Molecular Biology Reports

, Volume 41, Issue 4, pp 2177–2187 | Cite as

Suppression of expression of the putative receptor-like kinase gene NRRB enhances resistance to bacterial leaf streak in rice

  • Lijia Guo
  • Chiming Guo
  • Min Li
  • Wujing Wang
  • Chengke Luo
  • Yuxia Zhang
  • Liang Chen


Bacterial leaf streak (BLS) caused by Xanthomonas oryzae pv. oryzicola (Xoc) is an important disease of rice, which is responsible for the economic losses worldwide. Functional investigation of differentially expressed protein genes (DEPGs) from rice (Oryza sativa L.) upon Xoc infection provides insight into the molecular mechanism of rice–Xoc interactions. Here, we show that one of DEPGs designated NRRB plays a role in rice–Xoc interactions. NRRB, a receptor-like cytoplasmic kinase gene was preferentially expressed in leaf blades and leaf sheaths where the pathogen colonized. Its transcription was depressed by two defense-signal compounds salicylic acid and 1-aminocyclopropane-1-carboxylic-acid, but was activated by wounding and abscisic acid. Additionally, a plenty of cis-elements associated with stress responses were discovered in the promoter region of NRRB. These data suggest that NRRB is involved in stress responses. More importantly, the NRRB-suppressing rice plants exhibited enhanced resistance against BLS, with the markedly shorter average lesion length than that of the wild type. Furthermore, transcription of some salicylic acid synthesis-related and pathogenesis-related genes including PAD4, PR1a and WRKY13 in transgenic plants was activated, implying that enhanced resistance to BLS might be mediated by the activation of the SA signaling pathway. In conclusion, NRRB gene is involved in various stress responses and regulating resistance to BLS, therefore it might be one of useful genes for rice improvement in future.


Resistance Defense response Pathogenesis-related gene Bacterial leaf streak Stress Rice 



Abscisic acid


1-Aminocyclopropane-1-carboxylic acid


Two-dimensional gel electrophoresis


Matrix-assisted laser desorption/ionization time of flight mass spectrometry


Salicylic acid


Wild type



The authors acknowledge Mingfu Zhao (Fujian Academy of Agricultural Sciences) for providing the bacterial pathogen Xanthomonas oryzae pv. oryzicola RS105 strain, and also thank National Program of Transgenic Variety Development of China (Grant No. 2011ZX08001-001) and National Key Basic Researches Program of China (Grant No. 2012CB126312) for the financial support.


