Members of the meloidogyne avirulence protein family contain multiple plant ligand-like motifs

Phytopathology

Volumn 104, Issue 8, 2014, Pages 879-885

  Rutter, William B ^a   Hewezi, Tarek ^b   Maier, Tom R ^a   Mitchum, Melissa G ^c   Davis, Eric L ^d   Hussey, Richard S ^e   Baum, Thomas J ^a  

^a IOWA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF TENNESSEE   (United States)

^c UNIVERSITY OF MISSOURI   (United States)

^d NORTH CAROLINA STATE UNIVERSITY   (United States)

^e UNIVERSITY OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HELMINTH PROTEIN; LIGAND; MESSENGER RNA;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; CHEMISTRY; GENETICS; IN SITU HYBRIDIZATION; MOLECULAR GENETICS; MULTIGENE FAMILY; PARASITOLOGY; PHYSIOLOGY; PLANT DISEASE; PROTEIN MOTIF; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; TYLENCHOIDEA;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; HELMINTH PROTEINS; IN SITU HYBRIDIZATION; LIGANDS; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; PLANT DISEASES; RNA, MESSENGER; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; TYLENCHOIDEA;

EID: 84905396525     PISSN: 0031949X     EISSN: None     Source Type: Journal    
DOI: 10.1094/PHYTO-11-13-0326-R     Document Type: Article

References (44)

