Nematode CLE signaling in Arabidopsis requires CLAVATA2 and CORYNE

Plant Journal

Volumn 65, Issue 3, 2011, Pages 430-440

  Replogle, Amy ^a   Wang, Jianying ^a   Bleckmann, Andrea ^b   Hussey, Richard S ^c   Baum, Thomas J ^d   Sawa, Shinichiro ^e   Davis, Eric L ^f   Wang, Xiaohong ^g   Simon, Rüdiger ^b   Mitchum, Melissa G ^a  

^a UNIVERSITY OF MISSOURI   (United States)

^b HEINRICH HEINE UNIVERSITY   (Germany)

^c UNIVERSITY OF GEORGIA   (United States)

^d IOWA STATE UNIVERSITY   (United States)

^e UNIVERSITY OF TOKYO   (Japan)

^f NORTH CAROLINA STATE UNIVERSITY   (United States)

^g Department of Obstetrics Gynecology   (United States)

Author keywords

CLAVATA2; CLE peptide; CORYNE; nematode; receptor; syncytium

Indexed keywords

CLAVATA2; CLE PEPTIDE; CORYNE; NEMATODE; RECEPTOR; SYNCYTIUM;

SIGNALING;

PEPTIDES;

ARABIDOPSIS PROTEIN; BETA GLUCURONIDASE; CELL SURFACE RECEPTOR; CLV2 PROTEIN, ARABIDOPSIS; CORYNE PROTEIN, ARABIDOPSIS; MEMBRANE PROTEIN; PROTEIN SERINE THREONINE KINASE;

AMINO ACID SEQUENCE; ANIMAL; ARABIDOPSIS; ARTICLE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; MUTATION; NEMATODE; PARASITOLOGY; PROMOTER REGION; PROTEIN BINDING; PROTEIN MULTIMERIZATION; SIGNAL TRANSDUCTION; TRANSGENIC PLANT;

AMINO ACID SEQUENCE; ANIMALS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; GENE EXPRESSION REGULATION, PLANT; GLUCURONIDASE; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; MUTATION; NEMATODA; PLANTS, GENETICALLY MODIFIED; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION;

ARABIDOPSIS; NEMATODA;

EID: 79251583180     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2010.04433.x     Document Type: Article

References (52)

