Advertisement

Journal of Plant Growth Regulation

, Volume 34, Issue 3, pp 611–623 | Cite as

Volatile Organic Compounds Produced by the Rhizobacterium Arthrobacter agilis UMCV2 Modulate Sorghum bicolor (Strategy II Plant) Morphogenesis and SbFRO1 Transcription In Vitro

  • Diana Yazmin Castulo-Rubio
  • Nancy Araceli Alejandre-Ramírez
  • Ma del Carmen Orozco-Mosqueda
  • Gustavo Santoyo
  • Lourdes I. Macías-Rodríguez
  • Eduardo Valencia-CanteroEmail author
Article

Abstract

Different rhizobacteria may regulate plant growth using different mechanisms, including production of signal molecules that modulate plant morphogenesis and gene expression. Iron (Fe) is an essential micronutrient for plant growth and is frequently limited in plants. Plants with Strategy I Fe-uptake systems enhance root ferric reductase (FRO) activity to promote Fe absorption. Plants with Strategy II Fe-uptake systems increase Fe absorption by phytosiderophore production. However, recent reports have shown that plants with Strategy II systems also possess FRO genes that are expressed not in roots, but in shoots. Different rhizobacteria trigger plant Strategy I Fe-uptake systems via emission of volatile organic compounds (VOCs). In this work, we show that the plant growth-promoting rhizobacterium Arthrobacter agilis UMCV2 modulates the morphogenesis and FRO transcription of Sorghum bicolor, a plant with a Strategy II Fe-uptake system, via VOC emission. We found that in a system with separate compartments, VOCs emitted by A. agilis promoted plant growth, caused an increase in chlorophyll concentration, and modified the root architecture system. We tested the effect of the pure bacterial volatile compound dimethylhexadecylamine, produced by the UMCV2 strain, on plant growth and found an increase of 1.8-fold on shoot fresh weight, shoot length, chlorophyll concentration, and lateral root number at a concentration of 8 μM. This effect was dose dependent and was comparable to the effects produced by A. agilis VOCs. Simultaneously, we analyzed SbFRO1 expression using quantitative polymerase chain reaction and found that SbFRO1 expression was strongly modulated by VOCs produced by A. agilis, specifically dimethylhexadecylamine.

Keywords

SbFRO1 Dimethylhexadecylamine Arthrobacter agilis UMCV2 Sorghum bicolor Plant growth-promoting rhizobacteria Plant morphogenesis 

Notes

Acknowledgments

We thank the Consejo Nacional de Ciencia y Tecnología (Mexico) for funding this work via projects 165738 (LIMR) and 128341 (EVC).

Supplementary material

344_2015_9495_MOESM1_ESM.jpg (669 kb)
Phylogenetic analysis of putative SbIRT genes. A phylogenetic tree of the IRT genes and some related sequences were constructed employing the “maximum parsimony” algorithm. Numbers next to branches represent bootstrap values by performing 500 repetitions. Genes that were previously characterized are highlighted in bold letters. GenBank accession numbers are indicated in parentheses (JPEG 669 kb)

