Silencing of the Rac1 GTPase MtRoP9 in medicago truncatula stimulates early mycorrhizal and oomycete root colonizations but negatively affects rhizobial infection

Plant Physiology

Volumn 159, Issue 1, 2012, Pages 501-516

  Kiirika, Leonard Muriithi ^a   Bergmann, Hannah Friederike ^b   Schikowsky, Christine ^a   Wimmer, Diana ^a   Korte, Joschka ^a   Schmitz, Udo ^a   Niehaus, Karsten ^b   Colditz, Frank ^a  

^a LEIBNIZ UNIVERSITY HANNOVER   (Germany)

^b BIELEFELD UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AGROBACTERIUM RHIZOGENES; APHANOMYCES EUTEICHES; ARBUSCULAR; BACTERIA (MICROORGANISMS); FUNGI; GLOMUS INTRARADICES; MEDICAGO SATIVA; MEDICAGO TRUNCATULA; SINORHIZOBIUM MELILOTI;

EID: 84860549704     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.112.193706     Document Type: Article

References (47)

1. Agrawal GK, Iwahashi H, Rakwal R (2003) Small GTPase 'Rop': molecular switch for plant defense responses. FEBS Lett 546: 173-180
2. Baier R, Schiene K, Kohring B, Flaschel E, Niehaus K (1999) Alfalfa and tobacco cells react differently to chitin oligosaccharides and Sinorhizobium meliloti nodulation factors. Planta 210: 157-164
3. Bates D, Maechler M, Bolker B (2011) lme4: linear mixed-effects models using S4 classes. R package version 0.999375-42. http://CRAN.R-project.org/package=lme4 (December 5, 2011)
4. Bécard G, Fortin JA (1988) Early events of vesicular-arbuscular mycorrhiza formation on Ri T-DNA transformed roots. New Phytol 108: 211-218
5. Boisson-Dernier A, Chabaud M, Rosenberg C, Barker D (2001) Agrobacterium rhizogenes-transformed roots of Medicago truncatula for the study of nitrogen-fixing and endomycorrhizal symbiotic associations. Mol Plant Microbe Interact 14: 695-700
6. Bourne HR, Sanders DA, McCormick F (1990) The GTPase superfamily: a conserved switch for diverse cell functions. Nature 348: 125-132
7. Bourne HR, Sanders DA, McCormick F (1991) The GTPase superfamily: conserved structure and molecular mechanism. Nature 349: 117-127
8. Brecht M, Sewald K, Schiene K, Keen G, Fricke M, Sauer M, Niehaus K (2004) The use of surface plasmon resonance (SPR) and fluorescence resonance energy transfer (FRET) to monitor the interaction of the plant G-proteins Ms-Rac1 and Ms-Rac4 with GTP. J Biotechnol 112: 151-164
9. Carol RJ, Takeda S, Linstead P, Durrant MC, Kakesova H, Derbyshire P, Drea S, Zarsky V, Dolan L (2005) A RhoGDP dissociation inhibitor spatially regulates growth in root hair cells. Nature 438: 1013-1016
10. Chen L, Shiotani K, Togashi T, Miki D, Aoyama M, Wong HL, Kawasaki T, Shimamoto K (2010) Analysis of the Rac/Rop small GTPase family in rice: expression, subcellular localization and role in disease resistance. Plant Cell Physiol 51: 585-595
11. Colditz F, Braun H-P (2010) Medicago truncatula proteomics. J Proteomics 73: 1974-1985
12. Colditz F, Braun H-P, Jacquet C, Niehaus K, Krajinski F (2005) Proteomic profiling unravels insights into the molecular background underlying increased Aphanomyces euteiches-tolerance of Medicago truncatula. Plant Mol Biol 59: 387-406
13. Colditz F, Niehaus K, Krajinski F (2007) Silencing of PR-10-like proteins in Medicago truncatula results in an antagonistic induction of other PR proteins and in an increased tolerance upon infection with the oomycete Aphanomyces euteiches. Planta 226: 57-71
