Abstract
Polygalacturonase-inhibiting proteins (PGIPs) are typically leucine-rich repeat (LRR) proteins that can inhibit the activity of fungal polygalacturonases (PGs). In this study, two new Ospgip genes, named Ospgip6 and Ospgip7 with consensus sequence of ten imperfect LRR motif located on rice chromosomes 8 and 9, were identified using BLAST analysis. Both of them appear to be extracellular glycoproteins. To have a global view of the dynamic gene expression pattern, seven Ospgip genes were first analyzed using the Affymetrix rice genome array data from online resource. All of these seven Ospgip genes showed variable expression patterns among tissues/organs. In order to further investigate the potential function of these Ospgip genes, the responses of Ospgip genes to the treatment of various phytohormones (abscisic acid, brassinosteroid, gibberellic acid, 3-indole acetic acid, jasmonic acid, kinetin, naphthalene acetic acid and salicylic acid) as well as fungal infection were analyzed by real-time PCR using time course array. Generally, all the Ospgip genes were slightly up-regulated in the indica rice cultivar Minghui 63 under GA3, KT and NAA treatments (except Ospgip2, which was down-regulated under KT treatment). In the japonica rice cultivar Zhonghua 11, Ospgip genes were regulated by most treatments with the response time variability. We also analyzed putative cis-elements in the promoter regions of Ospgip genes. This dataset provided a versatile resource to understand the regulatory network of Ospgip genes during the process of phytohormones treatment and fungal infection in the model monocotyledonous plant, rice, and could aid in the transgenic breeding against rice fungal diseases.
Key message
All the seven Ospgip genes showed variable expression patterns in Minghui 63 and their expressions were regulated by different phytohormone treatments or fungal infection in Minghui 63 and Zhonghua 11.
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Abbreviations
- ABA:
-
Abscisic acid
- BR:
-
Brassinosteroid
- GA3 :
-
Gibberellic acid
- IAA:
-
3-Indole acetic acid
- JA:
-
Jasmonic acid
- KT:
-
Kinetin
- NAA:
-
Naphthalene acetic acid
- SA:
-
Salicylic acid
- LRR:
-
Leucine-rich repeat
References
Aguero CB, Uratsu SL, Greve C, Powell ALT, 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
Brown RL, Kazan K, McGrath KC, Maclean DJ, Manners JM (2003) A role for the GCC-box in jasmonate-mediated activation of the PDF1.2 gene of Arabidopsis. Plant Physiol 132:1020–1032
Buza NL, Krinitsyna AA, Protsenko AA, Vartapetyan VV (2004) Role of the polygalacturonase inhibitor protein in the ripening of apples and their resistance to Monilia fructigena, a causative agent of fruit rot. Appl Biochem Microbiol 40:89–92
Chen J, Ouyang Y, Wang L, Xie W, Zhang Q (2009) Aspartic proteases gene family in rice: gene structure and expression, predicted protein features and phylogenetic relation. Gene 442:108–118
Cheng Q, Cao YZ, Pan HX, Wang MX, Huang MR (2008) Isolation and characterization of two genes encoding polygalacturonase-inhibiting protein from Populus deltoides. J Genet Genomics 35:631–638
D’Ovidio R, Mattei B, Roberti S, Bellincampi D (2004a) Polygalacturonases, polygalacturonase-inhibiting proteins and pectic oligomers in plant–pathogen interactions. BBA Proteins Proteomics 1696:237–244
D’Ovidio R, Raiola A, Capodicasa C, Devoto A, Pontiggia D, Roberti S, Galletti R, Conti E, O’Sullivan D, De Lorenzo G (2004b) Characterization of the complex locus of bean encoding polygalacturonase-inhibiting proteins reveals subfunctionalization for defense against fungi and insects. Plant Physiol 135:2424–2435
D’Ovidio R, Roberti S, Di Giovanni M, Capodicasa C, Melaragni M, Sella L, Tosi P, Favaron F (2006) The characterization of the soybean polygalacturonase-inhibiting proteins (Pgip) gene family reveals that a single member is responsible for the activity detected in soybean tissues. Planta 224:633–645
De Lorenzo G, Ferrari S (2002) Polygalacturonase-inhibiting proteins in defense against phytopathogenic fungi. Curr Opin Plant Biol 5:295–299
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
