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.

Subscribe

Logo for

Science 299 (5603): 109-112

Copyright © 2003 by the American Association for the Advancement of Science

Long-Distance Signaling in Nodulation Directed by a CLAVATA1-Like Receptor Kinase

Iain R. Searle,12*dagger Artem E. Men,3dagger Titeki S. Laniya,3 Diana M. Buzas,3 Inaki Iturbe-Ormaetxe,3ddagger Bernard J. Carroll,12§parallel Peter M. Gresshoff3

Proliferation of legume nodule primordia is controlled by shoot-root signaling known as autoregulation of nodulation (AON). Mutants defective in AON show supernodulation and increased numbers of lateral roots. Here, we demonstrate that AON in soybean is controlled by the receptor-like protein kinase GmNARK (Glycine max nodule autoregulation receptor kinase), similar to Arabidopsis CLAVATA1 (CLV1). Whereas CLV1 functions in a protein complex controlling stem cell proliferation by short-distance signaling in shoot apices, GmNARK expression in the leaf has a major role in long-distance communication with nodule and lateral root primordia.

1 Biochemistry and Molecular Biology, School of Molecular and Microbial Sciences,
2 School of Land and Food Sciences,
3 Botany, School of Life Sciences, The University of Queensland, Brisbane, St. Lucia, QLD 4072, Australia.
*   Present address: Max-Planck-Institut für Züchtungsforschung, Carl-von-Linné-Weg 10, 50829, Köln, Germany.

dagger    These authors contributed equally to this work.

ddagger    Present address: Zoology and Entomology, School of Life Sciences, The University of Queensland, Brisbane, Australia.

§   Conjoint member of Institute of Molecular Bioscience, The University of Queensland.

parallel    To whom correspondence should be addressed. E-mail: b.carroll{at}mailbox.uq.edu.au



THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
The potential roles of strigolactones and brassinosteroids in the autoregulation of nodulation pathway.
E. Foo, B. J. Ferguson, and J. B. Reid (2014)
Ann. Bot.
   Abstract »    Full Text »    PDF »
Spatial expression of CLAVATA3 in the shoot apical meristem suggests it is not a stem cell marker in soybean.
C. E. Wong, M. B. Singh, and P. L. Bhalla (2013)
J. Exp. Bot. 64, 5641-5649
   Abstract »    Full Text »    PDF »
Structure-function analysis of the GmRIC1 signal peptide and CLE domain required for nodulation control in soybean.
D. E. Reid, D. Li, B. J. Ferguson, and P. M. Gresshoff (2013)
J. Exp. Bot. 64, 1575-1585
   Abstract »    Full Text »    PDF »
TOO MUCH LOVE, a Novel Kelch Repeat-Containing F-box Protein, Functions in the Long-Distance Regulation of the Legume-Rhizobium Symbiosis.
M. Takahara, S. Magori, T. Soyano, S. Okamoto, C. Yoshida, K. Yano, S. Sato, S. Tabata, K. Yamaguchi, S. Shigenobu, et al. (2013)
Plant Cell Physiol. 54, 433-447
   Abstract »    Full Text »    PDF »
Down-Regulation of NSP2 Expression in Developmentally Young Regions of Lotus japonicus Roots in Response to Rhizobial Inoculation.
Y. Murakami, H. Yokoyama, R. Fukui, and M. Kawaguchi (2013)
Plant Cell Physiol. 54, 518-527
   Abstract »    Full Text »    PDF »
Systemic Regulation of Soybean Nodulation by Acidic Growth Conditions.
M.-H. Lin, P. M. Gresshoff, and B. J. Ferguson (2012)
Plant Physiology 160, 2028-2039
   Abstract »    Full Text »    PDF »
Positive and negative regulation of cortical cell division during root nodule development in Lotus japonicus is accompanied by auxin response.
T. Suzaki, K. Yano, M. Ito, Y. Umehara, N. Suganuma, and M. Kawaguchi (2012)
Development 139, 3997-4006
   Abstract »    Full Text »    PDF »
Peptides and receptors controlling root development.
Y. Stahl and R. Simon (2012)
Phil Trans R Soc B 367, 1453-1460
   Abstract »    Full Text »    PDF »
The Autoregulation Gene SUNN Mediates Changes in Root Organ Formation in Response to Nitrogen through Alteration of Shoot-to-Root Auxin Transport.
J. Jin, M. Watt, and U. Mathesius (2012)
Plant Physiology 159, 489-500
   Abstract »    Full Text »    PDF »
WUSCHEL-RELATED HOMEOBOX5 Gene Expression and Interaction of CLE Peptides with Components of the Systemic Control Add Two Pieces to the Puzzle of Autoregulation of Nodulation.
M. A. Osipova, V. Mortier, K. N. Demchenko, V. E. Tsyganov, I. A. Tikhonovich, L. A. Lutova, E. A. Dolgikh, and S. Goormachtig (2012)
Plant Physiology 158, 1329-1341
   Abstract »    Full Text »    PDF »
Characterization of a dual-affinity nitrate transporter MtNRT1.3 in the model legume Medicago truncatula.
M.-C. Morere-Le Paven, L. Viau, A. Hamon, C. Vandecasteele, A. Pellizzaro, C. Bourdin, C. Laffont, B. Lapied, M. Lepetit, F. Frugier, et al. (2011)
J. Exp. Bot. 62, 5595-5605
   Abstract »    Full Text »    PDF »
Molecular mechanisms controlling legume autoregulation of nodulation.
D. E. Reid, B. J. Ferguson, S. Hayashi, Y.-H. Lin, and P. M. Gresshoff (2011)
Ann. Bot. 108, 789-795
   Abstract »    Full Text »    PDF »
Soybean Nodule-Enhanced CLE Peptides in Roots Act as Signals in GmNARK-Mediated Nodulation Suppression.
C. W. Lim, Y. W. Lee, and C. H. Hwang (2011)
Plant Cell Physiol. 52, 1613-1627
   Abstract »    Full Text »    PDF »
The ROOT DETERMINED NODULATION1 Gene Regulates Nodule Number in Roots of Medicago truncatula and Defines a Highly Conserved, Uncharacterized Plant Gene Family.
E. L. Schnabel, T. K. Kassaw, L. S. Smith, J. F. Marsh, G. E. Oldroyd, S. R. Long, and J. A. Frugoli (2011)
