Analysis of global host gene expression during the primary phase of the Arabidopsis thaliana–Plasmodiophora brassicae interaction
Arati Agarwal A B F , Vijay Kaul B C , Robert Faggian D , James E. Rookes A , Jutta Ludwig-Müller E and David M. Cahill A
+ Author Affiliations
- Author Affiliations
A School of Life and Environmental Sciences, Deakin University, Geelong Campus at Waurn Ponds, Vic. 3217, Australia.
B Department of Primary Industries, Private Bag 15, Ferntree Gully DC, Vic. 3156, Australia.
C Present address: School of Botany, The University of Melbourne, Parkville, Vic. 3010, Australia.
D Department of Primary Industries, 32 Lincoln Square Nth Carlton, PO Box 4166, Parkville, Vic. 3052, Australia.
E Department of Biology, Technische Universität Dresden, 01062 Dresden, Germany.
F Corresponding author. Email: arati.agarwal@dpi.vic.gov.au
Functional Plant Biology 38(6) 462-478 https://doi.org/10.1071/FP11026
Submitted: 24 January 2011 Accepted: 31 March 2011 Published: 3 June 2011
Abstract
Microarray analysis was used to investigate changes in host gene expression during the primary stages of the interaction between the susceptible plant Arabidopsis thaliana (L.) Heynh ecotype Col-0 and the biotrophic pathogen Plasmodiophora brassicae Woronin. Analyses were conducted at 4, 7 and 10 days after inoculation (DAI) and revealed significant induction or suppression of a relatively low number of genes in a range of functional categories. At 4 DAI, there was induced expression of several genes known to be critical for pathogen recognition and signal transduction in other resistant host–pathogen interactions. As the pathogen further colonised root tissue and progressed through the primary plasmodium stage to production of zoosporangia at 7 and 10 DAI, respectively, fewer genes showed changes in expression. The microarray results were validated by examining a subset of induced genes at 4 DAI by quantitative real-time reverse transcriptase PCR (RT-qPCR) analysis all of which correlated positively with the microarray data. The two A. thaliana mutants jar1 and coiI tested were found to be susceptible to P. brassicae. The involvement of defence-related hormones in the interaction was further investigated and the findings indicate that addition of salicylic acid can suppress clubroot disease in A. thaliana plants.
Additional keywords: ATH1 microarray chip, clubroot, compatibility, real-time RT-qPCR, salicylic acid.
References
Agarwal A (2009) Interactions of Plasmodiophora brassicae with Arabidopsis thaliana. PhD thesis, Deakin University, Australia.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. Australasian Plant Pathology 38, 120–127.
| Development and use of a model system to monitor clubroot disease progression with an Australian field population of Plasmodiophora brassicae.Crossref | GoogleScholarGoogle Scholar |
Aist JR, Williams PH (1971) The cytology and kinetics of cabbage root hair penetration by Plasmodiophora brassicae Woron. Canadian Journal of Botany 49, 2023–2034.
| The cytology and kinetics of cabbage root hair penetration by Plasmodiophora brassicae Woron.Crossref | GoogleScholarGoogle Scholar |
Anderson JP, Thatcher LF, Singh KB (2005) Plant defense responses: conservation between models and crops. Functional Plant Biology 32, 21–34.
| Plant defense responses: conservation between models and crops.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXnt1Sltw%3D%3D&md5=4c1fd833b91d83bbd300064393a8f3d4CAS |
Baker B, Zambryski P, Staskawicz B, Dinesh-Kumar SP (1997) Signalling in plant–microbe interactions. Science 276, 726–733.
| Signalling in plant–microbe interactions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXivFOltLg%3D&md5=5cc9fabda636619e44cd04a26bdcfb30CAS | 9115193PubMed |
Bhattarai KK, Xie Q-G, Mantelin S, Bishnoi U, Girke T, Navarre DA, Kaloshian I (2008) Tomato susceptibility to root-knot nematodes requires an intact jasmonic acid signalling pathway. Molecular Plant-Microbe Interactions 21, 1205–1214.