  1. 1.
    Nino-Liu DO, Ronald PC, Bogdanove AJ (2006) Xanthomonas oryzae pathovars: model pathogens of a model crop. Mol Plant Pathol 7(5):303–324. doi: 10.1111/j.1364-3703.2006.00344.x PubMedCrossRefGoogle Scholar
  2. 2.
    Rao KK, Lakshminarasu M, Jena KK (2002) DNA markers and marker-assisted breeding for durable resistance to bacterial blight disease in rice. Biotechnol Adv 20(1):33–47. doi: 10.1016/S0734-9750(02)00002-2 PubMedCrossRefGoogle Scholar
  3. 3.
    Kottapalli KR, Lakshmi Narasu M, Jena KK (2010) Effective strategy for pyramiding three bacterial blight resistance genes into fine grain rice cultivar, Samba Mahsuri, using sequence tagged site markers. Biotechnol Lett 32(7):989–996. doi: 10.1007/s10529-010-0249-1 PubMedCrossRefGoogle Scholar
  4. 4.
    Myint KK, Fujita D, Matsumura M, Sonoda T, Yoshimura A, Yasui H (2012) Mapping and pyramiding of two major genes for resistance to the brown planthopper (Nilaparvata lugens [Stal]) in the rice cultivar ADR52. TAG Theor Appl Genet Theoretische und angewandte Genetik 124(3):495–504. doi: 10.1007/s00122-011-1723-4 CrossRefGoogle Scholar
  5. 5.
    Dai L-Y, Liu X-L, Xiao Y-H, Wang G-L (2007) Recent advances in cloning and characterization of disease resistance genes in rice. J Integr Plant Biol 49(1):112–119. doi: 10.1111/j.1744-7909.2006.00413.x CrossRefGoogle Scholar
  6. 6.
    Zhao B, Lin X, Poland J, Trick H, Leach J, Hulbert S (2005) A maize resistance gene functions against bacterial streak disease in rice. Proc Natl Acad Sci USA 102(43):15383–15388. doi: 10.1073/pnas.0503023102 PubMedCentralPubMedCrossRefGoogle Scholar
  7. 7.
    Tang D, Wu W, Li W, Lu H, Worland AJ (2000) Mapping of QTLs conferring resistance to bacterial leaf streak in rice. Theor Appl Genet 101(1):286–291. doi: 10.1007/s001220051481 CrossRefGoogle Scholar
  8. 8.
    Tao Z, Liu H, Qiu D, Zhou Y, Li X, Xu C, Wang S (2009) A pair of allelic WRKY genes play opposite roles in rice-bacteria interactions. Plant Physiol 151(2):936–948. doi: 10.1104/pp.109.145623 PubMedCentralPubMedCrossRefGoogle Scholar
  9. 9.
    Shen X, Yuan B, Liu H, Li X, Xu C, Wang S (2010) Opposite functions of a rice mitogen-activated protein kinase during the process of resistance against Xanthomonas oryzae. Plant J 64(1):86–99. doi: 10.1111/j.1365-313X.2010.04306.x PubMedGoogle Scholar
  10. 10.
    Xiao W, Liu H, Li Y, Li X, Xu C, Long M, Wang S (2009) A rice gene of de novo origin negatively regulates pathogen-induced defense response. PLoS One 4(2):e4603. doi: 10.1371/journal.pone.0004603 PubMedCentralPubMedCrossRefGoogle Scholar
  11. 11.
    Fu J, Liu H, Li Y, Yu H, Li X, Xiao J, Wang S (2011) Manipulating broad-spectrum disease resistance by suppressing pathogen-induced auxin accumulation in rice. Plant Physiol 155(1):589–602. doi: 10.1104/pp.110.163774 PubMedCentralPubMedCrossRefGoogle Scholar
  12. 12.
    Kou Y, Wang S (2010) Broad-spectrum and durability: understanding of quantitative disease resistance. Curr Opin Plant Biol 13(2):181–185. doi: 10.1016/j.pbi.2009.12.010 PubMedCrossRefGoogle Scholar
  13. 13.
    Zhao CJ, Wang AR, Shi YJ, Wang LQ, Liu WD, Wang ZH, Lu GD (2008) Identification of defense-related genes in rice responding to challenge by Rhizoctonia solani. TAG Theor Appl Genet Theoretische und angewandte Genetik 116(4):501–516. doi: 10.1007/s00122-007-0686-y CrossRefGoogle Scholar
  14. 14.
    Mahmood T, Jan A, Kakishima M, Komatsu S (2006) Proteomic analysis of bacterial-blight defense-responsive proteins in rice leaf blades. Proteomics 6(22):6053–6065. doi: 10.1002/pmic.200600470 PubMedCrossRefGoogle Scholar
  15. 15.
    Guo L, Li M, Wang W, Wang L, Hao G, Guo C, Chen L (2012) Over-expression in the nucleotide-binding site-leucine rich repeat gene DEPG1 increases susceptibility to bacterial leaf streak disease in transgenic rice plants. Mol Biol Rep 39(4):3491–3504. doi: 10.1007/s11033-011-1122-6 PubMedCrossRefGoogle Scholar
  16. 16.