Plant Physiology 157, 328-340
   Abstract »    Full Text »    PDF »
Expression and Functional Analysis of a CLV3-Like Gene in the Model Legume Lotus japonicus.
S. Okamoto, T. Nakagawa, and M. Kawaguchi (2011)
Plant Cell Physiol. 52, 1211-1221
   Abstract »    Full Text »    PDF »
Search for nodulation-related CLE genes in the genome of Glycine max.
V. Mortier, B. A. Fenta, C. Martens, S. Rombauts, M. Holsters, K. Kunert, and S. Goormachtig (2011)
J. Exp. Bot. 62, 2571-2583
   Abstract »    Full Text »    PDF »
Phenotypic and Genomic Analyses of a Fast Neutron Mutant Population Resource in Soybean.
Y.-T. Bolon, W. J. Haun, W. W. Xu, D. Grant, M. G. Stacey, R. T. Nelson, D. J. Gerhardt, J. A. Jeddeloh, G. Stacey, G. J. Muehlbauer, et al. (2011)
Plant Physiology 156, 240-253
   Abstract »    Full Text »    PDF »
A functional-structural modelling approach to autoregulation of nodulation.
L. Han, P. M. Gresshoff, and J. Hanan (2011)
Ann. Bot. 107, 855-863
   Abstract »    Full Text »    PDF »
Autoregulation of Nodulation Interferes with Impacts of Nitrogen Fertilization Levels on the Leaf-Associated Bacterial Community in Soybeans.
S. Ikeda, M. Anda, S. Inaba, S. Eda, S. Sato, K. Sasaki, S. Tabata, H. Mitsui, T. Sato, T. Shinano, et al. (2011)
Appl. Envir. Microbiol. 77, 1973-1980
   Abstract »    Full Text »    PDF »
A holistic view of nitrogen acquisition in plants.
T. Kraiser, D. E. Gras, A. G. Gutierrez, B. Gonzalez, and R. A. Gutierrez (2011)
J. Exp. Bot. 62, 1455-1466
   Abstract »    Full Text »    PDF »
The receptor-like kinase KLAVIER mediates systemic regulation of nodulation and non-symbiotic shoot development in Lotus japonicus.
H. Miyazawa, E. Oka-Kira, N. Sato, H. Takahashi, G.-J. Wu, S. Sato, M. Hayashi, S. Betsuyaku, M. Nakazono, S. Tabata, et al. (2010)
Development 137, 4317-4325
   Abstract »    Full Text »    PDF »
The lss Supernodulation Mutant of Medicago truncatula Reduces Expression of the SUNN Gene.
E. Schnabel, A. Mukherjee, L. Smith, T. Kassaw, S. Long, and J. Frugoli (2010)
Plant Physiology 154, 1390-1402
   Abstract »    Full Text »    PDF »
plenty, a Novel Hypernodulation Mutant in Lotus japonicus.
C. Yoshida, S. Funayama-Noguchi, and M. Kawaguchi (2010)
Plant Cell Physiol. 51, 1425-1435
   Abstract »    Full Text »    PDF »
Misexpression of miR482, miR1512, and miR1515 Increases Soybean Nodulation.
H. Li, Y. Deng, T. Wu, S. Subramanian, and O. Yu (2010)
Plant Physiology 153, 1759-1770
   Abstract »    Full Text »    PDF »
CLE Peptides Control Medicago truncatula Nodulation Locally and Systemically.
V. Mortier, G. Den Herder, R. Whitford, W. Van de Velde, S. Rombauts, K. D'haeseleer, M. Holsters, and S. Goormachtig (2010)
Plant Physiology 153, 222-237
   Abstract »    Full Text »    PDF »
Inactivation of Duplicated Nod Factor Receptor 5 (NFR5) Genes in Recessive Loss-of-Function Non-Nodulation Mutants of Allotetraploid Soybean (Glycine max L. Merr.).
A. Indrasumunar, A. Kereszt, I. Searle, M. Miyagi, D. Li, C. D.T. Nguyen, A. Men, B. J. Carroll, and P. M. Gresshoff (2010)
Plant Cell Physiol. 51, 201-214
   Abstract »    Full Text »    PDF »
Enhanced Nodulation and Nitrogen Fixation in the Abscisic Acid Low-Sensitive Mutant enhanced nitrogen fixation1 of Lotus japonicus.
A. Tominaga, M. Nagata, K. Futsuki, H. Abe, T. Uchiumi, M. Abe, K.-i. Kucho, M. Hashiguchi, R. Akashi, A. M. Hirsch, et al. (2009)
Plant Physiology 151, 1965-1976
   Abstract »    Full Text »    PDF »
Molecular dissection of the pea shoot apical meristem.
D. Liang, C. E. Wong, M. B. Singh, C. A. Beveridge, B. Phipson, G. K. Smyth, and P. L. Bhalla (2009)
