Skip to main content

Advertisement

Log in

Transcriptional regulation of defence genes and involvement of the WRKY transcription factor in arbuscular mycorrhizal potato root colonization

  • Original Paper
  • Published:
Functional & Integrative Genomics Aims and scope Submit manuscript

Abstract

The establishment of arbuscular mycorrhizal associations causes major changes in plant roots and affects significantly the host in term of plant nutrition and resistance against biotic and abiotic stresses. As a consequence, major changes in root transcriptome, especially in plant genes related to biotic stresses, are expected. Potato microarray analysis, followed by real-time quantitative PCR, was performed to detect the wide transcriptome changes induced during the pre-, early and late stages of potato root colonization by Glomus sp. MUCL 41833. The microarray analysis revealed 526 up-regulated and 132 down-regulated genes during the pre-stage, 272 up-regulated and 109 down-regulated genes during the early stage and 734 up-regulated and 122 down-regulated genes during the late stage of root colonization. The most important class of regulated genes was associated to plant stress and in particular to the WRKY transcription factors genes during the pre-stage of root colonization. The expression profiling clearly demonstrated a wide transcriptional change during the pre-, early and late stages of root colonization. It further suggested that the WRKY transcription factor genes are involved in the mechanisms controlling the arbuscular mycorrhizal establishment by the regulation of plant defence genes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Balestrini R, Josè-Estanyol M, Puigdomènech P, Bonfante P (1997) Hydroxyproline rich glycoprotein mRNA accumulation in maize root cells colonized by the arbuscular mycorrhizal fungus as revealed by in situ hybridization. Protoplasma 19:36–42

    Article  Google Scholar 

  • Bolle C (2004) The role of GRAS proteins in plant signal transduction and development. Planta 218:683–692

    Article  PubMed  CAS  Google Scholar 

  • Brechenmacher L, Weidmann S, van Tuinen D, Chatagnier O, Gianinazzi S, Franken P, Gianinazzi-Pearson V (2004) Expression profiling of up-regulated plant and fungal genes in early and late stages of Medicago truncatula-Glomus mosseae interactions. Mycorrhiza 14:253–262

    Article  PubMed  CAS  Google Scholar 

  • Chabaud M, Genre A, Sieberer BJ, Faccio A, Fournier J, Novero M, Barker DG, Bonfante P (2011) Arbuscular mycorrhizal hyphopodia and germinated spore exudates trigger Ca2+ spiking in the legume and nonlegume root epidermis. New Phytol 189:347–355

    Article  PubMed  CAS  Google Scholar 

  • Chang MM, Hadwiger LA, Horovitz D (1992) Molecular characterization of a pea β-1,3-glucanase induced by Fusarium solani and chitosan challenge. Plant Mol Biol 20:609–618

    Article  PubMed  CAS  Google Scholar 

  • Colebatch G, Desbrosses G, Ott T, Krusell L, Montanari O, Kloska S, Kopka J, Udvardi MK (2004) Global changes in transcription orchestrate metabolic differentiation during symbiotic nitrogen fixation in Lotus japonicus. Plant J 39:487–512

    Article  PubMed  Google Scholar 

  • Cranenbrouck S, Voets L, Bivort C, Renard L, Stullu DG, Declerck S (2005) Methodologies for in vitro cultivation of arbuscular mycorrhizal fungi with root organs. In: Declerck S, Strullu DG, Fortin JA (eds) In vitro culture of mycorrhizas. Springer, Berlin, pp 341–348

    Chapter  Google Scholar 

  • Declerck S, Strullu DG, Plenchette C (1998) Monoxenic culture of the intraradical forms of Glomus sp. isolated from a tropical ecosystem: a proposed methodology for germplasm collection. Mycologia 90:579–585

