pp 1–10 | Cite as

Mapping quantitative trait loci conferring resistance to Marssonina leaf spot disease in Populus deltoides

  • Hairong Jiang
  • Zhibing Wan
  • Min Liu
  • Jing Hou
  • Tongming YinEmail author
Original Article
Part of the following topical collections:
  1. Phytopathology
  2. Phytopathology
  3. Phytopathology


Key message

Two large-effect QTLs and 14 candidate genes conferring resistance to Marssonina leaf spot disease were identified in an F1Populus deltoides pedigree, which provided valuable information for cloning the particular underlying genes in future.


Marssonina leaf spot disease (MLSD), which is caused by Marssonina brunnea, is a devastating threat to poplar plantations. To map quantitative trait loci (QTLs) underlying resistance to MLSD, an F1P. deltoides pedigree has been established and genetic maps were constructed for the mapping parents according to the two-way pseudo-testcross mapping strategy. The female map contained 913 markers spanning a total genetic distance of 3132 cM, with linkage groups (LGs) corresponding to the 19 haploid chromosomes in poplar, whereas the paternal map contained 252 markers distributed on 22 LGs and covered a genetic length of 1809 cM. The established maps were further aligned to the poplar consensus genetic map based on the integrated SSR markers. The resistance to MLSD was recorded as a complex binary trait based on the black spot symptom on leaves. Analyses of QTLs revealed two large-effect QTLs in LGs VI and XVI, namely qMLSD-VI-1 and qMLSD-XVI-2, which explained 50.3% and 34.5% of the total phenotypic variance, respectively. A significant interaction between these two QTLs was detected based on a two-way ANOVA. In this mapping pedigree, the female parent contributed all of the QTL alleles conferring resistance to M. brunnea. Genome sequences in the target regions were obtained by aligning the QTL intervals to the poplar genome sequence with the mapped SSR markers. The importance and utility of the 14 candidate genes associated with disease resistance identified in the QTL intervals should be more thoroughly characterized in future studies.


Marssonina brunnea Genetic map Sequence dissection Disease resistance gene 



The study was supported by the National Key Research and Development Plan of China (2016YFD0600101), and the National Natural Science Foundation of China (31500533 and 31570662). It was also supported by the PAPD (Priority Academic Program Development) program at Nanjing Forestry University.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

468_2018_1809_MOESM1_ESM.eps (2.6 mb)
Supplementary material 1 (EPS 2712 KB)
468_2018_1809_MOESM2_ESM.eps (2.2 mb)
Supplementary material 2 (EPS 2218 KB)
468_2018_1809_MOESM3_ESM.tif (4.9 mb)
Supplementary material 3 (TIF 5042 KB)
468_2018_1809_MOESM4_ESM.docx (11 kb)
Supplementary material 4 (DOCX 11 KB)
468_2018_1809_MOESM5_ESM.xlsx (21 kb)
Supplementary material 5 (XLSX 21 KB)


