Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.


Logo for

Science 327 (5969): 1122-1126

Copyright © 2010 by the American Association for the Advancement of Science

Plant Peptides Govern Terminal Differentiation of Bacteria in Symbiosis

Willem Van de Velde,1 Grigor Zehirov,2 Agnes Szatmari,1,3 Monika Debreczeny,4 Hironobu Ishihara,2 Zoltan Kevei,4 Attila Farkas,4 Kata Mikulass,4 Andrea Nagy,4 Hilda Tiricz,4 Beatrice Satiat-Jeunemaître,1 Benoit Alunni,1 Mickael Bourge,1 Ken-ichi Kucho,2 Mikiko Abe,2 Attila Kereszt,4 Gergely Maroti,4 Toshiki Uchiumi,2 Eva Kondorosi,1,4,* Peter Mergaert1

Abstract: Legume plants host nitrogen-fixing endosymbiotic Rhizobium bacteria in root nodules. In Medicago truncatula, the bacteria undergo an irreversible (terminal) differentiation mediated by hitherto unidentified plant factors. We demonstrated that these factors are nodule-specific cysteine-rich (NCR) peptides that are targeted to the bacteria and enter the bacterial membrane and cytosol. Obstruction of NCR transport in the dnf1-1 signal peptidase mutant correlated with the absence of terminal bacterial differentiation. On the contrary, ectopic expression of NCRs in legumes devoid of NCRs or challenge of cultured rhizobia with peptides provoked symptoms of terminal differentiation. Because NCRs resemble antimicrobial peptides, our findings reveal a previously unknown innovation of the host plant, which adopts effectors of the innate immune system for symbiosis to manipulate the cell fate of endosymbiotic bacteria.

1 Institut des Sciences du Végétal, Centre National de la Recherche Scientifique, 91198 Gif-sur-Yvette Cedex, France.
2 Graduate School of Science and Engineering, Kagoshima University, 890 0065 Kagoshima, Japan.
3 Plant Protection Institute of the Hungarian Academy of Sciences, 1022 Budapest, Hungary.
4 Institute for Plant Genomics, Human Biotechnology and Bioenergy, Bay Zoltan Foundation for Applied Research, 6726 Szeged, Hungary.

