Laser microdissection of Arabidopsis cells at the powdery mildew infection site reveals site-specific processes and regulators

Chandran D, Inada N, Hather G, Kleindt CK, Wildermuth MC (2010)
Proceedings of the National Academy of Sciences of the United States of America 107(1): 460-465.

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Abstract / Bemerkung
To elucidate host processes and components required for the sustained growth and reproduction of the obligate biotrophic fungus Golovinomyces orontii on Arabidopsis thaliana, laser microdissection was used to isolate cells at the site of infection at 5 days postinfection for downstream global Arabidopsis expression profiling. Site-specific profiling increased sensitivity dramatically, allowing us to identify specific host processes, process components, and their putative regulators hidden in previous whole-leaf global expression analyses. For example, 67 transcription factors exhibited altered expression at the powdery mildew (PM) infection site, with subsets of these playing known or inferred roles in photosynthesis, cold/dehydration responses, defense, auxin signaling, and the cell cycle. Using integrated informatics analyses, we constructed putative regulatory networks for a subset of these processes and provided strong support for host cell cycle modulation at the PM infection site. Further experimentation revealed induced host endoreduplication occurred exclusively at the infection site and led us to identify MYB3R4 as a transcriptional regulator of this process. Induced endoreduplication was abrogated in myb3r4 mutants, and G. orontii growth and reproduction were reduced. This suggests that, by increasing gene copy number, localized endoreduplication serves as a mechanism to meet the enhanced metabolic demands imposed by the fungus, which acquires all its nutrients from the plant host.
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Proceedings of the National Academy of Sciences of the United States of America
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107
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1
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460-465
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Chandran D, Inada N, Hather G, Kleindt CK, Wildermuth MC. Laser microdissection of Arabidopsis cells at the powdery mildew infection site reveals site-specific processes and regulators. Proceedings of the National Academy of Sciences of the United States of America. 2010;107(1):460-465.
Chandran, D., Inada, N., Hather, G., Kleindt, C. K., & Wildermuth, M. C. (2010). Laser microdissection of Arabidopsis cells at the powdery mildew infection site reveals site-specific processes and regulators. Proceedings of the National Academy of Sciences of the United States of America, 107(1), 460-465. doi:10.1073/pnas.0912492107
Chandran, D., Inada, N., Hather, G., Kleindt, C. K., and Wildermuth, M. C. (2010). Laser microdissection of Arabidopsis cells at the powdery mildew infection site reveals site-specific processes and regulators. Proceedings of the National Academy of Sciences of the United States of America 107, 460-465.
Chandran, D., et al., 2010. Laser microdissection of Arabidopsis cells at the powdery mildew infection site reveals site-specific processes and regulators. Proceedings of the National Academy of Sciences of the United States of America, 107(1), p 460-465.
D. Chandran, et al., “Laser microdissection of Arabidopsis cells at the powdery mildew infection site reveals site-specific processes and regulators”, Proceedings of the National Academy of Sciences of the United States of America, vol. 107, 2010, pp. 460-465.
Chandran, D., Inada, N., Hather, G., Kleindt, C.K., Wildermuth, M.C.: Laser microdissection of Arabidopsis cells at the powdery mildew infection site reveals site-specific processes and regulators. Proceedings of the National Academy of Sciences of the United States of America. 107, 460-465 (2010).
Chandran, Divya, Inada, Noriko, Hather, Greg, Kleindt, Christiane Katja, and Wildermuth, Mary C. “Laser microdissection of Arabidopsis cells at the powdery mildew infection site reveals site-specific processes and regulators”. Proceedings of the National Academy of Sciences of the United States of America 107.1 (2010): 460-465.

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Daten bereitgestellt von Europe PubMed Central.