  1. Alheit KV, Reif JC, Maurer HP, Hahn V, Weissmann EA, Miedaner T, Würschum T (2011) Detection of segregation distortion loci in triticale (× Triticosecale Wittmack) based on a high-density DArT marker consensus genetic linkage map. BMC Genom 12:380. CrossRefGoogle Scholar
  2. Anderson JP, Badruzsaufari E, Schenk PM, Manners JM, Desmond OJ, Ehlert C, Maclean DJ, Ebert PR, Kazan K (2004) Antagonistic interaction between abscisic acid and jasmonate-ethylene signaling pathways modulates defense gene expression and disease resistance in Arabidopsis. Plant Cell 16:3460–3479. CrossRefGoogle Scholar
  3. Cervera MT, Storme V, Ivens B, Gusmao J, Liu BH, Hostyn V, Van Slycken J, Van Montagu M, Boerjan W (2001) Dense genetic linkage maps of three Populus species (Populus deltoides, P. nigra and P. trichocarpa) based on AFLP and microsatellite markers. Genetics 158:787–809Google Scholar
  4. Charlesworth D, Charlesworth B (1987) Inbreeding depression and its evolutionary consequences. Ann Rev Ecol Syst 18:237–268. CrossRefGoogle Scholar
  5. de Torres-Zabala M, Truman W, Bennett MH, Lafforgue G, Mansfield JW, Egea PR, Bögre L, Grant M (2007) Pseudomonas syringae pv. tomato hijacks the Arabidopsis abscisic acid signaling pathway to cause disease. Embo J 26:1434–1443. CrossRefGoogle Scholar
  6. Doerge RW, Churchill GA (1996) Permutation tests for multiple loci affecting a quantitative character. Genetics 142:285–294Google Scholar
  7. Dowkiw A, Bastien C (2007) Presence of defeated qualitative resistance genes frequently has major impact on quantitative resistance to Melampsora larici-populina leaf rust in P. × interamericana hybrid poplars. Tree Genet Genomes 3:261–274. CrossRefGoogle Scholar
  8. Elberse IAM, Vanhala TK, Turin JHB, Stam P, van Damme JMM, van Tienderen PH (2004) Quantitative trait loci affecting growth-related traits in wild barley (Hordeum spontaneum) grown under different levels of nutrient supply. Heredity 93:22–33. CrossRefGoogle Scholar
  9. Fishman L, Kelly AJ, Morgan E, Willis JH (2001) A genetic map in the Mimulus guttatus species complex reveals transmission ratio distortion due to heterospecific interactions. Genetics 159:1701–1716Google Scholar
  10. Gaudet M, Jorge V, Paolucci I, Beritognolo I, Scarascia Mugnozza G, Sabatti M (2008) Genetic linkage maps of Populus nigra L. including AFLPs, SSRs, SNPs, and sex trait. Tree Genet Genomes 4:25–36. CrossRefGoogle Scholar
  11. Grattapaglia D, Sederoff R (1994) Genetic linkage maps of Eucalyptus grandis and Eucalyptus urophylla using a pseudo-testcross: mapping strategy and RAPD markers. Genetics 137:1121–1137Google Scholar
  12. Han Z, Li C, Huang M (1997) Further studies on the two specialized forms of Marssonina brunnea (ELL.& EV.) Magn. J Nanjing For Univ 21:40–44Google Scholar
  13. Han Z, Li C, Huang M (1998) Comparative studies of isolates of Marssonina brunnea in China. Sci Silvae Sin 34:59–65. Google Scholar
  14. Han Z, Yin T, Li C, Huang M, Wu R (2000) Host effect on genetic variation of Marssonina brunnea pathogenic to poplars. Theor Appl Genet 100:614–620. CrossRefGoogle Scholar
  15. Hartl DL (1974) Genetic dissection of segregation distortion. I. Suicide combinations of SD genes. Genetics 76:477–486Google Scholar
  16. He W, Yang W (1991) Host range and distribution of three Marssonina species pathogenic to poplars in part region of China. Sci Silvae Sin 27:560–564Google Scholar
  17. Jain SK, Singh P (2000) Economic analysis of industrial agroforestry: poplar (Populus deltoides) in Uttar Pradesh (India). Agrofor Syst 49:255–273. CrossRefGoogle Scholar
