Kondorosi Lab

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Get information about our research

Check our Topics

Get information about our research

Check our Topics

Widely conserved AHL transcription factors are essential for NCR gene expression and nodule development in Medicago

Zhang, Senlei; Wang, Ting; Lima, Rui M.; Pettkó-Szandtner, Aladár; Kereszt, Attila; Downie, J. Allan; Kondorosi, Eva

Legume Plant Peptides as Sources of Novel Antimicrobial Molecules Against Human Pathogens

Lima, Rui M.; Rathod, Balaji Baburao; Tiricz, Hilda; Howan, Dian H. O.; Al, Bouni Mohamad Anas; Jenei, Sandor; Timar, Edit; Endre, Gabriella; Toth, Gabor K.; Kondorosi, Eva

Why Should Nodule Cysteine-Rich (NCR) Peptides Be Absent From Nodules of Some Groups of Legumes but Essential for Symbiotic N-Fixation in Others?

Downie, J. Allan; Kondorosi, Eva

Éva Kondorosi

Biography and scientific career

Short Biography

Éva Kondorosi was born in Budapest, graduated (Biology) and received her PhD (Genetics) at the L. Eötvös University in Budapest. She was postdoc at the Max Planck Institut für Züchtungsforschung (Köln) and visiting scholar at the Sussex, Harvard and Cornell Universities. Éva Kondorosi was a founding member of the Institut des Science Végétales CNRS in Gif sur Yvette, France as one of the first research directors and group leaders and later the founding director of the BAYGEN Institute in Szeged, Hungary. Currently she is a research professor at the HUN-REN Biological Research Centre in Szeged, Hungary where she leads research on and symbiotic nitrogen fixation. She was the wife and an intellectual and research partner of Ádám Kondorosi (1946-2011), the renowned Széchenyi Prize-, and UNESCO Finley Prize-winning Hungarian geneticist who started the molecular genetic study of symbiotic nitrogen fixation and was its international leader.

Current position

2018-: Research Professor, Institute of Plant Biology HUN-REN Biological Research Centre, Szeged, Hungary

Previous positions

2013-2018: Directeur de Recherche Emérite – CNRS, Institute for Integrative Biology of the Cell (Institut de Biologie Intégrative de la Cellule), UMR 9198, Centre National de la Recherche Scientifique, 91198 Gif sur Yvette, France
2002-2013: Scientific director (DR1), group leader, Institut des Sciences du Végétal, UPR 2355, Centre National de la Recherche Scientifique, France
1989–2001: Scientific director (DR2), group leader, Institut des Sciences Végétales, CNRS UPR40, Centre National de la Recherche Scientifique, France
2011-2018: Research Professor, Head of the Symbiosis and Functional Genomics Unit, Institute of Biochemistry, Biological Research Centre, Hungarian Academy of Sciences, Szeged, Hungary
2007-2011: Director, Institute for Plant Genomics, Human Biotechnology and Bioenergy (BAYGEN), Bay Zoltán Foundation for Applied Research, Hungary
1987-1989: Project leader, Max Planck Institut für Züchtungsforschung Köln, Germany
1973-1989: Young scientist and then project and group leader, Institute of Biochemistry, Biological Research Centre, Hungarian Academy of Sciences, Szeged, Hungary

Publication list:

https://scholar.google.hu/citations?user=oqT63uIAAAAJ&hl=hu
https://www.researchgate.net/profile/Eva-Kondorosi
https://m2.mtmt.hu/gui2/?type=authors&mode=browse&sel=authors10000390

More details

Committee membership

Awards

Trained Young scientists

Mentored Nobel Price Winner

Current Research Funding

Balzan Research grant as part of the Balzan Prize from the International Balzan Foundation
Frontline Research project (KKP129924) from the Hungarian National Research, Development andInnovation Office
Hungarian Reasearch Network (HUN-REN)

Research interest

Nitrogen-fixing root nodule development in Rhizobium-legume symbiosis

Symbiosis between Rhizobium soil bacteria and legume plants leads to the development of root nodules where endosymbiotic Rhizobium bacteria, known as bacteroids, acquire the ability to fix nitrogen - converting atmospheric nitrogen into ammonia via the nitrogenase enzyme.

