Advertisement

Plant and Soil

, Volume 417, Issue 1–2, pp 403–413 | Cite as

Production of border cells and colonization of maize root tips by Herbaspirillum seropedicae are modulated by humic acid

  • Luciano Pasqualoto Canellas
  • Fabio Lopes Olivares
Regular Article

Abstract

Background and aims

The adaptation of plants to land ecosystems involves complex rhizosphere interactions between organic matter and microbial communities. Border cells (BC) constitute the first living boundary in plant-soil ecosystems and play an important role in environmental sensing and signaling in response to different biotic and abiotic conditions. In this study, we evaluate the effect of humic acid on the release of BCs and its impact on the colonization of Herbaspirillum seropedicae at maize root tips.

Methods

Maize seedlings (1.0 ± 0.05 cm root length) were immersed for 48 h in solutions with different concentrations of humic acid (0, 12, 42, 143 and 500 mg L−1). Light and scanning electron microscopy were used to evaluate the structural interaction between border cells and H. seropedicae at the root tips.

Results

The release of BCs from root tips was significantly increased by humic acid (HA) application and exhibited a bell-shaped dose-response curve; the highest release of BCs occurred at 143 mg HA L−1 and was confirmed by microscopy. The colonization of roots by H. seropedicae strain RAM10 (tagged with green fluorescent protein, GFP) was monitored by epifluorescence microscopy with and without exogenous humic acid (143 mg L−1). Increased BC release resulted in a high density of diazotrophic bacteria at root tips, and bacteria sometimes aggregated with mucilage and humic acid particles, thus enhancing their viability. Increased BC numbers in response to humic acid might explain previous studies showing a concomitant increase in H. seropedicae populations in the rhizosphere, rhizoplane, and endosphere of grasses.

Conclusions

The population of H. seropedicae strain RAM10 colonizing root caps and BCs increased in response to exogenous humic acids.

Keywords

Root tip Humic substances Nitrogen-fixing bacteria Plant-bacteria interactions Plant growth-promoting bacteria 

Notes

Acknowledgements

FAPERJ, CNPq, National Institute of Science and Technology for Biological Nitrogen Fixation, IFS, OWCP for financial support. Prof Rose Adele from Paraná Federal University that kindly provided the bacteria strain linked with gfp protein and Daniele Frade that collaborated with some the epifluorescent micrographs of the bacteria-humic acid interaction. The post-doctoral stage of LPC at ECW was possible due to Science without Border program of CNPq, Brazil.