How to make a tumour: cell type specific dissection of Ustilago maydis-induced tumour development in maize leaves.
Matei A, Ernst C, Günl M, Thiele B, Altmüller J, Walbot V, Usadel B, Doehlemann G., New Phytol 217(4), 2018
PMID: 29314018
Plant and animal PR1 family members inhibit programmed cell death and suppress bacterial pathogens in plant tissues.
Lincoln JE, Sanchez JP, Zumstein K, Gilchrist DG., Mol Plant Pathol 19(9), 2018
PMID: 29603552
A Spatiotemporal DNA Endoploidy Map of the Arabidopsis Root Reveals Roles for the Endocycle in Root Development and Stress Adaptation.
Bhosale R, Boudolf V, Cuevas F, Lu R, Eekhout T, Hu Z, Van Isterdael G, Lambert GM, Xu F, Nowack MK, Smith RS, Vercauteren I, De Rycke R, Storme V, Beeckman T, Larkin JC, Kremer A, Höfte H, Galbraith DW, Kumpf RP, Maere S, De Veylder L., Plant Cell 30(10), 2018
PMID: 30115738
Distinct Signatures of Host Defense Suppression by Plant-Feeding Mites.
Schimmel BCJ, Alba JM, Wybouw N, Glas JJ, Meijer TT, Schuurink RC, Kant MR., Int J Mol Sci 19(10), 2018
PMID: 30347842
Why do plants need so many cyclin-dependent kinase inhibitors?
Kumar N, Larkin JC., Plant Signal Behav 12(2), 2017
PMID: 28165885
Purification of High Molecular Weight Genomic DNA from Powdery Mildew for Long-Read Sequencing.
Feehan JM, Scheibel KE, Bourras S, Underwood W, Keller B, Somerville SC., J Vis Exp (121), 2017
PMID: 28448006
Evolution of the 3R-MYB Gene Family in Plants.
Feng G, Burleigh JG, Braun EL, Mei W, Barbazuk WB., Genome Biol Evol (), 2017
PMID: 28444194
Insights into Host Cell Modulation and Induction of New Cells by the Corn Smut Ustilago maydis.
Redkar A, Matei A, Doehlemann G., Front Plant Sci 8(), 2017
PMID: 28611813
Adapted Biotroph Manipulation of Plant Cell Ploidy.
Wildermuth MC, Steinwand MA, McRae AG, Jaenisch J, Chandran D., Annu Rev Phytopathol 55(), 2017
PMID: 28617655
Key Components of Different Plant Defense Pathways Are Dispensable for Powdery Mildew Resistance of the Arabidopsis mlo2 mlo6 mlo12 Triple Mutant.
Kuhn H, Lorek J, Kwaaitaal M, Consonni C, Becker K, Micali C, Ver Loren van Themaat E, Bednarek P, Raaymakers TM, Appiano M, Bai Y, Meldau D, Baum S, Conrath U, Feussner I, Panstruga R., Front Plant Sci 8(), 2017
PMID: 28674541
Laser Microdissection of Grapevine Leaves Reveals Site-Specific Regulation of Transcriptional Response to Plasmopara viticola.
Lenzi L, Caruso C, Bianchedi PL, Pertot I, Perazzolli M., Plant Cell Physiol 57(1), 2016
PMID: 26546320
Differential Roles of Two Homologous Cyclin-Dependent Kinase Inhibitor Genes in Regulating Cell Cycle and Innate Immunity in Arabidopsis.
Hamdoun S, Zhang C, Gill M, Kumar N, Churchman M, Larkin JC, Kwon A, Lu H., Plant Physiol 170(1), 2016
PMID: 26561564
Transcriptome dynamics of a susceptible wheat upon Fusarium head blight reveals that molecular responses to Fusarium graminearum infection fit over the grain development processes.
Chetouhi C, Bonhomme L, Lasserre-Zuber P, Cambon F, Pelletier S, Renou JP, Langin T., Funct Integr Genomics 16(2), 2016
PMID: 26797431
An Efficient LCM-Based Method for Tissue Specific Expression Analysis of Genes and miRNAs.
Gautam V, Singh A, Singh S, Sarkar AK., Sci Rep 6(), 2016
PMID: 26861910
Mildew-Omics: How Global Analyses Aid the Understanding of Life and Evolution of Powdery Mildews.
Bindschedler LV, Panstruga R, Spanu PD., Front Plant Sci 7(), 2016