    Serra O, Soler M, Hohn C, Franke R, Schreiber L, Prat S, Molinas M, Figueras M (2009) Silencing of StKCS6 in potato periderm leads to reduced chain lengths of suberin and wax compounds and increased peridermal transpiration. J Exp Bot 60(2):697–707. doi: 10.1093/jxb/ern314 PubMedCentralPubMedCrossRefGoogle Scholar
  17. 17.
    Nishimura A, Aichi I, Matsuoka M (2006) A protocol for Agrobacterium-mediated transformation in rice. Nat Protoc 1(6):2796–2802. doi: 10.1038/nprot.2006.469 PubMedCrossRefGoogle Scholar
  18. 18.
    Zou LF, Wang XP, Xiang Y, Zhang B, Li YR, Xiao YL, Wang JS, Walmsley AR, Chen GY (2006) Elucidation of the hrp clusters of Xanthomonas oryzae pv. oryzicola that control the hypersensitive response in nonhost tobacco and pathogenicity in susceptible host rice. Appl Environ Microbiol 72(9):6212–6224. doi: 10.1128/AEM.00511-06 PubMedCentralPubMedCrossRefGoogle Scholar
  19. 19.
    Zhou YL, Xu MR, Zhao MF, Xie XW, Zhu LH, Fu BY, Li ZK (2010) Genome-wide gene responses in a transgenic rice line carrying the maize resistance gene Rxo1 to the rice bacterial streak pathogen, Xanthomonas oryzae pv. oryzicola. BMC genomics 11:78. doi: 10.1186/1471-2164-11-78 PubMedCentralPubMedCrossRefGoogle Scholar
  20. 20.
    Vij S, Giri J, Dansana PK, Kapoor S, Tyagi AK (2008) The receptor-like cytoplasmic kinase (OsRLCK) gene family in rice: organization, phylogenetic relationship, and expression during development and stress. Mol Plant 1(5):732–750. doi: 10.1093/mp/ssn047 PubMedCrossRefGoogle Scholar
  21. 21.
    Kim TW, Guan S, Burlingame AL, Wang ZY (2011) The CDG1 kinase mediates brassinosteroid signal transduction from BRI1 receptor kinase to BSU1 phosphatase and GSK3-like kinase BIN2. Mol Cell 43(4):561–571. doi: 10.1016/j.molcel.2011.05.037 PubMedCentralPubMedCrossRefGoogle Scholar
  22. 22.
    Herrmann MM, Pinto S, Kluth J, Wienand U, Lorbiecke R (2006) The PTI1-like kinase ZmPti1a from maize (Zea mays L.) co-localizes with callose at the plasma membrane of pollen and facilitates a competitive advantage to the male gametophyte. BMC Plant Biol 6:22. doi: 10.1186/1471-2229-6-22 PubMedCentralPubMedCrossRefGoogle Scholar
  23. 23.
    Shen W, Gomez-Cadenas A, Routly EL, Ho TH, Simmonds JA, Gulick PJ (2001) The salt stress-inducible protein kinase gene, Esi47, from the salt-tolerant wheatgrass Lophopyrum elongatum is involved in plant hormone signaling. Plant Physiol 125(3):1429–1441. doi: 10.1104/pp.125.3.1429 PubMedCentralPubMedCrossRefGoogle Scholar
  24. 24.
    Shao F, Golstein C, Ade J, Stoutemyer M, Dixon JE, Innes RW (2003) Cleavage of Arabidopsis PBS1 by a bacterial type III effector. Science 301(5637):1230–1233. doi: 10.1126/science.1085671 PubMedCrossRefGoogle Scholar
  25. 25.
    Matsui H, Miyao A, Takahashi A, Hirochika H (2010) Pdk1 kinase regulates basal disease resistance through the OsOxi1-OsPti1a phosphorylation cascade in rice. Plant Cell Physiol 51(12):2082–2091. doi: 10.1093/pcp/pcq167 PubMedCrossRefGoogle Scholar
  26. 26.
    Zhou J, Loh YT, Bressan RA, Martin GB (1995) The tomato gene Pti1 encodes a serine/threonine kinase that is phosphorylated by Pto and is involved in the hypersensitive response. Cell 83(6):925–935. doi: 10.1016/0092-8674(95)90208-2 PubMedCrossRefGoogle Scholar
  27. 27.
    Lu D, Wu S, Gao X, Zhang Y, Shan L, He P (2010) A receptor-like cytoplasmic kinase, BIK1, associates with a flagellin receptor complex to initiate plant innate immunity. Proc Natl Acad Sci USA 107(1):496–501. doi: 10.1073/pnas.0909705107 PubMedCentralPubMedCrossRefGoogle Scholar
  28. 28.
    Shimizu T, Nakano T, Takamizawa D, Desaki Y, Ishii-Minami N, Nishizawa Y, Minami E, Okada K, Yamane H, Kaku H, Shibuya N (2010) Two LysM receptor molecules, CEBiP and OsCERK1, cooperatively regulate chitin elicitor signaling in rice. Plant J 64(2):204–214. doi: 10.1111/j.1365-313X.2010.04324.x PubMedCentralPubMedCrossRefGoogle Scholar
  29. 29.
    Oh CS, Martin GB (2011) Effector-triggered immunity mediated by the Pto kinase. Trends Plant Sci 16(3):132–140. doi: 10.1016/j.tplants.2010.11.001 PubMedCrossRefGoogle Scholar
  30. 30.
