Combinative effects of a bacterial type-III effector and a biocontrol bacterium on rice growth and disease resistance

Haiying Ren1, Ganyu Gu1, Juying Longa1, Qian Yin1, Tingquan Wu1, Tao Song1, Shujian Zhang1, Zhiyi Chen2, Hansong Dong1
1Key Laboratory of Monitoring and Management of Plant Pathogens and Insect Pests, Ministry of Agriculture of China, and Department of Plant Pathology, Nanjing Agricultural University, Nanjing, China
2Institute of Plant Protection, Jiangsu-Provincial Academy of Agricultural Sciences, Nanjing, China

Tóm tắt

Expression of HpaGXoo, a bacterial type-III effector, in transgenic plants induces disease resistance. Resistance also can be elicited by biocontrol bacteria. In both cases, plant growth is often promoted. Here we address whether biocontrol bacteria and HpaGXoo can act together to provide better results in crop improvement. We studied effects ofPseudomonas cepacia on the rice variety R109 and the hpaGXoo-expressing rice line HER1. Compared to R109, HER1 showed increased growth, grain yield, and defense responses toward diseases and salinity stress. Colonization of roots byP. cepacia caused 20% and 13% increase, in contrast to controls, in root growth of R109 and HER1. Growth of leaves and stems also increased in R109 but that of HER 1 was inhibited. WhenP. cepacia colonization was subsequent to plant inoculation withRhizoctonia solani, a pathogen that causes sheath blight, the disease was less severe than controls in both R109 and HER1; HER1, nevertheless, was more resistant, suggesting thatP.cepacia and HpaGXoo cooperate in inducing disease resistance. Several genes that critically regulate growth and defense behaved differentially in HER1 and R109 while responding toP. cepacia. In R109 leaves, theOsARF1 gene, which regulates plant growth, was expressed in consistence with growth promotion byP. cepacia. Inversely,OsARF1 expression was coincident with inhibition in growth of HER1 leaves. In both plants, the expression ofOsEXP1, which encodes an expansin protein involved in plant growth, was concomitant with growth promotion in leaves instead of roots, in response toP. cepacia. We also studiedOsMAPK, a gene that encodes a mitogen-activated protein kinase and controls defense responses toward salinity and infection by pathogens in rice. In response toP. cepacia, an early expression ofOsMAPK was coincident with R109 resistance to the disease, while HER1 expressed the gene similarly whetherP. cepacia was present or not. Evidently,P. cepacia and GXoo-gene mediated resistance may act differently in rice growth and resistance. Whereas combinative effectsof P. cepacia and HpaGXoo in disease resistance have a great potential in agricultural use, it is interesting to study mechanisms that underlie interactions involving biocontrol bacteria, type-III effectors and pathogens.

Từ khóa


Tài liệu tham khảo

Alfano J R and Collmer A 2004 Type III secretion system effector proteins: double agents in bacterial disease and plant defense;Annu. Rev. Phytopathol. 42 385–414

Belfield E J, Ruperti B, Roberts JA and McQueen-Mason S 2005 Changes in expansin activity and gene expression during ethylene-promoted leaflet abscission inSambucus nigra;J. Exp. Bot. 56 817–823

Berberich T, Sugawara K, Harada M and Kusano T 1995 Molecular cloning, characterization and expression of an elongation factor la gene in maize;Plant Mol. Biol. 28 611–615

Bostock R M 2005 Signal crosstalk and induced resistance: straddling the line between cost and benefit;Annu. Rev. Phytopathol. 43 545–480

Chen Z Y and Mew TW 1998 Relationship between the colonization, concentration and spray timing of antagonistic bacteria and sheath blight of rice;Jiang Su J. Agric. Sci. 14 31–35

Clark M S 1997Plant molecular biology, a laboratory manual (Berlin: Springer)

Dangl J L and Jones D G 2001 Plant pathogens and integrated defense responses to infection;Nature(London) 411 826–833

Dixon R A 2001 Natural products and plant disease resistance;Nature (London) 411 843–847

Dong H, Delaney T P, Bauer D W and Beer S V 1999 Harpin induces disease resistance inArabidopsis through the systemic acquired resistance pathway mediated by salicylic acid and theNIM1 gene;Plant J. 20 207–215

