, Volume 243, Issue 5, pp 1297–1308 | Cite as

The polygalacturonase-inhibiting protein 4 (OsPGIP4), a potential component of the qBlsr5a locus, confers resistance to bacterial leaf streak in rice

Original Article


Main conclusion

OsPGIP4overexpression enhances resistance to bacterial leaf streak in rice.

Polygalacturonase-inhibiting proteins are thought to play important roles in the innate immunity of rice against fungi. Here, we show that the chromosomal location of OsPGIP4 coincides with the major bacterial leaf streak resistance quantitative trait locus qBlsr5a on the short arm of chromosome 5. OsPGIP4 expression was up-regulated upon inoculation with the pathogen Xanthomonas oryzae pv. oryzicola strain RS105. OsPGIP4 overexpression enhanced the resistance of the susceptible rice variety Zhonghua 11 to RS105. In contrast, repressing OsPGIP4 expression resulted in an increase in disease lesions caused by RS105 in Zhonghua 11 and in Acc8558, a qBlsr5a resistance donor. More interestingly, upon inoculation, the activated expression of pathogenesis-related genes was attenuated for those genes involved in the salicylic acid pathway, while the activated expression of jasmonic acid pathway markers was increased in the overexpression lines. Our results not only provide the first report that rice PGIP could enhance resistant against a bacterial pathogen but also indicate that OsPGIP4 is a potential component of the qBlsr5a locus for bacterial leaf streak in rice.


Defense response Defense-related gene Jasmonic acid Quantitative resistance Xanthomonas oryzae 



Bacterial blight


Bacterial leaf streak




Jasmonic acid






Polygalacturonase-inhibiting protein




Salicylic acid


Xanthomonas oryzae pv. oryzicola


Xanthomonas oryzae pv. oryzae

Supplementary material

425_2016_2480_MOESM1_ESM.pdf (75 kb)
Suppl. Fig. S1 The inhibition of PG activity for OsPGIP4 overexpression rice. Three individual OsPGIP4 overexpression lines were performed for the inhibition of PG activity that compared with the wild type ZH11. Suppl. Fig. S2 The PG homologs of Xanthomonas oryzae. Alignment of PG homologs in the Xoo strains PXO99A and PXO86 and in the Xoc strains BLS256 and RS105. The substitution amino acids are highlighted in bold.Suppl. Fig. S3 The lesion areas to PXO99 for OsPGIP4 overexpression and RNAi plants. Lesion areas were counted by the ratio between the lesion length and leaf length after inoculation with the Xoo strain PXO99 in T1 generation. Each line included at least 5 positive individuals for the experiment (PDF 74 kb)