    Chen X, Shang J, Chen D, Lei C, Zou Y, Zhai W, Liu G, Xu J, Ling Z, Cao G, Ma B, Wang Y, Zhao X, Li S, Zhu L (2006) A B-lectin receptor kinase gene conferring rice blast resistance. Plant J 46(5):794–804. doi: 10.1111/j.1365-313X.2006.02739.x PubMedCrossRefGoogle Scholar
  31. 31.
    Hu H, Xiong L, Yang Y (2005) Rice SERK1 gene positively regulates somatic embryogenesis of cultured cell and host defense response against fungal infection. Planta 222(1):107–117. doi: 10.1007/s00425-005-1534-4 PubMedCrossRefGoogle Scholar
  32. 32.
    Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nurnberger T, Jones JD, Felix G, Boller T (2007) A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448(7152):497–500. doi: 10.1038/nature05999 PubMedCrossRefGoogle Scholar
  33. 33.
    Yang T, Chaudhuri S, Yang L, Chen Y, Poovaiah BW (2004) Calcium/calmodulin up-regulates a cytoplasmic receptor-like kinase in plants. J Biol Chem 279(41):42552–42559. doi: 10.1074/jbc.M402830200 PubMedCrossRefGoogle Scholar
  34. 34.
    Gomez-Gomez L, Boller T (2000) FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol Cell 5(6):1003–1011. doi: 10.1016/S1097-2765(00)80265-8 PubMedCrossRefGoogle Scholar
  35. 35.
    Song WY, Wang GL, Chen LL, Kim HS, Pi LY, Holsten T, Gardner J, Wang B, Zhai WX, Zhu LH, Fauquet C, Ronald P (1995) A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science 270(5243):1804–1806. doi: 10.1126/science.270 5243.1804PubMedCrossRefGoogle Scholar
  36. 36.
    Sun X, Cao Y, Yang Z, Xu C, Li X, Wang S, Zhang Q (2004) Xa26, a gene conferring resistance to Xanthomonas oryzae pv. oryzae in rice, encodes an LRR receptor kinase-like protein. Plant J 37(4):517–527. doi: 10.1046/j.1365-313X.2003.01976.x PubMedCrossRefGoogle Scholar
  37. 37.
    Castrillo G, Turck F, Leveugle M, Lecharny A, Carbonero P, Coupland G, Paz-Ares J, Onate-Sanchez L (2011) Speeding cis-trans regulation discovery by phylogenomic analyses coupled with screenings of an arrayed library of Arabidopsis transcription factors. PLoS One 6(6):e21524. doi: 10.1371/journal.pone.0021524 PubMedCentralPubMedCrossRefGoogle Scholar
  38. 38.
    Hartmann U, Sagasser M, Mehrtens F, Stracke R, Weisshaar B (2005) Differential combinatorial interactions of cis-acting elements recognized by R2R3-MYB, BZIP, and BHLH factors control light-responsive and tissue-specific activation of phenylpropanoid biosynthesis genes. Plant Mol Biol 57(2):155–171. doi: 10.1007/s11103-004-6910-0 PubMedCrossRefGoogle Scholar
  39. 39.
    Uno Y, Furihata T, Abe H, Yoshida R, Shinozaki K, Yamaguchi-Shinozaki K (2000) Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. Proc Natl Acad Sci USA 97(21):11632–11637. doi: 10.1073/pnas.190309197 PubMedCentralPubMedCrossRefGoogle Scholar
  40. 40.
    Kim SY, Chung HJ, Thomas TL (1997) Isolation of a novel class of bZIP transcription factors that interact with ABA-responsive and embryo-specification elements in the Dc3 promoter using a modified yeast one-hybrid system. Plant J 11(6):1237–1251. doi: 10.1046/j.1365-313X.1997.11061237.x PubMedCrossRefGoogle Scholar
  41. 41.
    Abe H, Yamaguchi-Shinozaki K, Urao T, Iwasaki T, Hosokawa D, Shinozaki K (1997) Role of arabidopsis MYC and MYB homologs in drought- and abscisic acid-regulated gene expression. Plant Cell 9(10):1859–1868. doi: 10.1105/tpc.9.10.1859 PubMedCentralPubMedGoogle Scholar
  42. 42.
    Debeaujon I, Nesi N, Perez P, Devic M, Grandjean O, Caboche M, Lepiniec L (2003) Proanthocyanidin-accumulating cells in Arabidopsis testa: regulation of differentiation and role in seed development. Plant Cell 15(11):2514–2531. doi: 10.1105/tpc.014043 PubMedCentralPubMedCrossRefGoogle Scholar
  43. 43.
    Simpson SD, Nakashima K, Narusaka Y, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Two different novel cis-acting elements of erd1, a clpA homologous Arabidopsis gene function in induction by dehydration stress and dark-induced senescence. Plant J 33(2):259–270. doi: 10.1046/j.1365-313X.2003.01624.x PubMedCrossRefGoogle Scholar
  44. 44.
