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Salicylic acid suppression of clubroot in broccoli (Brassicae oleracea var. italica) caused by the obligate biotroph Plasmodiophora brassicae

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Abstract

The obligate soil-borne biotroph Plasmodiophora brassicae has a significant economic impact on Brassicaceae crops. The pathogen severely disrupts the roots by inducing the production of galls which leads to malformation and reduced growth of the roots and a reduced ability to take up water and nutrients. Control of P. brassicae is difficult because it has a number of survival and dissemination strategies that involve both motile and resting stages that need to be targeted by any control agent. We investigated, under controlled conditions and in glasshouse and field experiments, the potential of salicylic acid (SA), a key phytohormone, that is required for defence against certain biotic and abiotic stresses, to reduce infection by P. brassicae in broccoli (Brassicae oleracea var. italica). Under controlled conditions in a growth cabinet exogenous application of SA to roots resulted in its transport systemically to the leaves where it promoted the up-regulation of the pathogenesis related genes PR-1 and PR-2 in an SAR-like response as early as 24 h post-treatment. Concentrations of SA >20 mM reduced significantly both shoot and root weights when applied exogenously but lower concentrations had little measureable effect on plant growth. When SA was applied to plants above 5 mM there was a significant reduction (25–65 %) in gall formation 6 weeks post-inoculation with P. brassicae, indicating that the pathogen was being controlled by the addition of SA. A combination of SA and JA was also shown to reduce severity (25–35 %) of disease associated with P. brassicae. These findings indicate that there may be SA inducible mechanisms in B. oleracea that if fine-tuned could provide enhanced resistance to clubroot disease.

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References

  • Agarwal A, Kaul V, Faggian R, Cahill DM (2009) Development and use of a model system to monitor clubroot disease progression with an Australian field population of Plasmodiophora brassicae. Australas Plant Pathol 38:120–127

    Article  Google Scholar 

  • Agarwal A, Kaul V, Faggian R, Rookes JE, Ludwig-Müller J, Cahill DM (2011) Analysis of global host gene expression during the primary phase of the Arabidopsis thaliana-Plasmodiophora brassicae interaction. Funct Plant Biol 38:462–478

    CAS  Google Scholar 

  • Ali Z, Smith I, Guest DI (2000) Combinations of potassium phosphonate and Bion (acibenzolar-S-methyl) reduce root infection and dieback of Pinus radiata, Banksia integrifolia and Isopogon cuneatus caused by Phytophthora cinnamomi. Australas Plant Pathol 29:59–63

    Article  Google Scholar 

  • Allardyce JA, Rookes JE, Cahill DM (2012) Defining plant resistance to Phytophthora cinnamomi: a standardized approach to assessment. J Phytopathol 160:269–276

    Article  Google Scholar 

  • Argueso CT, Ferreira FJ, Epple P, To JPC, Hutchison CE, Schaller GE, Dangl JL, Kiebler JJ (2012) Two-component elements mediate interactions between cytokinin and salicylic acid in plant immunity. PLoS Genet 8(1):e1002448. doi:10.1371/journal.pgen.1002448

    Article  PubMed  CAS  Google Scholar 

  • Birkenbihl RP, Diezel C, Somssich IE (2012) Arabidopsis WRKY33 is a key transcriptional regulator of hormonal and metabolic responses toward Botrytis cinerea infection. Plant Physiol 159:266–285

    Article  PubMed  CAS  Google Scholar 

  • Cao T, Srivastava S, Rahman MH, Kav NNV, Hotte N, Deyholol MK, Strelkov SE (2008) Proteome-level changes in the roots of Brassica napus as a result of Plasmodiophora brassicae infection. Plant Sci 174:97–115

    Article  CAS  Google Scholar 

  • Catinot J, Buchala A, Abou-Mansour E, Metraux J-P (2008) Salicylic acid production in response to biotic and abiotic stress depends on isochorismate in Nicotania benthamiana. FEBS Lett 582:473–478

    Article  PubMed  CAS  Google Scholar 

  • Colson-Hanks ES, Deverall BJ (2000) Effect of 2, 6-dichloroisonicotinic acid, its formulation materials and benzothiadiazole on systemic resistance to alternaria leaf spot in cotton. Plant Pathol 49:171–178

    Article  CAS  Google Scholar 

  • De Meyer G, Capieau K, Audenaert K, Buchala A, Métraux J-P, Höfte M (1999) Nanogram amounts of salicylic acid produced by the rhizobacterium Pseudomonas aeruginosa 7NSK2 activates the systemic acquired resistance pathway in bean. Mol Plant Microbe Interact 12:450–458