  1. Agüero CB, Uratsu SL, Greve C, Powell AT, Labavitch JM, Meredith CP, Dandekar AM (2005) Evaluation of tolerance to Pierce’s disease and Botrytis in transgenic plants of Vitis vinifera L. expressing the pear PGIP gene. Mol Plant Pathol 6:43–51CrossRefPubMedGoogle Scholar
  2. Benedetti M, Leggio C, Federici L, de Lorenzo G, Viorel Pavel N, Cervone F (2011) Structural resolution of the complex between a fungal polygalacturonase and a plant polygalacturonase-inhibiting protein by small-angel X-ray scattering. Plant Physiol 157:599–607CrossRefPubMedPubMedCentralGoogle Scholar
  3. Chen C, Zheng W, Huang X, Zhang D, Lin X (2006) Major QTL conferring resistance to rice bacterial leaf streak. Agric Sci China 5(3):216–220CrossRefGoogle Scholar
  4. Dai Y, Jia Y, Correll J, Wang X, Wang Y (2010) Diversification and evolution of the avirulence gene AVR-pita 1 in field isolates of Magnaporthe oryzae. Fungal Genet Biol 47:974–980CrossRefGoogle Scholar
  5. Di Matteo A, Federici L, Mattei B, Salvi G, Johnson KA, Savino C, de Lorenzo G, Tsernoglou D, Cervone F (2003) The crystal structure of polygalacturonase-inhibiting protein (PGIP), a leucine-rich repeat protein involved in plant defense. Proc Natl Acad Sci USA 100:10124–10128CrossRefPubMedPubMedCentralGoogle Scholar
  6. Feng W, Wang Y, Huang L, Feng C, Chu Z, Ding X, Yang L (2015) Genomic-associated markers and comparative genome maps of Xanthomonas oryzae pv. oryzae and X. oryzae pv. oryzicola. World J Microbiol Biotechnol 31:1353–1359CrossRefPubMedGoogle Scholar
  7. Ferrari S, Savatin DV, Sicilia F, Gramegna G, Cervone F, De Lorenzo G (2013) Oligogalacturonides: plant damage-associated molecular patterns and regulators of growth and development. Front Plant Sci 4:49CrossRefPubMedPubMedCentralGoogle Scholar
  8. Fu D, Uauy C, Distelfeld A, Blechl A, Epstein L, Chen X, Sela H, Fahima T, Dubcovsky J (2009) A kinase-START gene confers temperature-dependent resistance to wheat stripe rust. Science 323:1357–1360CrossRefPubMedPubMedCentralGoogle Scholar
  9. 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 155:589–602CrossRefPubMedPubMedCentralGoogle Scholar
  10. Fukuoka S, Saka N, Koga H, Ono K, Shimizu T, Ebana K, Hayashi N, Takahashi A, Hirochika H, Okuno K, Yano M (2009) Loss of function of a proline-containing protein confers durable disease resistance in rice. Science 325:998–1001CrossRefPubMedGoogle Scholar
  11. Ge X, Chu Z, Lin Y, Wang S (2006) A tissue culture system for different germplasms of indica rice. Plant Cell Rep 25:392–402CrossRefPubMedGoogle Scholar
  12. 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 increase susceptibility to bacterial leaf streak disease in transgenic rice plants. Mol Biol Rep 39:3491–3504CrossRefPubMedGoogle Scholar
  13. Guo L, Guo C, Li M, Wang W, Luo C, Zhang Y, Chen L (2014) Suppression of expression of the putative receptor-like kinase gene NRRB enhances resistance to bacterial leaf streak in rice. Mol Biol Rep 41:2177–2187CrossRefPubMedGoogle Scholar
  14. Gutierrez-Sanchez G, King D, Kemp G, Bergmann C (2012) SPR and differential proteolysis/MS provide further insight into the interaction between PGIP2 and EPGs. Fungal Biol 116:737–746CrossRefPubMedGoogle Scholar
  15. Han QD, Chen ZW, Deng Y, Lan T, Guan HZ, Duan YL, Zhou YC, Lin MC, Wu WR (2008) Fine mapping of qBlsr5a, a QTL controlling resistance to bacterial leaf streak in rice (in Chinese). Acta Agron Sin 34(4):587–590Google Scholar
  16. Hwang BH, Bae H, Lim HS, Kim KB, Kim SJ, Im MH, Park BS, Kim DS, Kim J (2010) Overexpression of polygalacturonase-inhibiting protein 2 (PGIP2) of Chinese cabbage (Brassica rapa ssp. pekinensis) increased resistance to the bacterial pathogen Pectobacterium carotovorum ssp. carotovorum. Plant Cell Tiss Organ Cult 103:293–305CrossRefGoogle Scholar
  17. Jang S, Lee B, Kim C, Kim SJ, Yim J, Han JJ, Lee S, Kim SR, An G (2003) The OsFOR1 gene encodes a polygalacturase-inhibiting protein (PGIP) that regulates floral organ number in rice. Plant Mol Biol 53:357–369CrossRefPubMedGoogle Scholar
  18. Janni M, Di Giovanni M, Roberti S, Capodicasa C, D’Ovidio R (2006) Characterization of expressed Pgip genes in rice and wheat reveals similar extent of sequence variation to dicot PGIPs and identifies an active PGIP lacking an entire LRR repeat. Theor Appl Genet 113:1233–1245CrossRefPubMedGoogle Scholar
  19. Kalunke RM, Tundo S, Benedetti M, Cervone F, De Lorenzo G, D’Ovidio R (2015) An undate on polygalacturonase-inhibiting protein (PGIP), a leucine-rich repeat protein that protects crop plants against pathogens. Front Plant Sci 6:146CrossRefPubMedPubMedCentralGoogle Scholar
  20. Kou Y, Wang S (2010) Broad-spectrum and durability: understanding of quantitative disease resistance. Curr Opin Plant Biol 13:181–185CrossRefPubMedGoogle Scholar