Braselton JP (1995) Current status of the plasmodiophorids. Critical Reviews in Microbiology 21, 263–275.
| Current status of the plasmodiophorids.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK287pt1Cjug%3D%3D&md5=01de44aebe8a4617264c0fd9a8821f71CAS | 8688155PubMed |
Cao T, Srivastava S, Rahman MH, Kav NNV, Hotte N, Deyholos MK, Strelkov SE (2008) Proteome-level changes in the roots of Brassica napus as a result of Plansmodiophora brassicae infection. Plant Science 174, 97–115.
Chen H, Lai Z, Shi J, Xiao Y, Chen Z, Xu X (2010) Roles of Arabidopsis WRKY18, WRKY40 and WRKY60 transcription factors in plant responses to abscisic acid and abiotic stress. BMC Plant Biology 10, 281
| Roles of Arabidopsis WRKY18, WRKY40 and WRKY60 transcription factors in plant responses to abscisic acid and abiotic stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmtFA%3D&md5=dc8c62551585308a9e7103b597e20c52CAS | 21167067PubMed |
Cheong YH, Chang H, Gupta R, Wang X, Zhu T, Luan S (2002) Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. Plant Physiology 129, 661–677.
| Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XkvV2jtrk%3D&md5=6214d91a5c6d1350f26cdb7aa7f4ed42CAS | 12068110PubMed |
Crute IR, Gray AR, Crisp P, Buczacki ST (1980) Variation in Plasmodiophora brassicae and resistance to clubroot disease in brassicas and allied crops – a critical review. Plant Breeding Abstracts 50, 91–104.
da Cunha L, Sreerekha MV, Mackey D (2007) Defense suppression by virulence effectors of bacterial phytopathogens. Current Opinion in Plant Biology 10, 349–357.
| Defense suppression by virulence effectors of bacterial phytopathogens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXosFGrsLc%3D&md5=bab21a3a0ec29fff83db09f8504436afCAS | 17625953PubMed |
Dekhuijzen HM (1979) Electron microscopic studies on the root hairs and cortex of a susceptible and a resistant variety of Brassica campestris infected with Plasmodiophora brassicae. Netherlands Journal of Plant Pathology 85, 1–17.
| Electron microscopic studies on the root hairs and cortex of a susceptible and a resistant variety of Brassica campestris infected with Plasmodiophora brassicae.Crossref | GoogleScholarGoogle Scholar |
Dellagi A, Heilbronn J, Avrova AO, Montesano M, Palva ET, Stewart HE, Toth IK, Cooke DEL, Lyon GD, Birch PRJ (2000) A potato gene encoding a WRKY-like transcription factor is induced in interactions with Erwinia carotovora subsp. atroseptica and Phytophthora infestans and is coregulated with class 1 endochitinase expression. Molecular Plant—Microbe Interactions 13, 1092–1101.
| A potato gene encoding a WRKY-like transcription factor is induced in interactions with Erwinia carotovora subsp. atroseptica and Phytophthora infestans and is coregulated with class 1 endochitinase expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXntVarsrs%3D&md5=f86e4bcf7c26084a0f4a10c7a171ad91CAS | 11043470PubMed |
Devos S, Vissenberg K, Verbelen JP, Prinsen E (2005) Infection of Chinese cabbage by Plasmodiophora brassicae leads to a stimulation of plant growth: impacts on cell wall metabolism and hormone balance. New Phytologist 166, 241–250.
| Infection of Chinese cabbage by Plasmodiophora brassicae leads to a stimulation of plant growth: impacts on cell wall metabolism and hormone balance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjtlaku7g%3D&md5=585f306bbf52f6f3ad3267e255918093CAS | 15760367PubMed |
Devos S, Laukens K, Deckers P, Straeten DVD, Beeckman T, Inze D, Onckelen HV, Witters P, Prinsen E (2006) A hormone and proteome approach to picturing the initial metabolic events during Plasmodiophora brassicae infection on Arabidopsis. Molecular Plant—Microbe Interactions 19, 1431–1443.
| A hormone and proteome approach to picturing the initial metabolic events during Plasmodiophora brassicae infection on Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1yjs7rO&md5=257f22597b85239e10a4dd8ecf93e8abCAS | 17153927PubMed |
Dixon GR (2009) The occurrence and economic impact of Plasmodiophora brassicae and clubroot disease. Journal of Plant Growth Regulation 28, 194–202.