Each plant has specific Rhizobium partners, and each Rhizobium has its plant partners. This partnership is achieved through consecutive and reciprocal molecular communication. Initially, plant flavonoids induce the production of Nod factors in their Rhizobium partners, which initiate nodule organogenesis and enable Rhizobium infection through infection threads formed in growing root hair cells from which rhizobia are released in the nodule cells as an organelle-like structure, called symbiosomes. The fate of endosymbiotic rhizobia depends on the host plant, which can be reversible, as in soybean or the model legume Lotus japonicus, or irreversible and terminal, as in the model legume Medicago truncatula or pea, vetch, and all Inverted Repeat Lacking Clade (IRLC) legumes converting rhizobia to polyploid, uncultivable large bacteroids, with increased membrane permeablity and altered physiology (Mergaert et al., 2006).

In the indeterminate nodules of M. truncatula, cell proliferation persists in the nodule meristem, leading to constant nodule growth and differentiation along its length, resulting in distinct nodule zones (ZI, ZII, IZ, ZIII) where all stages of symbiotic cell development are sequentially present from the youngest to fully differentiated stages (Figure 1); ZI: meristem, ZII: infection zone where symbiosomes proliferate in the host cell, IZ: differentiation zone where bacteroids undergo extreme morphological and physiological alterations and ZIII: nitrogen fixing zone (Kondorosi et al., 2013). Differentiation of bacteroids is coordinated with development of the symbiotic nodule cells which undergo repeated endoreduplication cycles increasing the cell volume with duplication of the genome from 2C/4C to 32C/64C (C: haploid DNA content) and (Cebolla et al., 1999, Vinardell et al., 2003, Nagymihály et al., 2017).

More details

Research Topics

Investigating the role of NCRs and nodGRPs in bacteroid differentiation and symbiotic cell development

Discovering the unique function of almost 800 peptides in nodule cells may take decades. Among the NCR peptides, we focus on those that are highly and specifically expressed in successive steps of symbiotic cell development. We aim to identify which NCR and nodGRP peptides act in the same cell and whether they act together and form complexes. Apart from the expression pattern, there is no information about the symbiotic functions of nodGRPs. To test the symbiotic phenotype of the selected NCR and nodGRP genes, we create stable transgenic M. truncatula lines with overexpression or downregulation/deletion of these genes.

Uncovering stage-specific regulation of symbiotic peptide genes

The extreme symbiotic cell-specific expression and dynamic developmental regulation of NCR and nodGRP genes is extraordinary (Maunoury et al., 2010; Roux et al., 2014). Recently we demonstrated that the MtAHL1 and MtAHL2 DNA-binding proteins are crucial for expression of many NCRs, bacteroid differentiation and development of nitrogen-fixing nodules (Zhang et al., 2023). In striking contrast, we do not yet know how the spatiotemporal regulation of NCRs is achieved.

We have been testing interactions of the nodule expressed MtAHL transcription factors (TFs) with each other and transcription factors identified among the nuclear proteins with Y2H interactions and pull-down experiments. In addition, Y1H screens, and DNA pull down experiments are in progress with various NCR and nodGRP promoters, representing different developmental, and protein extracts of the corresponding stage-specific nuclei. The DNA-protein interactions will be confirmed with complementary experiments (e.g. electrophoretic mobility shift assay: EMSA). The involvement of the potential TFs in NCR expression will be assessed in M. truncatula nodules lacking or overexpressing the TFs.

