Abstract
Main conclusion
OsPGIP4 overexpression 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.
Similar content being viewed by others
Abbreviations
- BB:
-
Bacterial blight
- BLS:
-
Bacterial leaf streak
- DR:
-
Defense-related
- JA:
-
Jasmonic acid
- OGs:
-
Oligogalacturonides
- PG:
-
Polygalacturonase
- PGIP:
-
Polygalacturonase-inhibiting protein
- R:
-
Resistance
- SA:
-
Salicylic acid
- Xoc:
-
Xanthomonas oryzae pv. oryzicola
- Xoo:
-
Xanthomonas oryzae pv. oryzae
References
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 6:43–51
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 157:599–607
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):216–220
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 47:974–980
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 100:10124–10128
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 31:1353–1359
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 4:49
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 323:1357–1360
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 155:589–602
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 325:998–1001
Ge X, Chu Z, Lin Y, Wang S (2006) A tissue culture system for different germplasms of indica rice. Plant Cell Rep 25:392–402
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 39:3491–3504
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 41:2177–2187
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 116:737–746
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):587–590
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 103:293–305
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 53:357–369
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 113:1233–1245
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 6:146
Kou Y, Wang S (2010) Broad-spectrum and durability: understanding of quantitative disease resistance. Curr Opin Plant Biol 13:181–185
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 323:1360–1363
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 55:316–324
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 115:429–441
Lin Y, Zhang Q (2005) Optimizing the tissue culture conditions for high efficiency transformation of indica rice. Plant Cell Rep 23:540–547
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):e113875
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 31:1173–1187
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 177:1152–1163
Nino-Liu DO, Ronald PC, Bogdanove AJ (2006) Xanthomonas oryzae pathovars: model pathogens of a model crop. Mol Plant Pathol 7:303–324
Poland JA, Balint-Kurti PJ, Wisser RJ, Pratt RC, Nelson RJ (2009) Shades of gray: the world of quantitative disease resistance. Trends Plant Sci 14:21–29
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 49:377–387
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 4:86–99
Skaminioti P, Gurr SJ (2009) Against the grain: safeguarding rice from blast disease. Trends Biotechnol 27:141–150
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 101:286–291
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 151:936–948
Thaler JS, Humphrey PT, Whiteman NK (2012) Evolution of jasmonate and salicylate signal crosstalk. Trends Plant Sci 17:260–270
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 102:779–786
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 87:181–191
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:e4603
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:e95751
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 31:877–885
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 102:15383–15388
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
Acknowledgments
This study was supported by the National Program of Transgenic Variety Development of China (2013ZX08009-004, 2014ZX08001-002), Foundation for the Author of National Excellent Doctoral Dissertation of PR China (Grant No. 201132), Shandong Provincial Natural Science Foundation, China (ZR2015CM004). Z.C. was funded by the Taishan Scholar Program of Shandong Province and by the Shandong Modern Agricultural Technology & Industry System.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical standard
The authors declare that the experiments comply with the laws of China.
Additional information
C. Feng and X. Zhang contributed equally to this work.
Electronic supplementary material
Below is the link to the electronic supplementary material.
425_2016_2480_MOESM1_ESM.pdf
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)
Rights and permissions
About this article
Cite this article
Feng, C., Zhang, X., Wu, T. et al. The polygalacturonase-inhibiting protein 4 (OsPGIP4), a potential component of the qBlsr5a locus, confers resistance to bacterial leaf streak in rice. Planta 243, 1297–1308 (2016). https://doi.org/10.1007/s00425-016-2480-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00425-016-2480-z