    Article  Google Scholar 

  • Dermatsev V, Weingarten-Baror C, Resnick N, Gadkar V, Wininger S, Kolotilin I, Mayzlish-Gati E, Zilberstein A, Koltai H, Kapulnik Y (2010) Microarray analysis and functional tests suggest the involvement of expansins in the early stages of symbiosis of the arbuscular mycorrhizal fungus Glomus intraradices on tomato (Solanum lycopersicum). Mol Plant Pathol 11:121–135

    Article  PubMed  CAS  Google Scholar 

  • Doner LW, Becard G (1991) Solubilisation of gellan gels by chelation of cations. Biotechnol Tech 5:25–28

    Article  CAS  Google Scholar 

  • Dubos C, Stracke R, Grotewold E, Weisshaar B, Martin C, Lepiniec L (2010) MYB transcription factors in Arabidopsis. Trends Plant Sci 15:573–581

    Article  PubMed  CAS  Google Scholar 

  • Fiorilli V, Catoni M, Miozzi L, Novero M, Accotto GP, Lanfranco L (2009) Global and cell-type gene expression profiles in tomato plants colonized by an arbuscular mycorrhizal fungus. New Phytol 184:975–987

    Article  PubMed  CAS  Google Scholar 

  • Franken P, Donges K, Grunwald U, Kost G, Rexr KH, Tamasloukht MB, Waschke A, Zeuske D (2007) Gene expression analysis of arbuscule development and functioning. Phytochemistry 68:68–74

    Article  PubMed  CAS  Google Scholar 

  • Gallou A, Cranenbrouck S, Declerck S (2009) Trichoderma harzianum elicit defence response genes in roots of potato plantlets challenged by Rhizoctonia solani. Eur J Plant Pathol 124:219–230

    Article  Google Scholar 

  • Gallou A, De Jaeger N, Cranenbrouck S, Declerck S (2010) Fast track in vitro mycorrhization of potato plantlets allow studies on gene expression dynamics. Mycorrhiza 20:201–207

    Article  PubMed  CAS  Google Scholar 

  • Genre A, Chabaud M, Timmers T, Bonfante P, Barker DG (2005) Arbuscular mycorrhizal fungi elicit a novel intracellular apparatus in Medicago truncatula root epidermal cells before infection. Plant Cell 17:3489–3499

    Article  PubMed  CAS  Google Scholar 

  • Gomez SK, Javot H, Deewatthanawong P, Torres-Jerez I, Tang Y, Blancaflor EB, Udvardi MK, Harrison MJ (2009) Medicago truncatula and Glomus intraradices gene expression in cortical cells harboring arbuscules in the arbuscular mycorrhizal symbiosis. BMC Plant Biol 9:10

    Article  PubMed  Google Scholar 

  • Guether M, Balestrini R, Hannah M, He J, Udvardi MK, Bonfante P (2009) Genome-wide reprogramming of regulatory networks, transport, cell wall and membrane biogenesis during arbuscular mycorrhizal symbiosis in Lotus japonicus. New Phytol 182:200–212

    Article  PubMed  CAS  Google Scholar 

  • Güimil S, Chang H-S, Zhu T, Sesma A, Osbourn A, Roux C, Ioannidis V, Oakeley EJ, Docquier M, Descombes P, Briggs SP, Paszkowski U (2005) Comparative transcriptomics of rice reveals an ancient pattern of response to microbial colonization. Proc Natl Acad Sci USA 102:8066–8070

    Article  PubMed  Google Scholar 

  • Hause B, Mrosk C, Isayenkov S, Strack D (2007) Jasmonates in arbuscular mycorrhizal interactions. Phytochemistry 68:101–110

    Article  PubMed  CAS  Google Scholar 

  • Heckmann AB, Lombardo F, Miwa H, Perry JA, Bunnewell S, Parniske M, Wang TL, Downie JA (2006) Lotus japonicus nodulation requires two GRAS-domain regulators, one of which is functionally conserved in a non-legume. Plant Physiol 142:1739–1750

    Article  PubMed  CAS  Google Scholar 

  • Herrera-Medina MJ, Steinkellner S, Vierheilig H, Ocampo JA, García-Garrido JM (2007) Abscisic acid determines arbuscule development and functionality in the tomato arbuscular mycorrhiza. New Phytol 175:554–564