Dong X, Li X, Zhang Y, Fan W, Kinkema M and Clarke J 2001 Regulation of systemic acquired resistance by NPR1 and its partners;Novartis Found. Symp. 236 165–173

Dong H P, Peng J L, Bao Z L, Meng X, Bonasera J M, Chen G, Beer S V and Dong H 2004 Downstream divergence of the ethylene signaling pathway for harpin-stimulatedArabidopsis growth and insect defense;Plant Physiol. 136 3628–3638

Dong H P, Yu H Q, Bao Z L, Guo X, Peng J, Yao Z, Chen G, Qu S and Dong H 2005 The ABI2-dependent abscissic acid signalling controls HrpN-induced drought tolerance inArabidopsis;Planta 211 313–327

Gerhardt P, Murray R G E, Costilow R N, Nester E W, Wood W A, Krieg N R and Phillips G B 1981Manual of methods for general bacteriology (Washington DC: USA American Society Microbiol)

Gielen S, Aerts R and Seels B 2004 Biocontrol agents ofBotrytis cinerea tested in climate chambers by making artificial infection on tomato leaves;Commun. Agric. Appl. Biol. Sci. 69 631–639

Jefferson R A, Kavanagh T A and Bevan M W 1987 GUS fusions: Β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants;EMBO J. 6 3901–3907

Johri B N, Sharma A and Virdi J S 2003 Rhizobacterial diversity in India and its influence on soil and plant health;Adv. Biochem. Eng. Biotechnol. 84 49–89

Kim J F and Beer S V 2000hrp genes and harpins ofErwinia amylovora: a decade of discovery; inFire blight and its causative agent, Erwinia amylovora (ed.) J L Vanneste (Wallingford, UK: CAB International) pp 141–162

Kim J G, Park B K, Yoo C H, Jeon E, Oh J and Hwang I 2003 Characterization of theXanthomonas axonopodis pv.glycines HpaG pathogenicity island;J. Bacteriol. 185 3155–3166

Klement Z, Rudolph K and Sands D C 1990Methods in phytobacteriology (AkadĒmiai KiadŌ, Budapest) pp 106–111

Lazo G R, Stein P A and Ludwig R A 1991 A DNA transformation-competentArabidopsis genomic library inAgrobacterium;Biotechnology. 9 963–967

Lee J, Klessig D F and Nurnberger T 2001 A harpin binding site in tobacco plasma membranes mediates activation of the pathogenesis-related geneHIN1 independent of extracellular calcium but dependent on mitogen-activated protein kinase activity;Plant Cell 13 1079–1093

Li Y, Jones L and McQueen-Mason S 2003 Expansins and cell growth;Curr. Opin. Plant Biol. 6 603–610

Maleck K and Dietrich R A 1999 Defense on multiple fronts: how do plants cope with diverse enemies?;Trends Plant Sci. 4 215–219

Nagarajkumar M, Jayaraj J, Muthukrishnan S, Bhaskaran R and Velazhahan R 2005 Detoxification of oxalic acid byPseudomonas fluorescens strain pfMDU2: implications for the biological control of rice sheath blight caused byRhizoctonia solani;Microbiol. Res. 160 291–298

Nandakumar R, Babu S, Viswanathan R, Raguchander T and Samiyappan R 2001 Induction of systemic resistance in rice against sheath blight disease byPseudomonas fluorescens;Soil Biol. Biochem. 33 603–612

Noel L, Thieme F, Nennstiel D and Bonas U 2002 Two novel type III-secreted proteinsof Xanthomonas campestris pv.vesicatoria are encoded within the HpaG pathogenicity island;J. Bacteriol. 184 1340–1348

Peng J, Dong H, Dong H P, Delaney T P, Bonaserab J M and Beer S V 2003 Harpin-elicited hypersensitive cell death and pathogen resistance require theNDR1 and EDS1 genes;Physiol. Mol. Plant Pathol. 62 317–326

Peng J, Bao Z, Li P, Chen, G, Wang J and Dong H 2004a HarpinXoo and its functional domains activate pathogen-inducible plant promoters inArabidopsis;Acta. Bot. Sinica 46 1083–1090

Peng J, Bao Z, Ren H, Wang J and Dong H 2004b Expression of harpinXoo in transgenic tobacco induces pathogen defense in the absence of hypersensitive response;Phytopathology 94 1048–1055

