Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Elevated temperature increases in planta expression levels of virulence related genes in Magnaporthe oryzae and compromises resistance in Oryza sativa cv. Nipponbare

Geoffrey Onaga A D E , Kerstin D. Wydra B , Birger Koopmann A , Yakouba Séré C and Andreas von Tiedemann A
+ Author Affiliations
- Author Affiliations

A Division of Plant Pathology and Crop Protection, Department of Crop Sciences, Georg-August-University, Grisebachstr. 6, 37077, Göttingen, Germany.

B Erfurt University of Applied Sciences, Horticulture - Plant Production and Climate Change, Leipziger Str. 77, 90085 Erfurt, Germany.

C Africa Rice Centre, P.O Box 33581, Dar es Salaam, Tanzania.

D National Crops Resources Research Institute (NaCRRI), PO Box 7084, Kampala, Uganda.

E Corresponding author. Email: gonaga@gwdg.de

Functional Plant Biology 44(3) 358-371 https://doi.org/10.1071/FP16151
Submitted: 21 April 2016  Accepted: 24 October 2016   Published: 15 December 2016

Abstract

Temperature changes have the potential to alter the incidence and severity of plant disease epidemics and pressures, as well as to reshape the co-evolutionary relationships between plants and pathogens. However, the molecular basis of temperature modulation of pathogenicity of plant pathogens is still unclear. Here, we studied the effect of temperature on biomass of Magnaporthe oryzae in planta using qPCR. Additionally, the transcriptomes of M. oryzae and rice were analysed using RNA-seq. Rice seedlings were exposed to 35°C and 28°C for 7 days before pathogen inoculation. Inoculated plants were kept in the dark at 28°C for 24 h and later re-exposed to 35°C and 28°C for an additional 24 h before sample collection. Plants grown and predisposed to 35°C prior to inoculation exhibited accelerated tissue necrosis compared with plants grown and inoculated at 28°C. In accordance with the disease severity observed on infected leaves, in planta fungal biomass was significantly higher at 35°C than 28°C. Moreover, M. oryzae exhibited increased expression levels of putative fungal effector genes in plants exposed to 35°C compared with plants exposed to 28°C. Collectively, this study revealed that temperature elevation could favour M. oryzae infection by compromising plant resistance and accelerating plant tissue colonisation with the pathogen.

Additional keywords: pathosystems, predisposition, rice blast, rice resistance, transcriptome.


References

Baminger U, Nidetzky B, Kulbe KD, Haltrich D (1999) A simple assay for measuring cellobiose dehydrogenase activity in the presence of laccase. Journal of Microbiological Methods 35, 253–259.
A simple assay for measuring cellobiose dehydrogenase activity in the presence of laccase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXitFantL4%3D&md5=9eb81ed81ed2614badee795c3139aca2CAS |

Ben-Dor A, Shamir R, Yakhini Z (1999) Clustering gene expression patterns. Journal of Computational Biology 6, 281–297.
Clustering gene expression patterns.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXns1enur4%3D&md5=119dddfd0a678fbe82fde5360651cc91CAS |

Bendtsen JD, Nielsen H, von Heijne G, Brunak S (2004) Improved prediction of signal peptides: SignalP 3.0. Journal of Molecular Biology 340, 783–795.
Improved prediction of signal peptides: SignalP 3.0.Crossref | GoogleScholarGoogle Scholar |

Biely P (2012) Microbial carbohydrate esterases deacetylating plant polysaccharides. Biotechnology Advances 30, 1575–1588.
Microbial carbohydrate esterases deacetylating plant polysaccharides.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xnslejsrs%3D&md5=b84cfa4148031457831bc487b67624c7CAS |

Blümke A, Falter C, Herrfurth C, Sode B, Bode R, Schäfer W, Feussner I, Voigt C (2014) Secreted fungal effector lipase releases free fatty acids to inhibit innate immunity-related callose formation during wheat head infection. Plant Physiology 165, 346–358.
Secreted fungal effector lipase releases free fatty acids to inhibit innate immunity-related callose formation during wheat head infection.Crossref | GoogleScholarGoogle Scholar |

