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Arthrobacter agilis UMCV2 induces iron acquisition in Medicago truncatula (strategy I plant) in vitro via dimethylhexadecylamine emission

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Abstract

Background and aims

Iron is an essential nutrient for plant growth. Although abundant in soil, iron is poorly available. Therefore, plants have evolved mechanisms for iron mobilization and uptake from the rhizospheric environment. In this study, we examined the physiological responses to iron deficiency in Medicago truncatula plants exposed to volatile organic compounds (VOCs) produced by Arthrobacter agilis UMCV2.

Methods

The VOC profiles of the plant and bacterium were determined separately and during interaction assays using gas chromatography. M. truncatula plants exposed to A. agilis VOCs and pure dimethylhexadecylamine were transferred to conditions of iron deficiency, and parameters associated with iron nutritional status were measured.

Results

The relative abundance of the bacterial VOC dimethylhexadecylamine increased 12-fold when in co-cultures of A. agilis and M. truncatula, compared to axenic cultures. Plants exposed to bacterial VOCs or dimethylhexadecylamine exhibited a higher rhizosphere acidification capacity, enhanced ferric reductase activity, higher biomass generation, and elevated chlorophyll and iron content relative to controls.

Conclusions

The VOCs emitted by A. agilis UMCV2 induce iron acquisition mechanisms in vitro in the Strategy I plant M. truncatula. Dimethylhexadecylamine is the signal molecule responsible for producing the beneficial effects.

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References

  • Aguirre E, Leménager D, Bacaicoa E, Fuentes M, Baigorri R, Zamarreño AM, García-Mina JM (2009) The root application of a purified leonardite humic acid modifies the transcriptional regulation of the main physiological root responses to Fe deficiency in Fe-sufficient cucumber plants. Plant Physiol Biochem 47:215–223. doi:10.1016/jplaphy.2808.11.013

    Article  PubMed  CAS  Google Scholar 

  • Andaluz S, Rodríguez-Chelma J, Abadía A, Abadía J, López-Millán AF (2009) Time course induction of several key enzymes in Medicago truncatula roots in response to Fe deficiency. Plant Physiol Biochem 47:1082–1088. doi:10.1016/j.plaphy.2009.07.009

    Article  PubMed  CAS  Google Scholar 

  • Bendimerad N, Bendiab SAT, Benabadji AB, Fernandez X, Valette L, Cuvelier LL (2005) Composition and antibacterial activity of Pseudocytisus integrifolius (Salisb.) essential oil from Algeria. J Agr Food Chem 53:2947–2952. doi:10.1021/jf047937u

    Article  CAS  Google Scholar 

  • Boisson-Dernier A, Andriankaja A, Chabaud M, Niebel A, Journet E-P, Barker D, de Carvalho-Neibel F (2005) MtENOD11 gene activation during rhizobial infection and mycorrhizal arbuscule development requires a common AT-rich-containing regulatory sequence. Mol Plant-Microbe Interact 18:1269–1276. doi:10.1094/MPMI-18-1269

    Article  PubMed  CAS  Google Scholar 

  • Boué S, Shih BY, Carter-Wientjes CH, Cleveland TE (2005) Effect of soybean lipoxygenase on volatile generation and inhibition of Aspergillus flavus mycelial growth. J Agr Food Chem 53:4778–4783. doi:10.1021/jf058038o

    Article  Google Scholar 

  • Buchanan BB, Gruissem W, Jones RL (2000) Biochemistry and molecular biology of plants. American Society of Plant Physiologists, Rockville

    Google Scholar 

  • Claeson AS, Sunesson AL (2005) Identification using versatile sampling and analytical methods of volatile compounds from Streptomyces albidoflavus grown on four humid building materials and one synthetic medium. Indoor Air 15:41–47. doi:10.1111/j.1600-0668.2005.00343.x

    Article  PubMed  Google Scholar 

  • Colangelo EP, Guerinot ML (2004) The essential basic helix-loop-helix protein FIT is required for the iron deficiency response. Plant Cell 16:3400–3412. doi:10.1105/tpc.104.024315