14. Colditz F, Nyamsuren O, Niehaus K, Eubel H, Braun H-P, Krajinski F (2004) Proteomic approach: identification of Medicago truncatula proteins induced in roots after infection with the pathogenic oomycete Aphanomyces euteiches. Plant Mol Biol 55: 109-120
15. Cole RA, Synek L, Zarsky V, Fowler JE (2005) SEC8, a subunit of the putative Arabidopsis exocyst complex, facilitates pollen germination and competitive pollen tube growth. Plant Physiol 138: 2005-2018
16. Djébali N, Mhadhbi H, Lafitte C, Dumas B, Esquerré-Tugayé MT, Aouani ME, Jacquet C (2011) Hydrogen peroxide scavenging mechanisms are components of Medicago truncatula partial resistance to Aphanomyces euteiches. Eur J Plant Pathol 131: 559-571
17. Esseling JJ, Lhuissier FG, Emons AMC (2003) Nod factor-induced root hair curling: continuous polar growth towards the point of nod factor application. Plant Physiol 132: 1982-1988
18. Harrison MJ (1999) Molecular and cellular aspects of the arbuscular mycorrhizal symbiosis. Annu Rev Plant Physiol Plant Mol Biol 50: 361-389
19. Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50: 346-363
20. Kawasaki T, Henmi K, Ono E, Hatakeyama S, Iwano M, Satoh H, Shimamoto K (1999) The small GTP-binding protein rac is a regulator of cell death in plants. Proc Natl Acad Sci USA 96: 10922-10926
21. Kawasaki T, Koita H, Nakatsubo T, Hasegawa K, Wakabayashi K, Takahashi H, Umemura K, Umezawa T, Shimamoto K (2006) Cinnamoyl-CoA reductase, a key enzyme in lignin biosynthesis, is an effector of small GTPase Rac in defense signaling in rice. Proc Natl Acad Sci USA 103: 230-235
22. Lamb C, Dixon RA (1997) The oxidative burst in plant disease resistance. Annu Rev Plant Physiol Plant Mol Biol 48: 251-275
23. Lauter J, Glimm E, Kropf S (1996) New multivariate tests for data with an inherent structure. Biom J 38: 5-23
24. Leigh JA, Signer ER, Walker GC (1985) Exopolysaccharide-deficient mutants of Rhizobium meliloti that form ineffective nodules. Proc Natl Acad Sci USA 82: 6231-6235
25. Limpens E, Mirabella R, Fedorova E, Franken C, Franssen H, Bisseling T, Geurts R (2005) Formation of organelle-like N2-fixing symbiosomes in legume root nodules is controlled by DMI2. Proc Natl Acad Sci USA 102: 10375-10380
26. Limpens E, Ramos J, Franken C, Raz V, Compaan B, Franssen H, Bisseling T, Geurts R (2004) RNA interference in Agrobacterium rhizogenes-transformed roots of Arabidopsis and Medicago truncatula. J Exp Bot 55: 983-992
27. Liu JY, Blaylock LA, Endre G, Cho J, Town CD, VandenBosch KA, Harrison MJ (2003) Transcript profiling coupled with spatial expression analyses reveals genes involved in distinct developmental stages of an arbuscular mycorrhizal symbiosis. Plant Cell 15: 2106-2123
28. Liu P, Li RL, Zhang L, Wang QL, Niehaus K, Baluska F, Samaj J, Lin JX (2009) Lipid microdomain polarization is required for NADPH oxidasedependent ROS signaling in Picea meyeri pollen tube tip growth. Plant J 60: 303-313
29. Liu W, Chen A-M, Luo L, Sun J, Cao L-P, Yu G-Q, Zhu J-B, Wang Y-Z (2010) Characterization and expression analysis of Medicago truncatula ROP GTPase family during the early stage of symbiosis. J Integr Plant Biol 52: 639-652
30. Lohar DP, Haridas S, Gantt JS, VandenBosch KA (2007) A transient decrease in reactive oxygen species in roots leads to root hair deformation in the legume-rhizobia symbiosis. New Phytol 173: 39-49
31. Markmann K, Parniske M (2009) Evolution of root endosymbiosis with bacteria: how novel are nodules? Trends Plant Sci 14: 77-86
