Poplar-root-knot nematode interaction: a model for perennial woody species

[en] Plant root-knot nematode interaction studies are performed on several host plant models. However, even though root-knot nematodes interact with trees, no perennial woody model has been explored so far. We show here that poplar (Populus tremula x Populus alba) grown in vitro is susceptible to Meloidogyne incognita as this nematode is able to penetrate, to induce feeding sites and to reproduce in poplar roots. As analyzed by Raman spectromicroscopy, the cell walls of the giant cells, with typical characteristics of transfer cell walls, were not lignified and were composed mainly of pectin and cellulose. To better depict the poplar-nematode interaction at the molecular level, a quantitative RT-PCR analysis was performed to study changes in poplar gene expression in galls compared to non-infected roots. Three marker genes, reported for other plant hosts, including expansin A, histone 3.1 and asparagine synthase, were conserved for poplar-nematode interaction. In addition, the down-regulation of four genes coding for enzymes of the lignin biosynthesis pathway was evidenced in galls, suggesting a modification in lignin composition within galls developed in poplar roots. Together, this study shows that poplar is a suitable model host for specific traits of tree-nematode interaction.

Research Center/Unit :

Centre Interfacultaire de Recherche du Médicament - CIRM

Disciplines :

Phytobiology (plant sciences, forestry, mycology...)

Author, co-author :

Baldacci-Cresp, Fabien

Sacre, Pierre-Yves ; Université de Liège > Département de pharmacie > Chimie analytique

Twyffels, Laure

Mol, Adeline

Vermeersch, Marjorie

Ziemons, Eric ; Université de Liège > Département de pharmacie > Département de pharmacie

Hubert, Philippe ; Université de Liège > Département de pharmacie > Chimie analytique

Pérez-Morga, David

El Jarizi, Mondher

de Almeida-Engler, Janice

Baucher, Marie

Language :

English

Title :

Poplar-root-knot nematode interaction: a model for perennial woody species

Publication date :

2016

Journal title :

Molecular Plant-Microbe Interactions

ISSN :

0894-0282

eISSN :

1943-7706

Publisher :

American Phytopathological Society, St Paul, United States - Minnesota

Volume :

Issue :

Pages :