1. Abad, P. 2009. Meloidogyne incognita resources. INRA, Sophia-Antipolis, France.
2. Abad, P., Gouzy, J., Aury, J. M., Castagnone-Sereno, P., Danchin, E. G. J., Deleury, E., Perfus-Barbeoch, L., Anthouard, V., Artiguenave, F., Blok, V. C., Caillaud, M. C., Coutinho, P. M., Dasilva, C., De Luca, F., Deau, F., Esquibet, M., Flutre, T., Goldstone, J. V., Hamamouch, N., Hewezi, T., Jaillon, O., Jubin, C., Leonetti, P., Magliano, M., Maier, T. R., Markov, G. V., McVeigh, P., Pesole, G., Poulain, J., Robinson-Rechavi, M., Sallet, E., Segurens, B., Steinbach, D., Tytgat, T., Ugarte, E., van Ghelder, C., Veronico, P., Baum, T. J., Blaxter, M., Bleve-Zacheo, T., Davis, E. L., Ewbank, J. J., Favery, B., Grenier, E., Henrissat, B., Jones, J. T., Laudet, V., Maule, A. G., Quesneville, H., Rosso, M. N., Schiex, T., Smant, G., Weissenbach, J., and Wincker, P. 2008. Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita. Nat. Biotechnol. 26: 909-915. Online publication. doi: 10.1038/Nbt.1482
3. Abad, P., and Williamson, V. M. 2010. Plant nematode interaction: A sophisticated dialogue. Pages 147-192 in: Advances in Botanical Research, Vol. 53. Elsevier Inc., Philadelphia, PA.
4. Adam, M. A. M., Phillips, M. S., Tzortzakakis, E. A., and Blok, V. C. 2009. Characterisation of mjap genes encoding novel secreted proteins from the root-knot nematode, Meloidogyne javanica. Nematology 11: 253- 265. Online publication. doi: 10.1163/156854109x429583
5. Bailey, T. L., Boden, M., Buske, F. A., Frith, M., Grant, C. E., Clementi, L., Ren, J. Y., Li, W. W., and Noble, W. S. 2009. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res. 37: W202-W208. Online publication. doi: 10.1093/Nar/Gkp335
6. Bird, D. M., and DiGennaro, P. M. 2012. Nematode communication with plants is surprisingly complex and multidimensional. Pages 213-230 In: Biocommunication of Plants. G. Witzany and F. Baluska, eds. Springer- Verlag, Berlin, Germany.
7. Castagnone-Sereno, P., Semblat, J. P., and Castagnone, C. 2009. Modular architecture and evolution of the map-1 gene family in the root-knot nematode Meloidogyne incognita. Mol. Genet. Genomics 282: 547-554. Online publication. doi: 10.1007/S00438-009-0487-X
8. Cock, J. M., and McCormick, S. 2001. A large family of genes that share homology with CLAVATA3. Plant Physiol. 126: 939-942.
9. Crooks, G. E., Hon, G., Chandonia, J. M., and Brenner, S. E. 2004. WebLogo: A sequence logo generator. Genome Res. 14: 1188-1190. Online publication. doi: 10.1101/gr.849004
10. Danchin, E. G. J., Rosso, M. N., Vieira, P., de Almeida-Engler, J., Coutinho, P. M., Henrissat, B., and Abad, P. 2010. Multiple lateral gene transfers and duplications have promoted plant parasitism ability in nematodes. Proc. Natl. Acad. Sci. USA 107: 17651-17656. Online publication. doi: 10.1073/pnas.1008486107
11. de Boer, J. M., Yan, Y., Smant, G., Davis, E. L., and Baum, T. J. 1998. Insitu hybridization to messenger RNA in Heterodera glycines. J. Nematol. 30: 309-312.
12. de Boer, J. M., Yan, Y., Wang, X., Smant, G., Hussey, R. S., Davis, E. L., and Baum, T. J. 1999. Developmental expression of secretory beta-1,4- endoglucanases in the subventral esophageal glands of Heterodera glycines. Mol. Plant-Microbe Interact. 12: 663-669. Online publication. doi: 10.1094/MPMI.1999.12.8.663
13. Fiers, M., Golemiec, E., van der Schors, R., van der Geest, L., Li, K. W., Stiekema, W. J., and Liu, C. M. 2006. The CLAVATA3/ESR motif of CLAVATA3 is functionally independent from the nonconserved flanking sequences. Plant Physiol. 141: 1284-1292. Online publication. doi: pp.106.080671 [pii] 10.1104/pp.106.080671
14. Gao, B. L., Allen, R., Maier, T., Davis, E. L., Baum, T. J., and Hussey, R. S. 2001. Identification of putative parasitism genes expressed in the esophageal gland cells of the soybean cyst nematode Heterodera glycines. Mol. Plant-Microbe Interact. 14: 1247-1254.
