Effects of the Plant Growth-Promoting Bacterium Burkholderia phytofirmans PsJN throughout the Life Cycle of Arabidopsis thaliana

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Poupin, María Josefina ^a   Timmermann, Tania ^a   Vega, Andrea ^b   Zuñiga, Ana ^a   González, Bernardo ^a  

^a UNIVERSIDAD ADOLFO IBÁÑEZ   (Chile)

^b PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

Author keywords

[No Author keywords available]

Indexed keywords

AUXIN; GIBBERELLIN; TRANSCRIPTOME;

ARABIDOPSIS THALIANA; ARTICLE; BACTERIAL STRAIN; BURKHOLDERIA; BURKHOLDERIA PHYTOFIRMANS; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION; GENETIC TRANSCRIPTION; GROWTH RATE; NONHUMAN; ONTOGENY; PLANT DEVELOPMENT; PLANT GENE; PLANT GROWTH; PLANT LIFE CYCLE STAGE; PLANT STRESS; PLANT-GROWTH PROMOTING BACTERIUM; RHIZOSPHERE BACTERIUM;

ARABIDOPSIS; BURKHOLDERIA; FLOWERS; GENE EXPRESSION REGULATION, PLANT; GERMINATION; PLANT DEVELOPMENT; RHIZOSPHERE; SEEDS;

EID: 84880300812     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0069435     Document Type: Article

References (84)