560-572

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 28 April 2016

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Bibliography

Agarwal, U. P., Reiner, R. R., and Ralph, S. A. 2013. Estimation of cellulose crystallinity of lignocelluloses using near-IR FT-Raman spectroscopy and comparison of the Raman and Segal-WAXS methods. J. Agric. Food Chem. 61:103-113.
Ali, N., Chapuis, E., Tavoillot, J., and Mateille, T. 2014. Plant-parasitic nematodes associated with olive tree (Olea europaea L.) with a focus on the Mediterranean basin: A review. C. R. Biol. 337:423-442.
Andersen, C. L., Jensen, J. L., and Ørntoft, T. F. 2004. Normalization of real-time quantitative reverse transcription-PCR data: A model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res. 64:5245-5250.
Aylott, M. J., Casella, E., Tubby, I., Street, N. R., Smith, P., and Taylor, G. 2008. Yield and spatial supply of bioenergy poplar and willow shortrotation coppice in the UK. New Phytol. 178:358-370.
Azaiez, A., Boyle, B., Levée, V., and Séguin, A. 2009. Transcriptome profiling in hybrid poplar following interactions with Melampsora rust fungi. Mol. Plant-Microbe Interact 22:190-200.
Baldacci-Cresp, F., Chang, C., Maucourt, M., Deborde, C., Hopkins, J., Lecomte, P., Bernillon, S., Brouquisse, R., Moing, A., Abad, P., Hérouart, D., Puppo, A., Favery, B., and Frendo, P. 2012. (Homo)glutathione deficiency impairs root-knot nematode development in Medicago truncatula. PLoS Pathog. 8:e1002471.
Baldacci-Cresp, F., Maucourt, M., Deborde, C., Pierre, O., Moing, A., Brouquisse, R., Favery, B., and Frendo, P. 2015a. Maturation of nematode-induced galls in Medicago truncatula is related to water status and primary metabolism modifications. Plant Sci. 232:77-85.
Baldacci-Cresp, F., Moussawi, J., Leplé, J. C., Van Acker, R., Kohler, A., Candiracci, J., Twyffels, L., Spokevicius, A. V., Bossinger, G., Laurans, F., Brunel, N., Vermeersch, M., Boerjan, W., El Jaziri, M., and Baucher, M. 2015b. PtaRHE1, a Populus tremula × Populus alba RING-H2 protein of the ATL family, has a regulatory role in secondary phloem fibre development. Plant J. 82:978-990.
Banora, M. Y., Rodiuc, N., Baldacci-Cresp, F., Smertenko, A., Bleve-Zacheo, T., Mellilo, M. T., Karimi, M., Hilson, P., Evrard, J. L., Favery, B., Engler, G., Abad, P., and de Almeida Engler, J. 2011. Feeding cells induced by phytoparasitic nematodes require g-tubulin ring complex for microtubule reorganization. PLoS Pathog. 7:e1002343.
Barcala, M., García, A., Cabrera, J., Casson, S., Lindsey, K., Favery, B., García-Casado, G., Solano, R., Fenoll, C., and Escobar, C. 2010. Early transcriptomic events in microdissected Arabidopsis nematode-induced giant cells. Plant J. 61:698-712.
Bartlem, D. G., Jones, M. G. K., and Hammes, U. Z. 2014. Vascularization and nutrient delivery at root-knot nematode feeding sites in host roots. J. Exp. Bot. 65:1789-1798.
Baucher, M., Oukouomi Lowe, Y., Vandeputte, O. M., Mukoko Bopopi, J., Moussawi, J., Vermeersch, M., Mol, A., El Jaziri, M., Homblé, F., and Pérez-Morga, D. 2011. Ntann12 annexin expression is induced by auxin in tobacco roots. J. Exp. Bot. 62:4055-4065.
Bellafiore, S., and Briggs, S. P. 2010. Nematode effectors and plant responses to infection. Curr. Opin. Plant Biol. 13:442-448.
Bellafiore, S., Shen, Z., Rosso, M. N., Abad, P., Shih, P., and Briggs, S. P. 2008. Direct identification of the Meloidogyne incognita secretome reveals proteins with host cell reprogramming potential. PLoS Pathog. 4:e1000192.