15. Golinowski, W., Sobczak, M., Kurek, W., and Grymaszewska, G. 1997. The structure of syncytia. In: Cellular and Molecular Aspects of Plant- Nematode Interactions, Vol. 10. C. Fenoll, F. M. W. Grundler, and S. A. Ohl, eds. Kluwer Academic Publishers, Dordrecht, The Netherlands.
16. Guo, Y. F., Ni, J., Denver, R., Wang, X. H., and Clark, S. E. 2011. Mechanisms of molecular mimicry of plant CLE peptide ligands by the parasitic nematode Globodera rostochiensis. Plant Physiol. 157: 476-484. Online publication. doi: 10.1104/Pp.111.180554
17. Hassan, S., Behm, C. A., and Mathesius, U. 2010. Effectors of plant parasitic nematodes that re-program root cell development. Funct. Plant Biol. 37: 933-942. Online publication. doi: 10.1071/Fp10112
18. Hewezi, T., and Baum, T. 2012. Manipulation of plant cells by cyst and root-knot nematode effectors. Mol. Plant-Microbe Interact. Online publication. doi: 10.1094/MPMI-05-12-0106-FI
19. Huang, G. Z., Dong, R. H., Allen, R., Davis, E. L., Baum, T. J., and Hussey, R. S. 2006. A root-knot nematode secretory peptide functions as a ligand for a plant transcription factor. Mol. Plant-Microbe Interact. 19: 463-470. Online publication. doi: 10.1094/mpmi-19-0463
20. Huang, G. Z., Gao, B. L., Maier, T., Allen, R., Davis, E. L., Baum, T. J., and Hussey, R. S. 2003. A profile of putative parasitism genes expressed in the esophageal gland cells of the root-knot nematode Meloidogyne incognita. Mol. Plant-Microbe Interact. 16: 376-381.
21. Ito, Y., Nakanomyo, I., Motose, H., Iwamoto, K., Sawa, S., Dohmae, N., and Fukuda, H. 2006. Dodeca-CLE peptides as suppressors of plant stem cell differentiation. Science 313: 842-845. Online publication. doi: 10.1126/science.1128436
22. Jun, J., Fiume, E., Roeder, A. H. K., Meng, L., Sharma, V. K., Osmont, K. S., Baker, C., Ha, C. M., Meyerowitz, E. M., Feldman, L. J., and Fletcher, J. C. 2010. Comprehensive analysis of CLE polypeptide signaling gene expression and overexpression activity in Arabidopsis. Plant Physiol. 154: 1721-1736. Online publication. doi: 10.1104/Pp.110.163683
23. Jun, J. H., Fiume, E., and Fletcher, J. C. 2008. The CLE family of plant polypeptide signaling molecules. Cell. Mol. Life Sci. 65: 743-755. Online publication. doi: 10.1007/S00018-007-7411-5
24. Katsir, L., Davies, K. A., Bergmann, D. C., and Laux, T. 2011. Peptide signaling in plant development. Curr. Biol. 21: R356-R364. Online publication. doi: 10.1016/J.Cub.2011.03.012
25. Kinoshita, A., Nakamura, Y., Sasaki, E., Kyozuka, J., Fukuda, H., and Sawa, S. 2007. Gain-of-function phenotypes of chemically synthetic CLAVATA3/ESR-related (CLE) peptides in Arabidopsis thaliana and Oryza sativa. Plant Cell Physiol. 48: 1821-1825. Online publication. doi: 10.1093/pcp/pcm154
26. Kondo, T., Sawa, S., Kinoshita, A., Mizuno, S., Kakimoto, T., Fukuda, H., and Sakagami, Y. 2006. A plant peptide encoded by CLV3 identified by in situ MALDI-TOF MS analysis. Science 313: 845-848. Online publication. doi: 10.1126/Science.1128439
27. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibson, T. J., and Higgins, D. G. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948. Online publication. doi: btm404 [pii]10.1093/bioinformatics/btm404
28. Lu, S. W., Chen, S. Y., Wang, J. Y., Yu, H., Chronis, D., Mitchum, M. G., and Wang, X. H. 2009. Structural and functional diversity of CLAVATA3/ ESR (CLE)-like genes from the potato cyst nematode Globodera rostochiensis. Mol. Plant-Microbe Interact. 22: 1128-1142. Online publication. doi: 10.1094/Mpmi-22-9-1128
29. Mitchum, M. G., Hussey, R. S., Baum, T. J., Wang, X., Elling, A. A., Wubben, M., and Davis, E. L. 2013. Nematode effector proteins: An emerging paradigm of parasitism. New Phytol. Online publication. doi: 10.1111/nph.12323
30. Mitchum, M. G., Wang, X., Wang, J., and Davis, E. L. 2012. Role of nematode peptides and other small molecules in plant parasitism. Annu. Rev. Phytopathol. 50: 175-195. Online publication. doi: 10.1146/annurevphyto- 081211-173008
31. Oelkers, K., Goffard, N., Weiller, G. F., Gresshoff, P. M., Mathesius, U., and Frickey, T. 2008. Bioinformatic analysis of the CLE signaling peptide family. BMC Plant Biol. 8. Online publication. doi: 10.1186/1471-2229-8-1