    Article  PubMed  Google Scholar 

  • Dixon GR (2009a) The occurrence and economic impact of Plasmodiophora brassicae and clubroot disease. J Plant Growth Regul 28:194–202

    Article  CAS  Google Scholar 

  • Dixon GR (2009b) Plasmodiophora brassicae in its environment. J Plant Growth Regul 28:212–228

    Article  CAS  Google Scholar 

  • Donald EC, Porter IJ (2009) Integrated control of clubroot. J Plant Growth Regul 28:289–303

    Article  CAS  Google Scholar 

  • Donald EC, Porter IJ, Lancaster RA (2001) Band incorporation of fluazinam (Shirlan) into soil to control clubroot of vegetable brassica crops. Aust J Exp Agric 41:1223–1226

    Article  CAS  Google Scholar 

  • Donald EC, Lawrence JM, Porter IJ (2004) Influence of particle size and application method of the efficacy of calcium cyanamide for control of clubroot of vegetable brassicas. Crop Prot 23:297–303

    Article  CAS  Google Scholar 

  • Edgar CI, McGrath KC, Dombrecht B, Manners JM, Maclean DC, Schenk PM, Kazan K (2006) Salicylic acid mediates resistance to the vascular wilt pathogen Fusarium oxysporum in the model host Arabidopsis thaliana. Australas Plant Pathol 35:581–591

    Article  CAS  Google Scholar 

  • El Oirdi M, El Rahman TA, Rigano L, El Hadrami A, Rodriguez MC, Daayf F, Vojnov A, Bouarab K (2011) Botrytis cinerea manipulates the antagonistic effects between immune pathways to promote disease development in tomato. Plant Cell 23:2405–2421

    Article  PubMed  Google Scholar 

  • El-Tayeb MA, El-Enany AE, Ahmed NL (2006) Salicylic acid induced adaptive response to copper stress in sunflower (Helianthus annuus L.). Plant Growth Regul 50:191–199

    Article  CAS  Google Scholar 

  • Fariduddin Q, Hayat S, Ahmad A (2003) Salicylic acid influences net photosynthetic rate, carboxylation efficiency, nitrate reductase activity, and seed yield in Brassica juncea. Photosynthetica 41:281–284

    Article  CAS  Google Scholar 

  • Fragniére C, Serrano M, Abou-Mansour E, Métraux J-P, L’Haridon F (2011) Salicylic acid and its location in response to biotic and abiotic stress. FEBS Lett 585:1847–1852

    Article  PubMed  Google Scholar 

  • Fugate KK, Ferrareze JP, Bolton MD, Deckard EL, Campbell LG (2012) Postharvest jasmonic acid treatment of sugarbeet roots reduces rot due to Botrytis cinerea, Penicillium claviforme and Phoma betae. Postharvest Biol Tech 65:1–4

    Article  CAS  Google Scholar 

  • Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227

    Article  PubMed  CAS  Google Scholar 

  • Grellet-Bournonville CF, Martinez-Zamora MG, Castagnaro AP (2012) Temporal accumulation of salicylic acid activates the defence response against Colletotrichum in strawberry. Plant Physiol Biochem 54:10–16

    Article  PubMed  CAS  Google Scholar 

  • Halim VA, Eschen-Lippold L, Altmann S, Birschwilks M, Scheel D, Rossahl S (2007) Salicylic acid is important for basal defence of Solanum tuberosum against Phytophthora infestans. Mol Plant Microbe Interact 20:1346–1352

    Article  PubMed  CAS  Google Scholar 

  • Hayat S, Ali B, Ahmad A (2007) Salicylic Acid: Biosynthesis, metabolism and physiological role in plants. In: Hayat S, Ahmad H (eds) Salicylic Acid: A plant hormone. Springer, Netherlands, pp 1–14

    Chapter  Google Scholar 

  • Horváth E, Szalai G, Janda T (2007) Induction of abiotic stress tolerance by salicylic acid signalling. J Plant Growth Regul 26:290–300

    Article  Google Scholar 

  • Hukkanen AT, Kokko HI, Buchala AJ, McDougall GJ, Stewart D, Karenlampi SO, Karjalainen RO (2007) Benzothiadiazole induces the accumulation of phenolics and improves resistance to powdery mildew in strawberries. J Agric Food Chem 55:1862–1870

