Advertisement

Journal of Applied Genetics

, Volume 59, Issue 4, pp 391–403 | Cite as

Identification and expression of genes in response to cassava bacterial blight infection

  • Piengtawan Tappiban
  • Supajit Sraphet
  • Nattaya Srisawad
  • Duncan R Smith
  • Kanokporn Triwitayakorn
Plant Genetics • Original Paper
  • 113 Downloads

Abstract

Cassava bacterial blight (CBB) caused by Xanthomonas axonopodis pv. manihotis (or XAM) is a serious disease of cassava (Manihot esculenta Crantz). In this study, quantitative trait loci (QTL) associated with CBB infection were identified in the F1 progenies of a cross between the “Huay Bong 60” and “Hanatee” cassava cultivars. The phenotype of disease severity was observed at 7, 10, and 12 days after inoculation (DAI). A total of 12 QTL were identified, of which 5, 6, and 1 were detected in 7, 10, and 12 DAI samples, respectively. Among all identified QTL, CBB14_10dai_1, CBB14_10dai_2, and CBB14_12dai showed the most significant (P < 0.0001) associations with CBB infection, and explained 21.3, 13.8, and 26.5% of phenotypic variation, respectively. Genes underlying the QTL were identified and their expression was investigated in resistant and susceptible cassava plants by real-time quantitative RT-PCR. The results identified candidate genes that showed significant differences in expression between resistant and susceptible lines, including brassinosteroid insensitive 1-associated receptor kinase 1-related (Manes.04G059100), cyclic nucleotide-gated ion channel 2 (Manes.02G051100), and autophagy-related protein 8a-related (Manes.17G026600) at 7 DAI, and regulator of nonsense transcripts 1 homolog (Manes.17G021900) at both 7 and 12 DAI. The expression pattern of all genes showed higher levels in resistant (B82, B32, B20, and B70) as compared to susceptible (HB60, B100, B95, and B47) plants. Overall, this study has identified QTL and markers linked to CBB infection trait, and identified candidate genes involved in CBB resistance. This information will be of use for better understanding defense mechanisms in cassava to bacterial blight disease.

Keywords

Cassava Cassava bacterial blight Xanthomonas axonopodis pv. manihotis QTL SSR markers Quantitative real-time PCR 

Notes

Acknowledgements

We thank Mr. Rungsi Charaensataporn, Department of Agriculture, for providing the XAM stock and Miss Saowaree Tangkasakul, Field Crops Experiment Station Ladbuakao, Sikhio, Nakhon Ratchasima, Thailand for providing plant materials.

Authors’ contributions

PT, SS, NS, and KT conceived, designed, and performed the experiments. PT, SS, NS, and KT analyzed the data. PT, DRS, and KT wrote the manuscript.

Funding information

This research is partially supported by the Center of Excellence on Agricultural Biotechnology (AG-BIO/PERDO-CHE), Thailand (AG-BIO/60-005-003), and Mahidol University. . PT was supported for Ph.D. study by the AG-BIO/PERDO-CHE.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Human and animal rights and informed consent

This article does not contain any studies with human participants or animals performed by any of the authors.

Supplementary material

13353_2018_457_MOESM1_ESM.docx (29 kb)
ESM 1 (DOCX 20 kb)
13353_2018_457_MOESM2_ESM.docx (13 kb)
ESM 2 (DOCX 13 kb)
13353_2018_457_MOESM3_ESM.docx (15 kb)
ESM 3 (DOCX 15 kb)