    Article  PubMed  CAS  Google Scholar 

  • Herrera-Medina MJ, Tamayo M, Vierheilig H, Ocampo JA, García-Garrido JM (2008) The jasmonic acid signalling pathway restricts the development of the arbuscular mycorrhizal association in tomato. J Plant Growth Regul 27:221–230

    Article  CAS  Google Scholar 

  • Hohnjec N, Vieweg MF, Pühler A, Becker A, Küster H (2005) Overlaps in the transcriptional profiles of Medicago truncatula roots inoculated with two different Glomus fungi provide insights into the genetic program activated during arbuscular mycorrhiza. Plant Physiol 137:1283–1301

    Article  PubMed  CAS  Google Scholar 

  • Hwang IS, Hwang BK (2010) The pepper 9-lipoxygenase gene CaLOX1 functions in defense and cell death responses to microbial pathogens. Plant Physiol 152:948–967

    Article  PubMed  CAS  Google Scholar 

  • Kapulnik Y, Volpin H, Itzhaki H, Ganon D, Galili S, David R, Shaul O, Elad Y, Chet I, Okon Y (1996) Suppression of defence responses in mycorrhizal alfalfa and tobacco roots. New Phytol 133:59–64

    Article  Google Scholar 

  • Kasprzewska A (2003) Plant chitinases—regulation and function. Cell Mol Biol Lett 8:809–824

    PubMed  CAS  Google Scholar 

  • Kloosterman B, De Koeyer D, Griffiths R, Flinn B, Steuernagel B, Scholz U, Sonnewald S, Sonnewald U, Bryan GJ, Prat S et al (2008) Genes driving potato tuber initiation and growth: identification based on transcriptional changes using the POCI array. Funct Integr Genomics 8:329–340

    Article  PubMed  CAS  Google Scholar 

  • Knoth C, Ringler J, Dangl JL, Eulgem T (2007) Arabidopsis WRKY70 is required for full RPP4-mediated disease resistance and basal defense against Hyaloperonospora parasitica. Mol Plant Microbe Interact 20:120–128

    Article  PubMed  CAS  Google Scholar 

  • Kosuta S, Hazledine S, Sun J, Miwa H, Morris RJ, Downie JA, Oldroyd GED (2008) Differential and chaotic calcium signatures in the symbiosis signaling pathway of legumes. Proc Natl Acad Sci USA 105:9823–9828

    Article  PubMed  CAS  Google Scholar 

  • Kurepa J, Smalle JA (2008) Structure, function and regulation of plant proteasomes. Biochimie 90:324–335

    Article  PubMed  CAS  Google Scholar 

  • Li J, Brader G, Kariola T, Tapio Palva E (2006) WRKY70 modulates the selection of signalling pathways in plant defense. Plant J 46:477–491

    Article  PubMed  CAS  Google Scholar 

  • Liu J, Blaylock LA, Endre G, Cho J, Town CD, Vanden Bosch KA, Harrison MJ (2003) Transcript profiling coupled with spatial expression analyses reveals genes involved in distinct developmental stages of the arbuscular mycorrhizal symbiosis. Plant Cell 15:2106–2123

    Article  PubMed  CAS  Google Scholar 

  • Liu J, Maldonado-Mendoza I, Lopez-Meyer M, Cheung F, Town CD, Harrison MJ (2007) Arbuscular mycorrhizal symbiosis is accompanied by local and systemic alterations in gene expression and an increase in disease resistance in the shoots. Plant J 50:529–544

    Article  PubMed  CAS  Google Scholar 

  • Lopez-Raez JA, Verhage A, Fernandez I, Garcia JM, Azcon-Aguilar C, Flors V, Pozo MJ (2010) Hormonal and transcriptional profiles highlight common and differential host responses to arbuscular mycorrhizal fungi and the regulation of the oxylipin pathway. J Exp Bot 10:2589–2601