    Article  PubMed  CAS  Google Scholar 

  • Dickschat JS, Helmke E, Schulz S (2005) Volatile organic compounds from arctic bacteria of the Cytophaga-Flavobacterium-Bacteroides group: a retrobiosynthetic approach. Chemotaxonomic Investigations. Chemi Biodivers 2:318–353. doi:10.1002/cbdv.200590014

    Article  CAS  Google Scholar 

  • Eide D, Broderius M, Fett J, Guerinot ML (1996) A novel iron–regulated metal transporter from plants identified by functional expression in yeast. Proc Nat Acad Sci USA 93:5624–5628

    Article  PubMed  CAS  Google Scholar 

  • Gutiérrez-Luna FM, López-Bucio J, Altamirano-Hernández J, Valencia-Cantero E, Reyes de la Cruz H, Macías-Rodríguez L (2010) Plant growth-promoting rhizobacteria modulate root-system architecture in Arabidopsis thaliana through volatile organic compound emission. Symbiosis 51:75–83. doi:10.1007/s13199-010-0066-2

    Article  Google Scholar 

  • Hansen NC, Schmitt MA, Anderson JE, Strock JS (2003) Iron deficiency in soybean in the upper midwest and associated soil properties. Agron J 95:1595–1601. doi:10.2134/agronj2003.1595

    Article  CAS  Google Scholar 

  • Hell R, Stephan UW (2003) Iron uptake, trafficking and homeostasis in plants. Planta 216:541–551. doi:10.1007/s00425-002-0920-4

    PubMed  CAS  Google Scholar 

  • Kai M, Piechulla B (2009) Plant growth promotion due to rhizobacterial volatiles – An effect of CO2? FEBS Lett 583:3473–3477. doi:10.1016/j.febslet.2009.09.053

    Article  PubMed  CAS  Google Scholar 

  • Kai M, Effmert U, Berg G, Piechulla B (2007) Volatiles of bacterial antagonists inhibit mycelial growth of the plant pathogen Rhizoctonia solani. Arch Microbiol 87:351–360. doi:10.1007/s00203-006-0199-0

    Article  Google Scholar 

  • Kai M, Vespermann A, Piechulla B (2008) The growth of fungi and Arabidopsis thaliana is influenced by bacterial volatiles. Plant Signal Behav 3:1–3. doi:10.4161/psb.3.7.5681

    Article  Google Scholar 

  • Lichtenthaler HK, Wellburn AR (1983) Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem Soc Trans 11:591–592. doi:10.1042/bst0110591

    CAS  Google Scholar 

  • Lin SF, Grant D, Cianzio S, Shoemaker R (2000) Molecular characterization of iron deficiency chlorosis in soybean. J Plant Nutr 23:1591–1606. doi:10.1080/01904160009382154

    Article  Google Scholar 

  • Masalha J, Kosegarten H, Elmaci O, Mengel K (2000) The central role of microbial activity for iron acquisition in maize and sunflower. Biol Fertil Soils 30:433–4399. doi:10.1007/s003740050021

    Article  CAS  Google Scholar 

  • Mathesius U, Mulders S, Gao M, Teplitski M, Caetano-Anollés G, Rolfe BG, Bauer WD (2003) Extensive and specific responses of a eukaryote to bacterial quorum-sensing signals. Proc Nat Acad Sci USA 100:1444–1449. doi:10.1073_pnas.262672599

    Article  PubMed  CAS  Google Scholar 

  • Müller H, Westendorf C, Leitner E, Chernin L, Riedel K, Schmidt S, Eberl L, Berg G (2008) Quorum-sensing efects in the antagonistic rhizosphere bacterium Serratia plymuthica HRO-C48. FEMS Microbiol Ecol 67:468–478. doi:10.1111/j.1574-6941.2008.00635.x

    Article  Google Scholar 

  • Ortíz-Castro R, Valencia-Cantero E, López-Bucio J (2008) Plant growth promotion by Bacillus megaterium involves cytokinin signaling. Plant Signal Behav 3:263–265. doi:10.1094/MPMI-20-2-0207

    Article  PubMed  Google Scholar 

  • Ortíz-Castro R, Díaz-Pérez C, Miguel Martínez-Trujillo, del Río RE, Campos-García J, López-Bucio J (2011) Transkingdom signaling based on bacterial cyclodipeptides with auxin activity in plants. Proc Nat Acad Sci USA 108:7253–7258. doi:10.1073/pnas.1006740108