1. van Loon LC, (2007) Plant responses to plant growth-promoting rhizobacteria. Eur J Plant Pathol 119: 243-254. doi:10.1007/s10658-007-9165-1.
2. Bais HP, Park SW, Weir TL, Callaway RM, Vivanco JM, (2004) How plants communicate using the underground information superhighway. Trends Plant Sci 9: 26-32. doi:10.1016/j.tplants.2003.11.008. PubMed: 14729216.
3. Dimkpa C, Weinand T, Asch F, (2009) Plant-rhizobacteria interactions alleviate abiotic stress conditions. Plant Cell Environ 32: 1682-1694. doi:10.1111/j.1365-3040.2009.02028.x. PubMed: 19671096.
4. Kloepper JW, Reddy MS, Rodriguez-Kabana R, Kenney DS, Kokalis-Burelle N, et al. (2004) Application for rhizobacteria in transplant production and yield enhancement. In: Nicola S, Nowak J, Vavrina CS, eds. Issues and Advances in Transplant Production and Stand Establishment Research. pp. pp. 217-229.
5. Lugtenberg B, Kamilova F, (2009) Plant-Growth-Promoting Rhizobacteria. Annu Rev Microbiol, 63: 541-556. PubMed: 19575558.
6. Yang J, Kloepper JW, Ryu CM, (2009) Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci 14: 1-4. doi:10.1016/j.tplants.2008.10.004. PubMed: 19056309.
7. Dobbelaere S, Vanderleyden J, Okon Y, (2003) Plant growth-promoting effects of diazotrophs in the rhizosphere. CRC Crit Rev Plants Sci 22: 107-149. doi:10.1080/713610853.
8. Vessey JK, (2003) Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255: 571-586. doi:10.1023/A:1026037216893.
9. Ortíz-Castro R, Valencia-Cantero E, López-Bucio J, (2008) Plant growth promotion by Bacillus megaterium involves cytokinin signaling. Plants Signal Behav 3: 263-265. doi:10.4161/psb.3.4.5204. PubMed: 19704649.
10. Persello-Cartieaux F, Nussaume L, Robaglia C, (2003) Tales from the underground: molecular plant-rhizobacteria interactions. Plant Cell Environ 26: 189-199. doi:10.1046/j.1365-3040.2003.00956.x.
11. 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. doi:10.1007/s00425-007-0530-2. PubMed: 17497164.
12. Ortiz-Castro R, Díaz-Pérez C, Martínez-Trujillo M, del Río RE, Campos-García J, et al. (2011) Transkingdom signaling based on bacterial cyclodipeptides with auxin activity in plants. Proc Natl Acad Sci U S A 108: 7253-7258. doi:10.1073/pnas.1006740108. PubMed: 21482761.
13. Glick BR, (2004) Bacterial ACC deaminase and the alleviation of plant stress. Adv Appl Microbiol 56: 291-312. doi:10.1016/S0065-2164(04)56009-4. PubMed: 15566983.
14. Glick BR, (2005) Modulation of plant ethylene levels by the bacterial enzyme ACC deaminase. FEMS Microbiol Lett 251: 1-7. doi:10.1016/j.femsle.2005.07.030. PubMed: 16099604.
15. Chen L, Dodd IC, Theobald JC, Belimov AA, Davies WJ, (2013) The rhizobacterium Variovorax paradoxus 5C-2, containing ACC deaminase, promotes growth and development of Arabidopsis thaliana via an ethylene-dependent pathway. J Exp Bot 64: 1565-1573. doi:10.1093/jxb/ert031. PubMed: 23404897.
16. Ortíz-Castro R, Martínez-Trujillo M, López-Bucio J, (2008) N-acyl-L-homoserine lactones: a class of bacterial quorum-sensing signals alter post-embryonic root development in Arabidopsis thaliana. Plant Cell Environ 31: 1497-1509. doi:10.1111/j.1365-3040.2008.01863.x. PubMed: 18657054.
17. Ryu CM, Farag MA, Hu CH, Reddy MS, Wei HX, et al. (2003) Bacterial volatiles promote growth in Arabidopsis. Proc Natl Acad Sci U S A 100: 4927-4932. doi:10.1073/pnas.0730845100. PubMed: 12684534.
18. Wang K, Conn K, Lazarovits G, (2006) Involvement of quinolinate phosphoribosyl transferase in promotion of potato growth by a Burkholderia strain. Appl Environ Microbiol 72: 760-768. doi:10.1128/AEM.72.1.760-768.2006. PubMed: 16391116.
