Ectopic expression of Kip-related proteins restrains root-knot nematode-feeding site expansion

New Phytologist

Volumn 199, Issue 2, 2013, Pages 505-519

  Vieira, Paulo ^a,e   Escudero, Carmen ^a   Rodiuc, Natalia ^a   Boruc, Joanna ^b,c,f   Russinova, Eugenia ^b,c   Glab, Nathalie ^d   Mota, Manuel ^e   De Veylder, Lieven ^b,c   Abad, Pierre ^a   Engler, Gilbert ^a   De Almeida Engler, Janice ^a  

^a CNRS   (France)

^b DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^c GHENT UNIVERSITY   (Belgium)

^d UNIVERSITÉ PARIS SACLAY   (France)

^e UNIVERSITY OF ÉVORA   (Portugal)

^f OHIO STATE UNIVERSITY   (United States)

Author keywords

Arabidopsis roots; Cell cycle; Giant cells; Meloidogyne; Nuclei

Indexed keywords

ARABIDOPSIS PROTEIN; CELL CYCLE PROTEIN; CYCLIN DEPENDENT KINASE INHIBITOR; ICK1 PROTEIN, ARABIDOPSIS; ICK2 PROTEIN, ARABIDOPSIS;

CELL ORGANELLE; DICOTYLEDON; ENZYME ACTIVITY; GALL; INHIBITOR; NEMATODE; PROTEIN; ROOT;

ANIMAL; ARABIDOPSIS; ARTICLE; CELL NUCLEUS; CYTOLOGY; FEEDING BEHAVIOR; GENE EXPRESSION REGULATION; GENETICS; GIANT CELL; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MITOSIS; ORGANELLE SIZE; PARASITOLOGY; PHYSIOLOGY; PLANT GENE; PLANT ROOT; PLANT TUMOR; PLOIDY; PROTEIN TRANSPORT; TRANSGENIC PLANT; TYLENCHOIDEA;

ANIMALS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL CYCLE PROTEINS; CELL NUCLEUS; CYCLIN-DEPENDENT KINASE INHIBITOR PROTEINS; FEEDING BEHAVIOR; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GIANT CELLS; MITOSIS; ORGANELLE SIZE; PLANT ROOTS; PLANT TUMORS; PLANTS, GENETICALLY MODIFIED; PLOIDIES; PROTEIN TRANSPORT; TYLENCHOIDEA;

ARABIDOPSIS; MELOIDOGYNE; MELOIDOGYNE INCOGNITA; MELOIDOGYNE JAVANICA;

EID: 84879687666     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12255     Document Type: Article

References (61)