References

  1. Asli S, Neumann PM (2010) Rhizosphere humic acid interacts with root cell walls to reduce hydraulic conductivity and plant development. Plant Soil 336:313–322. doi: 10.1007/s11104-010-0483-2 CrossRefGoogle Scholar
  2. Baldani J, Baldani V, Seldin L, Döbereiner J (1986) Characterization of Herbaspirillum seropedicae gen. Nov., sp. nov., a root-associated nitrogen-fixing bacterium. Int J Syst Evol Microbiol 36:86–93Google Scholar
  3. Baldotto LEB, Olivares FL, Bressan-Smith R (2011) Structural interaction between GFP-labeled diazotrophic endophytic bacterium Herbaspirillum seropedicae RAM10 and pineapple plantlets' Vitória'. Braz J Microbiol 42:114–125CrossRefGoogle Scholar
  4. Brigham LA, Woo H-H, Nicoll SM, Hawes MC (1995) Differential expression of proteins and mRNAs from border cells and root tips of pea. Plant Physiol 109:457–463CrossRefPubMedPubMedCentralGoogle Scholar
  5. Canellas LP, Olivares FL, Okorokova-Façanha AL, Façanha AR (2002) Humic acids isolated from earthworm compost enhance root elongation, lateral root emergence, and plasma membrane H+−ATPase activity in maize roots. Plant Physiol 130:1951–1957CrossRefPubMedPubMedCentralGoogle Scholar
  6. Canellas LP, Teixeira Junior LRL, Dobbss LB, Silva CA, Medici LO, Zandonadi DB, Façanha AR (2008) Humic acids crossinteractions with root and organic acids. Ann Appl Biol 153(2):157–166. doi: 10.1111/j.1744-7348.2008.00249.x Google Scholar
  7. Canellas LP et al (2011) Probing the hormonal activity of fractionated molecular humic components in tomato auxin mutants. Ann Appl Biol 159:202–211. doi: 10.1111/j.1744-7348.2011.00487.x CrossRefGoogle Scholar
  8. Canellas LP et al (2013) A combination of humic substances and Herbaspirillum seropedicae inoculation enhances the growth of maize (Zea mays L.) Plant Soil 366(1):119–132. doi: 10.1007/s11104-012-1382-5 CrossRefGoogle Scholar
  9. Carletti P et al (2008) Protein expression changes in maize roots in response to humic substances. J Chem Ecol 34:804. doi: 10.1007/s10886-008-9477-4 CrossRefPubMedGoogle Scholar
  10. Curlango-Rivera G, Duclos DV, Ebolo JJ, Hawes MC (2010) Transient exposure of root tips to primary and secondary metabolites: impact on root growth and production of border cells. Plant Soil 332:267–275. doi: 10.1007/s11104-010-0291-8 CrossRefGoogle Scholar
  11. Driouich A et al. (2012) Unity is strength: the power of border cells and border-like cells in relation with plant defense. In: Secretions and Exudates in Biological Systems. Springer, pp 91–107Google Scholar
  12. Elbeltagy A et al (2001) Endophytic colonization and in planta nitrogen fixation by a Herbaspirillum sp. isolated from wild Rice species. Appl Environ Microbiol 67:5285–5293. doi: 10.1128/aem.67.11.5285-5293.2001 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Hawes M, Brigham L (1992) Impact of root border cells on microbial populations in the rhizosphere. Adv Plant Pathol 8:119–148Google Scholar
  14. Hawes MC, Lin H-J (1990) Correlation of pectolytic enzyme activity with the programmed release of cells from root caps of pea (Pisum sativum). Plant Physiol 94:1855–1859CrossRefPubMedPubMedCentralGoogle Scholar
  15. Hawes M, Brigham L, Wen F, Woo H, Zhu Y (1998) Function of root border cells in plant health: pioneers 1 in the rhizosphere. Annu Rev Phytopathol 36:311–327CrossRefPubMedGoogle Scholar
  16. Hawes MC, Gunawardena U, Miyasaka S, Zhao X (2000) The role of root border cells in plant defense. Trends Plant Sci 5:128–133. doi: 10.1016/S1360-1385(00)01556-9 CrossRefPubMedGoogle Scholar
  17. Hawes MC, Curlango-Rivera G, Xiong Z, Kessler JO (2012) Roles of root border cells in plant defense and regulation of rhizosphere microbial populations by extracellular DNA ‘trapping’. Plant Soil 355:1–16. doi: 10.1007/s11104-012-1218-3 CrossRefGoogle Scholar
  18. Humphris SN et al (2005) Root cap influences root colonisation by Pseudomonas fluorescens SBW25 on maize. FEMS Microbiol Ecol 54:123–130. doi: 10.1016/j.femsec.2005.03.005 CrossRefPubMedGoogle Scholar
  19. James EK, Olivares FL (1998) Infection and colonization of sugar cane and other Graminaceous plants by endophytic Diazotrophs. Crit Rev Plant Sci 17:77–119. doi: 10.1080/07352689891304195 CrossRefGoogle Scholar
  20. James E, Reis V, Olivares F, Baldani J, Döbereiner J (1994) Infection of sugar cane by the nitrogen-fixing bacterium Acetobacter diazotrophicus. J Exp Bot 45:757–766CrossRefGoogle Scholar
  21. James E, Olivares F, Baldani J, Döbereiner J (1997) Herbaspirillum, an endophytic diazotroph colonizing vascular tissue 3Sorghum bicolor L. Moench. J Exp Bot 48:785–798CrossRefGoogle Scholar
  22. James EK et al (2002) Infection and colonization of rice seedlings by the plant growth-promoting bacterium Herbaspirillum seropedicae Z67. Mol Plant-Microbe Interact 15:894–906CrossRefPubMedGoogle Scholar
  23. Monteiro RA et al (2008) Early colonization pattern of maize (Zea mays L. Poales, Poaceae) roots by Herbaspirillum seropedicae (Burkholderiales, Oxalobacteraceae). Genet Mol Biol 31:932–937CrossRefGoogle Scholar
  24. Mora V, Baigorri R, Bacaicoa E, Zamarreño AM, García-Mina JM (2012) The humic acid-induced changes in the root concentration of nitric oxide, IAA and ethylene do not explain the changes in root architecture caused by humic acid in cucumber. Environ Exp Bot 76:24–32. doi: 10.1016/j.envexpbot.2011.10.001 CrossRefGoogle Scholar