Boerjan, W., Ralph, J., and Baucher, M. 2003. Lignin biosynthesis. Annu. Rev. Plant Biol. 54:519-546.
Brauchle, E., and Schenke-Layland, K. 2013. Raman spectroscopy in biomedicine - Non-invasive in vitro analysis of cells and extracellular matrix components in tissues. Biotechnol. J. 8:288-297.
Cabrera, J., Barcala, M., Fenoll, C., and Escobar, C. 2014. Transcriptomic signatures of transfer cells in early developing nematode feeding cells of Arabidopsis focused on auxin and ethylene signaling. Front. Plant Sci. 5:107.
Caillaud, M. C., Dubreuil, G., Quentin, M., Perfus-Barbeoch, L., Lecomte, P., de Almeida Engler, J., Abad, P., Rosso, M. N., and Favery, B. 2008. Root-knot nematodes manipulate plant cell functions during a compatible interaction. J. Plant Physiol. 165:104-113.
Chylińska, M., Szymańska-Chargot, M., and Zdunek, A. 2014. Imaging of polysaccharides in the tomato cell wall with Raman microspectroscopy. Plant Methods 10:14.
Clément, M., Ketelaar, T., Rodiuc, N., Banora, M. Y., Smertenko, A., Engler, G., Abad, P., Hussey, P. J., and de Almeida Engler, J. 2009. Actin-depolymerizing factor2-mediated actin dynamics are essential for root-knot nematode infection of Arabidopsis. Plant Cell 21:2963-2979.
Damiani, I., Baldacci-Cresp, F., Hopkins, J., Andrio, E., Balzergue, S., Lecomte, P., Puppo, A., Abad, P., Favery, B., and Hérouart, D. 2012. Plant genes involved in harbouring symbiotic rhizobia or pathogenic nematodes. New Phytol. 194:511-522.
de Almeida Engler, J., De Vleesschauwer, V., Burssens, S., Celenza, J. L., Jr., Inzé, D., Van Montagu, M., Engler, G., and Gheysen, G. 1999. Molecular markers and cell cycle inhibitors show the importance of cell cycle progression in nematode-induced galls and syncytia. Plant Cell 11: 793-808.
de Almeida Engler, J., Van Poucke, K., Karimi, M., De Groodt, R., Gheysen, G., Engler, G., and Gheysen, G. 2004. Dynamic cytoskeleton rearrangements in giant cells and syncytia of nematode-infected roots. Plant J. 38:12-26.
Donaldson, L. 2013. Softwood and hardwood lignin fluorescence spectra of wood cell walls in different mouting media. IAWA J. 34:3-19.
Eilers, P. H. C. 2004. Parametric time warping. Anal. Chem. 76:404-411.
Escobar, C., Barcala, M., Cabrera, J., and Fenoll, C. 2015. Overview of root-knot nematodes and giant cells. Pages 1-32 in: Advances in Botanical Research, Vol 73. Elsevier Ltd., Amsterdam.
Felten, J., Hall, H., Jaumot, J., Tauler, R., de Juan, A., and Gorzsás, A. 2015. Vibrational spectroscopic image analysis of biological material using multivariate curve resolution-alternating least squares (MCR-ALS). Nat. Protoc. 10:217-240.
Felten, J., Kohler, A., Morin, E., Bhalerao, R. P., Palme, K., Martin, F., Ditengou, F. A., and Legué, V. 2009. The ectomycorrhizal fungus Laccaria bicolor stimulates lateral root formation in poplar and Arabidopsis through auxin transport and signaling. Plant Physiol. 151:1991-2005.
Fernandez, D., Petitot, A.-S., Grossi de Sá, M., Nguŷn, V. P., de Almeida Engler, J., and Kyndt, T. 2015. Recent advances in understanding plantnematode interactions in monocots. Pages 189-219 in: Advances in Botanical Research, Vol 73. Elsevier Ltd., Amsterdam.
Franke, R., McMichael, C. M., Meyer, K., Shirley, A. M., Cusumano, J. C., and Chapple, C. 2000. Modified lignin in tobacco and poplar plants overexpressing the Arabidopsis gene encoding ferulate 5-hydroxylase. Plant J. 22:223-234.
Gal, T. Z., Aussenberg, E. R., Burdman, S., Kapulnik, Y., and Koltai, H. 2006. Expression of a plant expansin is involved in the establishment of root knot nematode parasitism in tomato. Planta 224:155-162.