1. de Almeida Engler J, De Veylder L, De Groodt R, Rombauts S, Boudolf V, De Meyer B, Hemerly A, Ferreira P, Beeckman T, Karimi M et al. 2009. Molecular markers and cell cycle inhibitors show the importance of cell cycle progression in nematode-induced galls and syncytia. Plant Journal 59: 645-660.
2. de Almeida Engler J, De Vleesschauwer V, Burssens S, Celenza JLJ, Inzé D, Van Montagu M, Engler G, Gheysen G. 1999. Molecular markers and cell cycle inhibitors show the importance of cell cycle progression in nematode-induced galls and syncytia. The Plant Cell 11: 793-808.
3. de Almeida Engler J, Engler G, Gheysen G. 2011. Unravelling the plant cell cycle in nematode induced feeding sites. In: Jones J, Gheysen G, Fenoll C, eds. Genomics and molecular genetics of plant-nematode interactions. Dordrecht, the Netherlands: Springer Science+Business Media, 349-368.
4. de Almeida Engler J, Gheysen G. 2013. Nematode-induced endoreduplication in plant host cells: why and how? Molecular Plant-Microbe Interactions 26: 17-24.
5. de Almeida Engler J, Kyndt T, Vieira P, Van Cappelle E, Bouldolf V, Sanchez V, Escobar C, De Veylder L, Engler G, Abad P et al. 2012. CCS52 and DEL1 genes are key components of the endocycle in nematode induced feeding sites. Plant Journal 72: 185-198.
6. Anzola JM, Sieberer T, Ortbauer M, Butt H, Korbei B, Weinhofer I, Mullner AE, Luschnig C. 2010. Putative Arabidopsis transcriptional adaptor protein (PROPORZ1) is required to modulate histone acetylation in response to auxin. Proceedings of the National Academy of Sciences, USA 107: 10308-10313.
7. Baldacci-Cresp F, Chang C, Maucourt M, Deborde C, Hopkins J, Lecomte P, Bernillon S, Broquisse R, Moing A, Abad P et al. 2012. (Homo)glutathione deficiency impairs root-knot nematode development in Medicago truncatula. Plos Pathogens 8: e1002471.
8. Barrôco RM, Peres A, Droual AM, De Veylder L, Nguyen LSL, De Wolf J, Mironon V, Peerbolte R, Beemster GTS, Inzé D et al. 2006. The cyclin-dependent kinase inhibitor Orysa KRP1 plays an important role in seed development of Oryza sativa. Plant Physiology 142: 1053-1064.
9. Beeckman T, Engler G. 1994. An easy technique for the clearing of histochemically stained plant tissue. Plant Molecular Biology Reporter 12: 37-42.
10. Bemis SM, Torii KU. 2007. Autonomy of cell proliferation and developmental programs during Arabidopsis aboveground organ morphogenesis. Developmental Biology 304: 367-381.
11. Benson A, Dowdy SF, Roberts JM. 2008. CDK inhibitors: cell cycle regulators and beyond. Developmental Cell 14: 159-169.
12. Berr A, Schubert I. 2007. Interphase chromosome arrangement in Arabidopsis thaliana is similar in differentiated and meristematic tissues and shows a transient mirror symmetry after nuclear division. Genetics 176: 853-863.
13. Bird DA, Buruiana MM, Zhou Y, Fowke LC, Wang H. 2007. Arabidopsis cyclin-dependent kinase inhibitors are nuclear-localized and show different localization patterns within the nucleoplasm. Plant Cell Reports 26: 861-872.
14. Bisbis B, Delmas F, Joubes J, Sicard A, Hernould M, Inzé D, Mouras A, Chevalier C. 2006. Cyclin-dependent kinase inhibitors regulate the CDK/cyclin complex activities in endoreduplicating cells of developing tomato fruit. The Journal of Biological Chemistry 281: 7374-7383.
15. Boruc J, Mylle E, Duda M, De Clercq R, Rombauts S, Geelen D, Hilson P, Inzé D, Van Damme D, Russinova E. 2010a. Systematic localization of the Arabidopsis core cell cycle proteins reveals novel cell division complexes. Plant Physiology 152: 553-565.
16. Boruc J, Van den Daele H, Hollunder J, Rombauts S, Mylle E, Hilson P, Inzé D, De Veylder L, Russinova E. 2010b. Functional modules in the Arabidopsis core cell cycle binary protein-protein interaction network. Plant Cell 22: 1264-1280.
17. Caillaud M-C, Dubreuil G, Quentin M, Perfus-Barbeoch L, Lecomte P, de Almeida Engler J, Abad P, Rosso MN, Favery B. 2008. Root-knot nematodes manipulate plant cell functions during a compatible interaction. Journal of Plant Physiology 165: 104-113.
18. Churchman ML, Brown ML, Kato N, Kirik V, Hülskamp M, Inzé D, De Veylder L, Walker JD, Zheng Z, Oppenheimer DG et al. 2006. SIAMESE, a novel plant-specific cell cycle regulator controls endoreplication onset in Arabidopsis thaliana. The Plant Cell 18: 3145-3157.