References

  1. Bansal V, Kharbanda P, Stringam G, Thiagarajah M, Tewari J (1994) A comparison of greenhouse and field screening methods for blackleg resistance in doubled haploid lines of Brassica napus. Plant Dis 78:276–281CrossRefGoogle Scholar
  2. Belhassen BB, Abbassian A, Alesiani A et al. (2016) Food outlook. Biannual Report on Global Food Markets Food and Agriculture Organization of the United Nations (FAO), RomeGoogle Scholar
  3. Bio-Rad (2006) Real-time PCR applications guide. Bio-Rad Laboratories, Inc.Google Scholar
  4. Boher B, Nicole M, Potin M, Geiger JP (1997) Extracellular polysaccharides from Xanthomonas axonopodis pv. manihotis interact with cassava cell walls during pathogenesis. Mol Plant-Microbe Interact 10:803–811.  https://doi.org/10.1094/MPMI.1997.10.7.803 CrossRefPubMedGoogle Scholar
  5. Boonchanawiwat A, Sraphet S, Boonseng O, Lightfoot DA, Triwitayakorn K (2011) QTL underlying plant and first branch height in cassava (Manihot esculenta Crantz). Field Crops Res 121:343–349.  https://doi.org/10.1016/j.fcr.2010.12.022 CrossRefGoogle Scholar
  6. Büttner D, Bonas U (2010) Regulation and secretion of Xanthomonas virulence factors. FEMS Microbiol Rev 34:107–133.  https://doi.org/10.1111/j.1574-6976.2009.00192.x CrossRefPubMedGoogle Scholar
  7. Chin K, DeFalco TA, Moeder W, Yoshioka K (2013) The Arabidopsis cyclic nucleotide-gated ion channels AtCNGC2 and AtCNGC4 work in the same signaling pathway to regulate pathogen defense and floral transition. Plant Physiol 163:611–624.  https://doi.org/10.1104/pp.113.225680 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Chin K, Moeder W, Yoshioka K (2009) Biological roles of cyclic-nucleotide-gated ion channels in plants: what we know and don’t know about this 20 member ion channel family. Botany 87:668–677.  https://doi.org/10.1139/B08-147 CrossRefGoogle Scholar
  9. Cohn M, Bart RS, Shybut M et al. (2014) Xanthomonas axonopodis virulence is promoted by a transcription activator-like effector-mediated induction of a SWEET sugar transporter in cassava. Mol Plant-Microbe Interact 27:1186–1198.  https://doi.org/10.1094/MPMI-06-14-0161-R CrossRefPubMedGoogle Scholar
  10. Collard BCY, Mackill DJ (2008) Marker-assisted selection: an approach for precision plant breeding in the twenty-first century. Philos Trans R Soc Lond Ser B Biol Sci 363:557–572.  https://doi.org/10.1098/rstb.2007.2170 CrossRefGoogle Scholar
  11. Delannoy E et al. (2005) Resistance of cotton towards Xanthomonas campestris pv. malvacearum. Annu Rev Phytopathol 43:63–82. doi: https://doi.org/10.1146/annurev.phyto.43.040204.140251 CrossRefPubMedGoogle Scholar
  12. Deretic V, Saitoh T, Akira S (2013) Autophagy in infection, inflammation, and immunity. Nat Rev Immunol 13:722–737.  https://doi.org/10.1038/nri3532 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Diola V, Fritsche-Neto R (2014) Biotechnology and Plant Breeding. Genes Prospection. Academic Press, San DiegoCrossRefGoogle Scholar
  14. Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15Google Scholar
  15. Du H, Wang Y, Yang J, Yang W (2015) Comparative transcriptome analysis of resistant and susceptible tomato lines in response to infection by Xanthomonas perforans race T3. Front Plant Sci 6:1173PubMedPubMedCentralGoogle Scholar