  21. Krattinger SG, Lagudah ES, Spielmeyer W, Singh RP, Huerta-Espino J, McFaddern H, Bossolini E, Selter LL, Keller B (2009) A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science 323:1360–1363CrossRefPubMedGoogle Scholar
  22. Li D, Wang L, Teng S, Zhang G, Guo L, Mao Q, Wang W, Li M, Chen L (2012) Proteomics analysis of rice proteins up-regulated in response to bacterial leaf streak disease. J Plant Biol 55:316–324CrossRefGoogle Scholar
  23. Li N, Kong L, Zhou W, Zhang X, Wei S, Ding X, Chu Z (2013) Overexpression of Os2H16 enhances resistance to phytopathogens and tolerance to drought stress in rice. Plant Cell Tiss Organ Cult 115:429–441CrossRefGoogle Scholar
  24. Lin Y, Zhang Q (2005) Optimizing the tissue culture conditions for high efficiency transformation of indica rice. Plant Cell Rep 23:540–547CrossRefPubMedGoogle Scholar
  25. Liu H, Chang Q, Feng W, Zhang B, Wu T, Li N, Yao F, Ding X, Chu Z (2014) Domain dissection of AvrRxo1 for suppressor, avirulence and cytotoxic functions. PLoS One 9(12):e113875CrossRefPubMedPubMedCentralGoogle Scholar
  26. Lu L, Zhou F, Zhou Y, Fan X, Ye S, Wang L, Chen H, Lin Y (2012) Expression profile analysis of polygalacturonase-inhibiting protein genes in rice and their responses to phytohormones and fungal infection. Plant Cell Rep 31:1173–1187CrossRefPubMedGoogle Scholar
  27. McCleary BV, McGeough P (2015) A comparison of polysaccharide substrates and reducing sugar methods for the measurement of endo-1,4-β-xylanase. Appl Biochem Biotechnol 177:1152–1163CrossRefPubMedPubMedCentralGoogle Scholar
  28. Nino-Liu DO, Ronald PC, Bogdanove AJ (2006) Xanthomonas oryzae pathovars: model pathogens of a model crop. Mol Plant Pathol 7:303–324CrossRefPubMedGoogle Scholar
  29. Poland JA, Balint-Kurti PJ, Wisser RJ, Pratt RC, Nelson RJ (2009) Shades of gray: the world of quantitative disease resistance. Trends Plant Sci 14:21–29CrossRefPubMedGoogle Scholar
  30. Schacht T, Unger C, Pich A, Wydra K (2011) Endo- and exopolygalactuonases of Rslstonia solanacearum are inhibited by polygalactuonase-inhibiting protein (PGIP) activity in tomato stem extracts. Plant Physiol Biochem 49:377–387CrossRefPubMedGoogle Scholar
  31. 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 4:86–99Google Scholar
  32. Skaminioti P, Gurr SJ (2009) Against the grain: safeguarding rice from blast disease. Trends Biotechnol 27:141–150CrossRefGoogle Scholar
  33. 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 101:286–291CrossRefGoogle Scholar
  34. 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 151:936–948CrossRefPubMedPubMedCentralGoogle Scholar
  35. Thaler JS, Humphrey PT, Whiteman NK (2012) Evolution of jasmonate and salicylate signal crosstalk. Trends Plant Sci 17:260–270CrossRefPubMedGoogle Scholar
  36. Wang Y, Wang D, Deng X, Liu J, Sun P, Liu Y, Huang H, Jiang N, Kang H, Ning Y, Wang Z, Xiao J, Liu X, Liu E, Dai L, Wang GL (2012) Molecular mapping of the blast resistance genes Pi2-1 and Pi51 (t) in the durably resistant rice ‘Tianjingyeshengdao’. Phytopathology 102:779–786CrossRefPubMedGoogle Scholar
  37. Wang R, Lu L, Pan X, Hu Z, Ling F, Yan Y, Liu Y, Lin Y (2015) Functional analysis of OsPGIP1 in rice sheath blight resistance. Plant Mol Biol 87:181–191CrossRefPubMedGoogle Scholar
  38. 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:e4603CrossRefPubMedPubMedCentralGoogle Scholar
  39. Xie X, Chen Z, Cao J, Guan H, Lin D, Li C, Lan T, Duan Y, Mao D, Wu W (2014) Toward the positional cloning of qBlsr5a, a QTL underlying resistance to bacterial leaf streak, using overlapping sub-CSSLs in rice. PLoS One 9:e95751CrossRefPubMedPubMedCentralGoogle Scholar
  40. Xu MR, Huang LY, Zhang F, Zhu LH, Zhou YL, Li ZK (2013) Genome-wide phylogenetic analysis of stress-activated protein kinase genes in rice (OsSAPKs) and expression profiling in response to Xanthomonas oryzae pv. oryzicola infection. Plant Mol Biol Rep 31:877–885CrossRefGoogle Scholar
  41. 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 102:15383–15388CrossRefPubMedPubMedCentralGoogle Scholar
  42. 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 11:78CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.State Key Laboratory of Crop Biology, Shandong Provincial Key Laboratory of Agricultural MicrobiologyShandong Agricultural UniversityTai’anPeople’s Republic of China
  2. 2.Institute of Plant Protection and Soil FertilizerHubei Academy of Agricultural SciencesWuhanPeople’s Republic of China
  3. 3.Biotechnology Research CenterShandong Academy of Agricultural ScienceJinanPeople’s Republic of China

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