References

  1. Abadía J, Vázquez S, Rellán-Álvarez R, El-Jendoubi H, Abadía A, Álvarez-Fernández A, López-Millán AF (2011) Towards a knowledge-based correction of Fe chlorosis. Plant Physiol Biochem 49:471–482. doi: 10.1016/j.plaphy.2011.01.02 CrossRefPubMedGoogle Scholar
  2. Alexandratos N, Bruinsma J (2012) World agriculture towards 2030/2050: the 2012 revision. Rome FAO ESA. Working paper No. 12-03Google Scholar
  3. Andaluz S, Rodríguez-Celma 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 CrossRefPubMedGoogle Scholar
  4. Arkhipova TN, Prinsen E, Veselov SU, Martinenko EV, Melentiev AI, Kudoyarova GR (2007) Cytokinin producing bacteria enhance plant growth in drying soil. Plant Soil 292:305–315. doi: 10.1007/s11104-007-9233-5 CrossRefGoogle Scholar
  5. Balk J, Schaedler TA (2014) Iron cofactor assembly in plants. Annu Rev Plant Biol 65:125–153. doi: 10.1146/annurev-arplant-050213-035759 CrossRefPubMedGoogle Scholar
  6. Chereskin BM, Castelfranco PA (1982) Effects of Fe and oxygen on chlorophyll biosynthesis II. Observations on the biosynthetic pathway in isolated etiochloroplasts. Plant Physiol 69:112–116. doi: 10.1104/pp.69.1.112 CrossRefPubMedCentralPubMedGoogle Scholar
  7. Enomoto Y, Goto F (2013) Long-distance signaling of iron deficiency in plants. In: Baluška F (ed) Long-distance systemic signaling and communication in plants. Springer, Berlin, pp 167–188. doi: 10.1007/978-3-642-36470-9_8
  8. Geer LY, Domrachev M, Lipman DJ, Bryant SH (2002) CDART: protein homology by domain architecture. Genome Res 12:1619–1623. doi: 10.1101/gr.278202 CrossRefPubMedCentralPubMedGoogle Scholar
  9. Hindt N, Gerinot ML (2012) Getting a sense for signals: regulation of the plant Fe deficiency response. Biochim Biophys Acta 1823:1521–1530. doi: 10.1016/j.bbamcr.2012.03.010 CrossRefPubMedCentralPubMedGoogle Scholar
  10. Ishimaru Y, Suzuki M, Tsukamoto T, Suzuki K, Nakazono M, Kobayashi T, Wada Y, Watanabe S, Matsuhashi S, Takahashi M, Nakanishi H, Mori S, Nishizawa NK (2006) Rice plants take up Fe as an Fe3+-phytosiderophore and as Fe2+. Plant J 45:335–346. doi: 10.1111/j.1365-313X.2005.02624.x CrossRefPubMedGoogle Scholar
  11. Jeong J, Cohu C, Kerkeb L, Pilon M, Connolly EL, Guerinot ML (2008) Chloroplast Fe(III) chelate reductase activity is essential for seedling viability under iron limiting conditions. Proc Natl Acad Sci USA 105:10619–10624. doi: 10.1073/pnas.0708367105 CrossRefPubMedCentralPubMedGoogle Scholar
  12. Kang JG, van Iersel MW (2004) Nutrient solution concentration affects shoot: root ratio, leaf area ratio, and growth of subirrigated salvia (Salvia splendens). HortScience 39:49–54Google Scholar
  13. Kobayashi T, Nishizawa NK (2012) Iron uptake, translocation, and regulation in higher plants. Annu Rev Plant Biol 63:131–152. doi: 10.1146/annurev-arplant-042811-105522 CrossRefPubMedGoogle Scholar
  14. Kobayashi T, Itai RN, Nishizawa NK (2014) Iron deficiency responses in rice roots. Rice 7:27CrossRefPubMedGoogle Scholar
  15. Li S, Zhou X, Huang Y, Zhu L, Zhang S, Zhao Y, Guo J, Chen J, Chen R (2013) Identification and characterization of the zinc-regulated transporters, iron-regulated transporter-like protein (ZIP) gene family in maize. BMC Plant Biol 13:10–1186CrossRefGoogle Scholar