    Article  Google Scholar 

  • Martin-Rodriguez JA, Leon-Morcillo R, Vierheilig H, Ocampo JA, Ludwig-Müller J, Garcia-Garrido JM (2011) Ethylene dependent⁄ethylene-independent ABA regulation of tomato plants colonized by arbuscular mycorrhiza fungi. New Phytol 190:193–205

    Article  CAS  Google Scholar 

  • Mauch F, Staehelin LA (1989) Functional implication of the subcellular localization of ethylene-induced chitinase and β-1,3-glucanase in bean leaves. Plant Cell 1:447–457

    Article  PubMed  CAS  Google Scholar 

  • McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA (1990) A new method which gives an objective measure of colonization of roots by vesicular–arbuscular mycorrhizal fungi. New Phytol 115:495–501

    Article  Google Scholar 

  • Medina MJH, Gagnon H, Piché Y, Ocampo JA, García Garrido JM, Vierheilig H (2003) Root colonization by arbuscular mycorrhizal fungi is affected by the salicylic acid content of the plant. Plant Sci 164:993–998

    Article  Google Scholar 

  • Meixner C, Ludwig-Müller J, Miersch O, Gresshoff P, Staehelin C, Vierheilig H (2005) Lack of mycorrhizal autoregulation and phytohormonal changes in the supernodulating soybean mutant nts1007. Planta 222:709–715

    Article  PubMed  CAS  Google Scholar 

  • Navazio L, Moscatiello R, Genre A, Novero M, Baldan B, Bonfante P, Mariani P (2007) A diffusible signal from arbuscular mycorrhizal fungi elicits a transient cytosolic calcium elevation in host plant cells. Plant Physiol 144:673–681

    Article  PubMed  CAS  Google Scholar 

  • Pandley SP, Somssich E (2009) The role of WRKY transcription factors in plant immunity. Plant Physiol 150:1648–1655

    Article  Google Scholar 

  • Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30:e36

    Article  PubMed  Google Scholar 

  • Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Brit Mycol Soc 55:158–161

    Article  Google Scholar 

  • Pozo MJ, Azcón-Aguilar C (2007) Unravelling mycorrhiza induced resistance. Curr Opin Plant Biol 10:393–398

    Article  PubMed  CAS  Google Scholar 

  • Pozo MJ, Verhage A, Jung SC, Lopez-Raez JA, Azcón-Aguilar C (2010) Impact of arbuscular mycorrhizal symbiosis on plant response to biotic stress: the role of plant defence mechanisms. In: Koltai H, Kapulnik Y (eds) Arbuscular mycorrhiza: physiology and function. Springer, Berlin, pp 193–207

    Chapter  Google Scholar 

  • Rausch C, Daram P, Brunner S, Jansa J, Laloi M, Leggewie G, Amrhein N, Bucher M (2001) A phosphate transporter expressed in arbuscule-containing cells in potato. Nature 414:462–466

    Article  PubMed  CAS  Google Scholar 

  • Riedel T, Groten K, Baldwin IT (2008) Symbiosis between Nicotiana attenuata and Glomus intraradices: ethylene plays a role, jasmonic acid does not. Plant Cell Environ 31:1203–1213

    Article  PubMed  CAS  Google Scholar 

  • Rotter A, Usadel B, Baebler S, Stitt M, Gruden K (2007) Adaptation of the MapMan ontology to biotic stress responses: application in solanaceous species. Plant Methods 3:1

    Article  Google Scholar 

  • Ruíz-Lozano JM, Roussel H, Gianinazzi S, Gianinazzi-Pearson V (1999) Defense genes are differentially induced by a mycorrhizal fungus and Rhizobium sp. in wild-type and symbiosis-defective pea genotypes. Mol Plant Microbe Interact 12:976–984

    Article  Google Scholar 

  • Rushton PJ, Somssich IE, Ringler P, Shen QJ (2010) WRKY transcription factors. Trends Plant Sci 15:247–258