19. Coelho CM, Dande RA, Sabelli PA, Sun Y, Dilkes BP, Gordon-Kamm WJ, Larkins BA. 2005. Cyclin-dependent kinase inhibitors in maize endosperm and their potential role in endoreduplication. Plant Physiology 138: 2323-2336.
20. Comai L. 2005. The advantages and disavantages of being polyploid. Nature Reviews Genetics 6: 836-846.
21. Damiani I, Baldacci-Cresp F, Hopkins J, Andrio E, Balzergue S, Lecomte P, Puppo A, Abad P, Favery B, Hérouart D. 2012. Plant genes involved in harbouring symbiotic rhizobia or pathogenic nematodes. New Phytologist 194: 511-522.
22. De Veylder L, Beeckman T, Beemster GT, Krois L, Terras F, Landrieu I, Van der Schueren E, Maes S, Naudts M, Inzé D. 2001. Functional analysis of cyclin-dependent kinase inhibitors of Arabidopsis. The Plant Cell 13: 1653-1667.
23. De Veylder L, Larkin JC, Schnittger A. 2011. Molecular control and function of endoreduplication in development and physiology. Trends in Plant Science 16: 1360-1385.
24. Edgar BA, Orr-Weaver TL. 2001. Endoreplication cell cycles: more for less. Cell 105: 297-306.
25. Fransz P, De Jong JH, Lysak M, Ruffini Castiglione M, Schubert I. 2002. Interphase chromosomes in Arabidopsis are organised as well-defined chromocenters from which euchromatin loops emanate. Proceedings of the National Academy of Sciences, USA 99: 14584-14589.
26. Galbraith DW, Harkins KR, Knapp S. 1991. Systemic endopolyploidy in Arabidopsis thaliana. Plant Physiology 96: 985-989.
27. Geelen DNV, Inzé DG. 2001. A bright future for the Bright Yellow-2 cell culture. Plant Physiology 127: 1375-1379.
28. Gheysen G, Fenoll C. 2002. Gene expression in nematode feeding sites. Annual Review of Phytopathology 40: 191-219.
29. Hofman J, Youssef-Banora M, de Almeida Engler J, Grundler FM. 2010. The role of callose deposition along plasmodesmata in nematode feeding sites. Molecular Plant-Microbe Interactions 23: 549-557.
30. Hoth S, Stadler R, Sauer N, Hammes UZ. 2008. Differential vascularization of nematode-induced feeding sites. Proceedings of the National Academy of Sciences, USA 105: 12617-12622.
31. Inzé D, De Veylder L. 2006. Cell cycle regulation in plant development. Annual Review of Genetics 40: 77-105.
32. Jammes F, Lecomte P, de Almeida Engler J, Bitton F, Martin-Magniette ML, Renou JP, Abad P, Favery B. 2005. Genome-wide expression profiling of the host response to root-knot nematode infection in Arabidopsis. Plant Journal 44: 447-458.
33. Jasinski S, Perennes C, Bergounioux C, Glab N. 2002. Comparative molecular and functional analyses of the tobacco cyclin-dependent kinase inhibitor NtKIS1a and its spliced variant NtKIS1b. Plant Physiology 130: 1871-1882.
34. Jones MGK, Northcote DH. 1972. Multinucleate transfer cells induced in coleus roots by the root-knot nematode, Meloidogyne arenaria. Protoplasma 75: 381-395.
35. Joubès J, Chevalier C. 2000. Endoreduplication in higher plants. Plant Molecular Biology 43: 735-745.
36. Kang J, Mizukami Y, Wang H, Fowke L, Dengler NG. 2007. Modification of cell proliferation patterns alters leaf vein architecture in Arabidopsis thaliana. Planta 226: 1207-1218.
37. Karimi M, Inzé D, Depicker A. 2002. GATEWAY™ vectors for Agrobacterium-mediated plant transformation. Trends in Plant Science 7: 193-195.
38. Kato N, Lam EJ. 2003. Chromatin of endoreduplicated pavement cells has greater range of movement than that of diploid guard cells in Arabidopsis thaliana. Journal of Cell Science 116: 2195-2201.
39. Kondorosi E, Kondorosi A. 2004. Endoreduplication and activation of the anaphase-promoting complex during symbiotic cell development. FEBS Letters 567: 152-157.
40. Malumbres M, Pevarello P, Barbacid M, Bischoff JR. 2007. CDK inhibitors in cancer therapy: what is next? Trends in Pharmacological Sciences 29: 16-21.
41. Maluszynska J, Heslop-Harrison JS. 1993. Molecular cytogenetics of the genus Arabidopsis: in situ localization of rDNA sites, chromosome numbers and diversity in centromeric heterochromatin. Annals of Botany 71: 479-484.
42. Niebel A, de Almeida Engler J, Hemerly A, Ferreira P, Van Montagu M, Gheysen G. 1996. Induction of cdc2a and cyc1At expression in Arabidopsis during early phases of nematode-induced feeding cell formation. Plant Journal 10: 1037-1043.
