RbohB, a Phaseolus vulgaris NADPH oxidase gene, enhances symbiosome number, bacteroid size, and nitrogen fixation in nodules and impairs mycorrhizal colonization

New Phytologist

Volumn 202, Issue 3, 2014, Pages 886-900

  Arthikala, Manoj Kumar ^a   Sánchez López, Rosana ^a   Nava, Noreide ^a   Santana, Olivia ^a   Cárdenas, Luis ^a   Quinto, Carmen ^a  

^a INSTITUTO DE BIOTECNOLOGÍA   (Mexico)

Author keywords

Arbuscular mycorrhizal fungi (AMF); Bacteroids; Infection threads; NADPH oxidase homologs; Nodule senescence; Phaseolus vulgaris symbiosis; Reactive oxygen species (ROS); Symbiosomes

Indexed keywords

COLONIZATION; CONCENTRATION (COMPOSITION); GENE EXPRESSION; HOMOLOGY; LEGUME; MYCORRHIZA; NITROGEN FIXATION; OXIDE; RHIZOBACTERIUM; SENESCENCE; SYMBIOSIS; TRANSGENIC PLANT; ULTRASTRUCTURE;

ARBUSCULAR; BACTERIA (MICROORGANISMS); BACTEROIDES; BACTEROIDES (CLASS); FUNGI; PHASEOLUS VULGARIS; RHIZOBIACEAE; RHIZOBIUM;

MESSENGER RNA; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; VEGETABLE PROTEIN;

BACTERIAL COUNT; BIOLOGICAL MODEL; BIOMASS; DOWN REGULATION; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; MOLECULAR CLONING; MYCORRHIZA; NITROGEN FIXATION; NODULATION; PHASEOLUS; PHYSIOLOGY; PLANT GENE; RHIZOBIUM; SYMBIOSIS; TRANSGENIC PLANT; ULTRASTRUCTURE;

BIOMASS; CLONING, MOLECULAR; COLONY COUNT, MICROBIAL; DOWN-REGULATION; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; MODELS, BIOLOGICAL; MYCORRHIZAE; NADPH OXIDASE; NITROGEN FIXATION; PHASEOLUS; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; REACTIVE OXYGEN SPECIES; RHIZOBIUM; RNA, MESSENGER; ROOT NODULES, PLANT; SYMBIOSIS;

EID: 84898023259     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12714     Document Type: Article

References (69)