Crooks GE, Hon G, Chandonia JM, Brenner SE (2004) WebLogo: a sequence logo generator. Genome Research 14, 1188–1190.
WebLogo: a sequence logo generator.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXkvFGht7Y%3D&md5=5a7969989e00b3d2c6d175007b9db35fCAS |

Döppler H, Storz P (2007) A novel tyrosine phosphorylation site in protein kinase D contributes to oxidative stress-mediated activation. Journal of Biological Chemistry 282, 31873–31881.
A novel tyrosine phosphorylation site in protein kinase D contributes to oxidative stress-mediated activation.Crossref | GoogleScholarGoogle Scholar |

Dunasevsky YE, Matveeva AR, Beliakova GA, Domash VI, Belozersky MA (2007) Extracellular alkaline proteinase of Colletotrichum gloeosporioides. Biochemistry 72, 345–350.

Elad Y, Pertot I (2014) Climate change impacts on plant pathogens and diseases. Journal of Crop Improvement 28, 99–139.
Climate change impacts on plant pathogens and diseases.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXht1Cjsb4%3D&md5=6d48d83c13adffe7d50b741b74e24790CAS |

Evans N, Baierl A, Semenov AM, Gladders P, Fitt BDL (2008) Range and severity of plant diseases increased by global warming. Journal of the Royal Society, Interface 5, 525–531.
Range and severity of plant diseases increased by global warming.Crossref | GoogleScholarGoogle Scholar |

Fernandez J, Wilson RA (2014) Cells in cells: morphogenetic and metabolic strategies conditioning rice infection by the blast fungus Magnaporthe oryzae. PLoS One 9, e87300
Cells in cells: morphogenetic and metabolic strategies conditioning rice infection by the blast fungus Magnaporthe oryzae.Crossref | GoogleScholarGoogle Scholar |

Finn RD, Mistry J, Tate J, Coggill P, Heger A, Pollington JE, Gavin OL, Gunasekaran P, Ceric G, Forslund K, Holm L, Sonnhammer ELL, Eddy SR, Bateman A (2010) The Pfam protein families database. Nucleic Acids Research 38, D211–D222.
The Pfam protein families database.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXktlyhsA%3D%3D&md5=0ef8ade94d0b20b0fac64ca3423be4aeCAS |

Garrett KA, Dendy SP, Frank EE, Rouse MN, Travers SE (2006) Climate change effects on plant disease: genomes to ecosystems. Annual Review of Phytopathology 44, 489–509.
Climate change effects on plant disease: genomes to ecosystems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVylsLfM&md5=6a07561e22dcbad30b81f71871df3a4cCAS |

Gregory PJ, Johnson SN, Newton AC, Ingram JSI (2009) Integrating pests and pathogens into the climate change/food security debate. Journal of Experimental Botany 60, 2827–2838.
Integrating pests and pathogens into the climate change/food security debate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXosFWjtb4%3D&md5=4fad0b28b4bd59b07197ee63bd810cefCAS |

Gruber S, Seidl-Seiboth V (2012) Self versus non-self: fungal cell wall degradation in Trichoderma. Microbiology 158, 26–34.
Self versus non-self: fungal cell wall degradation in Trichoderma.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XitVKnu7Y%3D&md5=f8ec4d66a1bec766e473bbfb4e89337eCAS |

Harmon PF, Dunkle LD, Latin R (2003) A rapid PCR-based method for the detection of Magnaporthe oryzae from infected perennial ryegrass. Plant Disease 87, 1072–1076.
A rapid PCR-based method for the detection of Magnaporthe oryzae from infected perennial ryegrass.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXns12qsLg%3D&md5=85af4ffd9464645bd5a286cd10847d78CAS |

Hashioka Y (1950) Studies on the mechanism of prevalence of the rice blast disease in the tropics. Technical Bulletin No. 8. Taiwan Agricultural Research Institute.