    Article  PubMed  CAS  Google Scholar 

  • Salzer P, Bonanomi A, Beyer K, Vogeli-Lange R, Aeschbacher RA, Lange J, Wiemken A, Kim D, Cook DR, Boller T (2000) Differential expression of eight chitinase genes in Medicago truncatula roots during mycorrhiza formation, nodulation, and pathogen infection. Mol Plant Microbe Interact 13:763–777

    Article  PubMed  CAS  Google Scholar 

  • Sanchez L, Weidmann S, Brechenmacher L, Batoux M, van Tuinen D, Lemanceau P, Gianinazzi S, Gianinazzi-Pearson V (2004) Common gene expression in Medicago truncatula roots in response to Pseudomonas fluorescens colonization, mycorrhiza development and nodulation. New Phytol 161:855–863

    Article  CAS  Google Scholar 

  • Schüβler A, Schwarzott D, Walker C (2001) A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 105:1413–1421

    Article  Google Scholar 

  • Siciliano V, Genre A, Balestrini R, Cappellazo G, de Wit PJGM, Bonfante P (2007) Transcriptome analysis of arbuscular mycorrhizal roots during development of the prepenetration appartus. Plant Physiol 144:1455–1466

    Article  PubMed  CAS  Google Scholar 

  • Smit P, Raedts J, Portyanko V, Debelle F, Gough C, Bisseling T, Geurts R (2005) NSP1 of the GRAS protein family is essential for rhizobial Nod factor-induced transcription. Science 308:1789–1791

    Article  PubMed  CAS  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic, Cambridge

    Google Scholar 

  • Stumpe M, Carsjens JG, Stenzel I, Gobel C, Lang I, Pawlowski K, Hause B, Feussner I (2005) Lipid metabolism in arbuscular mycorrhizal roots of Medicago truncatula. Phytochemistry 66:781–791

    Article  PubMed  CAS  Google Scholar 

  • Takeda N, Sato S, Asamizu E, Tabata S, Parniske M (2009) Apoplastic plant subtilases support arbuscular mycorrhiza development in Lotus japonicus. Plant J 58:766–777

    Article  PubMed  CAS  Google Scholar 

  • Thibaud-Nissen F, Wu H, Richmond T, Redman JC, Johnson C, Green R, Arias J, Town CD (2006) Development of Arabidopsis whole-genome microarrays and their application to the discovery of binding sites for the TGA2 transcription factor in salicylic acid-treated plants. Plant J 47:152–162

    Article  PubMed  CAS  Google Scholar 

  • Tkizawa M, Goto A, Watanabe Y (2005) The tobacco ubiquitin-activating enzymes NtE1A and NtE1B are induced by tobacco virus, wounding and stress hormones. Mol Cells 19:228–231

    Google Scholar 

  • Voets L, Dupré de Boulois H, Renard L, Strullu DG, Declerck S (2005) Development of an autotrophic culture system for the in vitro mycorrhization of potato plantlets. FEMS Microbiol Lett 248:111–118

    Article  PubMed  CAS  Google Scholar 

  • Voets L, de la Providencia IE, Fernandez K, IJdo M, Cranenbrouck S, Declerck S (2009) Extraradical mycelium network of arbuscular mycorrhizal fungi allows fast colonization of seedlings under in vitro conditions. Mycorrhiza 19:346–356

    Article  Google Scholar 

  • Walter MH, Floss DS, Hans J, Fester T, Strack D (2007) Apocarotenold biosynthesis in arbuscular mycorrhizal roots: contributions from methylerythritol phosphate pathway isogenes and tools for its manipulation. Phytochemistry 68:130–138

    Article  PubMed  CAS  Google Scholar 

  • Wang D, Amornsiripanitch N, Dong X (2006) A genomic approach to identify regulatory nodes in the transcriptional network of systemic acquired resistance in plants. PLoS Pathog 2:123