* To whom correspondence should be addressed. E-mail: eva.kondorosi{at}

Inclusive fitness in agriculture.
E. T. Kiers and R. F. Denison (2014)
Phil Trans R Soc B 369, 20130367
   Abstract »    Full Text »    PDF »
Medicago truncatula symbiotic peptide NCR247 contributes to bacteroid differentiation through multiple mechanisms.
A. Farkas, G. Maroti, H. Durgő, Z. Gyorgypal, R. M. Lima, K. F. Medzihradszky, A. Kereszt, P. Mergaert, and E. Kondorosi (2014)
PNAS 111, 5183-5188
   Abstract »    Full Text »    PDF »
Host plant peptides elicit a transcriptional response to control the Sinorhizobium meliloti cell cycle during symbiosis.
J. Penterman, R. P. Abo, N. J. De Nisco, M. F. F. Arnold, R. Longhi, M. Zanda, and G. C. Walker (2014)
PNAS 111, 3561-3566
   Abstract »    Full Text »    PDF »
Global analysis of cell cycle gene expression of the legume symbiont Sinorhizobium meliloti.
N. J. De Nisco, R. P. Abo, C. M. Wu, J. Penterman, and G. C. Walker (2014)
PNAS 111, 3217-3224
   Abstract »    Full Text »    PDF »
Enteric YaiW Is a Surface-Exposed Outer Membrane Lipoprotein That Affects Sensitivity to an Antimicrobial Peptide.
M. F. F. Arnold, P. Caro-Hernandez, K. Tan, G. Runti, S. Wehmeier, M. Scocchi, W. T. Doerrler, G. C. Walker, and G. P. Ferguson (2014)
J. Bacteriol. 196, 436-444
   Abstract »    Full Text »    PDF »
An RNA Sequencing Transcriptome Analysis Reveals Novel Insights into Molecular Aspects of the Nitrate Impact on the Nodule Activity of Medicago truncatula.
R. Cabeza, B. Koester, R. Liese, A. Lingner, V. Baumgarten, J. Dirks, G. Salinas-Riester, C. Pommerenke, K. Dittert, and J. Schulze (2014)
Plant Physiology 164, 400-411
   Abstract »    Full Text »    PDF »
Functional Characterization of SbmA, a Bacterial Inner Membrane Transporter Required for Importing the Antimicrobial Peptide Bac7(1-35).
G. Runti, M. d. C. Lopez Ruiz, T. Stoilova, R. Hussain, M. Jennions, H. G. Choudhury, M. Benincasa, R. Gennaro, K. Beis, and M. Scocchi (2013)
J. Bacteriol. 195, 5343-5351
   Abstract »    Full Text »    PDF »
Message in a bottle: small signalling peptide outputs during growth and development.
N. Czyzewicz, K. Yue, T. Beeckman, and I. D. Smet (2013)
J. Exp. Bot. 64, 5281-5296
   Abstract »    Full Text »    PDF »
Antimicrobial Nodule-Specific Cysteine-Rich Peptides Induce Membrane Depolarization-Associated Changes in the Transcriptome of Sinorhizobium meliloti.
H. Tiricz, A. Szucs, A. Farkas, B. Pap, R. M. Lima, G. Maroti, E. Kondorosi, and A. Kereszt (2013)
Appl. Envir. Microbiol. 79, 6737-6746
   Abstract »    Full Text »    PDF »
The C2H2 Transcription Factor REGULATOR OF SYMBIOSOME DIFFERENTIATION Represses Transcription of the Secretory Pathway Gene VAMP721a and Promotes Symbiosome Development in Medicago truncatula.
S. Sinharoy, I. Torres-Jerez, K. Bandyopadhyay, A. Kereszt, C. I. Pislariu, J. Nakashima, V. A. Benedito, E. Kondorosi, and M. K. Udvardi (2013)
PLANT CELL 25, 3584-3601
   Abstract »    Full Text »    PDF »
The Sinorhizobium meliloti sensor histidine kinase CbrA contributes to free-living cell cycle regulation.
C. S. Sadowski, D. Wilson, K. B. Schallies, G. Walker, and K. E. Gibson (2013)
Microbiology 159, 1552-1563
   Abstract »    Full Text »    PDF »
Small open reading frames associated with morphogenesis are hidden in plant genomes.
K. Hanada, M. Higuchi-Takeuchi, M. Okamoto, T. Yoshizumi, M. Shimizu, K. Nakaminami, R. Nishi, C. Ohashi, K. Iida, M. Tanaka, et al. (2013)
PNAS 110, 2395-2400
   Abstract »    Full Text »    PDF »
Partial Complementation of Sinorhizobium meliloti bacA Mutant Phenotypes by the Mycobacterium tuberculosis BacA Protein.
