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Janice de Almeida Engler

• Director of Research at the “Institut National de la Recherche Agronomique”
• UMR “Institut Sophia Agrobiotech” (ISA) grouping INRA/UCA/CNRS

Mailing Address

UMR Institut Sophia Agrobiotech
INRA 1355-UCA-CNRS 7254
400, Route des Chappes BP 167
06903 Sophia Antipolis, France
Tel: +33(0)492386459

Email: Janice.de-almeida@inrae.fr

Degree(s)

• HDR 2009 Université Nice-Sophia Antipolis
• PhD 1991 Universidade Federal do Rio de Janeiro
• MS 1985 Pennsylvania State University
• BSc 1978 Universidade de Brasilia

Research interests

My career has been committed to research in the field of plant biology and plant parasitic nematology. Until 2003 I have been a researcher at the Department of Plant System Biology at the VIB (Flemish Institute for Biotechnology) in Ghent (Belgium). Since 2003 I am a researcher and group leader at INRA UMR ISA at Sophia Antipolis (France). My group is interested in the “Identification and characterization of determinants of susceptibility of plant hosts to endoparasitic nematodes aiming the development of new strategies for phytoprotection”. My work focuses on the plant cell cycle and cytoskeleton rearrangements occurring in nematode-induced feeding sites (NFS) with as major goal to generate fundamental knowledge on the ontogeny of root-knot nematode (RKN)-induced galls and sideway plant cells, aiming to generate data that will allow us to develop novel strategies of resistance conducting to nematode control.

My studies have shown that nematodes are capable to maneuver the plant cell cycle (B2, B4, B5) as well as to disarray the cytoskeleton (B3) in their favor (10, 11). A focal approach is to identify and functionally analyze major components which drive the cell cycle machinery during nematode infection in plants, using Arabidopsis thaliana as a model host. For that, my group makes use of diverse methodologies from molecular to cell biology, Tap-TAG technology (collaboration with the PSB-VIB, Belgium) and MALDI-MSI imaging (collaboration with Embrapa, Brazil). Several microscopy techniques have been profoundly applied in my research during the last 25 years of my career (B2).

In order to identify key elements responsible for the induction of the aberrant cell cycles in nematode-induced giant-feeding cells (GC), my studies have gained depth by performing mRNA in situ hybridization (ISH) analyses of 61 core cell cycle genes in plants (9) and mitotic GC and in amitotic syncytia (induced by cyst nematodes). Functional studies performed in my group on genes involved in cell cycle progression and inhibition (KRP and SMR gene families and DEL1) (1, 2, 3, 4, 5) have shown that cell cycle activating and control genes are early expressed in galls and are important for NFS induction and development (CDKA;1, CDKB1;1, CYCB1;1; CYCA2;1, CKS1, CCS52A1, CCS52A2, CCS52B, WEE1, ABAP1, AIP10, E2Fa, E2Fb, ERF115, PAT1). My group has also demonstrated that all 7 members of the KRP gene family of cell cycle inhibitors when ectopically expressed drastically inhibit feeding sites induced by plant parasitic root-knot nematodes growth and development (1, 2, 3, 5). An interesting observation was that when 6 KRP genes inhibit the mitotic cycle, one (KRP6) induces mitotic nuclear division. Therefore, the KRP6 has been the first gene identified associated to giant-feeding cell multinucleation (2).

Former studies in my group have shown that in giant cells induced by RKN the mitotic microtubular and actin cytoskeleton are rearranged, partially broken down and disordered consequently leading to aborted cytokinetic events (10). We have shown that g-tubulin proteins are highly present in feeding cells and functional studies in vivo and in situ localization have illustrated the potential function of this protein complexed in gamma-TURCs, possibly regulating the dynamics of the MT cytoskeleton (6). By studying an actin depolymerizing factor protein (ADF2) in giant cells we found out that stabilization of the cytoplasmic cytoskeleton may affect nematode feeding (8).  Actually we are studying a family of actin cross-linking proteins of the Fimbrin family (5 members in Arabidopsis) and preliminary data suggest that FIM2 loss of function affects gall development and consequently nematode reproduction.

My work has also been devoted to methodology development which includes: Whole-mount (WISH; B6) and sectioned plant tissue ISH methods (B1); In situ localization of nematode secreted proteins in plants using nematode & gall tissue sections as well as vibroslices to visualize in vivo cytoskeleton and cell cycle proteins for studying their dynamics (7); Whole cleared galls for in depth 3D observations (5); Nuclear volume measurements combined with stains like DAPI adapted for nematode-induced galls; Protocol development for MALDI-MSI imaging of galls.

My group has tight international collaborations and recent studies on effectors during nematodes and rice interaction are performed with Ghent University (Agricultural Faculty, Belgium) and IRD (France). Studies with poplar as a model host for root-knot nematode infections are done in collaboration with the ULB and PSB/VIB (Belgium). Biotechnology approaches are on course via collaboration with the LIMPP laboratory at Embrapa/Cenargen (Brazil).

