Gall formation in clubroot-infected Arabidopsis results from an increase in existing meristematic activities of the host but is not essential for the completion of the pathogen life cycle

Plant Journal

Volumn 71, Issue 2, 2012, Pages 226-238

  Malinowski, Robert ^a   Smith, Jody A ^a   Fleming, Andrew J ^a   Scholes, Julie D ^a   Rolfe, Stephen A ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

development; hypocotyl; meristems; plant pathogens; Plasmodiophora brassicae; vascular cambium

Indexed keywords

DEVELOPMENT; HYPOCOTYL; MERISTEMS; PLANT PATHOGEN; PLASMODIOPHORA BRASSICAE; VASCULAR CAMBIUM;

CELL PROLIFERATION; LIFE CYCLE; MAINTENANCE; PLANTS (BOTANY); STEM CELLS;

PATHOGENS;

ARABIDOPSIS PROTEIN; HYBRID PROTEIN; PLANT RNA;

ANIMAL; ARABIDOPSIS; ARTICLE; BIOLOGICAL MODEL; CAMBIUM; CELL DIFFERENTIATION; CELL DIVISION; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HOST PATHOGEN INTERACTION; LIFE CYCLE STAGE; MERISTEM; METABOLISM; MUTATION; PARASITOLOGY; PATHOGENICITY; PHLOEM; PLANT GROWTH; PLANT ROOT; PLANT TUMOR; PLASMODIOPHORIDA; VIRULENCE; XYLEM;

ANIMALS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CAMBIUM; CELL DIFFERENTIATION; CELL DIVISION; GENE EXPRESSION REGULATION, PLANT; HOST-PATHOGEN INTERACTIONS; HYPOCOTYL; LIFE CYCLE STAGES; MERISTEM; MODELS, BIOLOGICAL; MUTATION; PHLOEM; PLANT ROOTS; PLANT TUMORS; PLASMODIOPHORIDA; RECOMBINANT FUSION PROTEINS; RNA, PLANT; VIRULENCE; XYLEM;

ARABIDOPSIS; ARABIDOPSIS THALIANA; BACTERIA (MICROORGANISMS); PLASMODIOPHORA; PLASMODIOPHORA BRASSICAE;

EID: 84864415531     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2012.04983.x     Document Type: Article

References (57)