PMID: 26913042
Integrating Large-Scale Data and RNA Technology to Protect Crops from Fungal Pathogens.
Girard IJ, Mcloughlin AG, de Kievit TR, Fernando DW, Belmonte MF., Front Plant Sci 7(), 2016
PMID: 27303409
Biotrophy at Its Best: Novel Findings and Unsolved Mysteries of the Arabidopsis-Powdery Mildew Pathosystem.
Kuhn H, Kwaaitaal M, Kusch S, Acevedo-Garcia J, Wu H, Panstruga R., Arabidopsis Book 14(), 2016
PMID: 27489521
Laser microdissection of tomato fruit cell and tissue types for transcriptome profiling.
Martin LB, Nicolas P, Matas AJ, Shinozaki Y, Catalá C, Rose JK., Nat Protoc 11(12), 2016
PMID: 27809311
DREAMs make plant cells to cycle or to become quiescent.
Magyar Z, Bögre L, Ito M., Curr Opin Plant Biol 34(), 2016
PMID: 27816815
A novel methyltransferase from the intracellular pathogen Plasmodiophora brassicae methylates salicylic acid.
Ludwig-Müller J, Jülke S, Geiß K, Richter F, Mithöfer A, Šola I, Rusak G, Keenan S, Bulman S., Mol Plant Pathol 16(4), 2015
PMID: 25135243
Proteomic analysis of responsive stem proteins of resistant and susceptible cashew plants after Lasiodiplodia theobromae infection.
Cipriano AK, Gondim DM, Vasconcelos IM, Martins JA, Moura AA, Moreno FB, Monteiro-Moreira AC, Melo JG, Cardoso JE, Paiva AL, Oliveira JT., J Proteomics 113(), 2015
PMID: 25289588
Pathogen associated molecular pattern (PAMP)-triggered immunity is compromised under C-limited growth.
Park HC, Lee S, Park B, Choi W, Kim C, Lee S, Chung WS, Lee SY, Sabir J, Bressan RA, Bohnert HJ, Mengiste T, Yun DJ., Mol Cells 38(1), 2015
PMID: 25387755
Building the interaction interfaces: host responses upon infection with microorganisms.
Yamazaki A, Hayashi M., Curr Opin Plant Biol 23(), 2015
PMID: 25621846
Arabidopsis flower specific defense gene expression patterns affect resistance to pathogens.
Ederli L, Dawe A, Pasqualini S, Quaglia M, Xiong L, Gehring C., Front Plant Sci 6(), 2015
PMID: 25750645
Members of the NPF3 transporter subfamily encode pathogen-inducible nitrate/nitrite transporters in grapevine and Arabidopsis.
Pike S, Gao F, Kim MJ, Kim SH, Schachtman DP, Gassmann W., Plant Cell Physiol 55(1), 2014
PMID: 24259683
Discovery of genes affecting resistance of barley to adapted and non-adapted powdery mildew fungi.
Douchkov D, Lück S, Johrde A, Nowara D, Himmelbach A, Rajaraman J, Stein N, Sharma R, Kilian B, Schweizer P., Genome Biol 15(12), 2014
PMID: 25476012
Gene expression in vessel-associated cells upon xylem embolism repair in Vitis vinifera L. petioles.
Chitarra W, Balestrini R, Vitali M, Pagliarani C, Perrone I, Schubert A, Lovisolo C., Planta 239(4), 2014
PMID: 24402563
Orchestration of plant defense systems: genes to populations.
Kliebenstein DJ., Trends Plant Sci 19(4), 2014
PMID: 24486317
Genetics and molecular mechanisms of resistance to powdery mildews in tomato (Solanum lycopersicum) and its wild relatives
Seifi A, Gao D, Zheng Z, Pavan S, Faino L, Visser RGF, Wolters AMA, Bai Y., Eur J Plant Pathol 138(3), 2014
PMID: IND500731321
Atypical E2F transcriptional repressor DEL1 acts at the intersection of plant growth and immunity by controlling the hormone salicylic acid.
Chandran D, Rickert J, Huang Y, Steinwand MA, Marr SK, Wildermuth MC., Cell Host Microbe 15(4), 2014
PMID: 24721578
Expression-based network biology identifies immune-related functional modules involved in plant defense.