  16. Liu F, Xing S, Ma H, Du Z, Ma B (2013) Cytokinin-producing, plant growth-promoting rhizobacteria that confer resistance to drought stress in Platycladus orientalis container seedlings. Appl Microbiol Biotechnol 97:9155–9164. doi: 10.1007/s00253-013-5193-2 CrossRefPubMedGoogle Scholar
  17. Long TA, Tsukagoshi H, Busch W, Lahner B, Salt DE, Benfey PN (2010) The bHLH transcription factor POPEYE regulates response to Fe deficiency in Arabidopsis roots. Plant Cell 22:2219–2236. doi: 10.1105/tpc.110.074096 CrossRefPubMedCentralPubMedGoogle Scholar
  18. Mace ES, Tai S, Gilding EK, Li Y, Prentis PJ, Bian L et al (2013) Whole-genome sequencing reveals untapped genetic potential in Africa’s indigenous cereal crop sorghum. Nat Commun 4:2320. doi: 10.1038/ncomms3320 PubMedCentralPubMedGoogle Scholar
  19. Mikami Y, Saito A, Miwa E, Higuchi K (2011) Allocation of Fe and ferric chelate reductase activities in mesophyll cells of barley and sorghum under Fe-deficient conditions. Plant Physiol Biochem 49:513–519. doi: 10.1016/j.plaphy.2011.01.009 CrossRefPubMedGoogle Scholar
  20. Mukherjee I, Campbell NH, Ash JS, Connolly EL (2006) Expression profiling of the Arabidopsis ferric chelate reductase (FRO) gene family reveals differential regulation by iron and copper. Planta 223:1178–1190. doi: 10.1007/s00425-005-0165-0 CrossRefPubMedGoogle Scholar
  21. Müller I, Schmid B, Weiner J (2000) The effect of nutrient availability on biomass allocation patterns in 27 species of herbaceous plants. Perspect Plant Ecol 3:115–127. doi: 10.1078/1433-8319-00007 CrossRefGoogle Scholar
  22. Orozco-Mosqueda MC, Santoyo G, Farías-Rodríguez R, Macías-Rodríguez L, Valencia-Cantero E (2012) Identification and expression analysis of multiple FRO gene copies in Medicago truncatula. Genet Mol Res 11:4402–4410. doi: 10.4238/2012.October.9.7 CrossRefGoogle Scholar
  23. Orozco-Mosqueda MC, Macías-Rodríguez LI, Santoyo G, Flores-Cortez I, Farías-Rodríguez R, Valencia-Cantero E (2013a) Medicago truncatula increases its Fe-uptake mechanisms in response to volatile organic compounds produced by Sinorhizobium meliloti. Folia Microbiol 58:579–585. doi: 10.1007/s12223-013-0243-9 CrossRefGoogle Scholar
  24. Orozco-Mosqueda MC, Velázquez-Becerra C, Macías-Rodríguez LI, Santoyo G, Flores-Cortez I, Alfaro-Cuevas R, Valencia-Cantero E (2013b) Arthrobacter agilis UMCV2 induces Fe acquisition in Medicago truncatula (strategy I plant) in vitro via dimethylhexadecylamine emission. Plant Soil 362:51–66. doi: 10.1007/s11104-012-1263-y CrossRefGoogle Scholar
  25. Peña-Uribe CA, García-Pineda E, Beltrán-Peña E, de la Cruz HR (2012) Oligogalacturonides inhibit growth and induce changes in S6 K phosphorylation in maize (Zea mays L. var. Chalqueño). Plant Growth Regul 67:151–159. doi: 10.1007/s10725-012-9672-8 CrossRefGoogle Scholar
  26. Puckette MC, Tang Y, Mahalingam R (2008) Transcriptomic changes induced by acute ozone in resistant and sensitive Medicago truncatula accessions. BMC Plant Biol 8(1):46. doi: 10.1186/1471-2229-8-46 CrossRefPubMedCentralPubMedGoogle Scholar
  27. Ryu CM, Farag MA, Hu CH, Reddy MS, Wei HX, Pare PW, Kloepper JW (2003) Bacterial volatiles promote growth in Arabidopsis. Proc Natl Acad Sci USA 100:4927–4932. doi: 10.1073/pnas.0730845100 CrossRefPubMedCentralPubMedGoogle Scholar