1. Bakhetia, M., Urwin, P.E., and, Atkinson, H.J., (2007) qPCR analysis and RNAi define pharyngeal gland cell-expressed genes of Heterodera glycines required for initial interactions with the host. Mol. Plant Microbe Interact. 20, 306-312.
2. Bleckmann, A., Weidtkamp-Peters, S., Seidel, C.A., and, Simon, R., (2010) Stem cell signaling in Arabidopsis requires CRN to localize CLV2 to the plasma membrane. Plant Physiol. 152, 166-176.
3. Boisnard-Lorig, C., Colon-Carmona, A., Bauch, M., Hodge, S., Doerner, P., Bancharel, E., Dumas, C., Haseloff, J., and, Berger, F., (2001) Dynamic analyses of the expression of the HISTONE::YFP fusion protein in Arabidopsis show that syncytial endosperm is divided in mitotic domains. Plant Cell, 13, 495-509.
4. Casamitjana-Martinez, E., Hofhuis, H.F., Xu, J., Liu, C.M., Heidstra, R., and, Scheres, B., (2003) Root-specific CLE19 overexpression and the sol1/2 suppressors implicate a CLV-like pathway in the control of Arabidopsis root meristem maintenance. Curr. Biol. 13, 1435-1441.
5. Clark, S.E., Running, M.P., and, Meyerowitz, E.M., (1993) CLAVATA1, a regulator of meristem and flower development in Arabidopsis. Development, 119, 397-418.
6. Clark, S.E., Williams, R.W., and, Meyerowitz, E.M., (1997) The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis. Cell, 89, 575-585.
7. Clough, S.J., and, Bent, A.F., (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
8. Curtis, M.D., and, Grossniklaus, U., (2003) A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol. 133, 462-469.
9. Davis, E.L., Hussey, R.S., and, Baum, T.J., (2004) Getting to the roots of parasitism by nematodes. Trends Parasitol. 20, 134-141.
10. Davis, E.L., Hussey, R.S., Mitchum, M.G., and, Baum, T.J., (2008) Parasitism proteins in nematode-plant interactions. Curr. Opin. Plant Biol. 11, 360-366.
11. DeYoung, B.J., and, Clark, S.E., (2008) BAM receptors regulate stem cell specification and organ development through complex interactions with CLAVATA signaling. Genetics, 180, 895-904.
12. DeYoung, B.J., Bickle, K.L., Schrage, K.J., Muskett, P., Patel, K., and, Clark, S.E., (2006) The CLAVATA1-related BAM1, BAM2 and BAM3 receptor kinase-like proteins are required for meristem function in Arabidopsis. Plant J. 45, 1-16.
13. Endo, B.Y., (1964) Penetration and development of Heterodera glycines in soybean roots and related anatomical changes. Phytopathology, 54, 79-88.
14. Fiers, M., Hause, G., Boutilier, K., Casamitjana-Martinez, E., Weijers, D., Offringa, R., van der Geest, L., van Lookeren Campagne, M., and, Liu, C.M., (2004) Mis-expression of the CLV3/ESR-like gene CLE19 in Arabidopsis leads to a consumption of root meristem. Gene, 327, 37-49.
15. Fiers, M., Golemiec, E., Xu, J., van der Geest, L., Heidstra, R., Stiekema, W., and, Liu, C.M., (2005) The 14-amino acid CLV3, CLE19, and CLE40 peptides trigger consumption of the root meristem in Arabidopsis through a CLAVATA2-dependent pathway. Plant Cell, 17, 2542-2553.
16. Fletcher, L.C., Brand, U., Running, M.P., Simon, R., and, Meyerowitz, E.M., (1999) Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science, 283, 1911-1914.
17. Gao, B., Allen, R., Maier, T., Davis, E.L., Baum, T.J., and, Hussey, R.S., (2003) The parasitome of the phytonematode Heterodera glycines. Mol. Plant Microbe Interact. 16, 720-726.
18. Guo, Y., Han, L., Hymes, M., Denver, R., and, Clark, S.E., (2010) CLAVATA2 forms a distinct CLE-binding receptor complex regulating Arabidopsis stem cell specification. Plant J. 63, 889-900.
19. Hofmann, J., Youssef-Banora, M., de Almeida-Engler, J., and, Grundler, F.M.W., (2010) The role of callose deposition along plasmodesmata in nematode feeding sites. Mol. Plant Microbe Interact. 23, 549-557.
20. Jefferson, R.A., Kavanagh, T.A., and, Bevan, M.W., (1987) GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6, 3901-3907.
21. Jeong, S., Trotochaud, A.E., and, Clark, S.E., (1999) The Arabidopsis CLAVATA2 gene encodes a receptor-like protein required for the stability of the CLAVATA1 receptor-like kinase. Plant Cell, 11, 1925-1934.
22. Kayes, J.M., and, Clark, S.E., (1998) CLAVATA2, a regulator of meristem and organ development in Arabidopsis. Development, 125, 3843-3851.
23. Koornneef, M., Van Eden, J., Hanhart, C.J., Stam, P., Braaksma, F.J., and, Feenstra, W.J., (1983) Linkage Map of Arabidopsis thaliana. J. Hered. 74, 265-272.
24. Laux, T., Mayer, K.F.X., Berger, J., and, Jurgens, G., (1996) The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development, 122, 87-96.
25. Lu, S.W., Chen, S., Wang, J., Yu, H., Chronis, D., Mitchum, M.G., and, Wang, X., (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.
26. Meng, L., and, Feldman, L., (2010) CLE14/CLE20 peptides may interact with CLAVATA2/CORYNE receptor-like kinases to irreversibly inhibit cell division in the root meristem of Arabidopsis. Planta, 232, 1061-1074.
27. Meng, L., Ruth, K.C., Fletcher, J.C., and, Feldman, L., (2010) The roles of different CLE domains in Arabidopsis CLE polypeptide activity and functional specificity. Mol. Plant, 3, 760-772.