19. Lucy M, Reed E, Glick BR, (2004) Applications of free living plant growth-promoting rhizobacteria. Antonie Van Leeuwenhoek 86: 1-25. doi:10.1023/B:ANTO.0000024903.10757.6e. PubMed: 15103234.
20. Babalola OO, (2010) Beneficial bacteria of agricultural importance. Biotechnol Lett 32: 1559-1570. doi:10.1007/s10529-010-0347-0. PubMed: 20635120.
21. Ait Barka E, Belarbi A, Hachet C, Nowak J, Audran JC, (2000) Enhancement of in vitro growth and resistance to gray mould of Vitis vinifera co-cultured with plant growth-promoting rhizobacteria. FEMS Microbiol Lett 186: 91-95. doi:10.1111/j.1574-6968.2000.tb09087.x. PubMed: 10779718.
22. Contesto C, Milesi S, Mantelin S, Zancarini A, Desbrosses G, et al. (2010) The auxin-signaling pathway is required for the lateral root response of Arabidopsis to the rhizobacterium Phyllobacterium brassicacearum. Planta 232: 1455-1470. doi:10.1007/s00425-010-1264-0. PubMed: 20844890.
23. Desbrosses G, Contesto C, Varoquaux F, Galland M, Touraine B, (2009) PGPR-Arabidopsis interactions is a useful system to study signaling pathways involved in plant developmental control. Plants Signal Behav 4: 321-323. PubMed: 19794852.
24. López-Bucio J, Campos-Cuevas JC, Hernández-Calderón E, Velásquez-Becerra C, Farías-Rodríguez R, et al. (2007) Bacillus megaterium rhizobacteria promote growth and alter root-system architecture through an auxin- and ethylene-independent signaling mechanism in Arabidopsis thaliana. Mol Plant Microbe Interact 20: 207-217. doi:10.1094/MPMI-20-2-0207. PubMed: 17313171.
25. Xie X, Zhang H, Paré PW, (2009) Sustained growth promotion in Arabidopsis with long-term exposure to the beneficial soil bacterium Bacillus subtilis (GB03). Plants Signal Behav 4: 948-953. doi:10.4161/psb.4.10.9709. PubMed: 19826235.
26. Cartieaux F, Thibaud MC, Zimmerli L, Lessard P, Sarrobert C, et al. (2003) Transcriptome analysis of Arabidopsis colonized by a plant-growth promoting rhizobacterium reveals a general effect on disease resistance. Plant J 36: 177-188. doi:10.1046/j.1365-313X.2003.01867.x. PubMed: 14535883.
27. Verhagen BWM, 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. doi:10.1094/MPMI.2004.17.8.895. PubMed: 15305611.
28. 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. doi:10.1094/MPMI-18-0385. PubMed: 15915637.
29. Schwachtje J, Karojet S, Thormählen I, Bernholz C, Kunz S, et al. (2011) A naturally associated rhizobacterium of Arabidopsis thaliana induces a starvation-like transcriptional response while promoting growth. PLOS ONE 6: e29382. doi:10.1371/journal.pone.0029382. PubMed: 22216267.
30. Cartieaux F, Contesto C, Gallou A, Desbrosses G, Kopka J, et al. (2008) Simultaneous interaction of Arabidopsis thaliana with Bradyrhizobium sp strain ORS278 and Pseudomonas syringae pv. tomato DC3000 leads to complex transcriptome changes. Mol Plant Microbe Interact 21: 244-259. doi:10.1094/MPMI-21-2-0244. PubMed: 18184068.
31. Stearns JC, Woody OZ, McConkey BJ, Glick BR, (2012) Effects of bacterial ACC deaminase on Brassica napus gene expression. Mol Plant Microbe Interact 25: 668-676. doi:10.1094/MPMI-08-11-0213. PubMed: 22352713.
32. Coenye T, Vandamme P, (2003) Diversity and significance of Burkholderia species occupying diverse ecological niches. Environ Microbiol 5: 719-729. doi:10.1046/j.1462-2920.2003.00471.x. PubMed: 12919407.
33. Compant S, Nowak J, Coenye T, Clément C, Barka EA, (2008) Diversity and occurrence of Burkholderia spp. in the natural environment. FEMS Microbiol Rev 32: 607-626. doi:10.1111/j.1574-6976.2008.00113.x. PubMed: 18422616.
34. Ait Barka E, Nowak J, Clément C, (2006) Enhancement of chilling resistance of inoculated grapevine plantlets with a plant growth-promoting rhizobacterium, Burkholderia phytofirmans strain PsJN. Appl Environ Microbiol 72: 7246-7252. doi:10.1128/AEM.01047-06. PubMed: 16980419.