1. Alesandrini F, Mathis R, Van de Sype G, Hérouart D, Puppo A. 2003. Possible roles of a cysteine protease and hydrogen peroxide in soybean nodule development and senescence. New Phytologist 158: 131-138.
2. Apel K, Hirt H. 2004. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology 55: 373-399.
3. Arthikala MK, Montíel J, Nava N, Santana O, Sánchez-López R, Cárdenas L, Quinto C. 2013. PvRbohB negatively regulates Rhizophagus irregularis colonization in Phaseolus vulgaris. Plant & Cell Physiology 54: 1391-1402.
4. Besserer A, Puech-Pagès V, Kiefer P, Gomez-Roldan V, Jauneau A, Roy S, Portais JC, Roux C, Bécard G, Séjalon-Delmas N. 2006. Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLoS Biology 4: e226.
5. Blanco L, Reddy PM, Silvente S, Bucciarelli B, Khandual S, Alvarado-Affantranger X, Sánchez F, Miller S, Vance C, Lara-Flores M. 2008. Molecular cloning, characterization and regulation of two different NADHglutamate synthase cDNAs in bean nodules. Plant, Cell & Environment 31: 454-472.
6. Borges A, Tsai SM, Caldas DG. 2012. Validation of reference genes for RT-qPCR normalization in common bean during biotic and abiotic stresses. Plant Cell Reports 31: 827-838.
7. Broughton WJ, Dilworth MJ. 1971. Control of leghemoglobin synthesis in snake beans. Biochemical Journal 125: 1075-1080.
8. Cárdenas L, Martínez A, Sánchez F, Quinto C. 2008. Fast, transient and specific intracellular ROS changes in living root hair cells responding to Nod factors (NFs). Plant Journal 56: 802-813.
9. Cermola M, Fedorova E, Taté R, Riccio A, Favre R, Patriarca EJ. 2000. Nodule invasion and symbiosome differentiation during Rhizobium etli-Phaseolus vulgaris symbiosis. Molecular Plant-Microbe Interactions 13: 733-741.
10. Christensen TM, Jochimsen BU. 1983. Enzymes of ureide synthesis in pea and soybean. Plant Physiology 72: 56-59.
11. De Smet I. 2012. Lateral root initiation: one step at a time. New Phytologist 193: 867-873.
12. Delaux PM, Bécard G, Combier JP. 2013. NSP1 is a component of the Myc signaling pathway. New Phytologist 199: 59-65.
13. Estrada-Navarrete G, Alvarado-Affantranger X, Olivares JE, Guillén G, Díaz-Camino C, Campos F, Quinto C, Gresshoff PM, Sánchez F. 2007. Fast, efficient and reproducible genetic transformation of Phaseolus spp. by Agrobacterium rhizogenes. Nature Protocol 2: 1819-1824.
14. Foreman J, Demidchik V, Bothwell JH, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JD et al. 2003. Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422: 442-446.
15. Fridovich I. 1998. The trail to superoxide dismutase. Protein Science 7: 2688-2690.
16. Gage DJ. 2002. Analysis of infection thread development using Gfp- and DsRed-expressing Sinorhizobium meliloti. Journal of Bacteriology 184: 7042-7046.
17. Gage DJ. 2004. Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes. Microbiology and Molecular Biology Reviews 68: 280-300.
18. 2+ spiking in Medicago truncatula roots and their production is enhanced by strigolactone. New Phytologist 198: 190-202.
19. Gobbato E, Marsh JF, Vernié T, Wang E, Maillet F, Kim J, Miller JB, Sun J, Bano SA, Ratet P et al. 2012. A GRAS-type transcription factor with a specific function in mycorrhizal signaling. Current Biology 22: 2236-2241.
20. Herder GD, Parniske M. 2009. The unbearable naivety of legumes in symbiosis. Current Opinion in Plant Biology 12: 491-499.
21. Hirsch S, Kim J, Muñoz A, Heckmann AB, Downie JA, Oldroyd GE. 2009. GRAS proteins form a DNA binding complex to induce gene expression during nodulation signaling in Medicago truncatula. Plant Cell 21: 545-557.
22. Islas-Flores T, Guillén G, Alvarado-Affantranger X, Lara-Flores M, Sánchez F, Villanueva MA. 2011. PvRACK1 loss-of-function impairs cell expansion and morphogenesis in Phaseolus vulgaris L. root nodules. Molecular Plant-Microbe Interactions 24: 819-826.
23. 2 is required for optimal establishment of the Medicago sativa/Sinorhizobium meliloti symbiosis. Journal of Bacteriology 189: 8741-8874.
24. Jefferson RA. 1987. Assaying chimeric genes in plants, the GUS gene fusion system. Plant Molecular Biology Reporter 5: 387-405.
25. Karimi M, Inzé D, Depicker A. 2002. Gateway vectors for Agrobacterium-mediated plant transformation. Trends in Plant Science 7: 193-195.