1. Aist, J.R., and, Williams, P.H., (1971) The cytology and kinetics of cabbage root hair penetration by Plasmodiophora brassicae. Can. J. Bot. 49, 2023-2034.
2. de Almeida Engler, J., De Vleesschauwer, V., Burssens, S., Celenza, J.L., Inzé, D., Van Montagu, M., Engler, G., and, Gheysen, G., (1999) Molecular markers and cell cycle inhibitors show the importance of cell cycle progression in nematode-induced galls and syncytia. Plant Cell, 11, 793-808.
3. Ando, S., Asano, T., Tsushima, S., Kamachi, S., Hagio, T., and, Tabei, Y., (2005) Changes in gene expression of putative isopentenyltransferase during clubroot development in Chinese cabbage (Brassica rapa L.). Physiol. Mol. Plant Pathol. 67, 59-67.
4. Avci, U., Earl Petzold, H., Ismail, I.O., Beers, E.P., and, Haigler, C.H., (2008) Cysteine proteases XCP1 and XCP2 aid micro-autolysis within the intact central vacuole during xylogenesis in Arabidopsis roots. Plant J. 56, 303-315.
5. Bonke, M., Thitamadee, S., Mähönen, A.P., Hauser, M.-T., and, Helariutta, Y., (2003) APL regulates vascular tissue identity in Arabidopsis. Nature, 426, 181-186. (Pubitemid 37442586)
6. Buczacki, S.T., (1983) Plasmodia-an inter-relationship between biological and practical problems. In Zoosporic Plant Pathogens. A modern perspective (, Buckzacki, S.T., ed), pp. 161-191. London: Academic Press.
7. Chomczynski, P., and, Sacchi, N., (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162, 156-159. (Pubitemid 17064313)
8. Dekhuijzen, H.M., (1981) The occurrence of free and bound cytokinins in plasmodia of Plasmodiophora brassicae isolated from tissue cultures of clubroots. Plant Cell Rep. 1, 18-20.
9. Dekhuijzen, H.M., and, Overeem, J.C., (1971) The role of cytokinins in clubroot formation. Physiol. Plant Path. 1, 151-161.
10. Devos, S., Vissenberg, K., Verbelen, J.-P., and, Prinsen, E., (2005) Infection of Chinese cabbage by Plasmodiophora brassicae leads to a stimulation of plant growth: impacts on cell wall metabolism and hormone balance. New Phytol. 166, 241-250. (Pubitemid 40428149)
11. Devos, S., Laukens, K., Deckers, P., Van Der Straeten, D., Beeckman, T., Inzé, D., Van Onckelen, H., Witters, E., and, Prinsen, E., (2006) A hormone and proteome approach to picturing the initial metabolic events during Plasmodiophora brassicae infection on Arabidopsis. Mol. Plant-Microbe Interact. 19, 1431-1443. (Pubitemid 44845782)
12. Donnelly, P.M., Bonetta, D., Tsukaya, H., Dengler, R.E., and, Dengler, N.G., (1999) Cell cycling and cell enlargement in developing leaves of Arabidopsis. Dev. Biol. 215, 407-419.
13. Etchells, J.P., and, Turner, S.R., (2010) The PXY-CLE41 receptor ligand pair defines a multifunctional pathway that controls the rate and orientation of vascular cell division. Development, 137, 767-774.
14. Evans, J.L., and, Scholes, J.D., (1995) How does clubroot alter the regulation of carbon metabolism in its host? Asp Appl. Biol. 42, 125-132.
15. Funk, V., Kositsup, B., Zhao, C., and, Beers, E.P., (2002) The Arabidopsis xylem peptidase XCP1 is a tracheary element vacuolar protein that may be a papain ortholog. Plant Physiol. 128, 84-94. (Pubitemid 34115312)
16. Gustafsson, M., and, Falt, A.S., (1986) Genetic studies on resistance to clubroot in Brassica napus. Ann. Appl. Biol. 108, 409-415.
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.
18. Hirakawa, Y., Shinohara, H., Kondo, Y., Inoue, A., Nakanomyo, I., Ogawa, M., Sawa, S., Ohashi-Ito, K., Matsubayashi, Y., and, Fukuda, H., (2008) Non-cell-autonomous control of vascular stem cell fate by a CLE peptide/receptor system. Proc. Natl Acad. Sci. USA, 105, 15208-15213.
19. Hirakawa, Y., Kondo, Y., and, Fukuda, H., (2010) TDIF peptide signaling regulates vascular stem cell proliferation via the WOX4 homeobox gene in Arabidopsis. Plant Cell, 22, 2618-2629.
