Root transcriptome analysis of Arabidopsis thaliana exposed to beneficial Bacillus subtilis FB17 rhizobacteria revealed genes for bacterial recruitment and plant defense independent of malate efflux

Planta

Volumn 238, Issue 4, 2013, Pages 657-668

  Lakshmanan, Venkatachalam ^a   Castaneda, Rafael ^a   Rudrappa, Thimmaraju ^b   Bais, Harsh P ^a  

^a UNIVERSITY OF DELAWARE   (United States)

^b Sri Biotech Laboratories India Limited   (India)

Author keywords

Bacillus subtilis; Biofilm; Plant growth promoting rhizobacteria (PGPRs); Rhizosphere

Indexed keywords

ARABIDOPSIS THALIANA; BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); LYCOPERSICON ESCULENTUM; PSEUDOMONAS SYRINGAE; PSEUDOMONAS SYRINGAE PV. TOMATO; RHIZOBIALES;

MALIC ACID; MALIC ACID DERIVATIVE; TRANSCRIPTOME;

ARABIDOPSIS; ARTICLE; BACILLUS SUBTILIS; DNA MICROARRAY; GENE EXPRESSION PROFILING; GENETICS; METABOLISM; MICROBIOLOGY; MUTATION; PHYSIOLOGY; PLANT GENE; PLANT ROOT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SYMBIOSIS;

ARABIDOPSIS; BACILLUS SUBTILIS; GENE EXPRESSION PROFILING; GENES, PLANT; MALATES; MUTATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PLANT ROOTS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SYMBIOSIS; TRANSCRIPTOME;

EID: 84884669977     PISSN: 00320935     EISSN: 14322048     Source Type: Journal    
DOI: 10.1007/s00425-013-1920-2     Document Type: Article

References (53)

