Plant Cell Reports

, Volume 36, Issue 11, pp 1731–1746 | Cite as

The cyclic lipopeptide orfamide induces systemic resistance in rice to Cochliobolus miyabeanus but not to Magnaporthe oryzae

Original Article

Abstract

Key message

The Pseudomonas- derived cyclic lipopeptide orfamide can induce resistance to Cochliobolus miyabeanus but not to Magnaporthe oryzae in rice. Abscisic acid signaling is involved in the induced systemic resistance response triggered by orfamide.

Abstract

Diverse natural products produced by beneficial Pseudomonas species have the potential to trigger induced systemic resistance (ISR) in plants, and thus may contribute to control of diseases in crops. Some beneficial Pseudomonas spp. can produce cyclic lipopeptides (CLPs), amphiphilic molecules composed of a fatty acid tail linked to an oligopeptide which is cyclized. CLPs can have versatile biological functions, but the capacity of Pseudomonas-derived CLPs in triggering ISR responses has barely been studied. Pseudomonas protegens and related species can produce orfamide-type CLPs. Here we show that in rice, orfamides can act as ISR elicitors against the necrotrophic fungus Cochliobolus miyabeanus, the causal agent of brown spot disease, but are not active against the blast fungus Magnaporthe oryzae. Orfamide A can trigger early defensive events and activate transcripts of defense-related genes in rice cell suspension cultures, but does not cause cell death. Further testing in rice cell suspension cultures and rice plants showed that abscisic acid signaling, the transcriptional activator OsWRKY4 and pathogenesis-related protein PR1b are triggered by orfamide A and may play a role in the ISR response against C. miyabeanus.

Keywords

Pseudomonas protegens CHA0 Orfamide Induced systemic resistance Cochliobolus miyabeanus Plant hormones Pathogenesis-related proteins 

Notes

Acknowledgements

ZM sincerely acknowledges PhD scholarships from China Scholarship Council (CSC, No.201204910376) and a special research fund (Bijzonder Onderzoeksfonds, BOF) from Ghent University. We would like to thank N. Lemeire (Ghent University) and I. Delaere (Ghent University) for technical assistance during this study.