M. F. F. Arnold, A. F. Haag, S. Capewell, H. I. Boshoff, E. K. James, R. McDonald, I. Mair, A. M. Mitchell, B. Kerscher, T. J. Mitchell, et al. (2013)
J. Bacteriol. 195, 389-398
   Abstract »    Full Text »    PDF »
Aphids evolved novel secreted proteins for symbiosis with bacterial endosymbiont.
S. Shigenobu and D. L. Stern (2012)
Proc R Soc B 280, 20121952
   Abstract »    Full Text »    PDF »
Cell Biology of Cnidarian-Dinoflagellate Symbiosis.
S. K. Davy, D. Allemand, and V. M. Weis (2012)
Microbiol. Mol. Biol. Rev. 76, 229-261
   Abstract »    Full Text »    PDF »
Multiple Domains in MtENOD8 Protein Including the Signal Peptide Target It to The Symbiosome.
M. H. Meckfessel, E. B. Blancaflor, M. Plunkett, Q. Dong, and R. Dickstein (2012)
Plant Physiology 159, 299-310
   Abstract »    Full Text »    PDF »
Plant-activated bacterial receptor adenylate cyclases modulate epidermal infection in the Sinorhizobium meliloti-Medicago symbiosis.
C. F. Tian, A.-M. Garnerone, C. Mathieu-Demaziere, C. Masson-Boivin, and J. Batut (2012)
PNAS 109, 6751-6756
   Abstract »    Full Text »    PDF »
Trafficking of protein into the recently established photosynthetic organelles of Paulinella chromatophora.
E. C. M. Nowack and A. R. Grossman (2012)
PNAS 109, 5340-5345
   Abstract »    Full Text »    PDF »
Role of Cysteine Residues and Disulfide Bonds in the Activity of a Legume Root Nodule-specific, Cysteine-rich Peptide.
A. F. Haag, B. Kerscher, S. Dall'Angelo, M. Sani, R. Longhi, M. Baloban, H. M. Wilson, P. Mergaert, M. Zanda, and G. P. Ferguson (2012)
J. Biol. Chem. 287, 10791-10798
   Abstract »    Full Text »    PDF »
Characterization of Galacturonosyl Transferase Genes rgtA, rgtB, rgtC, rgtD, and rgtE Responsible for Lipopolysaccharide Synthesis in Nitrogen-fixing Endosymbiont Rhizobium leguminosarum: LIPOPOLYSACCHARIDE CORE AND LIPID GALACTURONOSYL RESIDUES CONFER MEMBRANE STABILITY.
D. B. Brown, L. S. Forsberg, E. L. Kannenberg, and R. W. Carlson (2012)
J. Biol. Chem. 287, 935-949
   Abstract »    Full Text »    PDF »
The Integral Membrane Protein SEN1 is Required for Symbiotic Nitrogen Fixation in Lotus japonicus Nodules.
T. Hakoyama, K. Niimi, T. Yamamoto, S. Isobe, S. Sato, Y. Nakamura, S. Tabata, H. Kumagai, Y. Umehara, K. Brossuleit, et al. (2012)
Plant Cell Physiol. 53, 225-236
   Abstract »    Full Text »    PDF »
Antimicrobial Peptides Keep Insect Endosymbionts Under Control.
F. H. Login, S. Balmand, A. Vallier, C. Vincent-Monegat, A. Vigneron, M. Weiss-Gayet, D. Rochat, and A. Heddi (2011)
Science 334, 362-365
   Abstract »    Full Text »    PDF »
Whole-genome nucleotide diversity, recombination, and linkage disequilibrium in the model legume Medicago truncatula.
A. Branca, T. D. Paape, P. Zhou, R. Briskine, A. D. Farmer, J. Mudge, A. K. Bharti, J. E. Woodward, G. D. May, L. Gentzbittel, et al. (2011)
PNAS 108, E864-E870
   Abstract »    Full Text »    PDF »
Functional analysis of the nifQdctA1y4vGHIJ operon of Sinorhizobium fredii strain NGR234 using a transposon with a NifA-dependent read-out promoter.
C. Fumeaux, N. Bakkou, J. Kopcinska, W. Golinowski, D. J. Westenberg, P. Muller, and X. Perret (2011)
Microbiology 157, 2745-2758
   Abstract »    Full Text »    PDF »
An acpXL Mutant of Rhizobium leguminosarum bv. phaseoli Lacks 27-Hydroxyoctacosanoic Acid in Its Lipid A and Is Developmentally Delayed during Symbiotic Infection of the Determinate Nodulating Host Plant Phaseolus vulgaris.
D. B. Brown, Y.-C. Huang, E. L. Kannenberg, D. J. Sherrier, and R. W. Carlson (2011)
J. Bacteriol. 193, 4766-4778
   Abstract »    Full Text »    PDF »