    Article  PubMed  CAS  Google Scholar 

  • Ingram DS, Tommerup IC (1972) The life history of Plasmodiophora brassicae Woron. Proc R Soc London, Ser B 180(1058):103–112

    Article  Google Scholar 

  • Janda T, Szalai G, Tari I, Paldi E (1999) Hydroponic treatment with salicylic acid decreases the effects of chilling injury in maize (Zea mays L.) plants. Planta 208:175–180

    Article  CAS  Google Scholar 

  • Kinkema M, Fan W, Dong X (2000) Nuclear localization of NPR1 is required for activation of PR gene expression. Plant Cell 12:2339–2350

    PubMed  CAS  Google Scholar 

  • Kumar D, Patro S, Ghosh J, Das A, Maiti IB, Dey N (2012) Development of a salicylic acid inducible minimal sub-genomic transcript promoter from Figwort mosaic virus with enhanced root- and leaf-activity using TGACG motif rearrangement. Gene 503:36–47

    Article  PubMed  CAS  Google Scholar 

  • Kunkel BN, Brooks DM (2002) Cross talk between signalling pathways in pathogen defense. Curr Opin Plant Biol 5:325–331

    Article  PubMed  CAS  Google Scholar 

  • Lee J, Nam J, Park HC, Na G, Miura K, Jin JB, Yoo CY, Baek D, Kim DH, Jeong JC, Kim D, Lee SY, Salt DE, Mengiste T, Gong Q, Ma S, Bohnert HJ, Kwak S-S, Bressan RA, Hasegawa PM, Yun D-J (2006) Salicylic acid-mediated innate immunity in Arabidopsis is regulated by SIZ1 SUMO E3 ligase. Plant J 49:79–90

    Article  PubMed  Google Scholar 

  • Li X, Zhang Y, Clarke JD, Li Y, Dong X (1999) Identification and cloning of a negative regulator of systemic acquired resistance, SIN1, through a screen for suppressors of npr1-1. Cell 98:329–339

    Article  PubMed  CAS  Google Scholar 

  • Livak KJ, Schmittgen TG (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔ C T Method. Methods 25:402–408

    Article  PubMed  CAS  Google Scholar 

  • Ludwig-Müller J, Schuller A (2008) What can we learn from clubroots: alterations in host roots and hormone homeostasis caused by Plasmodiophora brassicae. Eur J Plant Pathol 121:291–302

    Article  Google Scholar 

  • Makandar R, Nalam V, Chaturvedi R, Jeannotte R, Sparks AA, Shah J (2010) Inovlement of salicylate and jasmonate signalling pathways in Arabidopsis interaction with Fusarium graminearum. Mol Plant Microbe Interact 23:861–870

    Article  PubMed  CAS  Google Scholar 

  • Mondal AH, Nehl DB, Allen SJ (2005) Acibenzolar-S-methyl induces systemic resistance in cotton against black root rot caused by Thielaviopsis basicola. Australas Plant Pathol 34:499–507

    Article  CAS  Google Scholar 

  • Niki T, Mitsuhara I, Seo S, Ohtsubo N, Ohashi Y (1998) Antagonistic effect of salicylic acid and jasmonic acid on the expression of pathogenesis-related (PR) Protein genes in wounded mature tobacco leaves. Plant Cell Physiol 39:500–507

    Article  CAS  Google Scholar 

  • Ogawa T, Ara T, Aoki K, Suzuki H, Shibata D (2010) Transient increases in salicylic acid and its glucose conjugates after wounding in Arabidopsis leaves. Plant Biotechnol 27:205–209

    Article  CAS  Google Scholar 

  • Osaki K, Fujiyama S, Nakayama A, Shimizu Y, Ito S, Tanaka S (2008) Relation between pathogenicity and genetic variation within Plasmodiophora brassicae. J Genet Plant Pathol 74:281–288

    Article  CAS  Google Scholar 

  • Pan X, Welti R, Wang X (2010) Quantitative analysis of major plant hormones in crude extracts by high-performance liquid chromatography-mass spectrometry. Nature 5:986–992

    CAS  Google Scholar 

  • Pancheva TV, Popova LP, Uzunova AN (1996) Effects of salicylic acid on growth and photosyntheis in barley plants. J Plant Physiol 149:57–63

    Article  CAS  Google Scholar 

  • Poór P, Gémes K, Horváth F, Szepesi Á, Simon ML, Tari I (2011) Salicylic acid treatment via the rooting medium interferes with stomatal response, CO2 fixation rate and carbohydrate metabolism in tomato, and decreases harmful effects of subsequent salt stress. Plant Biol 13:105–114