26. Kiirika LM, Bergmann HF, Schikowsky C, Wimmer D, Korte J, Schmitz U, Niehaus K, Colditz F. 2012. Silencing of the Rac1 GTPase MtROP9 in Medicago truncatula stimulates early mycorrhizal and oomycete root colonizations but negatively affects rhizobial infection. Plant Physiology 159: 501-516.
27. Larkan NJ, Ruzicka DR, Edmonds-Tibbett T, Durkin JM, Jackson LE, Smith FA, Schachtman DP, Smith SE, Barker SJ. 2013. The reduced mycorrhizal colonisation (rmc) mutation of tomato disrupts five gene sequences including the CYCLOPS/IPD3 homologue. Mycorrhiza 23: 573-584.
28. Lauressergues D, Delaux PM, Formey D, Lelandais-Brière C, Fort S, Cottaz S, Bécard G, Niebel A, Roux C, Combier JP. 2012. The microRNA miR171 h modulates arbuscular mycorrhizal colonization of Medicago truncatula by targeting NSP2. Plant Journal 72: 512-522.
29. Lee Y, Rubio MC, Alassimone J, Geldner N. 2013. A mechanism for localized lignin deposition in the endodermis. Cell 153: 402-412.
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 Phytologist 173: 39-49.
31. Madsen LH, Tirichine L, Jurkiewicz A, Sullivan JT, Heckmann AB, Bek AS, Ronson CW, James EK, Stougaard J. 2010. The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus. Nature Communication 1: 1-12.
32. Maeda D, Ashida K, Iguchi K, Chechetka SA, Hijikata A, Okusako Y, Deguchi Y, Izui K, Hata S. 2006. Knockdown of an arbuscular mycorrhiza-inducible phosphate transporter gene of Lotus japonicus suppresses mutualistic symbiosis. Plant & Cell Physiology 47: 807-817.
33. Maillet F, Poinsot V, André O, Puech-Pagès V, Haouy A, Gueunier M, Cromer L, Giraudet D, Formey D, Niebel A et al. 2011. Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469: 58-63.
34. Marino D, Andrio E, Danchin EG, Oger E, Gucciardo S, Lambert A, Puppo A, Pauly N. 2011. A Medicago truncatula NADPH oxidase is involved in symbiotic nodule functioning. New Phytologist 189: 580-592.
35. Marino D, Dunand C, Puppo A, Pauly N. 2012. A burst of plant NADPH oxidases. Trends in Plant Science 17: 9-15.
36. McGonigle TP, Millers MH, Evans DG, Fairchild GL, Swan JA. 1990. A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytologist 115: 495-501.
37. Middleton PH, Jakab J, Penmetsa RV, Starker CG, Doll J, Kaló P, Prabhu R, Marsh JF, Mitra RM, Kereszt A et al. 2007. An ERF transcription factor in Medicago truncatula that is essential for Nod factor signal transduction. Plant Cell 19: 1221-1234.
38. Montiel J, Arthikala MK, Quinto C. 2013. Phaseolus vulgaris RbohB functions in lateral root development. Plant Signaling & Behavior 8: e22694.
39. Montiel J, Nava N, Cárdenas L, Sánchez-López R, Arthikala MK, Santana O, Sánchez F, Quinto C. 2012. A Phaseolus vulgaris NADPH oxidase gene is required for root infection by Rhizobia. Plant & Cell Physiology 53: 1751-1767.
40. Mortier V, Holsters M, Goormachtig S. 2012. Never too many? How legumes control nodule numbers. Plant, Cell & Environment 35: 245-258.
41. Murphy J, Riley J. 1962. A modified single solution method for the determination of phosphate in natural waters. Analytica Chimica Acta 27: 31-36.
42. Murray JD, Cousins DR, Jackson KJ, Liu C. 2013. Signaling at the root surface: the role of cutin monomers in mycorrhization. Molecular Plant 6: 1381-1383.
43. Myouga F, Hosoda C, Umezawa T, Iizumi H, Kuromori T, Motohashi R, Shono Y, Nagata N, Ikeuchi M, Shinozaki K. 2008. A heterocomplex of iron superoxide dismutases defends chloroplast nucleoids against oxidative stress and is essential for chloroplast development in Arabidopsis. Plant Cell 20: 3148-3162.
44. Oldroyd GED, Downie JA. 2008. Coordinating nodule morphogenesis with rhizobial infection in legumes. Annual Review of Plant Biology 59: 519-546.
45. Peleg-Grossman S, Volpin H, Levine A. 2007. Root hair curling and Rhizobium infection in Medicago truncatula are mediated by phosphatidylinositide-regulated endocytosis and reactive oxygen species. Journal of Experimental Botany 58: 1637-1649.
46. Prell J, Poole P. 2006. Metabolic changes of rhizobia in legume nodules. Trends in Microbiology 14: 161-168.
47. Puppo A, Groten K, Bastian F, Carzaniga R, Soussi M, Lucas MM, de Felipe MR, Harrison J, Vanacker H, Foyer CH. 2005. Legume nodule senescence: roles for redox and hormone signalling in the orchestration of the natural aging process. New Phytologist 165: 683-701.
48. Puppo A, Pauly N, Boscari A, Mandon K, Brouquisse R. 2013. Hydrogen peroxide and nitric oxide: key regulators of the legume-Rhizobium and mycorrhizal symbioses. Antioxidants & Redox Signaling 18: 2202-2219.