35. Compant S, Reiter B, Sessitsch A, Nowak J, Clément C, et al. (2005) Endophytic colonization of Vitis vinifera L. by plant growth promoting bacterium Burkholderia sp strain PsJN. Appl Environ Microbiol 71: 1685-1693. doi:10.1128/AEM.71.4.1685-1693.2005. PubMed: 15811990.
36. Nowak J, Shulaev V, (2003) Priming for transplant stress resistance in in vitro propagation. In Vitro Cell Dev Biol Plant 39: 107-124. doi:10.1007/s11626-003-0001-4.
37. Sessitsch A, Coenye T, Sturz AV, Vandamme P, Barka EA, et al. (2005) Burkholderia phytofirmans sp. nov., a novel plant-associated bacterium with plant-beneficial properties. Int J Syst Evol Microbiol 55: 1187-1192. doi:10.1099/ijs.0.63149-0. PubMed: 15879253.
38. Sharma VK, Nowak J, (1998) Enhancement of verticillium wilt resistance in tomato transplants by in vitro co-culture of seedlings with a plant growth promoting rhizobacterium (Pseudomonas sp. Strain PsJN) (vol 44, pg 528, 1998). Can J Microbiol 44: 806-806. doi:10.1139/w98-111.
39. Nowak J, Sharma VK, A'Hearn E, (2004) Endophyte enhancement of transplant performance in tomato, cucumber and sweet pepper. Acta Hort 631: 253-263.
40. Theocharis A, Bordiec S, Fernandez O, Paquis S, Dhondt-Cordelier S, et al. (2012) Burkholderia phytofirmans strain PsJN primes Vitis vinifera L. and confers a better tolerance to low non-freezing temperatures. Mol Plant Microbe Interact 25: 496-504. doi:10.1094/MPMI-09-11-0245. PubMed: 22409157.
41. Fernandez O, Theocharis A, Bordiec S, Feil R, Jacquens L, et al. (2012) Burkholderia phytofirmans PsJN acclimates grapevine to cold by modulating carbohydrate metabolism. Mol Plant Microbe Interact 25: 496-504. doi:10.1094/MPMI-09-11-0245. PubMed: 22409157.
42. Nowak J, Asiedu SK, Bensalim S, Richards J, Stewart A, et al. (1998) From laboratory to applications: challenges and progress with in vitro dual cultures of potato and beneficial bacteria. Plant Cell Tissue Organ Cult 52: 97-103. doi:10.1023/A:1005965822698.
43. Frommel MI, Nowak J, Lazarovits G, (1991) Growth Enhancement and Developmental Modifications of in Vitro Grown Potato (Solanum tuberosum spp. tuberosum) as Affected by a Nonfluorescent Pseudomonas sp. Plant Physiol 96: 928-936. doi:10.1104/pp.96.3.928. PubMed: 16668277.
44. Lazarovits G, Nowak J, (1997) Rhizobacteria for improvement of plant growth and establishment. Hortscience 32: 188-192.
45. Ait Barka E, Gognies S, Nowak J, Audran JC, Belarbi A, (2002) Inhibitory effect of endophyte bacteria on Botrytis cinerea and its influence to promote the grapevine growth. Biol Contr 24: 135-142. doi:10.1016/S1049-9644(02)00034-8.
46. Sun YL, Cheng ZY, Glick BR, (2009) The presence of a 1-aminocyclopropane-1-carboxylate (ACC) deaminase deletion mutation alters the physiology of the endophytic plant growth-promoting bacterium Burkholderia phytofirmans PsJN. FEMS Microbiol Lett 296: 131-136.
47. Bordiec S, Paquis S, Lacroix H, Dhondt S, Barka EA, et al. (2011) Comparative analysis of defence responses induced by the endophytic plant growth-promoting rhizobacterium Burkholderia phytofirmans strain PsJN and the non-host bacterium Pseudomonas syringae pv. pisi in grapevine cell suspensions. J Exp Bot 62: 595-603. doi:10.1093/jxb/erq291. PubMed: 20881012.
48. Da K, Nowak J, Flinn B, (2012) Potato cytosine methylation and gene expression changes induced by a beneficial bacterial endophyte, Burkholderia phytofirmans strain PsJN. Plant Physiol Biochem 50: 24-34. doi:10.1016/j.plaphy.2011.09.013. PubMed: 22099516.
49. Boyes DC, Zayed AM, Ascenzi R, McCaskill AJ, Hoffman NE, et al. (2001) Growth stage-based phenotypic analysis of Arabidopsis: a model for high throughput functional genomics in plants. Plant Cell 13: 1499-1510. doi:10.2307/3871382. PubMed: 11449047.