  25. Nardi S, Carletti P, Pizzeghello D, Muscolo A (2009) Biological activities of humic substances. In: Senesi N, Xing B, Huang PM (eds) Biophysico-chemical processes involving natural nonliving organic matter in environmental systems. John Wiley & Sons, Inc., Hoboken. doi: 10.1002/9780470494950.ch8
  26. Njoloma JP, Oota M, Saeki Y, Akao S (2005) Detection of gfp expression from gfp-labelled bacteria spot inoculated onto sugarcane tissues. Afr J Biotechnol 4:1372–1377Google Scholar
  27. Olivares F, James E, Baldani J, Döbereiner J (1997) Infection of mottled stripe disease-susceptible and resistant sugar cane varieties by the endophytic diazotroph. Herbaspirilium New Phytologist 135:723–737CrossRefGoogle Scholar
  28. Pan J-W, Zhu M-Y, Peng H-Z, Wang L-L (2002) Developmental regulation and biological functions of root border cells in higher plants ACTA BOTANICA SINICA-CHINESE EDITION 44:1–8Google Scholar
  29. Piccolo A (1996) Humic substances in terrestrial ecosystems. Elsevier, Amsterdam, 675 ppGoogle Scholar
  30. Piccolo A (2002) The supramolecular structure of humic substances: a novel understanding of humus chemistry and implications in soil science. Adv Agron 75:57–134CrossRefGoogle Scholar
  31. Piccolo A (2012) The nature of soil organic matter and innovative soil managements to fight global changes and maintain agricultural productivity. In: Piccolo A (ed) Carbon sequestration in agricultural soils: a multidisciplinary approach to innovative methods. Springer Berlin Heidelberg, Berlin, pp 1–19. doi: 10.1007/978-3-642-23385-2_1 CrossRefGoogle Scholar
  32. Piccolo A, Spaccini R, Nieder R, Richter J (2004) Sequestration of a biologically labile organic carbon in soils by humified organic matter. Clim Chang 67:329–343CrossRefGoogle Scholar
  33. Puglisi E et al (2008) Carbon deposition in soil rhizosphere following amendments with compost and its soluble fractions, as evaluated by combined soil–plant rhizobox and reporter gene systems. Chemosphere 73:1292–1299. doi: 10.1016/j.chemosphere.2008.07.008 CrossRefPubMedGoogle Scholar
  34. Puglisi E et al (2009) Effects of a humic acid and its size-fractions on the bacterial community of soil rhizosphere under maize (Zea mays L.) Chemosphere 77:829–837. doi: 10.1016/j.chemosphere.2009.07.077 CrossRefPubMedGoogle Scholar
  35. Puglisi E et al (2013) Rhizosphere microbial diversity as influenced by humic substance amendments and chemical composition of rhizodeposits. J Geochem Explor 129:82–94. doi: 10.1016/j.gexplo.2012.10.006 CrossRefGoogle Scholar
  36. Quaggiotti S, Ruperti B, Pizzeghello D, Francioso O, Tugnoli V, Nardi S (2004) Effect of low molecular size humic substances on nitrate uptake and expression of genes involved in nitrate transport in maize (Zea mays L.) J Exp Bot 55:803–813CrossRefPubMedGoogle Scholar
  37. Roncato-Maccari LD et al (2003) Root colonization, systemic spreading and contribution of Herbaspirillum seropedicae to growth of rice seedling. Symbiosis 35:261–270Google Scholar
  38. Silva LG, Miguens FC, Olivares FL (2003) Herbaspirillum seropedicae and sugarcane endophytic interaction investigated by using high pressure freezing electron microscopy. Braz J Microbiol 34:69–71CrossRefGoogle Scholar
  39. Spaccini R, Piccolo A, Haberhauer G, Gerzabek M (2000) Transformation of organic matter from maize residues into labile and humic fractions of three European soils as revealed by 13C distribution and CPMAS-NMR spectra. Eur J Soil Sci 51:583–594CrossRefGoogle Scholar
  40. Spaccini R, Piccolo A, Conte P, Haberhauer G, Gerzabek M (2002) Increased soil organic carbon sequestration through hydrophobic protection by humic substances. Soil Biol Biochem 34:1839–1851CrossRefGoogle Scholar
  41. Stephenson MB, Hawes MC (1994) Correlation of pectin methylesterase activity in root caps of pea with root border cell separation. Plant Physiol 106:739–745CrossRefPubMedPubMedCentralGoogle Scholar
  42. Trevisan S, Botton A, Vaccaro S, Vezzaro A, Quaggiotti S, Nardi S (2011) Humic substances affect Arabidopsis physiology by altering the expression of genes involved in primary metabolism, growth and development. Environ Exp Bot 74:45–55. doi: 10.1016/j.envexpbot.2011.04.017 CrossRefGoogle Scholar
  43. Wen F, Zhu Y, Hawes MC (1999) Effect of pectin methylesterase gene expression on pea root development. Plant Cell 11:1129–1140CrossRefPubMedPubMedCentralGoogle Scholar
  44. Willemsen V et al (2008) The NAC domain transcription factors FEZ and SOMBRERO control the orientation of cell division plane in Arabidopsis root stem cells. Dev Cell 15:913–922CrossRefPubMedGoogle Scholar
  45. Zandonadi DB, Canellas LP, Façanha AR (2007) Indolacetic and humic acids induce lateral root development through a concerted plasmalemma and tonoplast H+ pumps activation. Planta 225:1583–1595. doi: 10.1007/s00425-006-0454-2 CrossRefPubMedGoogle Scholar
  46. Zhu Y, Pierson LS III, Hawes MC (1997) Induction of microbial genes for pathogenesis and symbiosis by chemicals from root border cells. Plant Physiol 115:1691–1698CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2017

Authors and Affiliations

  • Luciano Pasqualoto Canellas
    • 1
  • Fabio Lopes Olivares
    • 1
  1. 1.Núcleo de Desenvolvimento de Insumos Biológicos para a Agricultura (NUDIBA)Universidade Estadual do Norte Fluminense Darcy Ribeiro (UENF)Rio de JaneiroBrazil

Personalised recommendations