  18. Kartesz JT, Meacham CA (1999) Synthesis of the North American flora. North Carolina Botanical Garden, University of North Carolina at Chapel HillGoogle Scholar
  19. Kuang H, Richardson T, Carson S, Wilcox P, Bongarten B (1999) Genetic analysis of inbreeding depression in plus tree 850.55 of Pinus radiata D. Don. I. Genetic map with distorted markers. Theor Appl Genet 98:697–703. CrossRefGoogle Scholar
  20. Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE, Newburg L (1987) MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181. CrossRefGoogle Scholar
  21. Lange K, Boehnke M (1982) How many polymorphic genes will it take to span the human genome? Am J Hum Genet 34:842–845Google Scholar
  22. Li C (1984) Two specialized forms of Marssonina populi (Lib.) Magn. J Nanjing For Univ 8:10–17Google Scholar
  23. Li X, Quigg RJ, Zhou J, Xu S, Masinde G, Mohan S, Baylink DJ (2006a) A critical evaluation of the effect of population size and phenotypic measurement on QTL detection and localization using a large F2 murine mapping population. Genet Mol Biol 29:166–173. CrossRefGoogle Scholar
  24. Li C, Zhou A, Sang T (2006b) Rice domestication by reducing shattering. Science 311:1936–1939. CrossRefGoogle Scholar
  25. Li S, Jia J, Wei X et al (2007) A intervarietal genetic map and QTL analysis for yield traits in wheat. Mol Breed 20:167–178. CrossRefGoogle Scholar
  26. Liu J, Yin T, Ye N, Chen Y, Yin T, Liu M, Hassani D (2013) Transcriptome analysis of the differentially expressed genes in the male and female shrub willows (Salix suchowensis). PloS One 8:e60181. CrossRefGoogle Scholar
  27. Luo L, Zhang Y, Xu S (2005) A quantitative genetics model for viability selection. Heredity 94:347–355. CrossRefGoogle Scholar
  28. Luo X, Xu N, Huang J, Gao F, Zou H, Boudsocq M, Coaker G, Liu J (2017) A lectin receptor-like kinase mediates pattern-triggered salicylic acid signaling. Plant Physiol 174:2501–2514. CrossRefGoogle Scholar
  29. Merlot S, Gosti F, Guerrier D, Vavasseur A, Giraudat J (2001) The ABI1 and ABI2 protein phosphatases 2C act in a negative feedback regulatory loop of the abscisic acid signalling pathway. Plant J 25:295–303. CrossRefGoogle Scholar
  30. Niderman T, Genetet I, Bruyère T, Gees R, Stintzi A, Legrand M, Fritig B, Mösinger E (1995) Pathogenesis-related PR-1 proteins are antifungal: isolation and characterization of three 14-kilodalton proteins of tomato and of a basic PR-1 of tobacco with inhibitory activity against Phytophthora infestans. Plant Physiol 108:17–27. CrossRefGoogle Scholar
  31. Oh IS, Park AR, Bae MS et al (2005) Secretome analysis reveals an Arabidopsis lipase involved in defense against Alternaria brassicicola. Plant Cell 17:2832–2847. CrossRefGoogle Scholar
  32. Orr HA, Turelli M (2001) The evolution of postzygotic isolation: accumulating Dobzhansky-Muller incompatibilities. Evolution 55:1085–1094. CrossRefGoogle Scholar
  33. Remington DL, Whetten RW, Liu BH, O’Malley DM (1999) Construction of an AFLP genetic map with nearly complete genome coverage in Pinus taeda. Theor Appl Genet 98:1279–1292. CrossRefGoogle Scholar
  34. Sano Y (1990) The genic nature of gamete eliminator in rice. Genetics 125:183–191Google Scholar
  35. Spiers AG (1988) Comparative studies of type and herbarium specimens of Marssonina species pathogenic to poplars. Eur J For Pathol 18:140–156. CrossRefGoogle Scholar
  36. Spiers AG (1998) Melampsora and Marssonina pathogens of poplars and willows in New Zealand. Eur J For Path 28:233–240. CrossRefGoogle Scholar
  37. Spiers AG, Hopcroft DH (1983) Ultrastructure of conidial and microconidial ontogeny of Marssonina species pathogenic to poplars. Can J Bot 61:3529–3532. CrossRefGoogle Scholar