References

  1. Ahn IP, Kim S, Kang S, Suh SC, Lee YH (2005) Rice defense mechanisms against Cochliobolus miyabeanus and Magnaporthe grisea are distinct. Phytopathology 95:1248–1255. doi: 10.1094/PHYTO-95-1248 CrossRefPubMedGoogle Scholar
  2. Baba A, Hasezawa S, Syōno K (1986) Cultivation of rice protoplasts and their transformation mediated by Agrobacterium spheroplasts. Plant Cell Physiol 27:463–471Google Scholar
  3. Baetz U, Martinoia E (2014) Root exudates: the hidden part of plant defense. Trends Plant Sci 19:90–98. doi: 10.1016/j.tplants.2013.11.006 CrossRefPubMedGoogle Scholar
  4. Balmer A, Pastor V, Gamir J, Flors V, Mauch-Mani B (2015) The ‘prime-ome’: towards a holistic approach to priming. Trends Plant Sci 20:443–452. doi: 10.1016/j.tplants.2015.04.002 CrossRefPubMedGoogle Scholar
  5. Barnwal MK, Kotasthane A, Magculia N, Mukherjee PK, Savary S, Sharma AK, Singh HB, Singh US, Sparks AH, Variar M, Zaidi N (2013) A review on crop losses, epidemiology and disease management of rice brown spot to identify research priorities and knowledge gaps. Eur J Plant Pathol 136:443–457. doi: 10.1007/s10658-013-0195-6 CrossRefGoogle Scholar
  6. Berendsen RL, Pieterse CM, Bakker PA (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486. doi: 10.1016/j.tplants.2012.04.001 CrossRefPubMedGoogle Scholar
  7. Cawoy H, Mariutto M, Henry G, Fisher C, Vasilyeva N, Thonart P, Ongena M (2014) Plant defense stimulation by natural isolates of Bacillus depends on efficient surfactin production. Mol Plant Microbe Interact 27:87–100. doi: 10.1094/MPMI-09-13-0262-R CrossRefPubMedGoogle Scholar
  8. Chandler S, Van Hese N, Coutte F, Jacques P, Höfte M, De Vleesschauwer D (2015) Role of cyclic lipopeptides produced by Bacillus subtilis in mounting induced immunity in rice (Oryza sativa L.). Physiol Mol Plant Pathol 91:20–30. doi: 10.1016/j.pmpp.2015.05.010 CrossRefGoogle Scholar
  9. Chern MS, Fitzgerald HA, Yadav RC, Canlas PE, Dong X, Ronald PC (2001) Evidence for a disease-resistance pathway in rice similar to the NPR1-mediated signaling pathway in Arabidopsis. Plant J 27:101–113CrossRefPubMedGoogle Scholar
  10. Chujo T, Miyamoto K, Ogawa S, Masuda Y, Shimizu T, Kishi-Kaboshi M, Takahashi A, Nishizawa Y, Minami E, Nojiri H, Yamane H, Okada K (2014) Overexpression of phosphomimic mutated OsWRKY53 leads to enhanced blast resistance in rice. PLoS ONE 9:e98737. doi: 10.1371/journal.pone.0098737 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Conrath U (2011) Molecular aspects of defence priming. Trends Plant Sci 16:524–531. doi: 10.1016/j.tplants.2011.06.004 CrossRefPubMedGoogle Scholar
  12. D’aes J, Kieu NP, Léclère V, Tokarski C, Olorunleke FE, De Maeyer K, Jacques P, Höfte M, Ongena M (2014) To settle or to move? The interplay between two classes of cyclic lipopeptides in the biocontrol strain Pseudomonas CMR12a. Environ Microbiol 16:2282–2300. doi: 10.1111/1462-2920.12462 CrossRefPubMedGoogle Scholar
  13. De Coninck B, Timmermans P, Vos C, Cammue BP, Kazan K (2015) What lies beneath: belowground defense strategies in plants. Trends Plant Sci 20:91–101. doi: 10.1016/j.tplants.2014.09.007 CrossRefPubMedGoogle Scholar
  14. De Vleesschauwer D, Cornelis P, Höfte M (2006) Redox-active pyocyanin secreted by Pseudomonas aeruginosa 7NSK2 triggers systemic resistance to Magnaporthe grisea but enhances Rhizoctonia solani susceptibility in rice. Mol Plant Microbe Interact 19:1406–1419. doi: 10.1094/MPMI-19-1406 CrossRefPubMedGoogle Scholar
  15. De Vleesschauwer D, Djavaheri M, Bakker PA, Höfte M (2008) Pseudomonas fluorescens WCS374r-induced systemic resistance in rice against Magnaporthe oryzae is based on pseudobactin-mediated priming for a salicylic acid-repressible multifaceted defense response. Plant Physiol 148:1996–2012. doi: 10.1104/pp.108.127878 CrossRefPubMedPubMedCentralGoogle Scholar