Failure to fix nitrogen by non-reproductive symbiotic rhizobia triggers host sanctions that reduce fitness of their reproductive clonemates.
R. Oono, C. G. Anderson, and R. F. Denison (2011)
Proc R Soc B 278, 2698-2703
   Abstract »    Full Text »    PDF »
A Highway for War and Peace: The Secretory Pathway in Plant-Microbe Interactions.
D. Wang and X. Dong (2011)
Mol Plant
   Abstract »    Full Text »    PDF »
Involvement of the Azorhizobial Chromosome Partition Gene (parA) in the Onset of Bacteroid Differentiation during Sesbania rostrata Stem Nodule Development.
C.-T. Liu, K.-B. Lee, Y.-S. Wang, M.-H. Peng, K.-T. Lee, S. Suzuki, T. Suzuki, and H. Oyaizu (2011)
Appl. Envir. Microbiol. 77, 4371-4382
   Abstract »    Full Text »    PDF »
Role of BacA in Lipopolysaccharide Synthesis, Peptide Transport, and Nodulation by Rhizobium sp. Strain NGR234.
S. Ardissone, H. Kobayashi, K. Kambara, C. Rummel, K. D. Noel, G. C. Walker, W. J. Broughton, and W. J. Deakin (2011)
J. Bacteriol. 193, 2218-2228
   Abstract »    Full Text »    PDF »
Cupriavidus taiwanensis Bacteroids in Mimosa pudica Indeterminate Nodules Are Not Terminally Differentiated.
M. Marchetti, O. Catrice, J. Batut, and C. Masson-Boivin (2011)
Appl. Envir. Microbiol. 77, 2161-2164
   Abstract »    Full Text »    PDF »
Cysteine-Rich Peptides (CRPs) mediate diverse aspects of cell-cell communication in plant reproduction and development.
E. Marshall, L. M. Costa, and J. Gutierrez-Marcos (2011)
J. Exp. Bot. 62, 1677-1686
   Abstract »    Full Text »    PDF »
Complex Regulation of Symbiotic Functions Is Coordinated by MucR and Quorum Sensing in Sinorhizobium meliloti.
K. Mueller and J. E. Gonzalez (2011)
J. Bacteriol. 193, 485-496
   Abstract »    Full Text »    PDF »
Comparing Symbiotic Efficiency between Swollen versus Nonswollen Rhizobial Bacteroids.
R. Oono and R. F. Denison (2010)
Plant Physiology 154, 1541-1548
   Abstract »    Full Text »    PDF »
Internalization of a thiazole-modified peptide in Sinorhizobium meliloti occurs by BacA-dependent and -independent mechanisms.
S. Wehmeier, M. F. F. Arnold, V. L. Marlow, M. Aouida, K. K. Myka, V. Fletcher, M. Benincasa, M. Scocchi, D. Ramotar, and G. P. Ferguson (2010)
Microbiology 156, 2702-2713
   Abstract »    Full Text »    PDF »
The bacA Gene Homolog, mlr7400, in Mesorhizobium loti MAFF303099 is Dispensable for Symbiosis with Lotus japonicus but Partially Capable of Supporting the Symbiotic Function of bacA in Sinorhizobium meliloti.
J. Maruya and K. Saeki (2010)
Plant Cell Physiol. 51, 1443-1452
   Abstract »    Full Text »    PDF »
How Many Peas in a Pod? Legume Genes Responsible for Mutualistic Symbioses Underground.
H. Kouchi, H. Imaizumi-Anraku, M. Hayashi, T. Hakoyama, T. Nakagawa, Y. Umehara, N. Suganuma, and M. Kawaguchi (2010)
Plant Cell Physiol. 51, 1381-1397
   Abstract »    Full Text »    PDF »
Function of GRAS Proteins in Root Nodule Symbiosis is Retained in Homologs of a Non-Legume, Rice.
K. Yokota, T. Soyano, H. Kouchi, and M. Hayashi (2010)
Plant Cell Physiol. 51, 1436-1442
   Abstract »    Full Text »    PDF »
NENA, a Lotus japonicus Homolog of Sec13, Is Required for Rhizodermal Infection by Arbuscular Mycorrhiza Fungi and Rhizobia but Dispensable for Cortical Endosymbiotic Development.
M. Groth, N. Takeda, J. Perry, H. Uchida, S. Draxl, A. Brachmann, S. Sato, S. Tabata, M. Kawaguchi, T. L. Wang, et al. (2010)
PLANT CELL 22, 2509-2526
   Abstract »    Full Text »    PDF »

To Advertise     Find Products

Science Signaling. ISSN 1937-9145 (online), 1945-0877 (print). Pre-2008: Science's STKE. ISSN 1525-8882