32. Ohyama, K., Shinohara, H., Ogawa-Ohnishi, M., and Matsubayashi, Y. 2009. A glycopeptide regulating stem cell fate in Arabidopsis thaliana. Nat. Chem. Biol. 5: 578-580. Online publication. doi: 10.1038/nchembio.182
33. Olsen, A. N., and Skriver, K. 2003. Ligand mimicry? Plant-parasitic nematode polypeptide with similarity to CLAVATA3. Trends Plant Sci. 8: 55-57. Online publication. doi: S1360138503000037
34. Replogle, A., Wang, J., Bleckmann, A., Hussey, R. S., Baum, T. J., Sawa, S., Davis, E. L., Wang, X., Simon, R., and Mitchum, M. G. 2011. Nematode CLE signaling in Arabidopsis requires CLAVATA2 and CORYNE. Plant J. 65: 430-440. Online publication. doi: 10.1111/j.1365- 313X.2010.04433.x
35. Semblat, J. P., Rosso, M. N., Hussey, R. S., Abad, P., and Castagnone- Sereno, P. 2001. Molecular cloning of a cDNA encoding an amphid secreted putative avirulence protein from the root-knot nematode Meloidogyne incognita. Mol. Plant-Microbe Interact. 14: 72-79.
36. Strabala, T. J., O'Donnell P, J., Smit, A. M., Ampomah-Dwamena, C., Martin, E. J., Netzler, N., Nieuwenhuizen, N. J., Quinn, B. D., Foote, H. C., and Hudson, K. R. 2006. Gain-of-function phenotypes of many CLAVATA3/ESR genes, including four new family members, correlate with tandem variations in the conserved CLAVATA3/ESR domain. Plant Physiol. 140: 1331-1344. Online publication. doi: pp.105.075515
37. Tomalova, I., Iachia, C., Mulet, K., and Castagnone-Sereno, P. 2012. The map-1 gene family in root-knot nematodes, Meloidogyne spp.: A set of taxonomically restricted genes specific to clonal species. PLoS One 7: e38656. Online publication. doi: 10.1371/journal.pone.0038656
38. Tucker, M. L., and Yang, R. 2013. A gene encoding a peptide with similarity to the plant IDA signaling peptide (AtIDA) is expressed most abundantly in the root-knot nematode (Meloidogyne incognita) soon after root infection. Exp. Parasitol. 134: 165-170. Online publication. doi: 10.1016/j.exppara.2013.03.019
39. Vieira, P., Danchin, E. G., Neveu, C., Crozat, C., Jaubert, S., Hussey, R. S., Engler, G., Abad, P., de Almeida-Engler, J., Castagnone-Sereno, P., and Rosso, M. N. 2011. The plant apoplasm is an important recipient compartment for nematode secreted proteins. J. Exp. Bot. 62: 1241-1253. Online publication. doi: 10.1093/jxb/erq352
40. Wang, J., Replogle, A., Hussey, R., Baum, T., Wang, X., Davis, E. L., and Mitchum, M. G. 2011. Identification of potential host plant mimics of CLAVATA3/ESR (CLE)-like peptides from the plant-parasitic nematode Heterodera schachtii. Mol. Plant Pathol. 12: 177-186. Online publication. doi: 10.1111/j.1364-3703.2010.00660.x
41. Wang, J. Y., Lee, C., Replogle, A., Joshi, S., Korkin, D., Hussey, R., Baum, T. J., Davis, E. L., Wang, X. H., and Mitchum, M. G. 2010. Dual roles for the variable domain in protein trafficking and host-specific recognition of Heterodera glycines CLE effector proteins. New. Phytol. 187: 1003-1017. Online publication. doi: 10.1111/J.1469-8137.2010.03300.X
42. Wang, X., Allen, R., Ding, X., Goellner, M., Maier, T., de Boer, J. M., Baum, T. J., Hussey, R. S., and Davis, E. L. 2001. Signal peptideselection of cDNA cloned directly from the esophageal gland cells of the soybean cyst nematode Heterodera glycines. Mol. Plant-Microbe Interact. 14: 536-544. Online publication. doi: 10.1094/MPMI.2001.14.4.536
43. Wang, X., Mitchum, M. G., Gao, B., Li, C., Diab, H., Baum, T. J., Hussey, R. S., and Davis, E. L. 2005. A parasitism gene from a plantparasitic nematode with function similar to CLAVATA3/ESR (CLE) of Arabidopsis thaliana. Mol. Plant Pathol. 6: 187-191. Online publication. doi: 10.1111/j.1364-3703.2005.00270.x
44. Whitford, R., Fernandez, A., De Groodt, R., Ortega, E., and Hilson, P. 2008. Plant CLE peptides from two distinct functional classes synergistically induce division of vascular cells. Proc. Natl. Acad. Sci. USA 105: 18625-18630. Online publication. doi: 10.1073/Pnas.0809395105