28. Mitchum, M.G., Sukno, S., Wang, X., Shani, Z., Tsabary, G., Shoseyov, O., and, Davis, E.L., (2004) The promoter of the Arabidopsis thaliana Cel1 endo-1,4-beta glucanase gene is differentially expressed in plant feeding cells induced by root-knot and cyst nematodes. Mol. Plant Pathol. 5, 175-181.
29. Mitchum, M.G., Wang, X.H., and, Davis, E.L., (2008) Diverse and conserved roles of CLE peptides. Curr. Opin. Plant Biol. 11, 75-81.
30. Miwa, H., Betsuyaku, S., Iwamoto, K., Kinoshita, A., Fukuda, H., and, Sawa, S., (2008) The receptor-like kinase SOL2 mediates CLE signaling in Arabidopsis. Plant Cell Physiol. 49, 1752-1757.
31. Muller, R., Bleckmann, A., and, Simon, R., (2008) The receptor kinase CORYNE of Arabidopsis transmits the stem cell-limiting signal CLAVATA3 independently of CLAVATA1. Plant Cell, 20, 934-946.
32. Ogawa, M., Shinohara, H., Sakagami, Y., and, Matsubayashi, Y., (2008) Arabidopsis CLV3 peptide directly binds CLV1 ectodomain. Science, 319, 294.
33. Patel, N., Hamamouch, N., Chunying, L., Hussey, R., Mitchum, M., Baum, T., Wang, X., and, Davis, E.L., (2008) Similarity and functional analyses of expressed parasitism genes in Heterodera schachtii and Heterodera glycines. J. Nematol. 40, 299-310.
34. Rojo, E., Sharma, V.K., Kovaleva, V., Raikhel, N.V., and, Fletcher, J.C., (2002) CLV3 is localized to the extracellular space, where it activates the Arabidopsis CLAVATA stem cell signaling pathway. Plant Cell, 14, 969-977.
35. Sarkar, A.K., Luijten, M., Miyashima, S., Lenhard, M., Hashimoto, T., Nakajima, K., Scheres, B., Heidstra, R., and, Laux, T., (2007) Conserved factors regulate signaling in Arabidopsis thaliana shoot and root stem cell organizers. Nature, 446, 811-814.
36. Sasser, J.N., and, Freckman, D.W., (1987) A world perspective on nematology: the role of the society. In Vistas on Nematology (, Veech, J.A., and, Dickson, D.W., eds). Hyatssville, MD, USA: Society of Nematologists, pp. 7-14.
37. Sharma, V.K., Ramirez, J., and, Fletcher, J.C., (2003) The Arabidopsis CLV3-like (CLE) genes are expressed in diverse tissues and encode secreted proteins. Plant Mol. Biol. 51, 415-425.
38. Shiu, S.H., and, Bleecker, A.B., (2001) Plant receptor-like kinase gene family: diversity, function, and signaling. Sci. STKE, 2001, re22.
39. Siddique, S., Endres, S., Atkins, J.M., et al. (2009) Myo-inositol oxygenase genes are involved in the development of syncytia induced by Heterodera schachtii in Arabidopsis roots. New Phytol. 184, 457-472.
40. Sijmons, P.C., Grundler, F.M.W., Von Mende, N., Burrows, P.R., and, Wyss, U., (1991) Arabidopsis thaliana as a new model host for plant parasitic nematodes. Plant J. 1, 245-254.
41. Simon, R., and, Stahl, T., (2006) Plant cells CLEave their way to differentiation. Science, 313, 773-774.
42. Stahl, Y., Wink, R.H., Ingram, G.C., and, Simon, R., (2009) A signaling module controlling the stem cell niche in Arabidopsis root meristems. Curr. Biol. 19, 909-914.
43. 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.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.
44. Szakasits, D., Heinen, P., Wieczorek, K., Hoffman, J., Wagner, F., Kreil, D.P., Sykacek, P., Grundler, F.M.W., and, Bohlmann, H., (2009) The transcriptome of syncytia induced by the cyst nematode Heterodera schachtii in Arabidopsis roots. Plant J. 57, 771-784.
45. Trotochaud, A.E., Hao, T., Wu, G., Yang, Z., and, Clark, S.E., (1999) The CLAVATA1 receptor-like kinase requires CLAVATA3 for its assembly into a signaling complex that includes KAPP and a Rho-related protein. Plant Cell, 11, 393-406.
46. 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 peptide-selection of cDNA cloned directly from the esophageal gland cells of the soybean cyst nematode Heterodera glycines. Mol. Plant Microbe Interact. 14, 536-544.
47. 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 plant-parasitic nematode with function similar to CLAVATA3/ESR (CLE) of Arabidopsis thaliana. Mol. Plant Pathol. 6, 187-191.
48. Wang, X., Replogle, A., Davis, E.L., and, Mitchum, M.G., (2007) The tobacco Cel7 gene promoter is auxin-responsive and locally induced in nematode feeding sites of heterologous plants. Mol. Plant Pathol. 8, 423-436.
49. Wang, J., Lee, C., Replogle, A., Joshi, S., Korkin, D., Hussey, R., Baum, T.J., Davis, E.L., Wang, X., and, Mitchum, M.G., (2010a) Dual roles for the variable domain in protein trafficking and host-specific recognition of Heterodera glycines CLE effector proteins. New Phytol. 187, 1003-1017.
50. Wang, J., Replogle, A., Hussey, R., Baum, T., Wang, X., Davis, E.L., and, Mitchum, M.G., (2010b) Identification of potential host plant mimics of CLV3/ESR (CLE)-like peptides from the plant-parasitic nematode Heterodera schachtii. Mol. Plant Pathol. DOI:.
51. 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.
52. Zhu, Y., Wang, Y., Li, R., Song, X., Wang, Q., Huang, S., Jin, J.B., Liu, C.M., and, Lin, J., (2010) Analysis of interactions among the CLAVATA3 receptors reveals a direct interaction between CLAVATA2 and CORYNE in Arabidopsis. Plant J. 61, 223-233.