Federici L, Di Matte A, Fernandez-Recio J, Tsernoglou D, Cervone F (2006) Polygalacturonase inhibiting proteins: players in plant innate immunity? Trends Plant Sci 11:65–70
Ferrari S, Vairo D, Ausubel FM, Cervone F, De Lorenzo G (2003) Tandemly duplicated arabidopsis genes that encode polygalacturonase-inhibiting proteins are regulated coordinately by different signal transduction pathways in response to fungal infection. Plant Cell 15:93–106
Ferrari S, Galletti R, Vairo D, Cervone F, De Lorenzo G (2006) Antisense expression of the Arabidopsis thaliana AtPGIP1 gene reduces polygalacturonase-inhibiting protein accumulation and enhances susceptibility to Botrytis cinerea. Mol Plant Microbe Interact 19:931–936
Goldsbrough AP, Albrecht H, Stratford R (1993) Salicylic acid-inducible binding of a tobacco nuclear protein to a 10 bp sequence which is highly conserved amongst stress-inducible genes. Plant J Cell Mol Biol 3:563–571
Gomathi V, Gnanamanickam SS (2004) Polygalacturonase-inhibiting proteins in plant defence. Curr Sci 87:1211–1217
Hegedus DD, Li RG, Buchwaldt L, Parkin I, Whitwill S, Coutu C, Bekkaoui D, Rimmer SR (2008) Brassica napus possesses an expanded set of polygalacturonase inhibitor protein genes that are differentially regulated in response to Sclerotinia sclerotiorum infection, wounding and defense hormone treatment. Planta 228:241–253
Idnurm A, Howlett B (2001) Pathogenicity genes of phytopathogenic fungi. Mol Plant Pathol 2:241–255
Jang SH, Lee B, Kim C, Kim SJ, Yim J, Han JJ, Lee S, Kim SR, An G (2003) The OsFOR1 gene encodes a polygalacturonase-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
Janni M, Sella L, Favaron F, Blechl AE, De Lorenzo G, D’Ovidio R (2008) The expression of a bean PGIP in transgenic wheat confers increased resistance to the fungal pathogen Bipolaris sorokiniana. Mol Plant Microbe Interact 21:171–177
Joubert DA, Slaughter AR, Kemp G, Becker JVW, Krooshof GH, Bergmann C, Benen J, Pretorius IS, Vivier MA (2006) The grapevine polygalacturonase-inhibiting protein (VvPGIP1) reduces Botrytis cinerea susceptibility in transgenic tobacco and differentially inhibits fungal polygalacturonases. Transgenic Res 15:687–702
Joubert DA, Kars I, Wagemakers L, Bergmann C, Kemp G, Vivier MA, van Kan JAL (2007) A polygalacturonase-inhibiting protein from grapevine reduces the symptoms of the endopolygalacturonase BcPG2 from Botrytis cinerea in Nicotiana benthamiana leaves without any evidence for in vitro interaction. Mol Plant Microbe Interact 20:392–402
Juge N (2006) Plant protein inhibitors of cell wall degrading enzymes. Trends Plant Sci 11:359–367
Kemp G, Bergmann CW, Clay R, Van der Westhuizen AJ, Pretorius ZA (2003) Isolation of a polygalacturonase-inhibiting protein (PGIP) from wheat. Mol Plant Microbe Interact 16:955–961
Kim JK, Cao J, Wu R (1992) Regulation and interaction of multiple protein factors with the proximal promoter regions of a rice high pI alpha-amylase gene. Mol Genet Genomics 232:383–393
Kumar K, Poovannan K, Nandakumar R, Thamilarasi K, Geetha C, Jayashree N, Kokiladevi E, Raja J, Samiyappan R, Sudhakar D (2003) A high throughput functional expression assay system for a defence gene conferring transgenic resistance on rice against the sheath blight pathogen, Rhizoctonia solani. Plant Sci 165:969–976
Leckie F, Mattei B, Capodicasa C, Hemmings A, Nuss L, Aracri B, De Lorenzo G, Cervone F (1999) The specificity of polygalacturonase-inhibiting protein (PGIP): a single amino acid substitution in the solvent-exposed beta-strand/beta-turn region of the leucine-rich repeats (LRRs) confers a new recognition capability. EMBO J 18:2352
Lescot M, Dehais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouze P, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327
Li RG, Rimmer R, Yu M, Sharpe AG, Seguin-Swartz G, Lydiate D, Hegedus DD (2003) Two Brassica napus polygalacturonase inhibitory protein genes are expressed at different levels in response to biotic and abiotic stresses. Planta 217:299–308
Livak K, Schmittgen T (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−[Delta][Delta] CT method. Methods 25:402–408