Pieterse C M, van Wees S C, Hoffland E, van Pelt J A and van Loon L C 1996 Systemic resistance inArabidopsis induced by biocontrol bacteria is independent of salicylic acid accumulation and pathogenesis-related gene expression;Plant Cell 8 1225–1237

Raghothama K G, Maggio A, Narasimhan M L, Kononowicz A K, Wang G, D’Urzo M P, Hasegawa P M and Bressan R A 1997 Tissue-specific activation of the osmotin gene by ABA, C2H4 and NaCl involves the same promoter region;Plant Mol. Biol. 34 393–402

Rohilla R, Singh U S and Singh R L 2002 Mode of action of acibenzolar-S-methyl against sheath blight of rice, caused byRhizoctonia solani Kuhn;Pest Manag. Sci. 58 63–69

Romanenko V M and Alimov D M 2000 Ability of representatives ofPantoea agglomerans, as well asBacillus subtilis and somePseudomonas species to suppress the development of phytopathgenic bacteria and micromycetes in regulating plant growth;Mikrobiol. Z. 62 29–37

Shi Y H, Zhu S W, Mao X Z, Feng J X, Qin Y M, Zhang L, Cheng J, Wei L P, Wang Z Y and Zhu Y X 2006 Transcriptome profiling, molecular biological, and physiological studies reveal a major role for ethylene in cotton fiber cell elongation;Plant Cell 18 651–664

Staskawicz B J, Mudgett M B, Dangl J L and Galan J E 2001 Common and contrasting themes of plant and animal diseases;Science 292 2285–2289

Strobel R N, Gopalan J S, Kuc J A and He S Y 1996 Induction of systemic acquired resistance in cucumber byPseudomonas syringae pv.syringae 61 HrpZPss protein;Plant J. 9 431–439

Stuiver M H and Custers J H H V 2001 Engineering disease resistance in plants;Nature (London) 411 865–868

Thomas J C and Bohnert H J 1993 Salt stress perception and plant growth regulators in the halophyteMesembryanthemum crystallinum;Plant Physiol. 103 1299–1304

Tjamos S E 2005 Induction of resistance toVerticillium dahliae inArabidopsis thaliana by the biocontrol agent K-165 and pathogenesis-related proteins gene expression;Mol. Plant-Microbe Interact. 18 555–561

Vijayan P, Shockey J, Levesque C A, Cook R J and Browse J 1998 A role for jasmonate in pathogen defenseof Arabidopsis;Proc. Natl. Acad. Sci. USA 95 7209–7214

Vreeburg R A, Benschop J J, Peeters A J, Colmer T D, Ammerlaan A H, Staal M, Elzenga T M, Staals R H, Darley C P, McQueen-Mason S J and Voesenek L A 2005 Ethylene regulates fast apoplastic acidification and expansin α transcription during submergence-induced petiole elongation inRumex palustris;Plant J. 43 597–610

Waller F, Furuya M and Nick P 2002OsARF1, an auxin response factor from rice, is auxin-regulated and classifies as a primary auxin responsive gene;Plant Mol. Biol. 50 415–425

Wang Z and Tan G 2005 Effects of fungicide on temporal and spatial niches ofRhizoctonia solani;Ying Yong Sheng Tai Xue Bao 16 1493–1496

Wen W and Wang J 2001 Cloning and expressing a harpin gene fromXanthomonas oryzaepv. oryzae;Acta. Phytopathol. Sinica 31 296–300

Xiong L and Yang Y 2003 Disease resistance and abiotic stress tolerance in rice are inversely modulated by an abscisic acid-inducible mitogen-activated protein kinase;Plant Cell 15 745–759

Xu D, Duan X, Wang B, Hong B, Ho T and Wu R 1996 Expression of a late embryogenesis abundant protein gene,HVA1, from barley confers tolerance to water deficit and salt stress in transgenic rice;Plant Physiol. 110 249–257

Zasloff M 2001 Antimicrobial peptides of multicellular organisms;Nature (London) 415 389–395

Zhang Y and Shih D S 2006 Isolation of an osmotin-like protein gene from strawberry and analysis of the response of this gene to abiotic stresses;J. Plant Physiol. (Epub ahead of print, April 4, 2006)