Tully JP, Hill AE, Ahmed HM, Whitley R, Skjellum A, Mukhtar MS., BMC Genomics 15(), 2014
PMID: 24888606
Susceptibility genes 101: how to be a good host.
van Schie CC, Takken FL., Annu Rev Phytopathol 52(), 2014
PMID: 25001453
High-resolution transcript profiling of the atypical biotrophic interaction between Theobroma cacao and the fungal pathogen Moniliophthora perniciosa.
Teixeira PJ, Thomazella DP, Reis O, do Prado PF, do Rio MC, Fiorin GL, José J, Costa GG, Negri VA, Mondego JM, Mieczkowski P, Pereira GA., Plant Cell 26(11), 2014
PMID: 25371547
Altered expression of Arabidopsis genes in response to a multifunctional geminivirus pathogenicity protein.
Liu L, Chung HY, Lacatus G, Baliji S, Ruan J, Sunter G., BMC Plant Biol 14(), 2014
PMID: 25403083
Jasmonate controls leaf growth by repressing cell proliferation and the onset of endoreduplication while maintaining a potential stand-by mode.
Noir S, Bömer M, Takahashi N, Ishida T, Tsui TL, Balbi V, Shanahan H, Sugimoto K, Devoto A., Plant Physiol 161(4), 2013
PMID: 23439917
Host cell ploidy underlying the fungal feeding site is a determinant of powdery mildew growth and reproduction.
Chandran D, Rickert J, Cherk C, Dotson BR, Wildermuth MC., Mol Plant Microbe Interact 26(5), 2013
PMID: 23301616
Recovery from stolbur disease in grapevine involves changes in sugar transport and metabolism.
Santi S, De Marco F, Polizzotto R, Grisan S, Musetti R., Front Plant Sci 4(), 2013
PMID: 23761800
Susceptibility to plant disease: more than a failure of host immunity.
Lapin D, Van den Ackerveken G., Trends Plant Sci 18(10), 2013
PMID: 23790254
Involvement of the glutamate receptor AtGLR3.3 in plant defense signaling and resistance to Hyaloperonospora arabidopsidis.
Manzoor H, Kelloniemi J, Chiltz A, Wendehenne D, Pugin A, Poinssot B, Garcia-Brugger A., Plant J 76(3), 2013
PMID: 23952652
Tissue-specific transcriptome analysis in nodules of Lotus japonicus.
Takanashi K, Takahashi H, Sakurai N, Sugiyama A, Suzuki H, Shibata D, Nakazono M, Yazaki K., Mol Plant Microbe Interact 25(7), 2012
PMID: 22432875
CCS52 and DEL1 genes are key components of the endocycle in nematode-induced feeding sites.
de Almeida Engler J, Kyndt T, Vieira P, Van Cappelle E, Boudolf V, Sanchez V, Escobar C, De Veylder L, Engler G, Abad P, Gheysen G., Plant J 72(2), 2012
PMID: 22640471
Combining laser microdissection and RNA-seq to chart the transcriptional landscape of fungal development.
Teichert I, Wolff G, Kück U, Nowrousian M., BMC Genomics 13(), 2012
PMID: 23016559
Quantitative and temporal definition of the Mla transcriptional regulon during barley-powdery mildew interactions.
Moscou MJ, Lauter N, Caldo RA, Nettleton D, Wise RP., Mol Plant Microbe Interact 24(6), 2011
PMID: 21323465
Mycorrhizal symbiosis stimulates endoreduplication in angiosperms.
Bainard LD, Bainard JD, Newmaster SG, Klironomos JN., Plant Cell Environ 34(9), 2011
PMID: 21707648
Subtissue-specific evaluation of promoter efficiency by quantitative fluorometric assay in laser microdissected tissues of rapeseed.
Jasik J, Schiebold S, Rolletschek H, Denolf P, Van Adenhove K, Altmann T, Borisjuk L., Plant Physiol 157(2), 2011
PMID: 21825109
Salicylic Acid biosynthesis and metabolism.
Dempsey DA, Vlot AC, Wildermuth MC, Klessig DF., Arabidopsis Book 9(), 2011
PMID: 22303280