Ma K, Xiao J, Li X, Zhang Q, Lian X (2009) Sequence and expression analysis of the C3HC4-type RING finger gene family in rice. Gene 444:33–45
Manfredini C, Sicilia F, Ferrari S, Pontiggia D, Salvi G, Caprari C, Lorito M, De Lorenzo G (2005) Polygalacturonase-inhibiting protein 2 of Phaseolus vulgaris inhibits BcPG1, a polygalacturonase of Botrytis cinerea important for pathogenicity, and protects transgenic plants from infection. Physiol Mol Plant Pathol 67:108–115
McElroy D, Rothenberg M, Wu R (1990) Structural characterization of a rice actin gene. Plant Mol Biol 14:163–171
Mehli L, Schaart JG, Kjellsen TD, Tran DH, Salentijn EMJ, Schouten HJ, Iversen TH (2004) A gene encoding a polygalacturonase-inhibiting protein (PGIP) shows developmental regulation and pathogen-induced expression in strawberry. New Phytol 163:99–110
Nagao RT, Goekjian VH, Hong JC, Key JL (1993) Identification of protein-binding DNA sequences in an auxin-regulated gene of soybean. Plant Mol Biol 21:1147–1162
Nayidu N, Wang L, Xie W, Zhang C, Fan C, Lian X, Zhang Q, Xiong L (2008) Comprehensive sequence and expression profile analysis of PEX11 gene family in rice. Gene 412:59–70
Oelofse D, Dubery IA, Meyer R, Arendse MS, Gazendarn I, Berger DK (2006) Apple polygalacturonase inhibiting protein1 expressed in transgenic tobacco inhibits polygalacturonases from fungal pathogens of apple and the anthracnose pathogen of lupins. Phytochemistry 67:255–263
Powell A, van Kan J, ten Have A, Visser J, Greve L, Bennett A, Labavitch J (2000) Transgenic expression of pear PGIP in tomato limits fungal colonization. Mol Plant Microbe Interact 13:942–950
Richter A, de Kathen A, de Lorenzo G, Briviba K, Hain R, Ramsay G, Jacobsen HJ, Kiesecker H (2006) Transgenic peas (Pisum sativum) expressing polygalacturonase inhibiting protein from raspberry (Rubus idaeus) and stilbene synthase from grape (Vitis vinifera). Plant Cell Rep 25:1166–1173
Rushton PJ, Torres JT, Parniske M, Wernert P, Hahlbrock K, Somssich IE (1996) Interaction of elicitor-induced DNA-binding proteins with elicitor response elements in the promoters of parsley PR1 genes. EMBO J 15:5690–5700
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406
Shanmugam V (2005) Role of extracytoplasmic leucine rich repeat proteins in plant defence mechanisms. Microbiol Res 160:83–94
Shen Q, Uknes SJ, Ho TH (1993) Hormone response complex in a novel abscisic acid and cycloheximide-inducible barley gene. J Biol Chem 268:23652–23660
Sicilia F, Fernandez-Recio J, Caprari C, De Lorenzo G, Tsernoglou D, Cervone F, Federici L (2005) The polygalacturonase-inhibiting protein PGIP2 of Phaseolus vulgaris has evolved a mixed mode of inhibition of endopolygalacturonase PG1 of Botrytis cinerea. Plant Physiol 139:1380–1388
Song KH, Nam YW (2005) Genomic organization and differential expression of two polygalacturonase-inhibiting protein genes from Medicago truncatula. J Plant Biol 48:467–478
Straub PF, Shen Q, Ho TD (1994) Structure and promoter analysis of an ABA- and stress-regulated barley gene, HVA1. Plant Mol Biol 26:617–630
Sturn A, Quackenbush J, Trajanoski Z (2002) Genesis: cluster analysis of microarray data. Bioinformatics 18:207
Sutliff TD, Lanahan MB, Ho TH (1993) Gibberellin treatment stimulates nuclear factor binding to the gibberellin response complex in a barley alpha-amylase promoter. Plant cell 5:1681–1692
Szankowski I, Briviba K, Fleschhut J, Schonherr J, Jacobsen HJ, Kiesecker H (2003) Transformation of apple (Malus domestica Borkh.) with the stilbene synthase gene from grapevine (Vitis vinifera L.) and a PGIP gene from kiwi (Actinidia deliciosa). Plant Cell Rep 22:141–149
Tamura M, Gao M, Tao R, Labavitch JM, Dandekar AM (2004) Transformation of persimmon with a pear fruit polygalacturonase inhibiting protein (PGIP) gene. Sci Hortic (Amsterdam) 103:19–30
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596
Acknowledgments
This research was funded by the National Natural Science Foundation of China, the National High Technology Research and Development Program of China (863 Program) and the National Program on Research and Development of Transgenic Plants. We would like to thank Dr. M.W. Szczerba for helpful discussion and comments.