| The occurrence and economic impact of Plasmodiophora brassicae and clubroot disease.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVSisbvL&md5=a0a3ba198e749fa41abe8bd4d6c8ad21CAS |
Donald C, Porter I (2009) Integrated control of clubroot. Journal of Plant Growth Regulation 28, 289–303.
| Integrated control of clubroot.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVSisbjO&md5=239687368e1b58d48c8ad57a02b2c59bCAS |
Donald EC, Jaudzens G, Porter IJ (2008) Pathology of cortical invasion by Plasmodiophora brassicae in clubroot resistant and susceptible Brassica oleracea hosts. Plant Pathology 33, 585–589.
Dong X (1998) SA, JA, ethylene, and disease resistance in plants. Current Opinion in Plant Biology 1, 316–323.
| SA, JA, ethylene, and disease resistance in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXls1Kktrc%3D&md5=36ed7661b43926241400e607a5c8d621CAS | 10066607PubMed |
Estevez JM, Kieliszewski MJ, Khitrov N, Somerville C (2006) Characterization of synthetic hydroxyproline-rich proteoglycans with arabinogalactan protein and extensin motifs in Arabidopsis. Plant Physiology 142, 458–470.
| Characterization of synthetic hydroxyproline-rich proteoglycans with arabinogalactan protein and extensin motifs in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFarsbnK&md5=ae290f6ac1a3b0bbf73a46d5826892eaCAS | 16935991PubMed |
Eulgem T, Somssich IE (2007) Networks of WRKY transcription factors in defense signalling. Current Opinion in Plant Biology 10, 366–371.
| Networks of WRKY transcription factors in defense signalling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXosFGrsb8%3D&md5=cef975a0e5697504292b5465b698f2bfCAS | 17644023PubMed |
Eulgem T, Rushton PJ, Robatzek S, Somssich IE (2000) The WRKY superfamily of plant transcription factors. Trends in Plant Science 5, 199–206.
| The WRKY superfamily of plant transcription factors.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c3kvFalsw%3D%3D&md5=70d6abb3483b858a339410281f9dc395CAS | 10785665PubMed |
Feys BJ, Parker JE (2000) Interplay of signalling pathways in plant disease resistance. Trends in Genetics 16, 449–455.
| Interplay of signalling pathways in plant disease resistance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXotVSrsLc%3D&md5=9141807d465d580087ad163288baddc9CAS | 11050331PubMed |
Feys B, Benedetti CE, Penfold CN, Turner JG (1994) Arabidopsis mutants selected for resistance to the phytotoxin coronatine are male sterile, insensitive to methyl jasmonate, and resistant to a bacterial pathogen. The Plant Cell 6, 751–759.
Glazebrook J (2001) Genes controlling expression of defense responses in Arabidopsis – 2001 status. Current Opinion in Plant Biology 4, 301–308.
| Genes controlling expression of defense responses in Arabidopsis – 2001 status.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXksVykt7c%3D&md5=a4983be058620c7bbe5ee9b2b608625eCAS | 11418339PubMed |
Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annual Review of Phytopathology 43, 205–227.
| Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVOksrrN&md5=24b1f4ae6d066cd8397bbb74846acb69CAS | 16078883PubMed |
Glazebrook J, Chen W, Estes B, Chang HS, Nawrath C, Metraux JP, Zhu T, Katagiri F (2003) Topology of the network integrating salicylate and jasmonate signal transduction derived from global expression phenotyping. The Plant Journal 34, 217–228.
| Topology of the network integrating salicylate and jasmonate signal transduction derived from global expression phenotyping.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjvFOgt7g%3D&md5=f986225cab9e5819060fb370468dc894CAS | 12694596PubMed |
Halverson LJ, Stacey G (1986) Signal exchange in plant–microbe interactions. Microbiological Reviews 50, 193–225.