50. Katari MS, Nowicki SD, Aceituno FF, Nero D, Kelfer J, et al. (2010) VirtualPlant: a software platform to support systems biology research. Plant Physiol 152: 500-515. doi:10.1104/pp.109.147025. PubMed: 20007449.
51. Edgar R, Domrachev M, Lash AE, (2002) Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30: 207-210. doi:10.1093/nar/30.1.207. PubMed: 11752295.
52. Blázquez MA, Soowal LN, Lee I, Weigel D, (1997) LEAFY expression and flower initiation in Arabidopsis. Development 124: 3835-3844. PubMed: 9367439.
53. Corbesier L, Coupland G, (2006) The quest for florigen: a review of recent progress. J Exp Bot 57: 3395-3403. doi:10.1093/jxb/erl095. PubMed: 17030536.
54. Blázquez M, (2000) Flower development pathways. J Cell Sci 113(20):: 3547-3548. PubMed: 11017868.
55. Ng M, Yanofsky MF, (2001) Function and evolution of the plant MADS-box gene family. Nat Rev Genet 2: 186-195. doi:10.1038/35056041. PubMed: 11256070.
56. Belimov AA, Dodd IC, Safronova VI, Hontzeas N, Davies WJ, (2007) Pseudomonas brassicacearum strain Am3 containing 1-aminocyclopropane-1-carboxylate deaminase can show both pathogenic and growth-promoting properties in its interaction with tomato. J Exp Bot 58: 1485-1495. doi:10.1093/jxb/erm010. PubMed: 17322547.
57. Compant S, Kaplan H, Sessitsch A, Nowak J, Barka EA, et al. (2008) Endophytic colonization of Vitis vinifera L. by Burkholderia phytofirmans strain PsJN: from the rhizosphere to inflorescence tissues. FEMS Microbiol Ecol 63: 84-93. doi:10.1111/j.1574-6941.2007.00410.x. PubMed: 18081592.
58. Catalá C, Rose JKC, Bennett AB, (1997) Auxin regulation and spatial localization of an endo-1,4-beta-D-glucanase and a xyloglucan endotransglycosylase in expanding tomato hypocotyls. Plant J 12: 417-426. doi:10.1046/j.1365-313X.1997.12020417.x. PubMed: 9301092.
59. De Smet I, Lau S, Voss U, Vanneste S, Benjamins R, et al. (2010) Bimodular auxin response controls organogenesis in Arabidopsis. Proc Natl Acad Sci U S A 107: 2705-2710. doi:10.1073/pnas.0915001107. PubMed: 20133796.
60. Overvoorde P, Fukaki H, Beeckman T, (2010) Auxin Control of Root Development. Cold Spring Harb Perspect Biol 2: 1-16.
61. Chapman EJ, Estelle M, (2009) Cytokinin and auxin intersection in root meristems. Genome Biol 10: 210-215. doi:10.1186/gb-2009-10-2-210.
62. Zuniga A, Poupin MJ, Donoso R, Ledger T, Guiliani N, et al. (2013) Quorum Sensing and Indole-3-Acetic Acid Degradation Play a Role in Colonization and Plant Growth Promotion of Arabidopsis thaliana by Burkholderia phytofirmans PsJN. Mol Plant Microbe Interact 26: 546-553.
63. Sun TP, Gubler F, (2004) Molecular mechanism of gibberellin signaling in plants. Annu Rev Plant Biol 55: 197-223. doi:10.1146/annurev.arplant.55.031903.141753. PubMed: 15377219.
64. Swain SM, Singh DP, (2005) Tall tales from sly dwarves: novel functions of gibberellins in plant development. Trends Plant Sci 10: 123-129. doi:10.1016/j.tplants.2005.01.007. PubMed: 15749470.
65. Mitchum MG, Yamaguchi S, Hanada A, Kuwahara A, Yoshioka Y, et al. (2006) Distinct and overlapping roles of two gibberellin 3-oxidases in Arabidopsis development. Plant J 45: 804-818. doi:10.1111/j.1365-313X.2005.02642.x. PubMed: 16460513.
66. Hu JH, Mitchum MG, Barnaby N, Ayele BT, Ogawa M, et al. (2008) Potential sites of bioactive gibberellin production during reproductive growth in Arabidopsis. Plant Cell 20: 320-336. doi:10.1105/tpc.107.057752. PubMed: 18310462.
67. Wang K, Conn K, Lazarovits G, (2006) Involvement of quinolinate phosphoribosyl transferase in promotion of potato growth by a Burkholderia strain. Appl Environ Microbiol 72: 760-768. doi:10.1128/AEM.72.1.760-768.2006. PubMed: 16391116.