    Article  PubMed  Google Scholar 

  • Perkin-Elmer Corp. (1996) Analytical methods for atomic absorption spectroscopy. The Perkin-Elmer, USA, pp 141–143

  • Robinson NJ, Procter CM, Connolly EL, Guerinot ML (1999) A ferric-chelate reductase for iron uptake from soils. Nature 397:694–697. doi:10.1038/17800

    Article  PubMed  CAS  Google Scholar 

  • Römheld V (1987) Different strategies for iron acquisitionin higher plants. Physiol Plant 70:231–234. doi:10.1111/j.1399-3054.1987.tb06137.x

    Article  Google Scholar 

  • Römheld V, Marschner H (1986) Evidence for a specific uptake system for iron phytosiderophores in roots of grasses. Plant Physiol 80:175–180. doi:0032-0889/86/80/0175/06

    Article  PubMed  Google Scholar 

  • Santi S, Cesco S, Varanini Z, Pinton R (2005) Two plasma membrane H+−ATPase genes are differentially expressed in iron-deficent cucumber plants. Plant Physiol Biochem 43:287–292. doi:10.1016/j.plaphy.2005.02.007

    Article  PubMed  CAS  Google Scholar 

  • Schmidt W (1999) Mechanisms and regulation of reduction-based iron uptake in plants. New Phytol 141:1–26. doi:10.1046/j.1469-8137.1999.00331.x

    Article  CAS  Google Scholar 

  • Spaepen S, Vanderleyden J, Okon Y (2009) Plant growth-promoting actions of rhizobacteria. In: van Loon LC (ed) Advances in botanical research 51. Academic Press, Burlington, pp 283–320

  • Statsoft Inc. (2001) STATISTICA (data analysis software system), 6th edn. Tulsa, USA

  • Susín S, Abían J, Peleato ML, Sanchez-Baeza F, Abadía A, Gelpí E, Abadía J (1994) Flavin excretion from roots of iron-deficient sugar-beet (Beta vulagris L). Planta 193:514–519. doi:10.1007/BF02411556

    Article  Google Scholar 

  • Terry N, Abadia J (1986) Function of iron in chloroplasts. J Plant Nutr 9:609–646. doi:10.1080/01904168609363470

    Article  CAS  Google Scholar 

  • Thorn RMS, Reynolds DM, Greenman J (2011) Multivariate analysis of bacterial volatile compound profiles for discrimination between selected species and strains in vitro. J Microbiol Meth 84:258–264. doi:10.1016/j.mimet.2010.12.001

    Article  CAS  Google Scholar 

  • Valencia-Cantero E, Hernández-Calderón E, Velázquez-Becerra C, López-Meza JE, Alfaro-Cuevas R, López-Bucio J (2007) Role of dissimilatory fermentative iron-reducing bacteria in Fe uptake by common vean (Phaseolus vulgaris L.) plants grown in alkaline soil. Plant Soil 291:263–273. doi:10.1007/s11104-007-9191-y

    Article  CAS  Google Scholar 

  • Varsano T, Wolf SG, Pick U (2006) A chlorophyll a/b binding protein homolog which is induced by iron deficiency is associated with enlarged photosytem I units in the eukaryotic alga Dunaliella salina. J Biol Chem 281:10305–10315. doi:10.1074/jbc.M511057200

    Article  PubMed  CAS  Google Scholar 

  • Velázquez-Becerra C, Macías-Rodríguez LI, López-Bucio J, Altamirano-Hernández J, Flores-Cortez I, Valencia-Cantero E (2011) A volatile organic compound analysis from Arthrobacter agilis identifies dimethylhexadecylamine, an amino-containing lipid modulating bacterial growth and Medicago sativa morphogenesis in vitro. Plant Soil 339:329–340. doi:10.1007/s11104-010-0583-z

    Article  Google Scholar 

  • Vert G, Grotz N, Dédaldéchamp F, Gaymard F, Guerinot ML, Briat JF, Curie C (2002) IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth. Plant Cell 14:1223–1233. doi:10.1105/tpc.001388