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Communicated by Y. Lu.
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Appendix: accession numbers
Appendix: accession numbers
Protein accession numbers
AdPGIP (Actinidia deliciosa, NCBI ID: CAA88846); AtPGIP1-2 (Arabidopsis thaliana, NCBI ID: AAF69827, AAF69828); BnPGIP1-3, 5-17 (Brassica napus, NCBI ID: ABX46548-ABX46563); CmPGIP (Chamaebatiaria millefolium, NCBI ID: AAK43398); CsPGIP (Citrus sinensis, NCBI ID: CAA69910); EgPGIP (Eucalyptus grandis, NCBI ID: AAF22248); GmPGIP1-4 (Glycine max, NCBI ID: CAI99392–CAI99395); HaPGIP (Helianthus annuus, NCBI ID: ABW89508); OsPGIP1-7(Oryza sativa, NCBI ID: CAJ55691, CAJ55692, CAJ55693, CAJ55694, AAO17320, NP_001062185, EEE69955); PaPGIP (Phaseolus acutifolius, NCBI ID: CAR92533); PcPGIP (Pyrus communis, NCBI ID: AAA33865); PpPGIP (Pyrus pyrifolia, NCBI ID: ACY56891); PvPGIP1-4 (Phaseolus vulgaris, NCBI ID: CAH10215–CAH10218); RsPGIP (Rhodotypos scandens, NCBI ID: AAK43455); SbPGIP1-2 (Sorghum bicolor, NCBI ID: XP_002463048, XP_002439097); SlPGIP (Solanum lycopersicum, NCBI ID: AAA53547); SpPGIP (Solanum palustre, NCBI ID: AAT77428); TaPGIP1-2 (Triticum aestivum, NCBI ID: CAJ55695, CAJ55696); VvPGIP (Vitis vinifera, NCBI ID: AAM74142); ZmPGIP1-2 (Zea mays, NCBI ID: NP_001147517, NP_001150670).
Nucleotide accession numbers
Atpgip1-2 (Arabidopsis thaliana, NCBI ID: AF229249, AF229250); Bnpgip1-3, 5-17 (Brassica napus, NCBI ID: EU142023-EU142038); Hapgip (Helianthus annuus, NCBI ID: EU112834); Ospgip1-6 (Oryza sativa, NCBI ID: AM180652–AM180655, NM_001066567, NM_001068720); Rspgip (Rhodotypos scandens, NCBI ID: AF196946); Sbpgip1-2 (Sorghum bicolor, NCBI ID: XM_002463003, NM_001157198); Zmpgip1-2 (Zea mays, NCBI ID: NM_001154045, NM_001157198).
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Lu, L., Zhou, F., Zhou, Y. et al. Expression profile analysis of the polygalacturonase-inhibiting protein genes in rice and their responses to phytohormones and fungal infection. Plant Cell Rep 31, 1173–1187 (2012). https://doi.org/10.1007/s00299-012-1239-7
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DOI: https://doi.org/10.1007/s00299-012-1239-7