32. Moeder W, Yoshioka K, Klessig DF (2005) Involvement of the small GTPase Rac in the defense responses of tobacco to pathogens. Mol Plant Microbe Interact 18: 116-124
33. Nakashima A, Chen L, Thao NP, Fujiwara M, Wong HL, Kuwano M, Umemura K, Shirasu K, Kawasaki T, Shimamoto K (2008) RACK1 functions in rice innate immunity by interacting with the Rac1 immune complex. Plant Cell 20: 2265-2279
34. Nibau C, Wu HM, Cheung AY (2006) RAC/ROP GTPases: 'hubs' for signal integration and diversification in plants. Trends Plant Sci 11: 309-315
35. Niehaus K, Kapp D, Puhler A (1993) Plant defence and delayed infection of alfalfa pseudonodules induced by an exopolysaccharide (EPS I)deficient Rhizobium meliloti mutant. Planta 190: 415-425
36. Park J, Gu Y, Lee Y, Yang Z, Lee Y (2004) Phosphatidic acid induces leaf cell death in Arabidopsis by activating the Rho-related small G protein GTPase-mediated pathway of reactive oxygen species generation. Plant Physiol 134: 129-136
37. Peng M, Kuc J (1992) Peroxidase-generated hydrogen peroxide as a source of antifungal activity in vitro and on tobacco leaf disks. Phytopathology 82: 696-699
38. Quackenbush J, Cho J, Lee D, Liang F, Holt I, Karamycheva S, Parvizi B, Pertea G, Sultana R, White J (2001) The TIGR Gene Indices: analysis of gene transcript sequences in highly sampled eukaryotic species. Nucleic Acids Res 29: 159-164
39. Quandt HJ, Puhler A, Broer I (1993) Transgenic root nodules of Vicia hirsutea: a fast and efficient system for the study of gene expression in indeterminate-type nodules. Mol Plant Microbe Interact 6: 699-706
40. Ralph J, Lundquist K, Brunow G, Lu F, Kim H, Schatz PF, Marita JM, Hatfield RD, Ralph SA, Christensen JH, et al (2004) Lignins: natural polymers from oxidative coupling of 4-hydroxyphenylpropanoids. Phytochem Rev 3: 29-60
41. Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132: 365-386
42. Schenkluhn L, Hohnjec N, Niehaus K, Schmitz U, Colditz F (2010) Differential gel electrophoresis (DIGE) to quantitatively monitor early symbiosisand pathogenesis-induced changes of the Medicago truncatula root proteome. J Proteomics 73: 753-768
43. Schiene K, Puhler A, Niehaus K (2000) Transgenic tobacco plants that express an antisense construct derived from a Medicago sativa cDNA encoding a Rac-related small GTP-binding protein fail to develop necrotic lesions upon elicitor infiltration. Mol Gen Genet 263: 761-770
44. Trapphoff T, Beutner C, Niehaus K, Colditz F (2009) Induction of distinct defense-associated protein patterns in Aphanomyces euteiches (Oomycota)elicited and -inoculated Medicago truncatula cell-suspension cultures: a proteome and phosphoproteome approach. Mol Plant Microbe Interact 22: 421-436
45. Trouvelot A, Kough JL, Gianinazzi-Pearson V (1986) Mesure du taux de mycorhization VA d'un système radiculaire: recherche de signall d'estimation ayant une signification fonctionnelle. In V Gianinazzi-Pearson, S Gianinazzi, eds, Physiological and Genetical Aspects of Mycorrhizae. INRA Press, Paris, pp 217-221
46. Wong HL, Pinontoan R, Hayashi K, Tabata R, Yaeno T, Hasegawa K, Kojima C, Yoshioka H, Iba K, Kawasaki T, et al (2007) Regulation of rice NADPH oxidase by binding of Rac GTPase to its N-terminal extension. Plant Cell 19: 4022-4034
47. Yang Z, Fu Y (2007) ROP/RAC GTPase signaling. Curr Opin Plant Biol 10: 490-494