Hammond-Kosack KE, Parker JE (2003) Deciphering plant–pathogen communication: fresh perspectives for molecular resistance breeding. Current Opinion in Biotechnology 14, 177–193.
| Deciphering plant–pathogen communication: fresh perspectives for molecular resistance breeding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjsVGlu78%3D&md5=6244034965e20b2ce08a50363a0882d1CAS | 12732319PubMed |
Hardham AR, Jones DA, Takemoto D (2007) Cytoskeleton and cell wall function in penetration resistance. Current Opinion in Plant Biology 10, 342–348.
| Cytoskeleton and cell wall function in penetration resistance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXosFGrsLY%3D&md5=4c023cbed9cbaf6e0ccfa33ded4c4291CAS | 17627866PubMed |
Heath MC (1997) Signalling between pathogenic rust fungi and resistant or susceptible host plants. Annals of Botany 80, 713–720.
| Signalling between pathogenic rust fungi and resistant or susceptible host plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXlt1er&md5=56b3c6de49ab5194b7009762bd700615CAS |
Hirai M (2006) Genetic analysis of clubroot resistance in Brassica crops. Breeding Science 56, 223–229.
| Genetic analysis of clubroot resistance in Brassica crops.Crossref | GoogleScholarGoogle Scholar |
Ingram DS, Tommerup IC (1972) The life history of Plasmodiophora brassicae Woron. Proceedings of the Royal Society of London 180, 103–112.
| The life history of Plasmodiophora brassicae Woron.Crossref | GoogleScholarGoogle Scholar |
Irizarry RA, Hobbs B, Collin F, Bazer-Barclay YD, Antonrllis KJ, Scherf U, Speed TP (2003) Exploration, normalization and summaries of high density oligonucleotide array probe level data. Biostatistics 4, 249–264.
| Exploration, normalization and summaries of high density oligonucleotide array probe level data.Crossref | GoogleScholarGoogle Scholar | 12925520PubMed |
Jones JD, Dangl JL (2006) The plant immune system. Nature 444, 323–329.
| The plant immune system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1SgtbzO&md5=289500416c19947efd96d3e4aedb7bf5CAS | 17108957PubMed |
Jones DR, Ingram DS, Dixon GR (1982) Characterisation of isolates derived from single resting spores of Plasmodiophora brassicae and studies of their interaction. Plant Pathology 31, 239–246.
| Characterisation of isolates derived from single resting spores of Plasmodiophora brassicae and studies of their interaction.Crossref | GoogleScholarGoogle Scholar |
Kobelt P, Siemens J, Sacristan MD (2000) Histological characterisation of the incompatible interaction between Arabidopsis thaliana and the obligate biotrophic pathogen Plasmodiophora brassicae. Mycological Research 104, 220–225.
| Histological characterisation of the incompatible interaction between Arabidopsis thaliana and the obligate biotrophic pathogen Plasmodiophora brassicae.Crossref | GoogleScholarGoogle Scholar |
Kunkel BN, Brooks DM (2002) Cross talk between signalling pathways in pathogen defense. Current Opinion in Plant Biology 5, 325–331.
| Cross talk between signalling pathways in pathogen defense.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xls1ejtLs%3D&md5=14244877663fc48590afa26bf6ad63f3CAS | 12179966PubMed |
Leon-Reyes A, Du Y, Koorneef A, Proletti S, Korbes AP, Memelink J, Pieterse Corne MJ, Ritsema T (2010) Ethylene signalling renders the jasmonate response of Arabidopsis insensitive to future suppression by salicylic acid. Molecular Plant—Microbe Interactions 23, 187–197.
| Ethylene signalling renders the jasmonate response of Arabidopsis insensitive to future suppression by salicylic acid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXovVWktg%3D%3D&md5=a04b20ec69bee9944cd15bbc5d660beeCAS | 20064062PubMed |
Loake G, Grant M (2007) Salicylic acid in plant defense – the players and protagonists. Current Opinion in Plant Biology 10, 466–472.
| Salicylic acid in plant defense – the players and protagonists.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFekurjM&md5=ab1e160be0d214a7ec681367d9be164dCAS | 17904410PubMed |
Ludwig-Müller J, Schuller A (2008) What can we learn from clubroots: alterations in host roots and hormone homeostasis caused by Plasmodiophora brassicae. European Journal of Plant Pathology 121, 291–302.
| What can we learn from clubroots: alterations in host roots and hormone homeostasis caused by Plasmodiophora brassicae.Crossref | GoogleScholarGoogle Scholar |
Makandar R, Nalam V, Chaturvedi R, Jeannotte R, Sparks AA, Shah J (2010) Involvement of salicylate and jasmonate signalling pathways in Arabidopsis interaction with Fusarium graminearum. Molecular Plant—Microbe Interactions 23, 861–870.