Gheysen, G., and Mitchum, M. G. 2011. How nematodes manipulate plant development pathways for infection. Curr. Opin. Plant Biol. 14:415-421.
Gierlinger, N., Keplinger, T., and Harrington, M. 2012. Imaging of plant cell walls by confocal Raman microscopy. Nat. Protoc. 7:1694-1708.
Gierlinger, N., and Schwanninger, M. 2007. The potential of Raman microscopy and Raman imaging in plant research. Spectroscopy (Springf.) 21:69-89.
Goto, D. B., Miyazawa, H., Mar, J. C., and Sato, M. 2013. Not to be suppressed? Rethinking the host response at a root-parasite interface. Plant Sci. 213:9-17.
Grunewald, W., Karimi, M., Wieczorek, K., Van de Cappelle, E., Wischnitzki, E., Grundler, F., Inzé, D., Beeckman, T., and Gheysen, G. 2008. A role for AtWRKY23 in feeding site establishment of plantparasitic nematodes. Plant Physiol. 148:358-368.
Hamamouch, N., Li, C., Seo, P. J., Park, C. M., and Davis, E. L. 2011. Expression of Arabidopsis pathogenesis-related genes during nematode infection. Mol. Plant Pathol. 12:355-364.
Hipskind, J.,Wood, K., and Nicholson, R. L. 1996. Localized stimulation of anthocyanin accumulation and delineation of pathogen ingress in maize genetically resistant to Bipolaris maydis race O. Physiol. Mol. Plant Pathol. 49:247-256.
Holbein, J., Grundler, F. M. W., and Siddique, S. 2016. Plant basal resistance to nematodes: An update. J. Exp. Bot. 67:2049-2061.
Iberkleid, I., Sela, N., and Brown Miyara, S. 2015. Meloidogyne javanica fatty acid-and retinol-binding protein (Mj-FAR-1) regulates expression of lipid-, cell wall-, stress-and phenylpropanoid-related genes during nematode infection of tomato. BMC Genomics 16:272.
Ibrahim, H. M., Hosseini, P., Alkharouf, N. W., Hussein, E. H., Gamal El-Din, Ael. K., Aly, M. A., and Matthews, B. F. 2011. Analysis of gene expression in soybean (Glycine max) roots in response to the root knot nematode Meloidogyne incognita using microarrays and KEGG pathways. BMC Genomics 12:220.
Jammes, F., Lecomte, P., de Almeida-Engler, J., Bitton, F., Martin-Magniette, M. L., Renou, J. P., Abad, P., and Favery, B. 2005. Genomewide expression profiling of the host response to root-knot nematode infection in Arabidopsis. Plant J. 44:447-458.
Jansson, S., and Douglas, C. J. 2007. Populus: A model system for plant biology. Annu. Rev. Plant Biol. 58:435-458.
Jaubert, S., Ledger, T. N., Laffaire, J. B., Piotte, C., Abad, P., and Rosso, M. N. 2002. Direct identification of stylet secreted proteins from rootknot nematodes by a proteomic approach. Mol. Biochem. Parasitol. 121: 205-211.
Ji, H., Gheysen, G., Denil, S., Lindsey, K., Topping, J. F., Nahar, K., Haegeman, A., De Vos, W. H., Trooskens, G., Van Criekinge, W., De Meyer, T., and Kyndt, T. 2013. Transcriptional analysis through RNA sequencing of giant cells induced by Meloidogyne graminicola in rice roots. J. Exp. Bot. 64:3885-3898.
Ji, H., Kyndt, T., He, W., Vanholme, B., and Gheysen, G. 2015. b-Aminobutyric acid-induced resistance against root-knot nematodes in rice is based on increased basal defense.Mol. Plant-Microbe Interact 28:519-533.
Jones, M. G. K., and Northcote, D. H. 1972. Multinucleate transfer cells induced in coleus roots by the root-knot nematode, Meloidogyne arenaria. Protoplasma 75:381-395.
Karczmarek, A., Overmars, H., Helder, J., and Goverse, A. 2004. Feeding cell development by cyst and root-knot nematodes involves a similar early, local and transient activation of a specific auxin-inducible promoter element. Mol. Plant Pathol. 5:343-346.