1. Ahemad M, Khan MS (2011) Functional aspects of plant growth promoting rhizobacteria: recent advancements. Insight Microbiol 1: 39-54.
2. Arkhipova TN, Veselov SU, Melentiev AI, Martynenko EV, Kudoyarova GR (2005) Ability of bacterium Bacillus subtilis to produce cytokinins and to influence the growth and endogenous hormone content of lettuce plants. Plant Soil 272: 201-209.
3. Bais HP, Fall R, Vivanco JM (2004) Biocontrol of Bacillus subtilis against infection of Arabidopsis roots by Pseudomonas syringae is facilitated by biofilm formation and surfactin production. Plant Physiol 134: 307-319.
4. Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Ann Rev Plant Biol 57: 233-266.
5. Bakker P, Ran LX, Pieterse CMJ, van Loon LC (2003) Understanding the involvement of rhizobacteria-mediated induction of systemic resistance in biocontrol of plant diseases. Canad J Plant Pathol 25: 5-9.
6. Beauregard PB, Chai Y, Vlamakis H, Losick R, Kolter R (2013) Bacillussubtilis biofilm induction by plant polysaccharides. Proc Natl Acad Sci USA 110: E1621-E1630.
7. Bhattacharyya PN, Jha DK (2012) Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World J Microbiol Biotechnol 28: 1327-1350.
8. Brader G, Mikkelsen MD, Halkier BA, Palva ET (2006) Altering glucosinolate profiles modulates diseases resistance in plants. Plant J 46: 758-767.
9. Branda SS, Chu F, Kearns DB, Losick R, Kolter R (2006) A major protein component of the Bacillussubtilis biofilm matrix. Mol Microbiol 59: 1229-1238.
10. Brechenmacher L, Kim MY, Benitez M, Li M, Joshi T et al (2008) Transcription profiling of soybean nodulation by Bradyrhizobium japonicum. Mol Plant-Microbe Inter 21: 631-645.
11. Carpita N, McCann M (2000) The cell wall. In: Buchanan BB, Gruissem W, Jones RL (eds) Biochemistry and molecular biology of plants. American Society of Plant Physiologists, Rockville, pp 52-108.
12. Chen S, Glawischnig E, Jorgensen K, Naur P, Jorgensen B et al (2003) CYP79F1 and CYP79F2 have distinct functions in the biosynthesis of aliphatic glucosinolates in Arabidopsis. Plant J 33: 923-937.
13. Chen Y, Cao S, Chai Y, Clardy J, Kolter R et al (2012) A Bacillus subtilis sensor kinase involved in triggering biofilm formation on the roots of tomato plants. Mol Microbiol 85: 418-430.
14. Chen Y, Yan F, Chai Y, Liu H, Kolter R et al (2013) Biocontrol of tomato wilt disease by Bacillussubtilis isolates from natural environments depends on conserved genes mediating biofilm formation. Environ Microbiol 15: 848-864.
15. Choudhary D, Johri BN (2009) Interactionsof Bacillus spp. and plants-with special reference to induced systemic resistance (ISR). Microbiol Res 164: 493-513.
16. Conrath U, Pieterse CM, Mauch-Mani B (2002) Priming in plant pathogen interactions. Trends Plant Sci 7: 210-216.
17. Dodd C, Zinovkina NY, Safronova VI, Belimov AA (2010) Rhizobacterial mediation of plant hormone status. Ann Appl Biol 157: 361-379.
18. El Yahyaoui F, Kuster H, Ben Amor B, Hohnjec N, Puhler A et al (2004) Expression profiling in Medicago truncatula identifies more than 750 genes differentially expressed during nodulation, including many potential regulators of the symbiotic program. Plant Physiol 136: 3159-3176.
19. Fall R, Kinsinger RF, Wheeler KA (2004) A simple method to isolate biofilm-forming Bacillussubtilis and related species from plant roots. Syst Appl Microbiol 27: 372-379.
20. Hayat R, Ali S, Amara U, Khalid R, Ahmed I (2010) Soil beneficial bacteria and their role in plant growth promotion: a review. Ann Microbiol 60: 579-598.
21. Hein JW, Wolfe GV, Blee KA (2008) Comparison of rhizosphere bacterial communities in Arabidopsis thaliana mutants for systemic acquired resistance. Microbial Ecol 55: 333-343.
22. Hontzeas N, Saleh SS, Glick BR (2004) Changes in gene expression in canola roots induced by ACC-deaminase-containing plant-growth-promoting bacteria. Mol Plant-Microbe Interact 17: 865-871.
23. Hückelhoven R (2007) Cell wall associated mechanisms of disease resistance and susceptibility. Ann Rev Phytopathol 45: 101-127.
24. Kleijn RJ, Buescher JM, Le Chat L, Jules M, Aymerich S et al (2010) Metabolic fluxes during strong carbon catabolite repression by malate in Bacillussubtilis. J Biol Chem 285: 1587-1596.
25. Kloepper JW, Ryu CM, Zhang S (2004) Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathol 94: 1259-1266.
26. Kobayashi Y, Hoekenga OA, Itoh H, Nakashima M, Saito S et al (2007) Characterization of AtALMT1 expression in aluminum-inducible malate release and its role for rhizotoxic stress tolerance in Arabidopsis. Plant Physiol 145: 843-852.
27. Kristensen C, Morant M, Olsen CE, Ekstrøm CT, Galbraith DW et al (2005) Metabolic engineering of dhurrin in transgenic Arabidopsis plants with marginal inadvertent effects on the metabolome and transcriptome. Proc Natl Acad Sci USA 102: 1779-1784.