J. Exp. Bot. 60, 4201-4213
   Abstract »    Full Text »    PDF »
A Novel Plant Leucine-Rich Repeat Receptor Kinase Regulates the Response of Medicago truncatula Roots to Salt Stress.
L. de Lorenzo, F. Merchan, P. Laporte, R. Thompson, J. Clarke, C. Sousa, and M. Crespi (2009)
PLANT CELL 21, 668-680
   Abstract »    Full Text »    PDF »
Diverse Transcriptional Programs Associated with Environmental Stress and Hormones in the Arabidopsis Receptor-Like Kinase Gene Family.
L. Chae, S. Sudat, S. Dudoit, T. Zhu, and S. Luan (2009)
Mol Plant 2, 84-107
   Abstract »    Full Text »    PDF »
Nod Factor/Nitrate-Induced CLE Genes that Drive HAR1-Mediated Systemic Regulation of Nodulation.
S. Okamoto, E. Ohnishi, S. Sato, H. Takahashi, M. Nakazono, S. Tabata, and M. Kawaguchi (2009)
Plant Cell Physiol. 50, 67-77
   Abstract »    Full Text »    PDF »
De Novo Organ Formation from Differentiated Cells: Root Nodule Organogenesis.
M. Crespi and F. Frugier (2008)
Science Signaling 1, re11
   Abstract »    Full Text »    PDF »
Abscisic Acid Coordinates Nod Factor and Cytokinin Signaling during the Regulation of Nodulation in Medicago truncatula.
Y. Ding, P. Kalo, C. Yendrek, J. Sun, Y. Liang, J. F. Marsh, J. M. Harris, and G. E.D. Oldroyd (2008)
PLANT CELL 20, 2681-2695
   Abstract »    Full Text »    PDF »
EFD Is an ERF Transcription Factor Involved in the Control of Nodule Number and Differentiation in Medicago truncatula.
T. Vernie, S. Moreau, F. de Billy, J. Plet, J.-P. Combier, C. Rogers, G. Oldroyd, F. Frugier, A. Niebel, and P. Gamas (2008)
PLANT CELL 20, 2696-2713
   Abstract »    Full Text »    PDF »
Soybean Nodule Autoregulation Receptor Kinase Phosphorylates Two Kinase-associated Protein Phosphatases in Vitro.
A. Miyahara, T. A. Hirani, M. Oakes, A. Kereszt, B. Kobe, M. A. Djordjevic, and P. M. Gresshoff (2008)
J. Biol. Chem. 283, 25381-25391
   Abstract »    Full Text »    PDF »
Signaling of cell fate determination by the TPD1 small protein and EMS1 receptor kinase.
G. Jia, X. Liu, H. A. Owen, and D. Zhao (2008)
PNAS 105, 2220-2225
   Abstract »    Full Text »    PDF »
The Autoregulation of Nodulation Mechanism is Related to Leaf Development.
S. Ito, T. Kato, N. Ohtake, K. Sueyoshi, and T. Ohyama (2008)
Plant Cell Physiol. 49, 121-125
   Abstract »    Full Text »    PDF »
Ultrasensitive Determination of Absolute mRNA Amounts at Attomole Levels of Nearly Identical Plant Genes with High-Throughput Mass Spectrometry (MassARRAY).
R. Turakulov, S. Nontachaiyapoom, K. R. Mitchelson, P. M. Gresshoff, and A. E. Men (2007)
Plant Cell Physiol. 48, 1379-1384
   Abstract »    Full Text »    PDF »
Translocation in Legumes: Assimilates, Nutrients, and Signaling Molecules.
C. A. Atkins and P. M. C. Smith (2007)
Plant Physiology 144, 550-561
   Full Text »    PDF »
Reciprocal Phosphorylation and Glycosylation Recognition Motifs Control NCAPP1 Interaction with Pumpkin Phloem Proteins and Their Cell-to-Cell Movement.
K.-i. Taoka, B.-K. Ham, B. Xoconostle-Cazares, M. R. Rojas, and W. J. Lucas (2007)
PLANT CELL 19, 1866-1884
   Abstract »    Full Text »    PDF »
Overlap of Proteome Changes in Medicago truncatula in Response to Auxin and Sinorhizobium meliloti.
G. E. van Noorden, T. Kerim, N. Goffard, R. Wiblin, F. I. Pellerone, B. G. Rolfe, and U. Mathesius (2007)
Plant Physiology 144, 1115-1131
   Abstract »    Full Text »    PDF »
Medicago truncatula NIN Is Essential for Rhizobial-Independent Nodule Organogenesis Induced by Autoactive Calcium/Calmodulin-Dependent Protein Kinase.
J. F. Marsh, A. Rakocevic, R. M. Mitra, L. Brocard, J. Sun, A. Eschstruth, S. R. Long, M. Schultze, P. Ratet, and G. E.D. Oldroyd (2007)