Koenning, S. R., Overstreet, C., Noling, J. W., Donald, P. A., Becker, J. O., and Fortnum, B. A. 1999. Survey of crop losses in response to phytoparasitic nematodes in the United States for 1994. J. Nematol. 31 (4S):587-618.
Kyndt, T., Denil, S., Haegeman, A., Trooskens, G., Bauters, L., Van Criekinge, W., De Meyer, T., and Gheysen, G. 2012. Transcriptional reprogramming by root knot and migratory nematode infection in rice. New Phytol. 196:887-900.
Kyndt, T., Fernandez, D., and Gheysen, G. 2014. Plant-parasitic nematode infections in rice: Molecular and cellular insights. Annu. Rev. Phytopathol. 52:135-153.
Livak, K. J., and Schmittgen, T. D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2 D D C(T) method. Methods 25:402-408.
Lohar, D. P., Schaff, J. E., Laskey, J. G., Kieber, J. J., Bilyeu, K. D., and Bird, D. M. 2004. Cytokinins play opposite roles in lateral root formation, and nematode and rhizobial symbioses. Plant J. 38:203-214.
Mansfield, J. C., Littlejohn, G. R., Seymour, M. P., Lind, R. J., Perfect, S., and Moger, J. 2013. Label-free chemically specific imaging in planta with stimulated Raman scattering microscopy. Anal. Chem. 85: 5055-5063.
Mantelin, S., Thorpe, P., and Jones, J. T. 2015. Suppression of plant defences by plant-parasitic nematodes. Pages 325-337 in: Advances in Botanical Research, Vol 73. Elsevier Ltd., Amsterdam.
McClure, M. A., and Viglierchio, D. R. 1966. The influence of host nutrition and intensity of infection on the sex ratio and development of Meloidogyne incognita in sterile agar cultures of excised cucumber roots. Nematologica 12:248-258.
Meyer, K., Shirley, A. M., Cusumano, J. C., Bell-Lelong, D. A., and Chapple, C. 1998. Lignin monomer composition is determined by the expression of a cytochrome P450-dependent monooxygenase in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 95:6619-6623.
Moens, M., and Perry, R. N. 2009. Migratory plant endoparasitic nematodes: A group rich in contrasts and divergence. Annu. Rev. Phytopathol. 47:313-332.
Naoumkina, M. A., Zhao, Q., Gallego-Giraldo, L., Dai, X., Zhao, P. X., and Dixon, R. A. 2010. Genome-wide analysis of phenylpropanoid defence pathways. Mol. Plant Pathol. 11:829-846.
Ohri, P., and Pannu, S. K. 2010. Effect of phenolic compounds on nematodes - A review. J. App. Nat. Sci. 2:344-350.
Petry, R., Schmitt, M., and Popp, J. 2003. Raman spectroscopy - A prospective tool in the life sciences. ChemPhysChem 4:14-30.
Pettengill, E. A., Parmentier-Line, C., and Coleman, G. D. 2012. Evaluation of qPCR reference genes in two genotypes of Populus for use in photoperiod and low-temperature studies. BMC Res. Notes 5:366.
Polle, A., Janz, D., Teichmann, T., and Lipka, V. 2013. Poplar genetic engineering: Promoting desirable wood characteristics and pest resistance. Appl. Microbiol. Biotechnol. 97:5669-5679.
Portillo, M., Cabrera, J., Lindsey, K., Topping, J., Andrés, M. F., Emiliozzi, M., Oliveros, J. C., García-Casado, G., Solano, R., Koltai, H., Resnick, N., Fenoll, C., and Escobar, C. 2013. Distinct and conserved transcriptomic changes during nematode-induced giant cell development in tomato compared with Arabidopsis: A functional role for gene repression. New Phytol. 197:1276-1290.
Rodiuc, N., Vieira, P., Banora, M. Y., and de Almeida Engler, J. 2014. On the track of transfer cell formation by specialized plant-parasitic nematodes. Front. Plant Sci. 5:160.
Roman, M., Dobrowolski, J. C., Baranska, M., and Baranski, R. 2011. Spectroscopic studies on bioactive polyacetylenes and other plant components in wild carrot root. J. Nat. Prod. 74:1757-1763.