  16. El-Sharkawy MA (1993) Drought-tolerant cassava for Africa, Asia, and Latin America: breeding projects work to stabilize productivity without increasing pressures on limited natural resources. BioScience 43:441–451.  https://doi.org/10.2307/1311903 CrossRefGoogle Scholar
  17. Fanou AA, Zinsou VA, Wydra K (2018) Cassava bacterial blight: a devastating disease of cassava. In: Waisundara V (ed) Cassava. InTech, Rijeka, p Ch. 02.  https://doi.org/10.5772/intechopen.71527 Google Scholar
  18. Ferreira A, Silva MF, Silva LC et al. (2006) Estimating the effects of population size and type on the accuracy of genetic maps. Genetics and Molecular Biology 29(1):187–192CrossRefGoogle Scholar
  19. Fregene M, Angel F, Gomez R et al. (1997) A molecular genetic map of cassava (Manihot esculenta Crantz). Theore Appl Genet 95:431–441.  https://doi.org/10.1007/s001220050580 CrossRefGoogle Scholar
  20. Friedrichsen DM, Joazeiro CAP, Li J, Hunter T, Chory J (2000) Brassinosteroid-insensitive-1 is a ubiquitously expressed Leucine-rich repeat receptor serine/threonine kinase. Plant Physiol 123:1247–1256CrossRefPubMedPubMedCentralGoogle Scholar
  21. Goodstein DM, Shu S, Howson R et al. (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 40:D1178-D1186. doi: https://doi.org/10.1093/nar/gkr944 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Hammond-Kosack KE, Jones JD (1996) Resistance gene-dependent plant defense responses. Plant Cell 8:1773CrossRefPubMedPubMedCentralGoogle Scholar
  23. Jeong H-J, Kim YJ, Kim SH, Kim Y-H, Lee I-J, Kim YK, Shin JS (2011) Nonsense-mediated mRNA decay factors, UPF1 and UPF3, contribute to plant defense. Plant Cell Physiol 52:2147–2156.  https://doi.org/10.1093/pcp/pcr144 CrossRefPubMedGoogle Scholar
  24. Jorge V, Fregene M, Vélez CM, Duque MC, Tohme J, Verdier V (2001) QTL analysis of field resistance to Xanthomonas axonopodis pv. manihotis in cassava. Theor Appl Genet 102:564–571.  https://doi.org/10.1007/s001220051683 CrossRefGoogle Scholar
  25. Jorge V, Fregene MA, Duque MC, Bonierbale MW, Tohme J, Verdier V (2000) Genetic mapping of resistance to bacterial blight disease in cassava (Manihot esculenta Crantz). Theor Appl Genet 101:865–872.  https://doi.org/10.1007/s001220051554 CrossRefGoogle Scholar
  26. Jorge V, Verdier V (2002) Qualitative and quantitative evaluation of cassava bacterial blight resistance in F1 progeny of a cross between elite cassava clones. Euphytica 123:41–48.  https://doi.org/10.1023/A:1014400823817 CrossRefGoogle Scholar
  27. Kemp BP, Beeching JR, Cooper RM (2005) cDNA-AFLP reveals genes differentially expressed during the hypersensitive response of cassava. Mol Plant Pathol 6:113–123.  https://doi.org/10.1111/j.1364-3703.2005.00268.x CrossRefPubMedGoogle Scholar
  28. Kim SH, Kwon C, Lee JH, Chung T (2012) Genes for plant autophagy: functions and interactions. Mol Cells 34:413–423.  https://doi.org/10.1007/s10059-012-0098-y CrossRefPubMedPubMedCentralGoogle Scholar
  29. Kir G et al. (2015) RNA interference knockdown of BRASSINOSTEROID INSENSITIVE1 in maize reveals novel functions for Brassinosteroid signaling in controlling plant architecture. Plant Physiol 169:826–839.  https://doi.org/10.1104/pp.15.00367 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Krzewska M et al. (2012) Quantitative trait loci associated with androgenic responsiveness in triticale (×Triticosecale Wittm.) anther culture. Plant Cell Rep 31:2099–2108. doi: https://doi.org/10.1007/s00299-012-1320-2 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Kunkeaw S, Tangphatsornruang S, Smith DR, Triwitayakorn K (2010) Genetic linkage map of cassava (Manihot esculenta Crantz) based on AFLP and SSR markers. Plant Breed 129:112–115.  https://doi.org/10.1111/j.1439-0523.2009.01623.x CrossRefGoogle Scholar