Plant Physiology 144, 324-335
   Abstract »    Full Text »    PDF »
Factors involved in root formation in Medicago truncatula.
N. Imin, M. Nizamidin, T. Wu, and B. G. Rolfe (2007)
J. Exp. Bot. 58, 439-451
   Abstract »    Full Text »    PDF »
The Ethylene-Insensitive sickle Mutant of Medicago truncatula Shows Altered Auxin Transport Regulation during Nodulation.
J. Prayitno, B. G. Rolfe, and U. Mathesius (2006)
Plant Physiology 142, 168-180
   Abstract »    Full Text »    PDF »
Silencing the Flavonoid Pathway in Medicago truncatula Inhibits Root Nodule Formation and Prevents Auxin Transport Regulation by Rhizobia.
A. P. Wasson, F. I. Pellerone, and U. Mathesius (2006)
PLANT CELL 18, 1617-1629
   Abstract »    Full Text »    PDF »
Tracing Nonlegume Orthologs of Legume Genes Required for Nodulation and Arbuscular Mycorrhizal Symbioses.
H. Zhu, B. K. Riely, N. J. Burns, and J.-M. Ane (2006)
Genetics 172, 2491-2499
   Abstract »    Full Text »    PDF »
Defective Long-Distance Auxin Transport Regulation in the Medicago truncatula super numeric nodules Mutant.
G. E. van Noorden, J. J. Ross, J. B. Reid, B. G. Rolfe, and U. Mathesius (2006)
Plant Physiology 140, 1494-1506
   Abstract »    Full Text »    PDF »
Low Temperature Treatment at the Young Microspore Stage Induces Protein Changes in Rice Anthers.
N. Imin, T. Kerim, J. J. Weinman, and B. G. Rolfe (2006)
Mol. Cell. Proteomics 5, 274-292
   Abstract »    Full Text »    PDF »
SHR5: a novel plant receptor kinase involved in plant-N2-fixing endophytic bacteria association.
F. Vinagre, C. Vargas, K. Schwarcz, J. Cavalcante, E. M. Nogueira, J. I. Baldani, P. C. G. Ferreira, and A. S. Hemerly (2006)
J. Exp. Bot. 57, 559-569
   Abstract »    Full Text »    PDF »
Shoot-applied MeJA Suppresses Root Nodulation in Lotus japonicus.
T. Nakagawa and M. Kawaguchi (2006)
Plant Cell Physiol. 47, 176-180
   Abstract »    Full Text »    PDF »
Nod Factors Induce Nod Factor Cleaving Enzymes in Pea Roots. Genetic and Pharmacological Approaches Indicate Different Activation Mechanisms.
A. O. Ovtsyna, E. A. Dolgikh, A. S. Kilanova, V. E. Tsyganov, A. Y. Borisov, I. A. Tikhonovich, and C. Staehelin (2005)
Plant Physiology 139, 1051-1064
   Abstract »    Full Text »    PDF »
Grafting between model legumes demonstrates roles for roots and shoots in determining nodule type and host/rhizobia specificity.
D. P. Lohar and K. A. VandenBosch (2005)
J. Exp. Bot. 56, 1643-1650
   Abstract »    Full Text »    PDF »
The Sulfate Transporter SST1 Is Crucial for Symbiotic Nitrogen Fixation in Lotus japonicus Root Nodules.
L. Krusell, K. Krause, T. Ott, G. Desbrosses, U. Kramer, S. Sato, Y. Nakamura, S. Tabata, E. K. James, N. Sandal, et al. (2005)
PLANT CELL 17, 1625-1636
   Abstract »    Full Text »    PDF »
Bridging Model and Crop Legumes through Comparative Genomics.
H. Zhu, H.-K. Choi, D. R. Cook, and R. C. Shoemaker (2005)
Plant Physiology 137, 1189-1196
   Full Text »    PDF »
Proteomic Analysis of Somatic Embryogenesis in Medicago truncatula. Explant Cultures Grown under 6-Benzylaminopurine and 1-Naphthaleneacetic Acid Treatments.
N. Imin, M. Nizamidin, D. Daniher, K. E. Nolan, R. J. Rose, and B. G. Rolfe (2005)
Plant Physiology 137, 1250-1260
   Abstract »    Full Text »    PDF »
Characterization of the Lotus japonicus Symbiotic Mutant lot1 That Shows a Reduced Nodule Number and Distorted Trichomes.
Y. Ooki, M. Banba, K. Yano, J. Maruya, S. Sato, S. Tabata, K. Saeki, M. Hayashi, M. Kawaguchi, K. Izui, et al. (2005)
Plant Physiology 137, 1261-1271