References

Maunoury, N., Redondo-Nieto, M., Bourcy, M., Van de Velde, W., Alunni, B., Laporte, P., Durand, P., Agier, N., Marisa Maunoury, L., Vaubert, D., Delacroix, H., Duc, G., Ratet, P., Aggerbeck, L., Kondorosi, E., Mergaert, P., 2010. Differentiation of symbiotic cells and endosymbionts in Medicago truncatula nodulation are coupled to two transcriptome-switches. PLOS ONE 5, e9519.
https://doi.org/10.1371/journal.pone.0009519
Roux, B., Rodde, N., Jardinaud, M.-F., Timmers, T., Sauviac, L., Cottret, L., Carrère, S., Sallet, E., Courcelle, E., Moreau, S., Debellé, F., Capela, D., Carvalho‐Niebel, F. de, Gouzy, J., Bruand, C., Gamas, P., 2014. An integrated analysis of plant and bacterial gene expression in symbiotic root nodules using laser-capture microdissection coupled to RNA sequencing. Plant J. 77, 817–837.
https://doi.org/10.1111/tpj.12442
Zhang, S., Wang, T., Lima, R.M., Pettkó-Szandtner, A., Kereszt, A., Downie, J.A., Kondorosi, E., 2023. Widely conserved AHL transcription factors are essential for NCR gene expression and nodule development in Medicago. Nature Plants 9, 280–288. https://doi.org/10.1038/s41477-022-01326-4
https://doi.org/10.1038/s41477-022-01326-4

Discovery of antimicrobial properties of NCRs as potential new antimicrobial drug candidates

The rise of antibiotic-resistant bacteria has become a major public health problem, with antibiotic-resistant infections killing 700,000 people worldwide each year. The development of new antibiotics is key to addressing the growing threat of antibiotic resistance. Several studies, primarily from our laboratory, have confirmed that various cationic NCR peptides have antimicrobial and antifungal properties (see the selected publications below). In our most comprehensive study, we tested 78 NCR peptides from M. truncatula against eight pathogens, including the ESKAPE pathogens, and 26 of them showed antimicrobial activity (Lima et al. 2022). We have already designed shorter and substituted derivatives and even chimeric peptides from some peptides, and among them we have found promising drug candidates that are effective against human and plant pathogenic bacteria and fungi without being toxic to human cells.