| Involvement of salicylate and jasmonate signalling pathways in Arabidopsis interaction with Fusarium graminearum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXnvVart78%3D&md5=5b9b3133a7cfdfe00a878794db04cc7bCAS | 20521949PubMed |
Maleck K, Levine A, Eulgem T, Morgan A, Schmid J, Lawton KA, Dangl JL, Dietrich RA (2000) The transcriptome of Arabidopsis thaliana during systemic acquired resistance. Nature 26, 403–410.
Mellersh DG, Heath MC (2001) Plasma membrane–cell wall adhesion is required for expression of plant defense responses during fungal penetration. The Plant Cell 13, 413–424.
Mohr PG, Cahill DM (2007) Suppression of ABA of salicylic acid and lignin accumulation and the expression of multiple genes, in Arabidopsis infected with Pseudomonas syringae pv. Tomato. Functional & Integrative Genomics 7, 181–191.
| Suppression of ABA of salicylic acid and lignin accumulation and the expression of multiple genes, in Arabidopsis infected with Pseudomonas syringae pv. Tomato.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXls1SitLw%3D&md5=17280656328db8df35c0db7cc2617ac8CAS | 17149585PubMed |
Mok DWS, Mok MC (2001) Cytokinin metabolism and action. Annual Review of Plant Physiology and Plant Molecular Biology 52, 89–118.
| Cytokinin metabolism and action.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXkslWgsL8%3D&md5=41e6d9225c62d01294783894f27baae5CAS | 11337393PubMed |
Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassay with tobacco tissue culture. Physiologia Plantarum 15, 473–497.
| A revised medium for rapid growth and bioassay with tobacco tissue culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF3sXksFKm&md5=06c472aaff717f5157aa29da67ee5ad0CAS |
O’Connell RJ, Panstruga R (2006) Tete a tete inside a plant cell: establishing compatibility between plants and biotrophic fungi and oomycetes. New Phytologist 171, 699–718.
| Tete a tete inside a plant cell: establishing compatibility between plants and biotrophic fungi and oomycetes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVSku77F&md5=17649bfab9af6e31b1b71807f5e3829aCAS | 16918543PubMed |
Oliver RP, Ipcho SVS (2004) Arabidopsis pathology breathes new life into the necrotrophs-vs.-biotrophs classification of fungal pathogens. Molecular Plant Pathology 5, 347–352.
| Arabidopsis pathology breathes new life into the necrotrophs-vs.-biotrophs classification of fungal pathogens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmsl2ns7w%3D&md5=e0ca5da769490c60dbc69ac2f5d5c2c9CAS | 20565602PubMed |
Panstruga R (2003) Establishing compatibility between plants and obligate biotrophic pathogens. Current Opinion in Plant Biology 6, 320–326.
| Establishing compatibility between plants and obligate biotrophic pathogens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlsValt7c%3D&md5=12060abb1600a2dde9757c4aa3a931cdCAS | 12873525PubMed |
Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Research 29, e45
| A new mathematical model for relative quantification in real-time RT–PCR.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38nis12jtw%3D%3D&md5=0957e876af3eab3c669ce09b7afcfd19CAS | 11328886PubMed |
Rajeevan MS, Vernon SD, Tayranang N, Unger ER (2001) Validation of array-based gene expression profiles by real-time (kinetic) RT-PCR. The Journal of Molecular Diagnostics 3, 26–31.
| Validation of array-based gene expression profiles by real-time (kinetic) RT-PCR.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhsFahs7Y%3D&md5=4af53c03056c3c06d9674bdb6eb954e1CAS | 11227069PubMed |
Restrepo S, Myers KL, del Pozo O, Martin GB, Hart AL, Buell CR, Fry WE, Smart CD (2005) Gene profiling of a compatible interaction between Phytophthora infestans and Solanum tuberosum suggests a role for carbonic anhydrase. Molecular Plant—Microbe Interactions 18, 913–922.