Huang DW, Sherman BT, Lempicki RA (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nature Protocols 4, 44–57.
Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsFCkurnI&md5=1714e214d1090ff2cf7d52c4d6ee1306CAS |

Kall L, Krogh A, Sonnhammer EL (2007) Advantages of combined transmembrane topology and signal peptide prediction – the Phobius web server. Nucleic Acids Research 35, W429–W432.
Advantages of combined transmembrane topology and signal peptide prediction – the Phobius web server.Crossref | GoogleScholarGoogle Scholar |

Kato H, Kozaka T (1974) Effects of temperature on lesion enlargement and sporulation of Pyricularia oryzae in rice leaves. Phytopathology 64, 828–830.
Effects of temperature on lesion enlargement and sporulation of Pyricularia oryzae in rice leaves.Crossref | GoogleScholarGoogle Scholar |

Kawahara Y, Oono Y, Kanamori H, Matsumoto T, Itoh T, Minami E (2012) Simultaneous RNA-Seq analysis of a mixed transcriptome of rice and blast fungus interaction. PLoS One 7, e49423
Simultaneous RNA-Seq analysis of a mixed transcriptome of rice and blast fungus interaction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhslamu73E&md5=3750e516d8ad01931caf34af6496e8c1CAS |

Khaldi N, Seifuddin FT, Turner G, Haft D, Nierman WC, Wolfe KH, Fedorova ND (2010) SMURF: genomic mapping of fungal secondary metabolite clusters. Fungal Genetics and Biology 47, 736–741.
SMURF: genomic mapping of fungal secondary metabolite clusters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXps1Wrtr0%3D&md5=41a904203cf45e3c4be34f7d882fc29eCAS |

Khan R, Tan R, Mariscal AG, Straney D (2003) A binuclear zinc transcription factor binds the host isoflavonoid-responsive element in a fungal cytochrome p450 gene responsible for detoxification. Molecular Microbiology 49, 117–130.
A binuclear zinc transcription factor binds the host isoflavonoid-responsive element in a fungal cytochrome p450 gene responsible for detoxification.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlsVersbs%3D&md5=00dbc2276e85eee8538606ed32128f92CAS |

Köller W, Parker DM, Becker CM (1991) Role of cutinase in the penetration of apple leaves by Venturia inaequalis. Phytopathology 81, 1375–1379.
Role of cutinase in the penetration of apple leaves by Venturia inaequalis.Crossref | GoogleScholarGoogle Scholar |

Krogh A, Larsson B, von Heijne G, Sonnhammer EL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. Journal of Molecular Biology 305, 567–580.
Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXisFCguw%3D%3D&md5=21c506ebc21af5fb36f907866f9a7f38CAS |

Luo Y, Teng PS, Fabellar NG, TeBeest DO (1998) The effects of global temperature change on rice leaf blast epidemics: a simulation study in three agroecological zones. Agriculture, Ecosystems & Environment 68, 187–196.
The effects of global temperature change on rice leaf blast epidemics: a simulation study in three agroecological zones.Crossref | GoogleScholarGoogle Scholar |

MacIntosh GC (2011) RNase T2 Family: enzymatic properties, functional diversity, and evolution of ancient ribonucleases In ‘Ribonucleases 26: (Nucleic acids and molecular biology)’. (Ed. AW Nicholson) pp. 89–114. (Springer: New York)

Mauxion F, Le Borgne R, Munier-Lehmann H, Hoflack B (1996) A casein kinase II phosphorylation site in the cytoplasmic domain of the cation-dependent mannose 6-phosphate receptor determines the high affinity interaction of the AP-1 Golgi assembly proteins with membranes. Journal of Biological Chemistry 271, 2171–2178.
A casein kinase II phosphorylation site in the cytoplasmic domain of the cation-dependent mannose 6-phosphate receptor determines the high affinity interaction of the AP-1 Golgi assembly proteins with membranes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XnsF2qtw%3D%3D&md5=f9f2e933e83d7d2428f9f9fae24fa87dCAS |

Mboup M, Bahri B, Leconte M, De Vallavieille-Pope C, Kaltz O, Enjalbert J (2012) Genetic structure and local adaptation of European wheat yellow rust populations: the role of temperature-specific adaptation. Evolutionary Applications 5, 341–352.
Genetic structure and local adaptation of European wheat yellow rust populations: the role of temperature-specific adaptation.Crossref | GoogleScholarGoogle Scholar |