  16. De Vleesschauwer D, Chernin L, Höfte MM (2009) Differential effectiveness of Serratia plymuthica IC1270-induced systemic resistance against hemibiotrophic and necrotrophic leaf pathogens in rice. BMC Plant Biol 9:9. doi: 10.1186/1471-2229-9-9 CrossRefPubMedPubMedCentralGoogle Scholar
  17. De Vleesschauwer D, Yang Y, Cruz CV, Höfte M (2010) Abscisic acid-induced resistance against the brown spot pathogen Cochliobolus miyabeanus in rice involves MAP kinase-mediated repression of ethylene signaling. Plant Physiol 152:2036–2052. doi: 10.1104/pp.109.152702 CrossRefPubMedPubMedCentralGoogle Scholar
  18. De Vleesschauwer D, Gheysen G, Höfte M (2013) Hormone defense networking in rice: tales from a different world. Trends Plant Sci 18:555–565. doi: 10.1016/j.tplants.2013.07.002 CrossRefPubMedGoogle Scholar
  19. De Vleesschauwer D, Seifi HS, Filipe O, Haeck A, Huu SN, Demeestere K, Höfte M (2016) The DELLA protein SLR1 integrates and amplifies salicylic acid-and jasmonic acid-dependent innate immunity in rice. Plant Physiol 170:1831–1847. doi: 10.1104/pp.15.01515 PubMedPubMedCentralGoogle Scholar
  20. Dean R, Van Kan JA, Pretorius ZA, Hammond-Kosack KE, Di Pietro A, Spanu PD, Rudd JJ, Dickman M, Kahmann R, Ellis J, Foster GD (2012) The Top 10 fungal pathogens in molecular plant pathology. Mol Plant Pathol 13:414–430. doi: 10.1111/J.1364-3703.2011.00783.X CrossRefPubMedGoogle Scholar
  21. Debois D, Fernandez O, Franzil L, Jourdan E, Brogniez A, Willems L, Clément C, Dorey S, De Pauw E, Ongena M (2015) Plant polysaccharides initiate underground crosstalk with bacilli by inducing synthesis of the immunogenic lipopeptide surfactin. Environ Microbiol Rep 7:570–582. doi: 10.1111/1758-2229.12286 CrossRefPubMedGoogle Scholar
  22. Ding X, Cao Y, Huang L, Zhao J, Xu C, Li X, Wang S (2008) Activation of the indole-3-acetic acid–amido synthetase GH3-8 suppresses expansin expression and promotes salicylate-and jasmonate-independent basal immunity in rice. Plant Cell 20:228–240. doi: 10.1105/tpc.107.055657 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Dixon RA, Achnine L, Kota P, Liu CJ, Reddy M, Wang L (2002) The phenylpropanoid pathway and plant defence-a genomics perspective. Mol Plant Pathol 3:371–390. doi: 10.1046/j.1364-3703.2002.00131.x CrossRefPubMedGoogle Scholar
  24. Farace G, Fernandez O, Jacquens L, Coutte F, Krier F, Jacques P, Clément C, Barka EA, Jacquard C, Dorey S (2015) Cyclic lipopeptides from Bacillus subtilis activate distinct patterns of defence responses in grapevine. Mol Plant Pathol 16:177–187. doi: 10.1111/mpp.12170 CrossRefPubMedGoogle Scholar
  25. Flury P, Vesga P, Péchy-Tarr M, Aellen N, Bermudaz K, Dennert F, Hofer N, Kupferschmied P, Metla Z, Ma Z, Siegfried S, de Weert S, Bloemberg G, Höfte M, Keel C, Maurhofer M (2017) Antimicrobial and insecticidal: cyclic lipopeptides and hydrogen cyanide produced by plant-beneficial Pseudomonas strains CHA0, CMR12a and PCL1391 contribute to insect killing. Front Microbiol 8:100. doi: 10.3389/fmicb.2017.00100 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Freeman BC, Beattie GA (2008) An overview of plant defenses against pathogens and herbivores. Plant Health Instr. doi: 10.1094/PHI-I-2008-0226-01 Google Scholar
  27. Garcia-Brugger A, Lamotte O, Vandelle E, Bourque S, Lecourieux D, Poinssot B, Wendehenne D, Pugin A (2006) Early signaling events induced by elicitors of plant defenses. Mol Plant Microbe Interact 19:711–724CrossRefPubMedGoogle Scholar