| Gene profiling of a compatible interaction between Phytophthora infestans and Solanum tuberosum suggests a role for carbonic anhydrase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXpsFGju7Y%3D&md5=79a2c0b12cf6e172cca1ced2f994732aCAS | 16167762PubMed |
Rookes JE, Wright ML, Cahill DM (2008) Elucidation of defense responses and signalling pathways induced in Arabidopsis thaliana following challenge with Phytophthora cinnamomi. Physiological and Molecular Plant Pathology 72, 151–161.
| Elucidation of defense responses and signalling pathways induced in Arabidopsis thaliana following challenge with Phytophthora cinnamomi.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVKls7fM&md5=320806b507cda4234f5566157c115bc9CAS |
Rozen S, Skaletsky HJ (2000) Primer 3 on the WWW for general users and for biologist programmers. In: ‘Bioinformatics methods and protocols: methods in molecular biology’. (Eds S Krawetz, S Misener) pp. 365–386. (Humana Press: Totowa, NJ)
Schenk PM, Kazan K, Wilson I, Anderson JP, Richmond T, Somerville SC, Manners JM (2000) Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proceedings of the National Academy of Sciences of the United States of America 97, 11 655–11 660.
| Coordinated plant defense responses in Arabidopsis revealed by microarray analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXnsF2qtro%3D&md5=284bd9bb9001bcd89332bdd2da1dea63CAS |
Schulze-Lefert P (2004) Knocking on the heaven’s wall: pathogenesis of and resistance to biotrophic fungi at the cell wall. Current Opinion in Plant Biology 7, 377–383.
| Knocking on the heaven’s wall: pathogenesis of and resistance to biotrophic fungi at the cell wall.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlsVWhtLw%3D&md5=f956f020b740c45a7714f3dc55c4e38fCAS | 15231259PubMed |
Schulze-Lefert P, Panstruga R (2003) Establishment of biotrophy by parasitic fungi and reprogramming of host cells for disease resistance. Annual Review of Phytopathology 41, 641–667.
| Establishment of biotrophy by parasitic fungi and reprogramming of host cells for disease resistance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXptFWltr0%3D&md5=717b266d7466f985d8a285b7a5aa90eaCAS | 14527335PubMed |
Siemens J, Nagel M, Ludwig-Müller J, Sacristan MD (2002) The interaction of Plasmodiophora brassicae and Arabidopsis thaliana: parameters for disease quantification and screening of mutant lines. Journal of Phytopathology 150, 592–605.
| The interaction of Plasmodiophora brassicae and Arabidopsis thaliana: parameters for disease quantification and screening of mutant lines.Crossref | GoogleScholarGoogle Scholar |
Siemens J, Keller I, Sarx J, Kunz S, Schuller A, Nagel W, Schmulling T, Parniske M, Ludwig-Müller J (2006) Transcriptome analysis of Arabidopsis clubroots indicate a key role for cytokinins in disease development. Molecular Plant—Microbe Interactions 19, 480–494.
| Transcriptome analysis of Arabidopsis clubroots indicate a key role for cytokinins in disease development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XktVClsL8%3D&md5=225c70c818f0958357bf7341219cf286CAS | 16673935PubMed |
Staswick PE, Su W, Howell SH (1992) Methyl jasmonate inhibition of root growth and induction of a leaf protein are decreased in an Arabidopsis thaliana mutant. Proceedings of the National Academy of Sciences of the United States of America 89, 6837–6840.
Takahashi H, Ishikawa T, Kaido M, Takita K, Hayakawa T, Okazaki K, Itoh K, Mitsui T, Hori H (2006) Plasmodiophora brassicae-induced cell death and medium alkalization in clubroot-resistant cultured roots of Brassica rapa. Journal of Phytopathology 154, 156–162.
| Plasmodiophora brassicae-induced cell death and medium alkalization in clubroot-resistant cultured roots of Brassica rapa.Crossref | GoogleScholarGoogle Scholar |
Thatcher LF, Anderson JP, Singh KB (2005) Plant defence responses: what we have learnt from Arabidopsis? Functional Plant Biology 32, 1–19.
| Plant defence responses: what we have learnt from Arabidopsis?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXpt1CksA%3D%3D&md5=30c5c9eff3345e12313f0958503ea986CAS |
Thimm O, Blaesing O, Gibon Y, Nagel A, Meyer S, Krueger P, Selbig J, Mueller LA, Rhee SY, Stitt M (2004) MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. The Plant Journal 37, 914–939.
| MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjtFChu78%3D&md5=c2f785f57c6d48085d9cf7a5035146deCAS | 14996223PubMed |
Torres MA, Dangl JL (2005) Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. Current Opinion in Plant Biology 8, 397–403.
| Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXlsFGgtrg%3D&md5=e1258106ee77df6e695bb9c181ebbe3bCAS | 15939662PubMed |
Toxopeus H, Dixon GR, Mattusch P (1986) Physiologic specialisation in Plasmodiophora brassicae: an analysis by international experimentation. Transactions of the British Mycological Society 87, 279–287.
| Physiologic specialisation in Plasmodiophora brassicae: an analysis by international experimentation.Crossref | GoogleScholarGoogle Scholar |
Trusov Y, Rookes JE, Chakravorty D, Armour D, Schenk PM, Botella JR (2006) Heterotrimeric G proteins facilitate Arabidopsis resistance to necrotrophic pathogens and are involved in jasmonate signaling. Plant Physiology 140, 210–220.
| Heterotrimeric G proteins facilitate Arabidopsis resistance to necrotrophic pathogens and are involved in jasmonate signaling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVCgsbY%3D&md5=0b3faed151b673944c503fb5a6daa01dCAS | 16339801PubMed |
Unger C, Kleta S, Jandl G, Tiedemann AV (2005) Suppression of the defense-related oxidative burst in bean leaf tissue and bean suspension cells by the necrotrophic pathogen Botrytis cinerea. Journal of Phytopathology 153, 15–26.
| Suppression of the defense-related oxidative burst in bean leaf tissue and bean suspension cells by the necrotrophic pathogen Botrytis cinerea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhvVCktbg%3D&md5=b88f7b09be14b80637e9ad05786b539cCAS |
Wan J, Dunning FM, Bent AF (2002) Probing plant–pathogen interactions and downstream defense signalling using DNA microarrays. Functional & Integrative Genomics 2, 259–273.
| Probing plant–pathogen interactions and downstream defense signalling using DNA microarrays.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XovVWns78%3D&md5=cedcc0ee1b574553b3ad98815fb6fa19CAS | 12444419PubMed |
Wiermer M, Feys BJ, Parker JE (2005) Plant immunity: the EDS1 regulatory node. Current Opinion in Plant Biology 8, 383–389.
| Plant immunity: the EDS1 regulatory node.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXlsFGgtro%3D&md5=f3554e11686406e735bf182cc9fa4c7cCAS | 15939664PubMed |
Wise RP, Moscou MJ, Bogdanove AJ, Whitham SA (2007) Transcrpt profiling in host–pathogen interactions. Annual Review of Phytopathology 45, 329–369.
| Transcrpt profiling in host–pathogen interactions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVKls7vP&md5=e21dea8a8002a518a3cbdd35a3d89446CAS | 17480183PubMed |
Xu X, Chen C, Fan B, Chen Z (2006) Physical and functional interactions between pathogen-induced Arabidopsis WRKY18, WRKY40, and WRKY60 transcription factors. The Plant Cell 18, 1310–1326.
| Physical and functional interactions between pathogen-induced Arabidopsis WRKY18, WRKY40, and WRKY60 transcription factors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XkslCmu7c%3D&md5=6bffffcb4dd43b29f33845df3adc367cCAS | 16603654PubMed |
Zhao J, Davis LC, Verpoorte R (2005) Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnology Advances 23, 283–333.
| Elicitor signal transduction leading to production of plant secondary metabolites.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjsVehu7c%3D&md5=42748ccafff0e90e4d513961d2845905CAS | 15848039PubMed |
Zheng Z, Qamar SA, Chen Z, Mengiste T (2006) Arabidopsis WRKY33 transcription factor is required for resistance to necrotrophic fungal pathogens. The Plant Journal 48, 592–605.
| Arabidopsis WRKY33 transcription factor is required for resistance to necrotrophic fungal pathogens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1ylurfI&md5=32a7500a2f061fa5f0a3b670db33d6b8CAS | 17059405PubMed |