20. Hirakawa, Y., Kondo, Y., and, Fukuda, H., (2011) Establishment and maintenance of vascular cell communities through local signaling. Curr. Opin. Plant Biol. 14, 17-23.
21. Huang, G., Dong, R., 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. (Pubitemid 43668270)
22. Ingram, D.S., and, Tommerup, I.C., (1972) The life history of Plasmodiophora brassicae Woron. Proc. R. Soc. Lond., Ser. B: Biol. Sci. 180, 103-112.
23. 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. (Pubitemid 44223354)
24. Jefferson, R.A., Burgess, S.M., and, Hirsh, D., (1986) β-Glucuronidase from Escherichia coli as a gene-fusion marker. Proc. Natl Acad. Sci. USA, 83, 8447-8451. (Pubitemid 17194890)
25. TM vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7, 193-195. (Pubitemid 36725938)
26. Keen, N.T., and, Williams, P.H., (1969) Translocation of sugars into infected cabbage tissues during clubroot development. Plant Physiol. 44, 748-754.
27. Klewer, A., Luerßen, H., Graf, H., and, Siemens, J., (2001) Restriction fragment length polymorphism markers to characterize Plasmodiophora brassicae single-spore isolates with different virulence patterns. J. Phytopathol. 149, 121-127. (Pubitemid 32449471)
28. Kobelt, P., Siemens, J., and, Sacristan, M.D., (2000) Histological characterisation of the incompatible interaction between Arabidopsis thaliana and the obligate biotrophic pathogen Plasmodiophora brassicae. Mycol. Res. 2, 220-225. (Pubitemid 30446024)
29. Koch, E., Cox, R., and, Williams, P.H., (1991) Infection of Arabidopsis thaliana by Plasmodiophora brassicae. J. Phytopathol. 132, 99-104.
30. Krizek, B., (2009) AINTEGUMENTA and AINTEGUMENTA-LIKE6 act redundantly to regulate Arabidopsis floral growth and patterning. Plant Physiol. 150, 1916-1929.
31. Kubo, M., Udagawa, M., Nishikubo, N., Horiguchi, G., Yamaguchi, M., Ito, J., Mimura, T., Fukuda, H., and, Demura, T., (2005) Transcription switches for protoxylem and metaxylem vessel formation. Genes Dev. 19, 1855-1860. (Pubitemid 41186986)
32. Lalonde, S., Tegeder, M., Throne-Holst, M., Frommer, W.B., and, Patrick, J.W., (2003) Phloem loading and unloading of sugars and amino acids. Plant, Cell Environ. 26, 37-56. (Pubitemid 36117279)
33. Ludwig-Müller, J., Prinsen, E., Rolfe, S., and, Scholes, J., (2009) Metabolism and plant hormone action during clubroot disease. J. Plant Growth Regul. 28, 229-244.
34. Mähönen, A.P., Bishopp, A., Higuchi, M., Nieminen, K.M., Kinoshita, K., Törmäkangas, K., Ikeda, Y., Oka, A., Kakimoto, T., and, Helariutta, Y., (2006) Cytokinin signaling and its Inhibitor AHP6 regulate cell fate during vascular development. Science, 311, 94-98. (Pubitemid 43063066)
35. Malinowski, R., Kasprzewska, A., and, Fleming, A.J., (2011) Targeted manipulation of leaf form via local growth repression. Plant J. 66, 941-952.
36. Mitchell, D.T., and, Rice, K.A., (1979) Translocation of 14C-labelled assimilates in cabbage during club root development. Ann. Appl. Biol. 92, 143-152.
37. Mithen, R., and, Magrath, R., (1992) A contribution to the life history of Plasmodiophora brassicae: secondary plasmodia development in root galls of Arabidopsis thaliana. Mycol. Res. 96, 877-885.
38. Mizukami, Y., and, Fischer, R.L., (2000) Plant organ size control: AINTEGUMENTA regulates growth and cell numbers during organogenesis. Proc. Natl Acad. Sci. USA, 97, 942-947. (Pubitemid 30070414)
39. Müller, P., and, Hilgenberg, W., (1986) Isomers of zeatin and zeatin riboside in clubroot tissue: evidence for trans-zeatin biosynthesis by Plasmodiophora brassicae. Physiol. Plant. 66, 245-250.
40. Murashige, T., and, Skoog, F., (1962) A revised medium for rapid growth and bio-assays with tobacco tissue cultures. Physiol. Plant. 15, 473-497.