36 References

Daten bereitgestellt von Europe PubMed Central.


Dik AJ, Belanger RR, Carver TLW, Bushnell WR., 2002
The Arabidopsis Information Resource (TAIR): gene structure and function annotation.
Swarbreck D, Wilks C, Lamesch P, Berardini TZ, Garcia-Hernandez M, Foerster H, Li D, Meyer T, Muller R, Ploetz L, Radenbaugh A, Singh S, Swing V, Tissier C, Zhang P, Huala E., Nucleic Acids Res. 36(Database issue), 2007
PMID: 17986450

Micali C, Gollner K, Humphry M, Consonni C, Panstruga R., 2008
Temporal global expression data reveal known and novel salicylate-impacted processes and regulators mediating powdery mildew growth and reproduction on Arabidopsis.
Chandran D, Tai YC, Hather G, Dewdney J, Denoux C, Burgess DG, Ausubel FM, Speed TP, Wildermuth MC., Plant Physiol. 149(3), 2009
PMID: 19176722
Isochorismate synthase is required to synthesize salicylic acid for plant defence.
Wildermuth MC, Dewdney J, Wu G, Ausubel FM., Nature 414(6863), 2001
PMID: 11734859
The protective role of silicon in the Arabidopsis-powdery mildew pathosystem.
Fauteux F, Chain F, Belzile F, Menzies JG, Belanger RR., Proc. Natl. Acad. Sci. U.S.A. 103(46), 2006
PMID: 17082308
Genome-wide expression profiling Arabidopsis at the stage of Golovinomyces cichoracearum haustorium formation.
Fabro G, Di Rienzo JA, Voigt CA, Savchenko T, Dehesh K, Somerville S, Alvarez ME., Plant Physiol. 146(3), 2008
PMID: 18218973
Host and non-host pathogens elicit different jasmonate/ethylene responses in Arabidopsis.
Zimmerli L, Stein M, Lipka V, Schulze-Lefert P, Somerville S., Plant J. 40(5), 2004
PMID: 15546348
Powdery mildew induces defense-oriented reprogramming of the transcriptome in a susceptible but not in a resistant grapevine.
Fung RW, Gonzalo M, Fekete C, Kovacs LG, He Y, Marsh E, McIntyre LM, Schachtman DP, Qiu W., Plant Physiol. 146(1), 2007
PMID: 17993546
Photosynthesis, sugars and the regulation of gene expression.
Pego JV, Kortstee AJ, Huijser C, Smeekens SC., J. Exp. Bot. 51 Spec No(), 2000
PMID: 10938849
Plant physiology meets phytopathology: plant primary metabolism and plant-pathogen interactions.
Berger S, Sinha AK, Roitsch T., J. Exp. Bot. 58(15-16), 2007
PMID: 18182420
Respiration of leaves of barley infected with powdery mildew: Increased engagement of the alternative oxidase
Farrar JF, Rayns FW., 1987
Primary metabolism and plant defense--fuel for the fire.
Bolton MD., Mol. Plant Microbe Interact. 22(5), 2009
PMID: 19348567
Co-option of a default secretory pathway for plant immune responses.
Kwon C, Neu C, Pajonk S, Yun HS, Lipka U, Humphry M, Bau S, Straus M, Kwaaitaal M, Rampelt H, El Kasmi F, Jurgens G, Parker J, Panstruga R, Lipka V, Schulze-Lefert P., Nature 451(7180), 2008
PMID: 18273019
A glucosinolate metabolism pathway in living plant cells mediates broad-spectrum antifungal defense.
Bednarek P, Pislewska-Bednarek M, Svatos A, Schneider B, Doubsky J, Mansurova M, Humphry M, Consonni C, Panstruga R, Sanchez-Vallet A, Molina A, Schulze-Lefert P., Science 323(5910), 2008
PMID: 19095900
Glucosinolate metabolites required for an Arabidopsis innate immune response.
Clay NK, Adio AM, Denoux C, Jander G, Ausubel FM., Science 323(5910), 2008
PMID: 19095898
Identification of cold-inducible downstream genes of the Arabidopsis DREB1A/CBF3 transcriptional factor using two microarray systems.
Maruyama K, Sakuma Y, Kasuga M, Ito Y, Seki M, Goda H, Shimada Y, Yoshida S, Shinozaki K, Yamaguchi-Shinozaki K., Plant J. 38(6), 2004
PMID: 15165189
Antagonistic control of powdery mildew host cell entry by barley calcium-dependent protein kinases (CDPKs).
Freymark G, Diehl T, Miklis M, Romeis T, Panstruga R., Mol. Plant Microbe Interact. 20(10), 2007
PMID: 17918623
Mutations in AtCML9, a calmodulin-like protein from Arabidopsis thaliana, alter plant responses to abiotic stress and abscisic acid.
Magnan F, Ranty B, Charpenteau M, Sotta B, Galaud JP, Aldon D., Plant J. 56(4), 2008
PMID: 18643966
Plant immunity requires conformational changes [corrected] of NPR1 via S-nitrosylation and thioredoxins.
Tada Y, Spoel SH, Pajerowska-Mukhtar K, Mou Z, Song J, Wang C, Zuo J, Dong X., Science 321(5891), 2008
PMID: 18635760
Arabidopsis TCP20 links regulation of growth and cell division control pathways.
Li C, Potuschak T, Colon-Carmona A, Gutierrez RA, Doerner P., Proc. Natl. Acad. Sci. U.S.A. 102(36), 2005
PMID: 16123132
R1R2R3-Myb proteins positively regulate cytokinesis through activation of KNOLLE transcription in Arabidopsis thaliana.
Haga N, Kato K, Murase M, Araki S, Kubo M, Demura T, Suzuki K, Muller I, Voss U, Jurgens G, Ito M., Development 134(6), 2007
PMID: 17287251
Relationship between Endopolyploidy and Cell Size in Epidermal Tissue of Arabidopsis.
Melaragno JE, Mehrotra B, Coleman AW., Plant Cell 5(11), 1993
PMID: 12271050

