Hopkins DL, Levi A (2008) Progress in the development of Crimson sweet-type watermelon breeding lines with resistance to Acidovorax avenae subsp. citrulli. In: Pitrat M (ed) Cucurbitaceae 2008. Proceedings of the IXth EUCARPIA meeting on genetics and breeding of Cucurbitaceae. Il’institut National de la, Recherche Agronomique, Avignon
Hopkins DL, Thompson CM (2002) Seed transmission of Acidovorax avenae subsp. citrulli in cucurbits. HortScience 37:924–926
Hopkins DL, Thompson CM, Hilgren J, Lovic B (2003) Wet seed treatment with peroxyacetic acid for the control of bacterial fruit blotch and other seedborne diseases of watermelon. Plant Dis 87:195–1499
Jacobs JL, Damicone JP, McCraw BD (1992) First report of bacterial fruit blotch of watermelon in Oklahoma. Plant Dis 76:1185
Kousik CS, Shepard BM, Hassell R et al (2007) Potential sources of resistance to broad mites (Polyphagotarsonemus latus) in watermelon germplasm. HortScience 42:1539–1544
Kousik CS, Ikerd JL, Wechter P et al (2012) Resistance to phytophthora fruit rot of watermelon caused by Phytophthora capsici in US plant introductions. HortScience 47:1682–1689
Kruglyak L, Lander ES (1995) A nonparametric approach for mapping quantitative trait loci. Genetics 139:1421–1428
Kruskal WH, Wallis WA (1952) Use of ranks in one-criterion variance analysis. J Am Stat Assoc 47(260):583–621
Latin RX (1996) Bacterial fruit blotch. In: Zitter TA, Hopkins DL, Thomas CE (eds) Compendium of cucurbit diseases. APS Press, St. Paul
Latin RX, Rane KK (1990) Bacterial fruit blotch of watermelon in Indiana. Plant Dis 74:331
Levi A, Thomas CE, Wehner TC, Zhang X (2001) Low genetic diversity indicates the need to broaden the genetic base of cultivated watermelon. HortScience 36:1096–1101
Levi A, Thies JA, Wechter WP et al (2013) High frequency oligonucleotides: targeting active gene (HFO-TAG) markers revealed wide genetic diversity among Citrullus spp. accessions useful for enhancing disease or pest resistance in watermelon cultivars. Genet Resour Crop Evol 60:427–440. https://doi.org/10.1007/s10722-012-9845-3
Li B, Shi Y, Shan C, Zhou Q, Ibrahim M, Wang Y, Wu G, Li H, Xie G, Sun G (2013) Effect of chitosan solution on inhibition of Acidovorax citrulli causing bacterial fruit blotch of watermelon. J Sci Food Agric 93:1010–1015
Ma S, Wehner TC (2015) Flowering stage resistance to bacterial fruit blotch in the watermelon germplasm collection. Crop Sci 55:727–736. https://doi.org/10.2135/cropsci2014.01.0071
Manichaikul A, Moon JY, Sen Ś et al (2009) A model selection approach for the identification of quantitative trait loci in experimental crosses, allowing epistasis. Genetics 181:1077–1086. https://doi.org/10.1534/genetics.108.094565
Mindrinos M, Katagiri F, Yu GL, Ausubel FM (1994) The A. thaliana disease resistance gene RPS2 encodes a protein containing a nucleotide-binding site and leucine-rich repeats. Cell 78:1089–1099. https://doi.org/10.1016/0092-8674(94)90282-8
Mirik M, Aysan Y, Sahin F (2006) Occurrence of bacterial fruit blotch of watermelon caused by Acidovorax avenae subsp. citrulli in the eastern Mediterranean region of Turkey. Plant Dis 90:829
Mundt CC (2014) Durable resistance: a key to sustainable management of pathogens and pests. Infect Genet Evol 27:446–455
Palkovics L, Petróczy M, Kertész B, Németh J (2008) First report of bacterial fruit blotch caused by Acidovorax avenae subsp. citrulli in Hungary. Plant Dis 92:834
Popović T, Ivanović Ž (2015) Occurrence of Acidovorax citrulli causing bacterial fruit blotch of watermelon in Serbia. Plant Dis 99:886
Shapiro SS, Wilk MB (1965) An analysis of variance test for normality (complete samples). Biometrika 52:591–611