Sampedro, J., and Cosgrove, D. J. 2005. The expansin superfamily. Genome Biol. 6:242.
Santamour, F. S., Jr., and Batzli, J. M. 1990. Root-knot nematodes on willows: Screening of Salix species, cultivars, and hybrids for resistance. J. Arbor. 16:190-196.
Sasanelli, N., and Pierangeli, D. 1994. Response of selected forest trees to Meloidogyne incognita infections. Nematol. Medit. 22:83-85.
Savitzky, A., and Golay, M. J. E. 1964. Smoothing and differentiation of data by simplified least squares procedures. Anal. Chem. 36:1627-1639.
Shi, R., Sun, Y. H., Li, Q., Heber, S., Sederoff, R., and Chiang, V. L. 2010. Towards a systems approach for lignin biosynthesis in Populus trichocarpa: Transcript abundance and specificity of the monolignol biosynthetic genes. Plant Cell Physiol. 51:144-163.
Slavov, G., and Zhelev, P. 2010. Salient biological features, systematics, and genetic variation of Populus. Pages 15-38 in: Genetics and genomics of Populus. Springer, New York.
Triantaphyllou, A. C. 1960. Sex determination in Meloidogyne incognita Chitwood 1949 and intersexuality in M. javanica (Treub, 1885) Chitwood, 1949. Ann. Inst. Phytopath. Benaki 3:12-31.
Trudgill, D. L., and Blok, V. C. 2001. Apomictic, polyphagous root-knot nematodes: Exceptionally successful and damaging biotrophic root pathogens. Annu. Rev. Phytopathol. 39:53-77.
Uragami, C., Galzerano, D., Gall, A., Shigematsu, Y., Meisterhans, M., Oka, N., Iha, M., Fujii, R., Robert, B., and Hashimoto, H. 2014. Light-dependent conformational change of neoxanthin in a siphonous green alga, Codium intricatum, revealed by Raman spectroscopy. Photosynth. Res. 121:69-77.
Van Doorsselaere, J., Baucher, M., Chognot, E., Chabbert, B., Tollier, M.-T., Petit-Conil, M., Leplé, J.-C., Pilate, G., Cornu, D., Monties, B., Montagu, M., Inzé, D., Boerjan, W., and Jouanin, L. 1995. A novel lignin in poplar trees with a reduced caffeic acid/5-hydroxyferulic acid O-methyltransferase activity. Plant J. 8:855-864.
Vanholme, B., Cesarino, I., Goeminne, G., Kim, H., Marroni, F., Van Acker, R., Vanholme, R., Morreel, K., Ivens, B., Pinosio, S., Morgante, M., Ralph, J., Bastien, C., and Boerjan, W. 2013. Breeding with rare defective alleles (BRDA): A natural Populus nigra HCT mutant with modified lignin as a case study. New Phytol. 198:765-776.
Vanholme, R., Morreel, K., Darrah, C., Oyarce, P., Grabber, J. H., Ralph, J., and Boerjan,W. 2012a. Metabolic engineering of novel lignin in biomass crops. New Phytol. 196:978-1000.
Vanholme, R., Storme, V., Vanholme, B., Sundin, L., Christensen, J. H., Goeminne, G., Halpin, C., Rohde, A., Morreel, K., and Boerjan, W. 2012b. A systems biology view of responses to lignin biosynthesis perturbations in Arabidopsis. Plant Cell 24:3506-3529.
Vieira, P., Kyndt, T., Gheysen, G., and de Almeida Engler, J. 2013. An insight into critical endocycle genes for plant-parasitic nematode feeding sites establishment. Plant Signal. Behav. 8:e24223.
Wan, X., Landhäusser, S. M., Lieffers, V. J., and Zwiazek, J. J. 2006. Signals controlling root suckering and adventitious shoot formation in aspen (Populus tremuloides). Tree Physiol. 26:681-687.
Wieczorek, K. 2015. Cell wall alterations in nematode-infected roots. Pages 61-90 in: Advances in Botanical Research, Vol 73. Elsevier Ltd., Amsterdam.
Wuyts, N., Lognay, G., Swennen, R., and De Waele, D. 2006. Nematode infection and reproduction in transgenic and mutant Arabidopsis and tobacco with an altered phenylpropanoid metabolism. J. Exp. Bot. 57: 2825-2835.