  38. Springer NM (2010) Isolation of plant DNA for PCR and genotyping using organic extraction and CTAB. CSH Protoc. Google Scholar
  39. Stettler R, Bradshaw T, Heilman P, Hinckley T (1996) Biology of Populus and its implications for management and conservation. NRC Research Press, OttawaGoogle Scholar
  40. Tuskan GA, Gunter LE, Yang ZK, Yin T, Sewell MM, DiFazio SP (2004) Characterization of microsatellites revealed by genomic sequencing of Populus trichocarpa. Can J For Res 34:85–93. CrossRefGoogle Scholar
  41. Tuskan GA, DiFazio S, Jansson S et al (2006) The genome of black cottonwood, Populus trichocarpa (Torr.&Gray). Science 313:1596–1604. CrossRefGoogle Scholar
  42. Vales MI, Schön CC, Capettini F et al (2005) Effect of population size on the estimation of QTL: a test using resistance to barley stripe rust. Theor Appl Genet 111:1260–1270. CrossRefGoogle Scholar
  43. Van Ooijen JW (2004) MapQTL 5, software for the mapping of quantitative trait loci in experimental population. Kyazma BV, WageningenGoogle Scholar
  44. Vanden Broeck A, Villar M, Van Bockstaele E, Van Slycken J (2005) Natural hybridization between cultivated poplars and their wild relatives: evidence and consequences for native poplar populations. Ann For Sci 62:601–613. CrossRefGoogle Scholar
  45. Vogl C, Xu S (2000) Multipoint mapping of viability and segregation distorting loci using molecular markers. Genetics 155:1439–1447Google Scholar
  46. Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78. CrossRefGoogle Scholar
  47. Wan Z, Li Y, Liu M, Chen Y, Yin T (2015) Natural infectious behavior of the urediniospores of Melampsora larici-populina on poplar leaves. J For Res 26:225–231. CrossRefGoogle Scholar
  48. Wang X, Lu S (2012) Effect of marker density on QTL mapping in a backcross design. J Henan Inst Sci Technol 40:32–36. Google Scholar
  49. Wang Y, Bouwmeester K, Beseh P, Shan W, Govers F (2014) Phenotypic analyses of Arabidopsis T-DNA insertion lines and expression profiling reveal that multiple L-type lectin receptor kinases are involved in plant immunity. Mol Plant-Microbe Interact 27:1390–1402. CrossRefGoogle Scholar
  50. Wu H, Tian Y, Wan Q et al (2018) Genetics and evolution of MIXTA genes regulating cotton lint fiber development. New Phytol 217:883–895. CrossRefGoogle Scholar
  51. Yin T, DiFazio SP, Gunter LE, Riemenschneider D, Tuskan GA (2004) Large-scale heterospecific segregation distortion in Populus revealed by a dense genetic map. Theor Appl Genet 109:451–463. CrossRefGoogle Scholar
  52. Yin T, DiFazio SP, Gunter LE et al (2008) Genome structure and emerging evidence of an incipient sex chromosome in Populus. Genome Res 18:422–430. CrossRefGoogle Scholar
  53. Yuan K, Zhang B, Zhang Y, Cheng Q, Wang M, Huang M (2008) Identification of differentially expressed proteins in poplar leaves induced by Marssonina brunnea f. sp. Multigermtubi. J Genet Genom 35:49–60. CrossRefGoogle Scholar
  54. Zhou W, Tang Z, Hou J, Hu N, Yin T (2015) Genetic map construction and detection of genetic loci underlying segregation distortion in an intraspecific cross of Populus deltoides. PloS One 10:e0126077. CrossRefGoogle Scholar
  55. Zhu S, Cao Y, Jiang C et al (2012) Sequencing the genome of Marssonina brunnea reveals fungus-poplar co-evolution. BMC Genom 13:382. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Key Laboratory for Poplar Cultivar Innovation and Germplasm Improvement of Jiangsu Province, Southern Modern Forestry Collaborative Innovation Center, College of ForestryNanjing Forestry UniversityNanjingChina

Personalised recommendations