  28. Gross H, Stockwell VO, Henkels MD, Nowak-Thompson B, Loper JE, Gerwick WH (2007) The genomisotopic approach: a systematic method to isolate products of orphan biosynthetic gene clusters. Chem Biol 14:53–63. doi: 10.1016/j.chembiol.2006.11.007 CrossRefPubMedGoogle Scholar
  29. Han CU, Lee CH, Jang KS, Choi GJ, Lim HK, Kim JC, Ahn SN, Choi JE, Cha JS, Kim HT, Cho KY, Lee SW (2004) Identification of rice genes induced in a rice blast-resistant mutant. Mol Cells 17:462–468PubMedGoogle Scholar
  30. Höfte M, Altier N (2010) Fluorescent pseudomonads as biocontrol agents for sustainable agricultural systems. Res Microbiol 161:464–471. doi: 10.1016/j.resmic.2010.04.007 CrossRefPubMedGoogle Scholar
  31. Iavicoli A, Boutet E, Buchala A, Métraux JP (2003) Induced systemic resistance in Arabidopsis thaliana in response to root inoculation with Pseudomonas fluorescens CHA0. Mol Plant Microbe Interact 16:851–858CrossRefPubMedGoogle Scholar
  32. Jang JY, Yang SY, Kim YC, Lee CW, Park MS, Kim JC, Kim IS (2013) Identification of orfamide A as an insecticidal metabolite produced by Pseudomonas protegens F6. J Agric Food Chem 61:6786–6791. doi: 10.1021/jf401218w CrossRefPubMedGoogle Scholar
  33. Jiang CJ, Shimono M, Sugano S, Kojima M, Yazawa K, Yoshida R, Inoue H, Hayashi N, Sakakibara H, Takatsuji H (2010) Abscisic acid Interacts antagonistically with salicylic acid signaling pathway in rice-Magnaporthe grisea interaction. Mol Plant–Microbe Interact 23:791–798CrossRefPubMedGoogle Scholar
  34. Jourdan E, Henry G, Duby F, Dommes J, Barthelemy JP, Thonart P, Ongena M (2009) Insights into the defense-related events occurring in plant cells following perception of surfactin-type lipopeptide from Bacillus subtilis. Mol Plant Microbe Interact 22:456–468. doi: 10.1094/MPMI-22-4-0456 CrossRefPubMedGoogle Scholar
  35. Jwa N-S, Agrawal GK, Rakwal R, Park CH, Agrawal VP (2001) Molecular cloning and characterization of a novel jasmonate inducible pathogenesis-related class 10 protein gene, JIOsPR10, from rice (Oryza sativa L.) seedling leaves. Biochem Biophys Res Commun 286:973–983CrossRefPubMedGoogle Scholar
  36. Kawagoe Y, Shiraishi S, Kondo H, Yamamoto S, Aoki Y, Suzuki S (2015) Cyclic lipopeptide iturin A structure-dependently induces defense response in Arabidopsis plants by activating SA and JA signaling pathways. Biochem Biophys Res Commun 460:1015–1020. doi: 10.1016/j.bbrc.2015.03.143 CrossRefPubMedGoogle Scholar
  37. Kidou S, Ejiri S (1998) Isolation, characterization and mRNA expression of four cDNAs encoding translation elongation factor 1A from rice (Oryza sativa L.). Plant Mol Biol 36:137–148CrossRefPubMedGoogle Scholar
  38. King EO, Ward MK, Raney DE (1954) Two simple media for the demonstration of pyocyanin and fluorescin. J Lab Clin Med 44:301–307PubMedGoogle Scholar
  39. Kishimoto K, Kouzai Y, Kaku H, Shibuya N, Minami E, Nishizawa Y (2010) Perception of the chitin oligosaccharides contributes to disease resistance to blast fungus Magnaporthe oryzae in rice. Plant J 64:343–354. doi: 10.1111/j.1365-313X.2010.04328.x CrossRefPubMedGoogle Scholar
  40. Lee MW, Qi M, Yang Y (2001) A novel jasmonic acid-inducible rice myb gene associates with fungal infection and host cell death. Mol Plant Microbe Interact 14:527–535CrossRefPubMedGoogle Scholar
  41. Ma Z, Geudens N, Kieu NP, Sinnaeve D, Ongena M, Martins J, Höfte M (2016a) Biosynthesis, chemical structure and structure-activity relationship of orfamide lipopeptides produced by Pseudomonas protegens and related species. Front Microbiol 7:382. doi: 10.3389/fmicb.2016.00382 PubMedPubMedCentralGoogle Scholar
  42. Ma Z, Hua GK, Ongena M, Höfte M (2016b) Role of phenazines and cyclic lipopeptides produced by Pseudomonas sp. CMR12a in induced systemic resistance on rice and bean. Environ Microbiol Rep 8:896–904. doi: 10.1111/1758-2229.12454 CrossRefGoogle Scholar