28. Lakshmanan V, Kitto SL, Caplan JL, Hsueh Y-H, Kearns DB et al (2012) Microbe-Associated Molecular Patterns (MAMPs)-triggered root responses mediate beneficial rhizobacterial recruitment in Arabidopsis. Plant Physiol 160: 1642-1662.
29. Lin W, Okon Y, Hardy RWF (1983) Enhanced mineral uptake by Zea mays and Sorghum bicolor roots inoculated with Azospirillum brasilense. Appl Environ Microbiol 45: 1775-1779.
30. Lugtenberg B, Kamilova F (2009) Plant growth-promoting rhizobacteria. Ann Rev Microbiol 63: 541-556.
31. Maleck K, Levine A, Eulgem T, Morgan A, Schmid J et al (2000) The transcriptome of Arabidopsis thaliana during systemic acquired resistance. Nat Genet 26: 403-410.
32. Marschner P, Neumann G, Kania A, Weisskopf L, Lieberei R (2002) Spatial and temporal dynamics of the microbial community structure in the rhizosphere of cluster roots of white lupin (Lupinusalbus L.). Plant Soil 246: 167-174.
33. Millet YA, Danna CH, Clay NK, Songnuan W, Simon MD et al (2010) Innate immune responses activated in Arabidopsis roots by microbe-associated molecular patterns. Plant Cell 22: 973-990.
34. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiol Plant 15: 473-479.
35. Neumann G, Martinoia E (2002) Cluster roots-an underground adaptation for survival in extreme environments. Trends Plant Sci 7: 162-167.
36. Niu DD, Liu HX, Jiang CH, Wang YP, Wang QY et al (2011) The plant growth-promoting rhizobacterium Bacillus cereus AR156 induces systemic resistance in Arabidopsis thaliana by simultaneously activating salicylate- and Jasmonate/Ethylene-dependent signaling pathways. Mol Plant-Microbe Interact 24: 533-542.
37. Ongena M, Thonart P (2006) Resistance induced in plants by nonpathogenic microorganisms: Elicitation and defense responses. In: Jaime A, Da Silva T (eds) Floriculture, ornamental and plant biotechnology: advances and topical issues, 1st edn. Global Science Books, London, pp 447-463.
38. Pérez-García A, Romero D, de Vicente A (2011) Plant protection and growth stimulation by microorganisms: biotechnological applications of Bacilli in agriculture. Curr Opin Biotechnol 22: 187-193.
39. Pineda A, Zhengg S-J, van Loon JJA, Pieterse CMJ, Dicke M (2010) Helping plants to deal with insects: the role of beneficial soil-borne microbes. Trends Plant Sci 15: 507-514.
40. Priest F (1993) Systematics and ecology of Bacillus. In: Hoch JA, Losick R (eds) Bacillussubtilis and other gram-positive bacteria: biochemistry, physiology, and molecular genetics. American Society for Microbiology Press, Washington, pp 3-16.
41. Raaijmakers JM, Paulitz TC, Steinberg C, Alabouvette C, Moënne-Loccoz Y (2008) The rhizosphere: a playground and battle field for soil borne pathogens and beneficial microorganisms. Plant Soil 321: 341-361.
42. Rudrappa T, Czymmek KJ, Paré PW, Bais HP (2008) Root-secreted malic acid recruits beneficial soil bacteria. Plant Physiol 148: 1547-1556.
43. Rudrappa T, Biedrzycki ML, Kunjeti SG, Donofrio NM, Czymmek KJ et al (2010) The rhizobacterial elicitor acetoin induces systemic resistance in Arabidopsis thaliana. Commun Integr Biol 3: 130-138.
44. Schenk PM, Kazan K, Wilson I, Anderson JP, Richmond T et al (2000) Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proc Natl Acad Sci USA 97: 11655-11660.
45. Schwachtje J, Karojet S, Thormählen I, Bernholz C, Kunz S et al (2011) A naturally associated rhizobacterium of Arabidopsisthaliana induces a starvation-like transcriptional response while promoting growth. PLoS ONE 6: e29382.
46. Trosvik P, Rudi K, Naes T, Kohler A, Chan K-S et al (2008) Characterizing mixed microbial population dynamics using time-series analysis. ISME J 2: 707-715.
47. van Loon LC, Bakker PAHM (2005) Induced systemic resistance as a mechanism of disease suppression by rhizobacteria. In: Siddiqui ZA (ed) PGPR: biocontrol and biofertilization. Springer, Dordrecht, pp 39-66.
48. Verhagen BW, Glazebrook J, Zhu T, Chang HS, van Loon LC et al (2004) The transcriptome of rhizobacteria-induced systemic resistance in Arabidopsis. Mol Plant-Microbe Interact 17: 895-908.
49. Wang YQ, Ohara Y, Nakayashiki H, Tosa Y, Mayama S (2005) Microarray analysis of the gene expression profile induced by the endophytic plant growth-promoting rhizobacteria, Pseudomonas fluorescens FPT9601-T5 in Arabidopsis. Mol Plant-Microbe Interact 18: 385-396.
50. Welbaum G, Sturz AV, Dong Z, Nowak J (2004) Fertilizing soil microorganisms to improve productivity of agroecosystems. Crit Rev Plant Sci 23: 175-193.
51. Zamioudis C, Pieterse CMJ (2012) Modulation of host immunity by beneficial microbes. Mol Plant Microbe Interact 25: 139-150.
52. Zhang H, Kim MS, Krishnamachari V, Payton P, Sun Y et al (2007) Rhizobacterial volatile emissions regulate auxin homeostasis and cell expansion in Arabidopsis. Planta 226: 839-851.
53. Zhang M, Murzello C, Sun Y, Kim M-S, Xie X et al (2010) Choline and osmotic-stress tolerance induced in Arabidopsis by the soil microbe Bacillus subtilis (GB03). Mol Plant-Microbe Interact 23: 1097-1104.