68. Trognitz F, Scherwinski K, Fekete A, Schmidt S, Eberl L, et al. (2008) Interaction Between Potato and the Endophyte Burkholderia phytofirmans. Tagung der Vereinigung der Pflanzenzüchter und Saatgutkaufl eute Österreichs: pp. 63-66.
69. Issartel J, Coiffard C, (2011) Extreme longevity in trees: live slow, die old? Oecologia 165: 1-5. doi:10.1007/s00442-010-1807-x. PubMed: 20963610.
70. Pearl R, (1928) Experiments on longevity. Q Rev Biol 3: 391-407. doi:10.1086/394311.
71. Metcalfe NB, Monaghan P, (2003) Growth versus lifespan: perspectives from evolutionary ecology. Exp Gerontol 38: 935-940. doi:10.1016/S0531-5565(03)00159-1. PubMed: 12954479.
72. Dorn E, Hellwig M, Reineke W, Knackmus Hj, (1974) Isolation and characterization of a 3-chlorobenzoate degrading pseudomonad. Arch Microbiol 99: 61-70. doi:10.1007/BF00696222. PubMed: 4852581.
73. Murashige T, Skoog F, (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15: 473-497. doi:10.1111/j.1399-3054.1962.tb08052.x.
74. Deal RB, Kandasamy MK, McKinney EC, Meagher RB, (2005) The nuclear actin-related protein ARP6 is a pleiotropic developmental regulator required for the maintenance of FLOWERING LOCUS C expression and repression of flowering in Arabidopsis. Plant Cell 17: 2633-2646. doi:10.1105/tpc.105.035196. PubMed: 16141450.
75. Lartey R, Ghoshroy S, Ho J, Citovsky V, (1997) Movement and subcellular localization of a tobamovirus in Arabidopsis. Plant J 12: 537-545. doi:10.1046/j.1365-313X.1997.00537.x. PubMed: 9351241.
76. Porra R, Thompson W, Kriedmann P, (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophyll a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim Biophys Acta 975: 384-394. doi:10.1016/S0005-2728(89)80347-0.
77. Sokal R, Rohlf F, editors (1997) Biometry: The Principles and Practice of Statistics in Biological Research, 3rd edition. New York: W H Freeman and Co.
78. Poupin MJ, Federici F, Medina C, Matus JT, Timmermann T, et al. (2007) Isolation of the three grape sub-lineages of B-class MADS-box TM6, PISTILLATA and APETALA3 genes which are differentially expressed during flower and fruit development. Gene 404: 10-24. doi:10.1016/j.gene.2007.08.005. PubMed: 17920788.
79. Dauelsberg P, Matus JT, Poupin MJ, Leiva-Ampuero A, Godoy F, et al. (2011) Effect of pollination and fertilization on the expression of genes related to floral transition, hormone synthesis and berry development in grapevine. J Plant Physiol 168: 1667-1674. doi:10.1016/j.jplph.2011.03.006. PubMed: 21497942.
80. Czechowski T, Stitt M, Altmann T, Udvardi MK, Scheible WR, (2005) Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol 139: 5-17. doi:10.1104/pp.105.063743. PubMed: 16166256.
81. Remans T, Smeets K, Opdenakker K, Mathijsen D, Vangronsveld J, et al. (2008) Normalisation of real-time RT-PCR gene expression measurements in Arabidopsis thaliana exposed to increased metal concentrations. Planta 227: 1343-1349. doi:10.1007/s00425-008-0706-4. PubMed: 18273637.
82. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, et al. (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4: 249-264. doi:10.1093/biostatistics/4.2.249. PubMed: 12925520.
83. Gautier L, Cope L, Bolstad BM, Irizarry RA, (2004) affy-analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 20: 307-315. doi:10.1093/bioinformatics/btg405. PubMed: 14960456.
84. Breitling R, Armengaud P, Amtmann A, Herzyk P, (2004) Rank products: a simple, yet powerful, new method to detect differentially regulated genes in replicated microarray experiments. FEBS Lett 573: 83-92. doi:10.1016/j.febslet.2004.07.055. PubMed: 15327980.