Generation of fundamental knowledge on how nematode-induced giant-feeding cells function, is crucial to comprehend feeding site functioning during parasitism as well as to design novel strategies to control nematode infection in important worldwide crops.

Current Position

• Research director and group leader within the « Interactions Plantes-Nématodes-IPN » team: “Identification and characterization of determinants of susceptibility of plant hosts to endoparasitic nematodes aiming the development of new strategies for phytoprotection”.
• Scientific responsible of the Microscopy & Cell Biology platform (part of the SPIBOC) at the UMR ISA, France.
• 2013- One year mission of INRA and invited visiting professor at the “University of Brasilia”; research developed at Embrapa/Cenargen (Brasilia, Brasil).

Past Research Activities

• 2000-2003: Groupleader « In situ expression profiling ». Functional genomics division at the PSB-VIB, Ghent University (Belgium).
• 1993-2003: Researcher « Vlaams Instituut voor Biotechnologie » (VIB). Laboratorium voor Genetika, Universiteit Gent, Belgique directed by Prof. Dr. Marc Van Montagu later named « Department of Plant Systems Biology (PSB) » at the Flanders Interuniversity Institute for Biotechnology (VIB) actually directed by Prof. Dr. Dirk Inzé. Subject of research: « Identification and characterization of molecular and cellular determinants of plant susceptibility to infection by root-knot and cyst nematodes».
• Responsible of the «histology laboratory within the Platform of Cell Biology».
• 1991-1992: Post-doctorate in the laboratory of Genetics, directed by Marc Van Montagu, Ghent, Belgium. Subject of research: “Functional analysis of genes induced by the root-knot and cyst nematodes Meloidogyne incognita and Heterodera schachtii”.

Research interests

• Plant biology, plant biotechnology, cellular aspects interaction between plants and endoparasitic nematodes
• The plant cell cycle: functional studies during the susceptible interaction between plants and RKN
• Exploiting nematode feeding sites to dissect the plant cell cycle gene function
• The plant cytoskeleton rearrangement and players: particularly in nematode feeding sites
• In situ localization of nematode secreted effectors during nematode infection

Selected Publications in the field

1. Roberta Ramos Coelho, Paulo Vieira, José Dijair Antonino de Souza Júnior, Cristina M. Jimenez, Lieven De Veylder, Gilbert Engler, Maria Fatima Grossi de Sá and Janice de Almeida Engler. Unraveling the function of the cell cycle inhibitors KRP3,KRP5and KRP7 during root-knot nematode feeding site development.Plant Cell and Environment.In press.
2. Vieira, P., De Clercq, A., Stals, H., Van Leene, J., Van De Slijke, E., Van Isterdael, G., Eeckhout, Geert Persiau, D., Van Damme, D., Verkest, A., Antonino de Souza Júnior, J.D., Glab, N., Abad, P., Engler, G., Inzé, D., De Veylder, L., De Jaeger, G. & de Almeida Engler, J. (2014). The cyclin-depedent kinase inhibitor KRP6 induces mitosis and impairs cytokinesis in giant cells induced by plant-parasitic nematodes in Arabidopsis. Plant Cell, 26:2633-2647. Doi.​org/​10.​1105/​tpc.​114.​126425.
3. Vieira, P., Escudero, C., Rodiuc N., Boruc, J., Russinova, E., Glab, N., Mota, M., De Veylder, L., Abad, P., Engler, G. and de Almeida Engler, J. (2013). Ectopic expression of kip-related proteins restrains root-knot nematode-feeding site expansion. New Phytologist. 199, (2) 505–519 Doi:10.1111/nph.12255.
4. DE ALMEIDA ENGLER, J., KYNDT, T., VIEIRA, P., VAN CAPELLE, E., BOUDOLF, V., SANCHEZ, V., ESCOBAR, C., DE VEYLDER, L., ENGLER, G., ABAD, P. AND GHEYSEN, G. (2012) CCS52 and DEL1 genes are key components of the endocycle in nematode-induced feeding sites. The Plant Journal. Doi: 10.1111/j.1365-313X.2012.05054.x.         
5. VIEIRA, P., ENGLER, G. AND DE ALMEIDA ENGLER, J. (2012) Whole-mount confocal imaging of nuclei in giant feeding cells induced by root-knot nematodes in Arabidopsis.New Phytologist. 2012: 195(2): 488-496. Doi: 10.1111/j.1469-8137.2012.04175.x
6. BANORA, M.Y.; RODIUC, N., BALDACCI-CRESP, F.; SMERTENKO, A., BLEVE-ZACHEO, T., MELILLO, M.T., KARIMI, M., HILSON, P., EVRARD, J.L., FAVERY, B., ENGLER, G., ABAD, P., DE ALMEIDA-ENGLER, J. (2011) Feeding Cells Induced by Phytoparasitic Nematodes Require γ-Tubulin Ring Complex for Microtubule Reorganisation. PloS Pathogen., 2011 December: Volume 7: Issue 12. Doi:10.1371/journal.ppat.1002343.
7. VIEIRA P., DANCHIN E.G.J., NEVEU C., CROZAT C., JAUBERT S., HUSSEY R.S., ENGLER G., ABAD, P., DE ALMEIDA ENGLER J., CASTAGNONE-SERENO P., ROSSO M.N. (2010) The plant apoplasm is an important recipient compartment for nematode effectors.J. Exp. Botany2-13. Doi: 10.1093/jxb/erq352.Co-last author.
8. CLEMENT, M., KETELAAR, T., RODIUC, N., YOUSSEF BANORA, M, SMERTENKO, A., ENGLER, G., ABAD, P., HUSSEY, P. and DE ALMEIDA-ENGLER, J. (2009). ADF-dependent actin cytoskeleton remodeling is essential for embryo development and plant parasitic nematode infection. The Plant Cell, Vol 21: 2963-2979.
9. DE ALMEIDA ENGLER, J, DE VEYLDER, L., RUTH DE GROODT, STEPHANE ROMBAUTS, VERONIQUE BOUDOLF, BJORN DE MEYER, ADRIANA HEMERLY, PAULO FERREIRA, TOM BEECKMAN, MANSOUR KARIMI, PIERRE HILSON, DIRK INZE, and GILBERT ENGLER^. (2009). Systematic analysis of cell cycle gene expression during Arabidopsis development. The Plant Journal, 59: 645-660.
10. DE ALMEIDA ENGLER, J., VAN POUCKE, K., KARIMI, M., DE GROODT, R., GHEYSEN, G., ENGLER, G., and GHEYSEN, G. Dynamic cytoskeleton rearrangements in giant cells and syncytia of nematode‑infected roots. Plant Journal 38 (1) 12-26 (2004).
11. 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, 793‑807.