  43. McElroy D, Rothenberg M, Reece KS, Wu R (1990) Characterization of the rice (Oryza sativa) actin gene family. Plant Mol Biol 15:257–268CrossRefPubMedGoogle Scholar
  44. Newman MA, Sundelin T, Nielsen JT, Erbs G (2013) MAMP (microbe-associated molecular pattern) triggered immunity in plants. Front Plant Sci 4:139. doi: 10.3389/fpls.2013.00139 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Olorunleke FE, Hua GKH, Kieu NP, Ma Z, Höfte M (2015) Interplay between orfamides, sessilins and phenazines in the control of Rhizoctonia diseases by Pseudomonas sp. CMR12a. Environ Microbiol Rep 7:774–781. doi: 10.1111/1758-2229.12310 CrossRefPubMedGoogle Scholar
  46. Ongena M, Jacques P (2008) Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends Microbiol 16:115–125. doi: 10.1016/j.tim.2007.12.009 CrossRefPubMedGoogle Scholar
  47. Ongena M, Jourdan E, Adam A, Paquot M, Brans A, Joris B, Arpigny JL, Thonart P (2007) Surfactin and fengycin lipopeptides of Bacillus subtilis as elicitors of induced systemic resistance in plants. Environ Microbiol 9:1084–1090. doi: 10.1111/j.1462-2920.2006.01202.x CrossRefPubMedGoogle Scholar
  48. Perneel M, Heyrman J, Adiobo A, De Maeyer K, Raaijmakers JM, De Vos P et al (2007) Characterization of CMR5c and CMR12a, novel fluorescent Pseudomonas strains from the cocoyam rhizosphere with biocontrol activity. J Appl Microbiol 103:1007–1020. doi: 10.1111/j.1365-2672.2007.03345.x CrossRefPubMedGoogle Scholar
  49. Pieterse CM, Zamioudis C, Berendsen RL, Weller DM, Van Wees SC, Bakker PA (2014) Induced systemic resistance by beneficial microbes. Annu Rev Phytopathol 52:347–375. doi: 10.1146/annurev-phyto-082712-102340 CrossRefPubMedGoogle Scholar
  50. Raaijmakers JM, De Bruijn I, Nybroe O, Ongena M (2010) Natural functions of lipopeptides from Bacillus and Pseudomonas: more than surfactants and antibiotics. FEMS Microbiol Rev 34:1037–1062. doi: 10.1111/j.1574-6976.2010.00221.x CrossRefPubMedGoogle Scholar
  51. Sambrook J, Fritsch EF (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp 11–18Google Scholar
  52. Shimono M, Sugano S, Nakayama A, Jiang CJ, Ono K, Toki S, Takatsuji H (2007) Rice WRKY45 plays a crucial role in benzothiadiazole-inducible blast resistance. Plant Cell 19:2064–2076. doi: 10.1105/tpc.106.046250 CrossRefPubMedPubMedCentralGoogle Scholar
  53. Sinha M, Singh RP, Kushwaha GS, Iqbal N, Singh A, Kaushik S, Kaur P, Sharma S, Singh TP (2014) Current overview of allergens of plant pathogenesis related protein families. Scientific World J 2014:543195. doi: 10.1155/2014/543195 Google Scholar
  54. Spence C, Alff E, Johnson C, Ramos C, Donofrio N, Sundaresan V, Bais H (2014) Natural rice rhizospheric microbes suppress rice blast infections. BMC Plant Biol 14:130. doi: 10.1186/1471-2229-14-130 CrossRefPubMedPubMedCentralGoogle Scholar
  55. Stutz EW, Défago G, Kern H (1986) Naturally occurring fluorescent pseudomonads involved in suppression of black root rot of tobacco. Phytopathology 76:181–185CrossRefGoogle Scholar
  56. Talbot NJ, Ebbole DJ, Hamer JE (1993) Identification and characterization of MPG1, a gene involved in pathogenicity from the rice blast fungus Magnaporthe grisea. Plant Cell 5:1575–1590CrossRefPubMedPubMedCentralGoogle Scholar
  57. Thordal-Christensen H, Zhang Z, Wei Y, Collinge DB (1997) Subcellular localization of H202 in plants. H202 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J 11:1187–1194CrossRefGoogle Scholar
  58. Thuan NTN, Bigirimana J, Roumen E, Van Der Straeten D, Höfte M (2006) Molecular and pathotype analysis of the rice blast fungus in North Vietnam. Eur J Plant Pathol 114:381–396CrossRefGoogle Scholar