Somodi GC, Jones JB, Hopkins DL, Stall RE, Kucharek TA, Hodge NC, Watterson JC (1991) Occurrence of a bacterial watermelon fruit blotch in Florida. Plant Dis 75:1053–1056
Song W, Wang G-L, Chen L et al (1995) A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science 270:1804–1806
Tetteh AY, Wehner TC, Davis AR (2010) Identifying resistance to powdery mildew race 2 W in the USDA-ARS watermelon germplasm collection. Crop Sci 50:933–939. https://doi.org/10.2135/cropsci2009.03.0135
Thies JA, Levi A (2007) Characterization of watermelon (Citrullus lanatus var. citroides) germplasm for resistance to root-knot nematodes. HortScience 42:1530–1533
Walcott RR, Gitaitis RD (2000) Detection of Acidovorax avenae subsp. citrulli in watermelon seed using immunomagnetic separation and the polymerase chain reaction. Plant Dis 84:470–474
Walcott RR, Gitaitis RD, Castro AC (2003) Role of blossoms in watermelon seed infestation by Acidovorax avenae subsp. citrulli. Phytopathology 93:528–534
Walcott RR, Fessehaie A, Castro AC (2004) Differences in pathogenicity between two genetically distinct groups of Acidovorax avenae subsp. citrulli on cucurbit hosts. J Phytopathol 152:277–285
Wang T, Sun B, Yang Y, Zhao T (2015) Genome sequence of Acidovorax citrulli Group 1 strain pslb65 causing bacterial fruit blotch of melons. Genome Announc 3:e00310–e00315. https://doi.org/10.1128/genomeA.00327-15
Webb RE, Goth RW (1965) A seed-borne bacterium isolated from watermelon. Plant Dis Report 49:818–821
Wechter WP, Levi A, Ling KS, Kousik C (2011) Identification of resistance to Acidovorax avenae subsp. citrulli among melon (Cucumis spp) plant introductions. HortScience 46:207–212
Wechter WP, Kousik C, McMillan M, Levi A (2012) Identification of resistance to Fusarium oxysporum f. sp. niveum race 2 in Citrullus lanatus var. citroides plant introductions. HortScience 47:334–338. https://doi.org/10.1002/ird.1717
Wechter WP, Katawczik ML, Farnham MW, Levi A (2016) Watermelon germplasm lines USVL246-FR2 and USVL252-FR2 tolerant to Fusarium oxysporum f. sp. niveum race 2. HortScience 51:1065–1067
Yoshimura S, Yamanouchi U, Katayose Y et al (1998) Expression of Xa1, a bacterial blight-resistance gene in rice, is induced by bacterial inoculation. Proc Natl Acad Sci USA 95:1663–1668. https://doi.org/10.1073/pnas.95.4.1663
Zhang H, Guo S, Gong G et al (2011) Sources of resistance to race 2WF powdery mildew in U.S. watermelon plant introductions. HortScience 46:1349–1352
Zipfel C, Robatzek S, Navarro L et al (2004) Bacterial disease resistancein Arabidopsis through flagellin perception. Nature 428:1–4. https://doi.org/10.1038/nature02485
Zipfel C, Kunze G, Chinchilla D et al (2006) Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125:749–760. https://doi.org/10.1016/j.cell.2006.03.037
Acknowledgements
This research used resources provided by the SCINet project of the USDA Agricultural Research Service, ARS Project Number 0500-00093-001-00-D.
Funding
This study was funded, in part, by the United States Department of Agriculture (USDA) Project Number 6080-22000-028-00 and the National Institute of Food and Agriculture, Specialty Crops Research Initiative project number 6080-21000-019-08.
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Communicated by Michael J. Havey.
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Chromosomal location and functional information for 1916 genes that collocated with QTLs that confer resistance to Acidovorax citrulli (CSV 340 kb)
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Branham, S.E., Levi, A., Katawczik, M.L. et al. QTL mapping of resistance to bacterial fruit blotch in Citrullus amarus. Theor Appl Genet 132, 1463–1471 (2019). https://doi.org/10.1007/s00122-019-03292-6
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DOI: https://doi.org/10.1007/s00122-019-03292-6