    Article  Google Scholar 

  • Wasternack C, Stenzel I, Hause B, Hause G, Kutter C, Maucher H, Neumerkel J, Feussner I, Miersch O (2006) The wound response in tomato—role of jasmonic acid. J Plant Physiol 163:297–306

    Article  PubMed  CAS  Google Scholar 

  • Weidmann S, Sanchez L, Descombin J, Chatagnier O, Gianinazzi S, Gianinazzi-Pearson V (2004) Fungal elicitation of signal transduction-related plant genes precedes mycorrhiza establishment and requires the dmi3 gene in Medicago truncatula. Mol Plant Microbe Interact 17:1385–1393

    Article  PubMed  CAS  Google Scholar 

  • Zhang Q, Blaylock LA, Harrison MJ (2010) Two Medicago truncatula half-ABC transporters are essential for arbuscule development in arbuscular mycorrhizal symbiosis. Plant Cell 22:1483–1497

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This research was supported by the Direction générale opérationnelle de l’Agriculture, des Ressources naturelles et de l’Environnement du service public de wallonie under contract number D31-1149, entitled Valorisation de la microflore bénéfique des sols pour le contrôle de la flore pathogène des productions de pomme de terre comme alternative à l’utilisation des pesticides. S.C. gratefully acknowledges the financial contribution of the Belgian Federal Science Policy Office (contract BCCM C4/00/001). We thank André Clippe, Institut of Life Science of the Université catholique de Louvain, for technical assistance in microarray experiment.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sylvie Cranenbrouck.

Electronic supplementary materials

Below is the link to the electronic supplementary material.

Fig. S1

The MapMan Metabolism Overview display created using the 865 regulated genes identified from the late stage versus the control comparison. This figure shows the impact of Glomus sp. MUCL 41833 during the late stage of potato roots colonization on the genes involved in metabolism process. In particular, the induction of the genes related to the biosynthesis of mycorradicin (i.e. 1-deoxy-d-xylulose 5-phosphate synthase 2 (DXS-2; MICRO.13123.C1), 1-deoxy-d-xylulose 5-phosphate reductoisomerase (DXR; MICRO.5323.C2), phytoene desaturase (PDS; MICRO.11694.C2 and MICRO.5233.C2), zeta-carotene desaturase (ZDS; MICRO.4706.C1) and carotenoid isomerase (CRTISO)) in the secondary metabolism process of terpenes. The fold change is displayed as illustrated in the fold change colour bar in the upper right of each panel (blue is repressed and red is induced) (DOC 101 kb)

Table S1

Primer sequences and amplification length of the genes used in the real-time quantitative PCR analysis (DOC 42.5 kb)

Table S2

Root colonization and total phosphorus content of the leaves of potato plantlets grown 12 days in presence (i.e. +AMF) or absence (i.e. −AMF) of an actively growing extra-radical mycelium networks of Glomus sp. MUCL 41833 (DOC 35.5 kb)

Table S3

The 658 genes regulated during the pre-stage of potato root colonization by Glomus sp. MUCL 41833 as compared with the control treatment, and their changes in expression (XLS 117 kb)

Table S4

The 381 genes regulated during the early stage of potato root colonization by Glomus sp. MUCL 41833 as compared with the control treatment, and their changes in expression (XLS 74.5 kb)

Table S5

The 865 genes regulated during the late stage of potato root colonization by Glomus sp. MUCL 41833 as compared with the control treatment, and their changes in expression (XLS 146 kb)

Table S6

Overview of the ethylene (ET), acid salicylic (SA) and jasmonic acid (JA) marker genes during the pre-, early and late stages of potato root colonization by Glomus sp. MUCL 41833 as compared with the control treatments, and their changes in expression (XLS 24.0 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gallou, A., Declerck, S. & Cranenbrouck, S. Transcriptional regulation of defence genes and involvement of the WRKY transcription factor in arbuscular mycorrhizal potato root colonization. Funct Integr Genomics 12, 183–198 (2012). https://doi.org/10.1007/s10142-011-0241-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10142-011-0241-4

Keywords

Navigation