Plant roots employ cell-layer-specific programs to respond to pathogenic and beneficial microbes

被引:61
作者
Froschel, Christian [1 ]
Komorek, Jaqueline [1 ]
Attard, Agnes [2 ]
Marsell, Alexander [1 ]
Lopez-Arboleda, William A. [3 ]
Le Berre, Joelle [2 ]
Wolf, Elmar [4 ]
Geldner, Niko [5 ]
Waller, Frank [1 ]
Korte, Arthur [3 ]
Droge-Laser, Wolfgang [1 ]
机构
[1] Julius Maximilians Univ Wurzburg, Julius von Sachs Inst, Dept Pharmaceut Biol, Julius von Sachs Pl 2, D-97082 Wurzburg, Germany
[2] Univ Cote dAzur, ISA, CNRS, INRAE, 400 Route Chappes, F-06903 Sophia Antipolis, France
[3] Julius Maximilians Univ Wurzburg, Ctr Computat & Theoret Biol, CCTB, Klara Oppenheimer Weg 32, D-97074 Wurzburg, Germany
[4] Julius Maximilians Univ Wurzburg, Bioctr, Dept Biochem & Mol Biol, D-97074 Wurzburg, Germany
[5] Univ Lausanne, Dept Plant Mol Biol, Biophore Bldg, CH-1015 Lausanne, Switzerland
关键词
ARABIDOPSIS ROOTS; PIRIFORMOSPORA-INDICA; IMMUNE-RESPONSES; GENE-EXPRESSION; VERTICILLIUM-LONGISPORUM; MESSENGER-RNA; GENOME-SCALE; ETHYLENE; DEFENSE; IMMUNOPURIFICATION;
D O I
10.1016/j.chom.2020.11.014
中图分类号
Q93 [微生物学];
学科分类号
071005 ; 100705 ;
摘要
Plant roots are built of concentric cell layers that are thought to respond to microbial infections by employing specific, genetically defined programs. Yet, the functional impact of this radial organization remains elusive, particularly due to the lack of genome-wide techniques for monitoring expression at a cell-layer resolution. Here, cell-type-specific expression of tagged ribosomes enabled the isolation of ribosome-bound mRNA to obtain cell-layer translatomes (TRAP-seq, translating ribosome affinity purification and RNA sequencing). After inoculation with the vascular pathogen Verticillium longisporum, pathogenic oomycete Phytophthora parasitica, or mutualistic endophyte Serendipita indica, root cell-layer responses reflected the fundamentally different colonization strategies of these microbes. Notably, V. longisporum specifically suppressed the endodermal barrier, which restricts fungal progression, allowing microbial access to the root central cylinder. Moreover, localized biosynthesis of antimicrobial compounds and ethylene differed in response to pathogens and mutualists. These examples highlight the power of this resource to gain insights into root-microbe interactions and to develop strategies in crop improvement.
引用
收藏
页码:299 / +
页数:19
相关论文
共 79 条
[1]   Phytoalexins in defense against pathogens [J].
Ahuja, Ishita ;
Kissen, Ralph ;
Bones, Atle M. .
TRENDS IN PLANT SCIENCE, 2012, 17 (02) :73-90
[2]   A critical review on fungi mediated plant responses with special emphasis to Piriformospora indica on improved production and protection of crops [J].
Ansari, Mohammad Wahid ;
Trivedi, Dipesh Kumar ;
Sahoo, Ranjan Kumar ;
Gill, Sarvajeet Singh ;
Tuteja, Narendra .
PLANT PHYSIOLOGY AND BIOCHEMISTRY, 2013, 70 :403-410
[3]   Transcriptome dynamics of Arabidopsis thaliana root penetration by the oomycete pathogen Phytophthora parasitica [J].
Attard, Agnes ;
Evangelisti, Edouard ;
Kebdani-Minet, Naima ;
Panabieres, Franck ;
Deleury, Emeline ;
Maggio, Cindy ;
Ponchet, Michel ;
Gourgues, Mathieu .
BMC GENOMICS, 2014, 15
[4]   The immediate activation of defense responses in Arabidopsis roots is not sufficient to prevent Phytophthora parasitica infection [J].
Attard, Agnes ;
Gourgues, Mathieu ;
Callemeyn-Torre, Nicolas ;
Keller, Harald .
NEW PHYTOLOGIST, 2010, 187 (02) :449-460
[5]   Microgenomics: Genome-Scale, Cell-Specific Monitoring of Multiple Gene Regulation Tiers [J].
Bailey-Serres, J. .
ANNUAL REVIEW OF PLANT BIOLOGY, VOL 64, 2013, 64 :293-325
[6]   Physical and Chemical Barriers in Root Tissues Contribute to Quantitative Resistance to Fusarium oxysporum f. sp pisi in Pea [J].
Bani, Moustafa ;
Perez-De-Luque, Alejandro ;
Rubiales, Diego ;
Rispail, Nicolas .
FRONTIERS IN PLANT SCIENCE, 2018, 9
[7]   Adaptation of Root Function by Nutrient-Induced Plasticity of Endodermal Differentiation [J].
Barberon, Marie ;
Vermeer, Joop Engelbertus Martinus ;
De Bellis, Damien ;
Wang, Peng ;
Naseer, Sadaf ;
Andersen, Tonni Grube ;
Humbel, Bruno Martin ;
Nawrath, Christiane ;
Takano, Junpei ;
Salt, David Edward ;
Geldner, Niko .
CELL, 2016, 164 (03) :447-459
[8]   A Glucosinolate Metabolism Pathway in Living Plant Cells Mediates Broad-Spectrum Antifungal Defense [J].
Bednarek, Pawel ;
Pislewska-Bednarek, Mariola ;
Svatos, Ales ;
Schneider, Bernd ;
Doubsky, Jan ;
Mansurova, Madina ;
Humphry, Matt ;
Consonni, Chiara ;
Panstruga, Ralph ;
Sanchez-Vallet, Andrea ;
Molina, Antonio ;
Schulze-Lefert, Paul .
SCIENCE, 2009, 323 (5910) :101-106
[9]   Cell type-specific expression profiting in plants via cell sorting of protoplasts from fluorescent reporter lines [J].
Birnbaum, K ;
Jung, JW ;
Wang, JY ;
Lambert, GM ;
Hirst, JA ;
Galbraith, DW ;
Benfey, PN .
NATURE METHODS, 2005, 2 (08) :615-619
[10]   Selective mRNA translation coordinates energetic and metabolic adjustments to cellular oxygen deprivation and reoxygenation in Arabidopsis thaliana [J].
Branco-Price, Cristina ;
Kaiser, Kayla A. ;
Jang, Charles J. H. ;
Larive, Cynthia K. ;
Bailey-Serres, Julia .
PLANT JOURNAL, 2008, 56 (05) :743-755