49. Ramel F, Sulmon C, Bogard M, Couée I, Gouesbet G. 2009. Differential patterns of reactive oxygen species and antioxidative mechanisms during atrazine injury and sucrose-induced tolerance in Arabidopsis thaliana plantlets. BMC Plant Biology 9: 28.
50. Ramírez M, Valderrama B, Arredondo-Peter R, Soberón M, Mora J, Hernández G. 1999. Rhizobium etli genetically engineered for the heterologous expression of Vitreoscilla sp. hemoglobin: effects on free-living and symbiosis. Molecular Plant-Microbe Interactions 12: 1008-1015.
51. Ramu SK, Peng HM, Cook DR. 2002. Nod factor induction of reactive oxygen species production is correlated with expression of the early nodulin gene rip1 in Medicago truncatula. Molecular Plant-Microbe Interactions 15: 522-528.
52. Redondo FJ, de la Peña TC, Morcillo CN, Lucas MM, Pueyo JJ. 2009. Overexpression of flavodoxin in bacteroids induces changes in antioxidant metabolism leading to delayed senescence and starch accumulation in alfalfa root nodules. Plant Physiology 149: 1166-1178.
53. Richardson AD, Duigan SP, Berlyn GP. 2002. An evaluation of noninvasive methods to estimate foliar chlorophyll content. New Phytologist 153: 185-194.
54. Robaglia C, Thomas M, Meyer C. 2012. Sensing nutrient and energy status by SnRK1 and TOR kinases. Current Opinion in Plant Biology 15: 301-307.
55. Rubio MC, Becana M, Sato S, James EK, Tabata S, Spaink HP. 2007. Characterization of genomic clones and expression analysis of the three types of superoxide dismutases during nodule development in Lotus japonicus. Molecular Plant-Microbe Interactions 20: 262-275.
56. Rubio MC, James EK, Clemente MR, Bucciarelli B, Fedorova M, Vance CP, Becana M. 2004. Localization of superoxide dismutases and hydrogen peroxide in legume root nodules. Molecular Plant-Microbe Interactions 17: 1294-1305.
57. Salzer P, Corbiere H, Boller T. 1999. Hydrogen peroxide accumulation in Medicago truncatula roots colonized by the arbuscular mycorrhiza-forming fungus Glomus intraradicies. Planta 208: 319-325.
58. Sánchez-López R, Jáuregui D, Nava N, Alvarado-Affantranger X, Montiel J, Santana O, Sánchez F, Quinto C. 2011. Down-regulation of SymRK correlates with a deficiency in vascular bundle development in Phaseolus vulgaris nodules. Plant, Cell & Environment 34: 2109-2121.
59. Silvente S, Camas A, Lara M. 2003. Heterogeneity of sucrose synthase genes in bean (Phaseolus vulgaris L.): evidence for a nodule-enhanced sucrose synthase gene. Journal of Experimental Botany 54: 749-755.
60. Smit P, Raedts J, Portyanko V, Debelle F, Gough C, Bisseling T, Geurts R. 2005. NSP1 of the GRAS protein family is essential for rhizobial Nod factor-induced transcription. Science 308: 1789-1791.
61. Smith SE, Smith FA, Jakobsen I. 2003. Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiology 133: 16-20.
62. Stougaard J. 2000. Regulators and regulation of legume root nodule development. Plant Physiology 124: 531-540.
63. Torres MA, Dangl JL, Jones JD. 2002. Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proceedings of National Academy of Sciences, USA 99: 517-522.
64. Tsukagoshi H, Busch W, Benfey PN. 2010. Transcriptional regulation of ROS controls transition from proliferation to differentiation in the root. Cell 143: 606-616.
65. Udvardi MK, Day DA. 1997. Metabolite transport across symbiotic membranes of legume nodules. Annual Review of Plant Physiology and Plant Molecular Biology 48: 493-523.
66. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F. 2002. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal reference genes. Genome Biology 3: research0034.1-0034.11.
67. Vinuesa P, Neumann-Silkow F, Pacios-Bras C, Spaink HP, Martínez-Romero E, Werner D. 2003. Genetic analysis of a pH-regulated operon from Rhizobium tropici CIAT899 involved in acid tolerance and nodulation competitiveness. Molecular Plant-Microbe Interactions 16: 159-168.
68. Wisniewski JP, Rathbun EA, Knox JP, Brewin NJ. 2000. Involvement of diamine oxidase and peroxidase in insolubilization of the extracellular matrix: implications for pea nodule initiation by Rhizobium leguminosarum. Molecular Plant-Microbe Interactions 13: 413-420.
69. York GM, Lupberger J, Tian J, Lawrence AG, Stubbe J, Sinskey AJ. 2003. Ralstonia eutropha H16 encodes two and possibly three intracellular poly[D-(-)-3-hydroxybutyrate] depolymerase genes. Journal of Bacteriology 185: 3788-3794.