    Chen C, Chen Z (2002) Potentiation of developmentally regulated plant defense response by AtWRKY18, a pathogen-induced Arabidopsis transcription factor. Plant Physiol 129(2):706–716. doi: 10.1104/pp.001057 PubMedCentralPubMedCrossRefGoogle Scholar
  45. 45.
    Haralampidis K, Milioni D, Rigas S, Hatzopoulos P (2002) Combinatorial interaction of cis elements specifies the expression of the Arabidopsis AtHsp90-1 gene. Plant Physiol 129(3):1138–1149. doi: 10.1104/pp.004044 PubMedCentralPubMedCrossRefGoogle Scholar
  46. 46.
    Bari R, Jones JD (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69(4):473–488. doi: 10.1007/s11103-008-9435-0 PubMedCrossRefGoogle Scholar
  47. 47.
    Qiu D, Xiao J, Ding X, Xiong M, Cai M, Cao Y, Li X, Xu C, Wang S (2007) OsWRKY13 mediates rice disease resistance by regulating defense-related genes in salicylate- and jasmonate-dependent signaling. Mol Plant Microbe Interact MPMI 20(5):492–499. doi: 10.1094/MPMI-20-5-0492 CrossRefGoogle Scholar
  48. 48.
    Datta K, Velazhahan R, Oliva N, Ona I, Mew T, Khush GS, Muthukrishnan S, Datta SK (1999) Over-expression of the cloned rice thaumatin-like protein (PR-5) gene in transgenic rice plants enhances environmental friendly resistance to Rhizoctonia solani causing sheath blight disease. Theor Appl Genet 98(6):1138–1145. doi: 10.1007/s001220051178 CrossRefGoogle Scholar
  49. 49.
    Nakashita H, Yoshioka K, Takayama M, Kuga R, Midoh N, Usami R, Horikoshi K, Yoneyama K, Yamaguchi I (2001) Characterization of PBZ1, a probenazole-inducible gene, in suspension-cultured rice cells. Biosci Biotechnol Biochem 65(1):205–208. doi: 10.1271/bbb.65.205 PubMedCrossRefGoogle Scholar
  50. 50.
    Hashimoto M, Kisseleva L, Sawa S, Furukawa T, Komatsu S, Koshiba T (2004) A novel rice PR10 protein, RSOsPR10, specifically induced in roots by biotic and abiotic stresses, possibly via the jasmonic acid signaling pathway. Plant Cell Physiol 45(5):550–559. doi: 10.1093/pcp/pch063 PubMedCrossRefGoogle Scholar
  51. 51.
    Yuan Y, Zhong S, Li Q, Zhu Z, Lou Y, Wang L, Wang J, Wang M, Yang D, He Z (2007) Functional analysis of rice NPR1-like genes reveals that OsNPR1/NH1 is the rice orthologue conferring disease resistance with enhanced herbivore susceptibility. Plant Biotechnol J 5(2):313–324. doi: 10.1111/j.1467-7652.2007.00243.x PubMedCrossRefGoogle Scholar
  52. 52.
    Shiu SH, Karlowski WM, Pan R, Tzeng YH, Mayer KF, Li WH (2004) Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. Plant Cell 16(5):1220–1234. doi: 10.1105/tpc.020834 PubMedCentralPubMedCrossRefGoogle Scholar
  53. 53.
    Tao Z, Kou Y, Liu H, Li X, Xiao J, Wang S (2011) OsWRKY45 alleles play different roles in abscisic acid signalling and salt stress tolerance but similar roles in drought and cold tolerance in rice. J Exp Bot 62(14):4863–4874. doi: 10.1093/jxb/err144 PubMedCentralPubMedCrossRefGoogle Scholar
  54. 54.
    Iwai T, Seo S, Mitsuhara I, Ohashi Y (2007) Probenazole-induced accumulation of salicylic acid confers resistance to Magnaporthe grisea in adult rice plants. Plant Cell Physiol 48(7):915–924. doi: 10.1093/pcp/pcm062 PubMedCrossRefGoogle Scholar
  55. 55.
    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(1):228–240. doi: 10.1105/tpc.107.055657 PubMedCentralPubMedCrossRefGoogle Scholar
  56. 56.
    Lu H (2009) Dissection of salicylic acid-mediated defense signaling networks. Plant Signal Behav 4(8):713–717. doi: 10.4161/psb.4.8.9173 PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Lijia Guo
    • 1
    • 2
  • Chiming Guo
    • 1
  • Min Li
    • 1
  • Wujing Wang
    • 1
  • Chengke Luo
    • 1
  • Yuxia Zhang
    • 1
  • Liang Chen
    • 1
  1. 1.Xiamen Key Laboratory for Plant Genetics, School of Life SciencesXiamen UniversityXiamenPeople’s Republic of China
  2. 2.Key Laboratory of Integrated Pest Management on Tropical Crops, Ministry of Agriculture, Environment and Plant Protection InstituteChinese Academy of Tropical Agricultural SciencesHaikouPeople’s Republic of China

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