Book Chapters (B1 to B6)

1. Antonino de Souza Júnior, J. D.; Grossi-de-Sá, M. F.; Engler, G.; de Almeida Engler, J. (2016). Nuclear morphology and organization by clearing plant tissues under cell cycle inhibitors treatment. In: Caillaud, M-C (ed). Methods in Molecular Biology. Springer, TheNetherlands.Springer, vol 1370, pp 59-68. DOI 10.1007/978-1-4939-3142-2_11. PMID: 26659960.
2. de Almeida Engler, J., Vieira, P., Rodiuc N., Grossi De Sa, F. and Engler G. (2015). The plant cell cycle machinery: usurped and modulated by plant parasitic nematodes. Advances in Botanical Research-Plant nematodes interactions. The Plant Cell Cycle Machinery: Usurped and Modulated by Plant-Parasitic Nematodes. In C. Escobar & C. Fenoll (Eds.),Plant Nematode Interactions: AView on Compatible Interrelationships(pp. 91–118).ISBN: 9780124171619.
3. DE ALMEIDA-ENGLER, J. AND FAVERY, (2011). The plant cytoskeleton remodelling in nematode induced feeding sites. In: Jones J, Gheysen G, Fenoll C, eds. Genomics and molecular genetics of plant-nematode interactions. Dordrecht, the Netherlands: Springer Science+Business Media, 369-393.
4. DE ALMEIDA-ENGLER, J., ENGLER G. AND GHEYSEN G. (2011). Unravelling the plant cell cycle in nematode induced feeding sites. In: Jones J, Gheysen G, Fenoll C, eds. Genomics and molecular genetics of plant-nematode interactions. Dordrecht, the Netherlands: Springer Science + Business Media, 349-368.
5. GHEYSEN, G., DE ALMEIDA ENGLER, J., and VAN MONTAGU, M. (1997). Cell cycle regulation in nematode feeding sites. In Cellular and Molecular Aspects of Plant‑Nematode Interactions, (Developments in Plant Pathology, Vol. 10), C. Fenoll, F.M.W. Grundler, and S.A. Ohl (Eds.). Dordrecht, Kluwer Academic Publishers, pp. 120‑132. [ISBN 0-7329-4637-8].
6. DE ALMEIDA ENGLER, J., VAN MONTAGU, M., and ENGLER, G. (1998). Whole‑Mount in situ hybridization in plants. In Arabidopsis Protocols, (Methods in Molecular Biology, Vol. 82), J.M. Martínez‑Zapater, and J. Salinas (Eds.). Totowa, Humana Press, pp. 373‑384. [ISBN 0‑89603‑391‑0].

Past and present lab members (since 2003)

• Post-Doctorants: 11 (2017: 3).
• Short term scientific visitors: 9 (2017: 2).
• PhD students: 5 (2017: 2 and 4 sandwich).
• Master Students and Erasmus: Master 5 (France); Erasmus 25 (Spain) (2017: 2).
• Technical Students: BTSA. 7 (2017: 4).