Production of border cells and colonization of maize root tips by Herbaspirillum seropedicae are modulated by humic acid
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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.
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.
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.
The population of H. seropedicae strain RAM10 colonizing root caps and BCs increased in response to exogenous humic acids.
KeywordsRoot tip Humic substances Nitrogen-fixing bacteria Plant-bacteria interactions Plant growth-promoting bacteria
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.
- 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
- 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
- Hawes M, Brigham L (1992) Impact of root border cells on microbial populations in the rhizosphere. Adv Plant Pathol 8:119–148Google Scholar
- 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
- 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
- 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
- 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
- Piccolo A (1996) Humic substances in terrestrial ecosystems. Elsevier, Amsterdam, 675 ppGoogle Scholar
- 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
- 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