  28. Sivitz AB, Hermand V, Curie C, Vert G (2012) Arabidopsis bHLH100 and bHLH101 control Fe homeostasis via a FIT-independent pathway. PLoS ONE 7(9):e44843. doi: 10.1371/journal.pone.0044843 CrossRefPubMedCentralPubMedGoogle Scholar
  29. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. doi: 10.1093/molbev/mst197 CrossRefPubMedCentralPubMedGoogle Scholar
  30. Tusnády GE, Simon I (2001) The HMMTOP transmembrane topology prediction Server. Bioinformatics 17:849–850CrossRefPubMedGoogle Scholar
  31. Valencia-Cantero E, Hernández-Calderón E, Velázquez-Becerra C, López-Meza JE, Alfaro-Cuevas R, López-Bucio J (2007) Role of dissimilatory fermentative Fe-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 CrossRefGoogle Scholar
  32. 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 CrossRefGoogle Scholar
  33. Velázquez-Becerra C, Macías-Rodríguez LI, López-Bucio J, Flores-Cortez I, Santoyo G, Hernández-Soberano C, Valencia-Cantero E (2013) The rhizobacterium Arthrobacter agilis produces dimethylhexadecylamine, a compound that inhibits growth of phytopathogenic fungi in vitro. Protoplasma 250:1251–1262. doi: 10.1007/s00709-013-0506-y CrossRefPubMedGoogle Scholar
  34. Victoria FC, Bervald CMP, da Maia LC, de Sousa RO, Panaud O, de Oliveira AC (2012) Phylogenetic relationships and selective pressure on gene families related to Fe homeostasis in land plants. Genome 55:883–900. doi: 10.1139/gen-2012-0064 CrossRefGoogle Scholar
  35. Vigani G, Zocchi G, Bashir K, Philippar K, Briat JF (2013) Signals from chloroplasts and mitochondria for Fe homeostasis regulation. Trends Plant Sci 18:305–311. doi: 10.1016/j.tplants.2013.01.006 CrossRefPubMedGoogle Scholar
  36. Wu H, Li L, Du J, Yuan Y, Cheng X, Ling HQ (2005) Molecular and biochemical characterization of the Fe(III) chelate reductase gene family in Arabidopsis thaliana. Plant Cell Physiol 46:1505–1514. doi: 10.1093/pcp/pci163 CrossRefPubMedGoogle Scholar
  37. Yuan Y, Wu H, Wang N, Li J, Zhao W, Du J, Wang D, Ling HQ (2008) FIT interacts with AtbHLH38 and AtbHLH39 in regulating Fe uptake gene expression for Fe homeostasis in Arabidopsis. Cell Res 18:385–397. doi: 10.1038/cr.2008.26 CrossRefPubMedGoogle Scholar
  38. Zhang H, Kim MS, Krishnamachari V, Payton P, Sun Y, Grimson M, Farag MA, Ryu CM, Allen R, Melo IS, Paré PW (2007) Rhizobacterial volatile emissions regulate auxin homeostasis and cell expansion in Arabidopsis. Planta 226:839–851. doi: 10.1007/s00425-007-0530-2 CrossRefPubMedGoogle Scholar
  39. Zhang H, Sun Y, Xie X, Kim MS, Dowd SE, Paré PW (2009) A soil bacterium regulates plant acquisition of Fe via deficiency-inducible mechanisms. Plant J 58:568–577. doi: 10.1111/j.1365-313X.2009.03803.x CrossRefPubMedGoogle Scholar
  40. Zuo Y, Zhang F (2011) Soil and crop management strategies to prevent Fe deficiency in crops. Plant Soil 339:83–95. doi: 10.1007/s11104-010-0566-0 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Diana Yazmin Castulo-Rubio
    • 1
    • 2
  • Nancy Araceli Alejandre-Ramírez
    • 1
  • Ma del Carmen Orozco-Mosqueda
    • 1
  • Gustavo Santoyo
    • 1
  • Lourdes I. Macías-Rodríguez
    • 1
  • Eduardo Valencia-Cantero
    • 1
    Email author
  1. 1.Instituto de Investigaciones Químico BiológicasUniversidad Michoacana de San Nicolás de HidalgoMoreliaMexico
  2. 2.Facultad de BiologíaUniversidad Michoacana de San Nicolás de HidalgoMoreliaMexico

Personalised recommendations