   Abstract »    Full Text »    PDF »
Structure-Function Analysis of Cf-9, a Receptor-Like Protein with Extracytoplasmic Leucine-Rich Repeats.
R. A.L. van der Hoorn, B. B.H. Wulff, S. Rivas, M. C. Durrant, A. van der Ploeg, P. J.G.M. de Wit, and J. D.G. Jones (2005)
PLANT CELL 17, 1000-1015
   Abstract »    Full Text »    PDF »
Expression Profiling in Medicago truncatula Identifies More Than 750 Genes Differentially Expressed during Nodulation, Including Many Potential Regulators of the Symbiotic Program.
F. El Yahyaoui, H. Kuster, B. Ben Amor, N. Hohnjec, A. Puhler, A. Becker, J. Gouzy, T. Vernie, C. Gough, A. Niebel, et al. (2004)
Plant Physiology 136, 3159-3176
   Abstract »    Full Text »    PDF »
Control of Nodule Number by the Phytohormone Abscisic Acid in the Roots of Two Leguminous Species.
A. Suzuki, M. Akune, M. Kogiso, Y. Imagama, K.-i. Osuki, T. Uchiumi, S. Higashi, S.-Y. Han, S. Yoshida, T. Asami, et al. (2004)
Plant Cell Physiol. 45, 914-922
   Abstract »    Full Text »    PDF »
National Science Foundation-Sponsored Workshop Report. Draft Plan for Soybean Genomics.
G. Stacey, L. Vodkin, W. A. Parrott, and R. C. Shoemaker (2004)
Plant Physiology 135, 59-70
   Abstract »    Full Text »    PDF »
Comparative Analysis of the Receptor-Like Kinase Family in Arabidopsis and Rice.
S.-H. Shiu, W. M. Karlowski, R. Pan, Y.-H. Tzeng, K. F. X. Mayer, and W.-H. Li (2004)
PLANT CELL 16, 1220-1234
   Abstract »    Full Text »    PDF »
Switch from intracellular to intercellular invasion during water stress-tolerant legume nodulation.
S. Goormachtig, W. Capoen, E. K. James, and M. Holsters (2004)
PNAS 101, 6303-6308
   Abstract »    Full Text »    PDF »
Synergistic interaction of three ERECTA-family receptor-like kinases controls Arabidopsis organ growth and flower development by promoting cell proliferation.
E. D. Shpak, C. T. Berthiaume, E. J. Hill, and K. U. Torii (2004)
Development 131, 1491-1501
   Abstract »    Full Text »    PDF »
LRR-containing receptors regulating plant development and defense.
A. Dievart and S. E. Clark (2004)
Development 131, 251-261
   Abstract »    Full Text »    PDF »
Characterization of Four Lectin-Like Receptor Kinases Expressed in Roots of Medicago truncatula. Structure, Location, Regulation of Expression, and Potential Role in the Symbiosis with Sinorhizobium meliloti.
M.-T. Navarro-Gochicoa, S. Camut, A. C.J. Timmers, A. Niebel, C. Herve, E. Boutet, J.-J. Bono, A. Imberty, and J. V. Cullimore (2003)
Plant Physiology 133, 1893-1910
   Abstract »    Full Text »
Auxin Up-Regulates MtSERK1 Expression in Both Medicago truncatula Root-Forming and Embryogenic Cultures.
K. E. Nolan, R. R. Irwanto, and R. J. Rose (2003)
Plant Physiology 133, 218-230
   Abstract »    Full Text »    PDF »
Suppression of arbuscular mycorrhizal colonization and nodulation in split-root systems of alfalfa after pre-inoculation and treatment with Nod factors.
J.-G. Catford, C. Staehelin, S. Lerat, Y. Piche, and H. Vierheilig (2003)
J. Exp. Bot. 54, 1481-1487
   Abstract »    Full Text »    PDF »
Summaries of Legume Genomics Projects from around the Globe. Community Resources for Crops and Models.
K. A. VandenBosch and G. Stacey (2003)
Plant Physiology 131, 840-865
   Full Text »    PDF »
Symbiosis, Inventiveness by Recruitment?.
K. Szczyglowski and L. Amyot (2003)
Plant Physiology 131, 935-940
   Full Text »    PDF »
Dual Genetic Pathways Controlling Nodule Number in Medicago truncatula.
R. V. Penmetsa, J. A. Frugoli, L. S. Smith, S. R. Long, and D. R. Cook (2003)
Plant Physiology 131, 998-1008
   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