Morelle W, Bernard M, Debeaupuis JP, Buitrago M, Tabouret M, Latgé J (2005) Galactomannoproteins of Aspergillus fumigatus. Eukaryotic Cell 4, 1308–1316.
Galactomannoproteins of Aspergillus fumigatus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmvVertr0%3D&md5=b5561e1f13419f949e3392e7b9a9c4b6CAS |

Morisseau C, Hammock BD (2013) Impact of soluble epoxide hydrolase and epoxyeicosanoids on human health. Annual Reviews in Pharmacology and Toxicology 53, 37–58.
Impact of soluble epoxide hydrolase and epoxyeicosanoids on human health.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjt1WgtLk%3D&md5=5f2d2f5c549ddbf851593e3ca5a8d998CAS |

Oh Y, Donofrio N, Pan H, Coughlan S, Brown D, Meng S, Mitchell T, Dean R (2008) Transcriptome analysis reveals new insight into appressorium formation and function in the rice blast fungus Magnaporthe oryzae. Genome Biology 9, R85
Transcriptome analysis reveals new insight into appressorium formation and function in the rice blast fungus Magnaporthe oryzae.Crossref | GoogleScholarGoogle Scholar |

Ohtaki S, Maeda H, Takahashi T, Yamagata Y, Hasegawa F, Gomi K, Nakajima T, Abe K (2006) Novel hydrophobic surface binding protein, HsbA, produced by Aspergillus oryzae. Applied and Environmental Microbiology 72, 2407–2413.
Novel hydrophobic surface binding protein, HsbA, produced by Aspergillus oryzae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XktFagtL0%3D&md5=a67f61ffab2fb583ef230049ac003852CAS |

Onaga G, Wydra K, Koopmann B, Séré Y, von Tiedemann A (2015) Population structure, pathogenicity, and mating type distribution of Magnaporthe oryzae isolates from East Africa. Phytopathology 105, 1137–1145.
Population structure, pathogenicity, and mating type distribution of Magnaporthe oryzae isolates from East Africa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XkvVOisrw%3D&md5=32b3896af787080c48cebfab7c94d24aCAS |

Ou SH (1985) ‘Rice diseases’. (2nd edn) (Commonwealth Mycological Institute: Kew, UK)

Park S-Y, Choi J, Lim S-E, Lee G-W, Park J, Kim Y, Kong S, Kim SR, Rho H-S, Jeon J, Chi M-H, Kim S, Khang CH, Kang S, Lee Y-H (2013) Global expression profiling of transcription factor genes provides new insights into pathogenicity and stress responses in the rice blast fungus. PLoS Pathogens 9, e1003350
Global expression profiling of transcription factor genes provides new insights into pathogenicity and stress responses in the rice blast fungus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtFCntrfE&md5=dd98ffcfeba39e0fbd08735f661c52eaCAS |

Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT PCR. Nucleic Acids Research 29, e45
A new mathematical model for relative quantification in real-time RT PCR.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38nis12jtw%3D%3D&md5=79c488a0ef278e2273a84ed788c02263CAS |

Rauyaree P, Choi W, Fang E, Blackmon B, Dean RA (2001) Genes expressed during early stages of rice infection with the rice blast fungus Magnaporthe grisea. Molecular Plant Pathology 2, 347–354.
Genes expressed during early stages of rice infection with the rice blast fungus Magnaporthe grisea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjvFGntr8%3D&md5=01317e3661cd15787f47774c635ee721CAS |

Rawlings ND, Barrett AJ, Bateman A (2010) MEROPS: the peptidase database. Nucleic Acids Research 38, D227–D233.
MEROPS: the peptidase database.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXktlyltQ%3D%3D&md5=42b82b755b651bb261b76b82c6b12fc8CAS |

Schacht T, Unger C, Pich A, Wydra K (2011) Endo- and exopolygalacturonases of Ralstonia solanacearum are inhibited by polygalacturonase-inhibiting protein (PGIP) activity in tomato stem extracts. Plant Physiology and Biochemistry 49, 377–387.
Endo- and exopolygalacturonases of Ralstonia solanacearum are inhibited by polygalacturonase-inhibiting protein (PGIP) activity in tomato stem extracts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjvV2rsr4%3D&md5=481337ca204dcd29310c0f593e87dbf1CAS |