Selected publications

Balogh, Emese Petra, Tímea Mosolygó, Hilda Tiricz, Ágnes Mira Szabó, Adrienn Karai, Fanni Kerekes, Dezső P. Virók, Éva Kondorosi, and Katalin Burián. 2014. “Anti-Chlamydial Effect of Plant Peptides.” ACTA MICROBIOLOGICA ET IMMUNOLOGICA HUNGARICA 61 (2): 229–239.
https://doi.org/10.1556/AMicr.61.2014.2.12
Farkas, A, G Maroti, H Durgo, Z Gyorgypal, RM Lima, KF Medzihradszky, A Kereszt, P Mergaert, and E Kondorosi. 2014. “Medicago Truncatula Symbiotic Peptide NCR247 Contributes to Bacteroid Differentiation through Multiple Mechanisms.” PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 111 (14): 5183–5188.
https://doi.org/10.1073/pnas.1404169111
Farkas, A, G Maroti, A Kereszt, and E Kondorosi. 2017. “Comparative Analysis of the Bacterial Membrane Disruption Effect of Two Natural Plant Antimicrobial Peptides.” FRONTIERS IN MICROBIOLOGY 8: 51.
https://doi.org/10.3389/fmicb.2017.00051
Jenei, S., Tiricz, H., Szolomájer, J., Tímár, E., Klement, É., Al Bouni, M.A., Lima, R.M., Kata, D., Harmati, M., Buzás, K., Földesi, I., Tóth, G.K., Endre, G., Kondorosi, É., 2020. Potent chimeric antimicrobial derivatives of the Medicago truncatula NCR247 symbiotic peptide. Front. Microbiol. 11.
https://doi.org/10.3389/fmicb.2020.00270
Montiel, J, JA Downie, A Farkas, P Bihari, R Herczeg, B Balint, P Mergaert, A Kereszt, and E Kondorosi. 2017. “Morphotype of Bacteroids in Different Legumes Correlates with the Number and Type of Symbiotic NCR Peptides.” PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 114 (19): 5041–5046.
https://doi.org/10.1073/pnas.1704217114
Lima, R.M., Kylarová, S., Mergaert, P., Kondorosi, É., 2020. Unexplored arsenals of legume peptides with potential for their applications in medicine and agriculture. Front. Microbiol. 11.
https://doi.org/10.3389/fmicb.2020.01307
Lima, R.M., Rathod, B.B., Tiricz, H., Howan, D.H.O., Al Bouni, M.A., Jenei, S., Tímár, E., Endre, G., Tóth, G.K., Kondorosi, É., 2022. Legume plant peptides as sources of novel antimicrobial molecules against human pathogens. Front. Mol. Biosci. 9.
https://doi.org/10.3389/fmolb.2022.870460
Maróti, G., Downie, J.A., Kondorosi, É., 2015. Plant cysteine-rich peptides that inhibit pathogen growth and control rhizobial differentiation in legume nodules. Curr. Opin. Plant Biol. 26, 57–63.
https://doi.org/10.1016/j.pbi.2015.05.031
Mikulass, KR, K Nagy, B Bogos, Z Szegletes, E Kovacs, A Farkas, G Varo, E Kondorosi, and A Kereszt. 2016. “Antimicrobial Nodule-Specific Cysteine-Rich Peptides Disturb the Integrity of Bacterial Outer and Inner Membranes and Cause Loss of Membrane Potential.” ANNALS OF CLINICAL MICROBIOLOGY AND ANTIMICROBIALS 15 (1): 43..
https://doi.org/10.1186/s12941-016-0159-8
Ördögh, Lilla, Andrea Voros, I Nagy, E Kondorosi, and A Kereszt. 2014. “Symbiotic Plant Peptides Eliminate Candida Albicans Both In Vitro and in an Epithelial Infection Model and Inhibit the Proliferation of Immortalized Human Cells.” BIOMED RESEARCH INTERNATIONAL 2014..
https://doi.org/10.1155/2014/320796
Szerencsés, B., Gácser, A., Endre, G., Domonkos, I., Tiricz, H., Vágvölgyi, C., Szolomajer, J., Howan, D.H.O., Tóth, G.K., Pfeiffer, I., Kondorosi, É., 2021. Symbiotic NCR peptide fragments affect the viability, morphology and biofilm formation of Candida species. Int. J. Mol. Sci. 22, 3666.
https://doi.org/10.3390/ijms22073666
Tiricz, H., Szűcs, A., Farkas, A., Pap, B., Lima, R.M., Maróti, G., Kondorosi, É., Kereszt, A., 2013. Antimicrobial nodule-specific cysteine-rich peptides induce membrane depolarization-associated changes in the transcriptome of Sinorhizobium meliloti. Appl. Environ. Microbiol. 79, 6737–6746.
https://doi.org/10.1128/AEM.01791-13

Identifying the sequential and reciprocal molecular interactions between the host plant and its endosymbiont required for terminal bacteroid differentiation in M. truncatula nodules

Expression of NCRs and nodGRPs requires the presence of bacteria in the symbiotic nodule cells. Some of them are induced in the early, others in the middle or later stages of the nodule development in coordination with the differentiation stages of bacteroids. In our previous work, we have demonstrated that M. truncatula uses trans Golgi vesicles for delivering NCRs and nodGRPs to the bacteroids. In view of this intimate coexistence, it appears therefore logical to assume that bacteria interact similarly with the host cell. We focus on the identification of bacterial signals and understanding of the dynamics of molecular events occurring simultaneously in plant cells and bacteroids.

Molecular interactions between the host cell and the bacterium leading to development of nitrogen fixing root nodules.

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