  59. Tran H, Ficke A, Asiimwe T, Höfte M, Raaijmakers JM (2007) Role of the cyclic lipopeptide massetolide A in biological control of Phytophthora infestans and in colonization of tomato plants by Pseudomonas fluorescens. New Phytol 175:731–742. doi: 10.1111/j.1469-8137.2007.02138.x CrossRefPubMedGoogle Scholar
  60. Trdá L, Boutrot F, Claverie J, Brulé D, Dorey S, Poinssot B (2015) Perception of pathogenic or beneficial bacteria and their evasion of host immunity: pattern recognition receptors in the frontline. Front Plant Sci 6:219. doi: 10.3389/fpls.2015.00219 CrossRefPubMedPubMedCentralGoogle Scholar
  61. Van Bockhaven J, De Vleesschauwer D, Höfte M (2013) Towards establishing broad-spectrum disease resistance in plants: silicon leads to way. J Exp Bot 64:1281–1293. doi: 10.1093/jxb/ers329 CrossRefPubMedGoogle Scholar
  62. Van Bockhaven J, Spíchal L, Novák O, Strnad M, Asano T, Kikuchi S, Höfte M, De Vleesschauwer D (2015) Silicon induces resistance to the brown spot fungus Cochliobolus miyabeanus by preventing the pathogen from hijacking the rice ethylene pathway. New Phytol 206:761–773. doi: 10.1111/nph.13270 CrossRefPubMedGoogle Scholar
  63. Van Loon LC, Rep M, Pieterse C (2006) Significance of inducible defense-related proteins in infected plants. Annu Rev Phytopathol 44:135–162. doi: 10.1146/annurev.phyto.44.070505.143425 CrossRefPubMedGoogle Scholar
  64. Verhagen BW, Trotel-Aziz P, Couderchet M, Höfte M, Aziz A (2009) Pseudomonas spp.-induced systemic resistance to Botrytis cinerea is associated with induction and priming of defence responses in grapevine. J Exp Bot 61:249–260. doi: 10.1093/jxb/erp295 CrossRefGoogle Scholar
  65. Wang H, Meng J, Peng X, Tang X, Zhou P, Xiang J, Deng X (2015) Rice WRKY4 acts as a transcriptional activator mediating defense responses toward Rhizoctonia solani, the causing agent of rice sheath blight. Plant Mol Biol 89:157–171. doi: 10.1007/s11103-015-0360-8 CrossRefPubMedGoogle Scholar
  66. Weller DM, Mavrodi DV, van Peltm JA, Pieterse CM, van Loon LC, Bakker PA (2012) Induced systemic resistance in Arabidopsis thaliana against Pseudomonas syringae pv. tomato by 2,4-diacetylphloroglucinol-producing Pseudomonas fluorescens. Phytopathology 102:403–412. doi: 10.1094/PHYTO-08-11-0222 CrossRefPubMedGoogle Scholar
  67. Xu J, Audenaert K, Hofte M, De Vleesschauwer D (2013) Abscisic acid promotes susceptibility to the rice leaf blight pathogen Xanthomonas oryzae pv oryzae by suppressing salicylic acid-mediated defenses. PLoS ONE 8:e67413. doi: 10.1371/journal.pone.0067413 CrossRefPubMedPubMedCentralGoogle Scholar
  68. Yang G, Inoue A, Takasaki H, Kaku H, Akao S, Komatsu S (2005) A proteomic approach to analyze auxin-and zinc-responsive protein in rice. J Prote Res 4:456–463CrossRefGoogle Scholar
  69. Zarembinski TI, Theologis A (1997) Expression characteristics of OS-ACS1 and OS-ACS2, two members of the 1-aminocyclopropane-1-carboxylate synthase gene family in rice (Oryza sativa L. cv. Habiganj Aman II) during partial submergence. Plant Mol Biol 33:71–77CrossRefPubMedGoogle Scholar
  70. Zhu Q, Dabi T, Beeche A, Yamamoto R, Lawton MA, Lamb C (1995) Cloning and properties of a rice gene encoding phenylalanine ammonia-lyase. Plant Mol Biol 29:535–550CrossRefPubMedGoogle Scholar
  71. Zhu H, Xu X, Xiao G, Yuan L, Li B (2007) Enhancing disease resistances of super hybrid rice with four antifungal genes. Sci China C Life Sci 50:31–39CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.Laboratory of Phytopathology, Faculty of Bioscience EngineeringGhent UniversityGhentBelgium
  2. 2.Microbial Processes and Interactions Unit, Faculty of Gembloux Agro-Bio TechUniversity of LiègeGemblouxBelgium

Personalised recommendations