Larkin J, Brown ML, Churchman J., 2007
Transcriptional control of the cell cycle.
Berckmans B, De Veylder L., Curr. Opin. Plant Biol. 12(5), 2009
PMID: 19700366
Mitotic cyclins stimulate the activity of c-Myb-like factors for transactivation of G2/M phase-specific genes in tobacco.
Araki S, Ito M, Soyano T, Nishihama R, Machida Y., J. Biol. Chem. 279(31), 2004
PMID: 15175336
SIAMESE, a plant-specific cell cycle regulator, controls endoreplication onset in Arabidopsis thaliana.
Churchman ML, Brown ML, Kato N, Kirik V, Hulskamp M, Inze D, De Veylder L, Walker JD, Zheng Z, Oppenheimer DG, Gwin T, Churchman J, Larkin JC., Plant Cell 18(11), 2006
PMID: 17098811

Vlieghe K, Inze D, De L., 2007

Gheysen G, Mitchum MG., 2009
MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes.
Thimm O, Blasing O, Gibon Y, Nagel A, Meyer S, Kruger P, Selbig J, Muller LA, Rhee SY, Stitt M., Plant J. 37(6), 2004
PMID: 14996223
ATTED-II provides coexpressed gene networks for Arabidopsis.
Obayashi T, Hayashi S, Saeki M, Ohta H, Kinoshita K., Nucleic Acids Res. 37(Database issue), 2008
PMID: 18953027

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