Sharma RC, Duveiller E, Ortiz-Ferrara G (2007) Progress and challenge towards reducing wheat spot blotch threat in the Eastern Gangetic plains of South Asia: is climate change already taking its toll? Field Crops Research 103, 109–118.
Progress and challenge towards reducing wheat spot blotch threat in the Eastern Gangetic plains of South Asia: is climate change already taking its toll? Crossref | GoogleScholarGoogle Scholar |

Sidoux-Walter F, Pettersson N, Hohmann S (2004) The Saccharomyces cerevisiae aquaporin Aqy1 is involved in sporulation. Proceedings of the National Academy of Sciences of the United States of America 101, 17422–17427.
The Saccharomyces cerevisiae aquaporin Aqy1 is involved in sporulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhslKquw%3D%3D&md5=74c687486829e130b2b9671e08d03148CAS |

Sigal YJ, McDermott MI, Morris AJ (2005) Integral membrane lipid phosphatases/phosphotransferases: common structure and diverse functions. The Biochemical Journal 387, 281–293.
Integral membrane lipid phosphatases/phosphotransferases: common structure and diverse functions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXivFWls74%3D&md5=94ba9f5aefd64449dc29311082c818d1CAS |

Teng PS (1994) The epidemiological basis for blast management. In ‘Rice blast disease’. (Eds RS Zeigler, SA Leong, PS Teng) pp. 409–433. (CABI: Wallingford, UK)

Xue MF, Yang J, Li ZG, Hu SNA, Yao N, Dean RA, Zhao WS, Shen M, Zhang HW, Li C, et al (2012) Comparative analysis of the genomes of two field isolates of the rice blast fungus Magnaporthe oryzae. PLOS Genetics 8, e1002869
Comparative analysis of the genomes of two field isolates of the rice blast fungus Magnaporthe oryzae.Crossref | GoogleScholarGoogle Scholar |

Thon MR, Martin SL, Goff S, Wing RA, Dean RA (2004) BAC end sequences and a physical map reveal transposable element content and clustering patterns in the genome of Magnaporthe grisea. Fungal Genetics and Biology 41, 657–666.
BAC end sequences and a physical map reveal transposable element content and clustering patterns in the genome of Magnaporthe grisea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlsl2iu7c%3D&md5=bd7c01ffb22672b79b38dba4303cf72bCAS |

Wang Y, Bao Z, Zhu Y, Hua J (2009) Analysis of temperature modulation of plant defense against biotrophic microbes. Molecular Plant-Microbe Interactions 22, 498–506.
Analysis of temperature modulation of plant defense against biotrophic microbes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXks1WnsrY%3D&md5=4e92e1a01d8e038096da1609840db1f6CAS |

Wilson RA, Talbot NJ (2009) Under pressure: investigating the biology of plant infection by Magnaporthe oryzae. Nature Reviews. Microbiology 7, 185–195.
Under pressure: investigating the biology of plant infection by Magnaporthe oryzae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhvFKisL8%3D&md5=753645ec7a8d959fe13877b892708157CAS |

Wydra K, Beri H (2006) Structural changes of homogalacturonan, rhamnogalacturonan I and arabinogalactan protein in xylem cell walls of tomato genotypes in reaction to Ralstonia solanacearum. Physiological and Molecular Plant Pathology 68, 41–50.
Structural changes of homogalacturonan, rhamnogalacturonan I and arabinogalactan protein in xylem cell walls of tomato genotypes in reaction to Ralstonia solanacearum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFersrfM&md5=ad9a24f5a1815848a88f1a1507ebd8f9CAS |

Zhang S, Xu J-R (2014) Effectors and effector delivery in Magnaporthe oryzae. PLoS Pathogens 10, e1003826
Effectors and effector delivery in Magnaporthe oryzae.Crossref | GoogleScholarGoogle Scholar |

Zvereva EL, Kozlov MV (2006) Consequences of simultaneous elevation of carbon dioxide and temperature for plant-herbivore interactions: a metaanalysis. Global Change Biology 12, 27–41.
Consequences of simultaneous elevation of carbon dioxide and temperature for plant-herbivore interactions: a metaanalysis.Crossref | GoogleScholarGoogle Scholar |