    Article  PubMed  Google Scholar 

  • Rivas-San Vicente M, Plasencia J (2011) Salicylic acid beyond defence: its role in plant growth and development. J Exp Bot 62:3321–3338

    Article  PubMed  CAS  Google Scholar 

  • Siemens J, González M-C, Wolf S, Hofmann C, Griener S, Du Y, Rausch T, Roitsch T, Ludwig-Müller J (2011) Extracelleular invertase is involved in the regulation of clubroot disease in Arabidopsis thaliana. Mol Plant Pathol 12:247–262

    Article  PubMed  CAS  Google Scholar 

  • Spoel SH, Dong X (2012) How do plants achieve immunity? Defence without specialized immune cells. Nature 12:89–100

    CAS  Google Scholar 

  • Spoel SH, Johnson JS, Dong X (2007) Regulation of tradeoffs between plant defenses against pathogens with different lifestyles. Proc Natl Acad Sci U S A 104:18842–18847

    Article  PubMed  CAS  Google Scholar 

  • Strobel NE, Kuc A (1995) Chemical and biological inducers of systemic acquired resistance to pathogens protect cucumber and tobacco from damage caused by paraquat and cupric chloride. Phytopathology 85:1306–1310

    Article  CAS  Google Scholar 

  • Tsuda K, Sato M, Stoddard T, Glazebrook J, Katagiri F (2009) Network properties of robust immunity in plants. PLoS Genet 5:e1000772. doi:10.1371/journal.pgen.1000772

    Article  PubMed  Google Scholar 

  • Vlot AC, Dempsey D’MA, Klessig DF (2009) Salicylic acid, a multifaceted hormone to combat disease. Annu Rev Phytopathol 47:177–206

    Article  PubMed  CAS  Google Scholar 

  • Ward ER, Uknes JS, Williams SC, Dincher SS, Wiederhold DL, Alexander DC, Ahl-Goy P, Metraux JP, Ryals JA (1991) Coordinate gene activity in response to agents that induce systemic acquired resistance. Plant Cell 3:1085–1094

    PubMed  CAS  Google Scholar 

  • Wathugala DL, Hemsley PA, Moffat CS, Cremelie P, Knight MR, Knight H (2012) The mediator subunit SFR6/MED16 controls defence gene expression mediated by salicylic aciod and jasmonate responsive pathways. New Phytol 195:217–230

    Article  PubMed  CAS  Google Scholar 

  • Yalpani N, Silverman P, Wilson TM, Kleier DA, Raskin I (1991) Salicylic acid is a systemic signal and an inducer of pathogenesis-related proteins in virus-infected tobacco. Plant Cell Online 3:809–818

    CAS  Google Scholar 

  • Yoshioka Y, Ichikawa H, Naznin HA, Kogure A, Hyakumachi M (2012) Systemic resistance iduced in Arabidopsis by Trichoderma asperellum SKT-1, a microbial pesticide of seedborne diseases of rice. Pesticide Manag Sci 68:60–66

    Article  CAS  Google Scholar 

  • Zhang J, Du X, Wang Q, Chen X, Lv D, Xu K, Qu S, Zhang Z (2010) Expression of pathogneisis related genes in response to salicylic acid, methyl jasmonate and 1-aminocyclopropane-1-carboxylic acid in Malus hupehensis (Pamp.) Rehd. BMC Res Notes 3:208

    Article  PubMed  Google Scholar 

  • Ziadi S, Poupard P, Brisset M, Paulin J-P, Simoneau P (2001) Characterization in apple leaves of two subclasses of PR-10 transcripts inducible by acibenzolar-S-methyl, a functional analogue of salicylic acid. Physiol Mol Plant Pathol 59:33–43

    Article  CAS  Google Scholar 

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Acknowledgments

This research was funded by the Department of Primary Industries Victoria and Horticulture Australia Limited (HAL) using the vegetable levy and matched funds from the Australian Government. DAL was supported by a Deakin University—Department of Primary Industries postgraduate scholarship. The authors thank DPI Victoria for providing access to and use of facilities and Benjamin Jewell for assistance with glass house and field trials.

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Correspondence to David A. Lovelock.

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Lovelock, D.A., Donald, C.E., Conlan, X.A. et al. Salicylic acid suppression of clubroot in broccoli (Brassicae oleracea var. italica) caused by the obligate biotroph Plasmodiophora brassicae . Australasian Plant Pathol. 42, 141–153 (2013). https://doi.org/10.1007/s13313-012-0167-x

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