43. Ormenese S, de Almeida Engler J, de Groot R, de Veylder L, Inzé D, Jacqmard A. 2004. Analysis of the spatial expression pattern of seven Kip related proteins (KRPs) in the shoot apex of Arabidopsis thaliana. Annals of Botany 93: 575-580.
44. Peres A, Churchman ML, Hariharan S, Himanen K, Verkest A, Vandepoele K, Magyar Z, Hatzfeld Y, Van Der Schueren E, Beemster GT et al. 2007. Novel plant-specific cyclin-dependent kinase inhibitors induced by biotic and abiotic stresses. The Journal of Biological Chemistry 282: 25588-25596.
45. Pettko-Szandtner A, Meszaros T, Horvath GV, Bakó L, Csordás-Tóth E, Blastyák A, Zhiponova M, Miskotczi P, Dudits P. 2006. Activation of an alfalfa cyclin-dependent kinase inhibitor by calmodulin-like domain protein kinase. Plant Journal 46: 111-123.
46. Roeder AHK, Chickarmane V, Cunha A, Obara B, Manjunath BS, Meyerowitz EM. 2010. Variability in the control of cell division underlies sepal epidermal patterning in Arabidopsis thaliana. PLoS Biology: 8 e1000367.
47. Sanz L, Dewitte W, Forzani C, Patell F, Nieuwland J, Wen B, Quelhas P, De Jager S, Titmus C, Campilho A et al. 2011. The Arabidopsis D-type cyclin CYCD2;1 and the inhibitor ICK2/KRP2 modulate auxin-induced lateral root formation. The Plant Cell 23: 1-20.
48. Schubert V, Klatte M, Pecinka A, Meister A, Jasencakova Z, Schubert I. 2006. Sister chromatids are often incompletely aligned in meristematic and endopolyploid interphase nuclei of Arabidopsis thaliana. Genetics 172: 467-475.
49. Sugimoto-Shirasu K, Roberts K. 2003. "Bit it up": endoreduplication and cell-size control in plants. Current Opinion in Plant Biology 6: 544-553.
50. Van de Capelle E, Plovie E, Kyndt T, Grunewald W, Cannoot B, Gheysen G. 2008. AtCDK;1 silencing in Arabidopsis thaliana reduces reproduction of sedentary plant-parasitic nematodes. Plant Biotechnology Journal 6: 749-757.
51. Van Leene J, Boruc J, De Jaeger G, Russinova E, De Veylder L. 2010b. A Kaleidoscopic view of the Arabidopsis core cell cycle interactome. Trends in Plant Science 16: 141-150.
52. Van Leene J, Hollunder J, Eeckhout D, Persiau G, Van De Slijke E, Stals H, Van Isterdael G, Verkest A, Neirynck S, Buffel Y et al. 2010a. Targeted interactomics reveals a complex core cell cycle machinery in Arabidopsis thaliana. Molecular Systems Biology 6: 397.
53. Verkest A, de O Manes C-L, Vercruysse M, Maes S, Van Der Schueren E, Beeckman T, Genschik P, Kuiper M, Inzé D, De Veylder L. 2005b. The cyclin-dependent kinase inhibitor KRP2 controls the mitosis-to-endocycle transition during Arabidopsis leaf development through a specific inhibition of the mitotic CDKA;1 kinase complexes. The Plant Cell 17: 1723-1736.
54. Verkest A, Weinl C, Inzé D, De Veylder L, Schnittger A. 2005a. Switching the cell cycle. Kip-Related Proteins in plant cell cycle control. Plant Physiology 139: 1099-1106.
55. Vieira P, Engler G, de Almeida Engler J. 2012. Whole-mount confocal imaging of nuclei in giant feeding-cells induced by root-knot nematodes in Arabidopsis. New Phytologist 195: 488-496.
56. Wang H, Fowke LC, Crosby WL. 1997. A plant cyclin-dependent kinase inhibitor gene. Nature 386: 451-452.
57. Wang H, Zhou Y, Bird DA, Fowke LC. 2008. Functions, regulation and cellular localization of plant cyclin-dependent kinase inhibitors. Journal of Microscopy 231: 234-246.
58. Wang H, Zhou Y, Gilmer S, Whitwill S, Fowke LC. 2000. Expression of the plant cyclin-dependent kinase inhibitor ICK1 affects cell division, plant growth and morphology. Plant Journal 24: 613-623.
59. Weinl C, Marquardt S, Kuijt SJ, Nowack MK, Jacoby MJ, Hülskamp M, Schnittger A. 2005. Novel functions of plant cyclin-dependent kinase inhibitors, ICK1/KRP1, can act non-cell-autonomously and inhibit entry into mitosis. The Plant Cell 17: 1704-1722.
60. Wiggers RJ, Starr JL, Price HJ. 1990. DNA content and variation in chromosome number in plant cells affected by Meloidogyne incognita and M. arenaria. Phytopathology 80: 1391-1395.
61. Zhou Y, Fowke LC, Wang H. 2002. Plant CDK inhibitors: studies of interactions with cell cycle regulators in the yeast two-hybrid system and functional comparisons in transgenic Arabidopsis plants. Plant Cell Reports 20: 967-975.