  32. Lagrimini LM, Vaughn J, Erb WA, Miller SA (1993) Peroxidase overproduction in tomato: wound-induced polyphenol deposition and disease resistance. Hortscience 28:218–221Google Scholar
  33. Lecourieux D, Ranjeva R, Pugin A (2006) Calcium in plant defence-signalling pathways. New Phytol 171:249–269.  https://doi.org/10.1111/j.1469-8137.2006.01777.x CrossRefPubMedGoogle Scholar
  34. Lehmann E (1975) Nonparametrics: statistical methods based on ranks. McGrew-Hill, San FranciscoGoogle Scholar
  35. Liu P, Wang L, Wong S-M, Yue GH (2016) Fine mapping QTL for resistance to VNN disease using a high-density linkage map in Asian seabass. Sci Rep 6:32122.  https://doi.org/10.1038/srep32122 https://www.nature.com/articles/srep32122#supplementary-information
  36. Liu X-H et al. (2017) Autophagy-related protein MoAtg14 is involved in differentiation, development and pathogenicity in the rice blast fungus Magnaporthe oryzae. Sci Rep 7:1415–1425.  https://doi.org/10.1038/srep40018 https://www.nature.com/articles/srep40018#supplementary-information
  37. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408.  https://doi.org/10.1006/meth.2001.1262 CrossRefGoogle Scholar
  38. Lopez C, Soto M, Restrepo S et al. (2005) Gene expression profile in response to Xanthomonas axonopodis pv. manihotis infection in cassava using a cDNA microarray. Plant Mol Biol 57:393–410.  https://doi.org/10.1007/s11103-004-7819-3
  39. López CE, Bernal AJ (2012) Cassava bacterial blight: using genomics for the elucidation and management of an old problem. Trop Plant Biol 5:117–126.  https://doi.org/10.1007/s12042-011-9092-3 CrossRefGoogle Scholar
  40. López CE, Quesada-Ocampo LM, Bohórquez A, Duque MC, Vargas J, Tohme J, Verdier V (2007) Mapping EST-derived SSRs and ESTs involved in resistance to bacterial blight in Manihot esculenta. Genome 50:1078–1088.  https://doi.org/10.1139/G07-087 CrossRefPubMedGoogle Scholar
  41. Lozano JC (1975) Bacterial blight of cassava. PANS 21:38–43.  https://doi.org/10.1080/09670877509411485 CrossRefGoogle Scholar
  42. Lozano JC (1986) Cassava bacterial blight: a manageable disease. Plant Dis 70:1089–1093CrossRefGoogle Scholar
  43. Lozano JC, Laberry R (1982) Screening for resistance to cassava bacterial blight. Plant Dis 66:316–318CrossRefGoogle Scholar
  44. Maqbool A et al. (2016) Structural basis of host Autophagy-related protein 8 (ATG8) binding by the Irish potato famine pathogen effector protein PexRD54. J Biol Chem 291:20270–20282CrossRefPubMedGoogle Scholar
  45. Moeder W, Urquhart W, Ung H, Yoshioka K (2011) The role of cyclic nucleotide-gated ion channels in plant immunity. Mol Plant 4:442–452.  https://doi.org/10.1093/mp/ssr018 CrossRefPubMedGoogle Scholar
  46. Muengula-Manyi M, Nkongolo KK, Bragard C, Tshilenge-Djim P, Winter S, Kalonji-Mbuyi A (2012) Incidence, severity and gravity of cassava mosaic disease in savannah agro-ecological region of DR-Congo: analysis of agro-environmental factors. Am J Plant Sci 03:512–519.  https://doi.org/10.4236/ajps.2012.34061 CrossRefGoogle Scholar