41. 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.
42. Samalova, M., Brzobohaty, B., and, Moore, I., (2005) pOp6/LhGR: a stringently regulated and highly responsive dexamethasone-inducible gene expression system for tobacco. Plant J. 41, 919-935. (Pubitemid 40398719)
43. Siemens, J., Nagel, M., Ludwig-Müller, J., and, Sacristán, M.D., (2002) The interaction of Plasmodiophora brassicae and Arabidopsis thaliana: parameters for disease quantification and screening of mutant lines. J. Phytopathol. 150, 592-605. (Pubitemid 36108329)
44. Siemens, J., Keller, I., Sarx, J., Kunz, S., Schuller, A., Nagel, W., Schmülling, T., Parniske, M., and, Ludwig-Müller, J., (2006) Transcriptome analysis of Arabidopsis clubroots and disease resistance of cytokinin oxidase/dehydrogenase gene overexpressing plants indicate a key role for cytokinin in disease development. Mol. Plant-Microbe Interact. 19, 480-494. (Pubitemid 43668272)
45. Siemens, J., Graf, H., Bulman, S., In, O., and, Ludwig-Müller, J., (2009) Monitoring expression of selected Plasmodiophora brassicae genes during clubroot development in Arabidopsis thaliana. Plant. Pathol. 58, 130-136.
46. Siemens, J., González, M.-C., Wolf, S., Hofmann, C., Greiner, S., Du, Y., Rausch, T., Roitsch, T., and, Ludwig-Müller, J., (2011) Extracellular invertase is involved in the regulation of clubroot disease in Arabidopsis thaliana. Mol. Plant Pathol. 12, 247-262.
47. Suer, S., Agusti, J., Sanchez, P., Schwarz, M., and, Greb, T., (2011) WOX4 imparts auxin responsiveness to cambium cells in Arabidopsis. Plant Cell 23, 3247-3259.
48. Truernit, E., and, Sauer, N., (1995) The promoter of the Arabidopsis thaliana SUC2 sucrose-H+ symporter gene directs expression of β-glucuronidase to the phloem: evidence for phloem loading and unloading by SUC2. Planta, 196, 564-570.
49. Voorrips, R.E., (1995) Plasmodiophora brassicae- aspects of pathogenesis and resistance in Brassica oleracea. Euphytica, 83, 139-146.
50. Wang, H., Qi, Q., Schorr, P., Cutler, A.J., Crosby, W.L., and, Fowke, L.C., (1998) ICK1, a cyclin-dependent protein kinase inhibitor from Arabidopsis thaliana interacts with both Cdc2a and CycD3, and its expression is induced by abscisic acid. Plant J. 15, 501-510.
51. Wang, H., Zhou, Y., Gilmer, S., Cleary, A., John, P., Whitwill, S., and, Fowke, L., (2003) Modifying plant growth and development using the CDK inhibitor ICK1. Cell Biol. Int. 27, 297-299. (Pubitemid 36398150)
52. Wang, X.H., Mitchum, M.G., Gao, B.L., Li, C.Y., 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. (Pubitemid 40554784)
53. Warton, K., Foster, N.C., Gold, W.A., and, Stanley, K.K., (2004) A novel gene family induced by acute inflammation in endothelial cells. Gene, 342, 85-95. (Pubitemid 39457181)
54. Yamaguchi, M., Kubo, M., Fukuda, H., and, Demura, T., (2008) VASCULAR-RELATED NAC-DOMAIN7 is involved in the differentiation of all types of xylem vessels in Arabidopsis roots and shoots. Plant J. 55, 652-664.
55. Yamaguchi, M., Ohtani, M., Mitsuda, N., Kubo, M., Ohme-Takagi, M., Fukuda, H., and, Demura, T., (2010) VND-INTERACTING2, a NAC domain transcription factor, negatively regulates xylem vessel formation in Arabidopsis. Plant Cell, 22, 1249-1263.
56. Yamaguchi, M., Mitsuda, N., Ohtani, M., Ohme-Takagi, M., Kato, K., and, Demura, T., (2011) VASCULAR-RELATED NAC-DOMAIN 7 directly regulates the expression of a broad range of genes for xylem vessel formation. Plant J. 66, 579-590.
57. Zhao, C., Avci, U., Grant, E.H., Haigler, C.H., and, Beers, E.P., (2008) XND1, a member of the NAC domain family in Arabidopsis thaliana, negatively regulates lignocellulose synthesis and programmed cell death in xylem. Plant J. 53, 425-436. (Pubitemid 351172015)