    Article  PubMed  CAS  Google Scholar 

  • Wang D, Rose C, Kinkel L, Cao A, Tharayil N, Gerik J (2009) Production of methyl sulfide and dimethyl disulfide from soil-incorporated plant materials and implications for controlling soilborne pathogens. Plant Soil 324:185–197. doi:10.1007/s11104-009-9943-y

    Article  CAS  Google Scholar 

  • Welkie GW, Miller GW (1988) Riboflavin excretion from roots of iron‐stressed and reciprocally grafted tobacco and tomato plants. J Plant Nutr 11:691–700. doi:10.1080/01904168809363834

    Google Scholar 

  • Wilkins K, Schöller C (2009) Volatile organic metabolites from selected Streptomyces strains. Actinomycetologica 23:27–33. doi:10.3209/saj.SAJ230202

    Article  CAS  Google Scholar 

  • Xu C, Mo M, Zhang L, Zhang K (2004) Soil volatile fungistasis and volatile fungistatic compounds. Soil Biol Biochem 36:1997–2004. doi:10.1016/j.soilbio.2004.07.020

    Article  CAS  Google Scholar 

  • Yi Y, Guerinot ML (1996) Genetic evidence that induction of root Fe (III) chelate reductase activity is necessary for iron uptake under iron deficiency. Plant J 10:835–844. doi:10.1046/j.1365-313X.1996.10050835.x

    Article  PubMed  CAS  Google Scholar 

  • Zhang H, Sun Y, Xie X, Kim MS, Dowd SE, Paré PW (2009) A soil bacterium regulates plant acquisition of iron via deficiency-inducible mechanisms. Plant J 58:568–577. doi:10.1111/j.1365-313X.2009.03803.x

    Article  PubMed  CAS  Google Scholar 

  • Zou CS, Mo MH, Gu YQ, Zhou JP, Zhang KQ (2007) Possible contributions of volatile-producing bacteria to soil fungistasis. Soil Biol Biochem 39:2371–2379. doi:10.1016/j.soilbio.2007.04.009

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank the Consejo Nacional de Ciencia y Tecnología, México (Grant 128341) and Coordinación de la Investigación Científica-Universidad Michoacana de San Nicolás de Hidalgo (Grant 2.22) for financial support. MCOM received the PhD Scholarship 21559 from Consejo Nacional de Ciencia y Tecnología, México.

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Authors and Affiliations

  1. Instituto de Investigaciones Químico-Biológicas, Universidad Michoacana de San Nicolás de Hidalgo. Edificio B5, Ciudad Universitaria, C. P. 58030, Morelia, Michoacán, Mexico

    Ma del Carmen Orozco-Mosqueda, Crisanto Velázquez-Becerra, Lourdes I. Macías-Rodríguez, Gustavo Santoyo, Idolina Flores-Cortez, Ruth Alfaro-Cuevas & Eduardo Valencia-Cantero

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  1. Ma del Carmen Orozco-Mosqueda
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  2. Crisanto Velázquez-Becerra
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  3. Lourdes I. Macías-Rodríguez
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  5. Idolina Flores-Cortez
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  6. Ruth Alfaro-Cuevas
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  7. Eduardo Valencia-Cantero
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Correspondence to Eduardo Valencia-Cantero.

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Responsible Editor: Hans Lambers.

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Logarithmic scanning of the effect of DMHDA on M. truncatula plants. Vernalized seeds were placed on 1 side of a divided Petri dish and after 4 days, 0, 0.05, 0.5., and 5 nmol of DMHDA were spotted on the other side. At day 6, plant length and fresh weight were determined. The panels show the plant fresh weight (a), plant length (b), and representative images of 6-day-old plants at different concentrations of DMHDA. Bars represent mean (SE) (n = 16). Lower-case letters indicate significant differences (p < 0.05; Duncan’s multiple range test) (JPEG 505 kb)

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del Carmen Orozco-Mosqueda, M., Velázquez-Becerra, C., Macías-Rodríguez, L.I. et al. Arthrobacter agilis UMCV2 induces iron acquisition in Medicago truncatula (strategy I plant) in vitro via dimethylhexadecylamine emission. Plant Soil 362, 51–66 (2013). https://doi.org/10.1007/s11104-012-1263-y

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