  47. Nakatogawa H, Ichimura Y, Ohsumi Y (2007) Atg8, a ubiquitin-like protein required for autophagosome formation, mediates membrane tethering and Hemifusion. Cell 130:165–178.  https://doi.org/10.1016/j.cell.2007.05.021 CrossRefPubMedGoogle Scholar
  48. Nicaise V, Roux M, Zipfel C (2009) Recent advances in PAMP-triggered immunity against bacteria: pattern recognition receptors watch over and raise the alarm. Plant Physiol 150:1638–1647.  https://doi.org/10.1104/pp.109.139709 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Ooijen JW, Voorrips RE (2001) JoinMap 3.0 Software for the calculation of genetic linkage maps. Plant Research International, Wageningen, the NetherlandsGoogle Scholar
  50. Pereira LF, Goodwin PH, Erickson L (2003) Cloning of a peroxidase gene from cassava with potential as a molecular marker for resistance to bacterial blight. Braz Arch BiolTechnol 46:149–154CrossRefGoogle Scholar
  51. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Res 29:e45–e45CrossRefPubMedPubMedCentralGoogle Scholar
  52. Prince DC, Drurey C, Zipfel C, Hogenhout SA (2014) The leucine-rich repeat receptor-like kinase brassinosteroid insensitive1-associated kinase1 and the cytochrome p450 phytoalexin deficient3 contribute to innate immunity to aphids in arabidopsis. Plant Physiol 164:2207–2219.  https://doi.org/10.1104/pp.114.235598 CrossRefPubMedPubMedCentralGoogle Scholar
  53. Rayson S et al. (2012) A role for nonsense-mediated mRNA decay in plants: pathogen responses are induced in Arabidopsis thaliana NMD mutants. PLoS One 7:e31917. doi: https://doi.org/10.1371/journal.pone.0031917 CrossRefPubMedPubMedCentralGoogle Scholar
  54. Sánchez T, Salcedo E, Ceballos H et al. (2009) Screening of starch quality traits in cassava (Manihot esculenta Crantz). Starch-Starke 61:12–19. doi: https://doi.org/10.1002/star.200800058 CrossRefGoogle Scholar
  55. Semagn K, Bjørnstad Å, Skinnes H, Marøy AG, Tarkegne Y, William M (2006) Distribution of DArT, AFLP, and SSR markers in a genetic linkage map of a doubled-haploid hexaploid wheat population. Genome 49:545–555.  https://doi.org/10.1139/g06-002 CrossRefPubMedGoogle Scholar
  56. Soto-Suárez M, Bernal D, González C, Szurek B, Guyot R, Tohme J, Verdier V (2010) In planta gene expression analysis of Xanthomonas oryzae pathovar oryzae, African strain MAI1. BMC Microbiol 10:170.  https://doi.org/10.1186/1471-2180-10-170 CrossRefPubMedPubMedCentralGoogle Scholar
  57. Soto Sedano C, Mora Moreno RE, Calle F, López Carrascal CE (2017) QTL identification for cassava bacterial blight resistance under natural infection conditions. Acta biol Colomb 22:19.  https://doi.org/10.15446/abc.v22n1.57951 CrossRefGoogle Scholar
  58. SPSS Inc (2010) IBM SPSS Statistics 19.0 core system user’s guide. New YorkGoogle Scholar
  59. Sraphet S, Boonchanawiwat A, Thanyasiriwat T et al. (2011) SSR and EST-SSR-based genetic linkage map of cassava (Manihot esculenta Crantz). Theor Appl Genet 122:1161–1170.  https://doi.org/10.1007/s00122-010-1520-5 CrossRefPubMedGoogle Scholar
  60. Sukhuman W, Supajit S, Ratchadaporn T, Opas B, Duncan RS, Kanokporn T (2015) Validation of a reference gene for transcript analysis in cassava (Manihot esculenta Crantz) and its application in analysis of linamarase and -hydroxynitrile lyase expression at different growth stages. Afr J Biotechnol 14:745–751.  https://doi.org/10.5897/ajb2014.14316 CrossRefGoogle Scholar
  61. Thro AM, Taylor N, Raemakers K et al. (1998) Maintaining the cassava biotechnology network. Nat Biotech 16:428–430CrossRefGoogle Scholar
  62. Van Ooijen JW, Boer MP, Jansen RC, Maliepaard C (2002) MapQTL 4.0. Software for the calculation of QTL positions on genetic maps. Plant Research International, Wageningen, the Netherlands,Google Scholar
  63. Verdier V, Restrepo S, Mosquera G, Jorge V, Lopez C (2004) Recent progress in the characterization of molecular determinants in the Xanthomonas axonopodis pv. manihotis–cassava interaction. Plant Mol Biol 56:573–584.  https://doi.org/10.1007/s11103-004-5044-8 CrossRefPubMedGoogle Scholar
  64. Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78CrossRefPubMedGoogle Scholar
  65. Wang Y, Nishimura MT, Zhao T, Tang D (2011) ATG2, an autophagy-related protein, negatively affects powdery mildew resistance and mildew-induced cell death in Arabidopsis. Plant J 68:74–87.  https://doi.org/10.1111/j.1365-313X.2011.04669.x CrossRefPubMedGoogle Scholar
  66. War AR, Paulraj MG, War MY, Ignacimuthu S (2011) Role of salicylic acid in induction of plant defense system in chickpea (Cicer arietinum L.). Plant Signal Behav 6:1787–1792.  https://doi.org/10.4161/psb.6.11.17685 CrossRefPubMedPubMedCentralGoogle Scholar
  67. Whankaew S, Poopear S, Kanjanawattanawong S, Tangphatsornruang S, Boonseng O, Lightfoot DA, Triwitayakorn K (2011) A genome scan for quantitative trait loci affecting cyanogenic potential of cassava root in an outbred population. BMC Genomics 12:266.  https://doi.org/10.1186/1471-2164-12-266 CrossRefPubMedPubMedCentralGoogle Scholar
  68. Wydra K, Verdier V (2002) Occurrence of cassava diseases in relation to environmental, agronomic and plant characteristics. Agricult Ecosys Environ 93:211–226.  https://doi.org/10.1016/S0167-8809(01)00349-8 CrossRefGoogle Scholar
  69. Wydra K, Zinsou V, Jorge V, Verdier V (2004) Identification of pathotypes of Xanthomonas axonopodis pv. manihotis in Africa and detection of quantitative trait loci and markers for resistance to bacterial blight of cassava. Phytopathology 94:1084–1093.  https://doi.org/10.1094/PHYTO.2004.94.10.1084 CrossRefPubMedGoogle Scholar
  70. Yoshimoto K (2012) Beginning to understand autophagy, an intracellular self-degradation system in plants. Plant Cell Physiol 53:1355–1365.  https://doi.org/10.1093/pcp/pcs099 CrossRefPubMedGoogle Scholar
  71. Yoshimoto K et al. (2009) Autophagy negatively regulates cell death by controlling NPR1-dependent salicylic acid signaling during senescence and the innate immune response in Arabidopsis. Plant Cell 21:2914–2927CrossRefGoogle Scholar
  72. Zhang J, Liu T, Feng R et al. (2015) Genetic Map Construction and Quantitative Trait Locus (QTL) Detection of Six Economic Traits Using an F2 Population of the Hybrid from Saccharina longissima and Saccharina japonica. PLoS ONE 10(5):e0128588Google Scholar

Copyright information

© Institute of Plant Genetics, Polish Academy of Sciences, Poznan 2018

Authors and Affiliations

  • Piengtawan Tappiban
    • 1
    • 2
  • Supajit Sraphet
    • 1
  • Nattaya Srisawad
    • 1
  • Duncan R Smith
    • 1
  • Kanokporn Triwitayakorn
    • 1
    • 2
  1. 1.Institute of Molecular BiosciencesMahidol UniversityNakhorn PathomThailand
  2. 2.Center of Excellence on Agricultural Biotechnology: (AG-BIO/PERDO-CHE)BangkokThailand

Personalised recommendations