CONCLUSION
The inoculum ofR. clarusevaluated was very competitive against endogenous AMF and also increased plant growth and yield.
R. clarus obtained in vitroand tested in the field was efficient in starting early AMF infection in seedlings, improving AM colonization in soybean and cotton. The inoculum ofR. clarus helped plants to take up P from fertilizer and showed high potential for use in combination with conventional fertilization, for intensive agriculture system in large areas in tropical soils, increasing P absorption and more efficient fertilization use, this is fundamental for the actual challenge of crops production.
AUTHOR CONTRIBUTIONS
All authors listed, have made substantial, direct and intellectual contribution to the work, and approved it for publication.
FUNDING
The National Council of Scientific and Technological Development (CNPq) who made this study possible by awarding PIBIC, MSc., Ph.D. and Productivity in Research grants.
and wheat root growth and properties. Field Crops. Res. 166, 1–19. doi:
10.1016/j.fcr.2014.06.016
Miransari, M. (2011). Soil microbes and plant fertilization. Appl. Microbiol.
Biotechnol.92, 875–885. doi: 10.1007/s00253-011-3521-y
Murphy, J., and Riley, J. P. A. (1962). Modified single solution method for the determination of phosphate in natural waters.Anal. Chim. Acta27, 31–36. doi:
10.1016/S0003-2670(00)88444-5
Neumann, E., and George, E. (2010). “Nutrient uptake: the arbuscular mycorrhiza fungal symbiosis as a plant nutrient acquisition strategy,” in Arbuscular Mycorrhizas: Physiology and Function, eds H. Koltai and Y. Kapulnik (New York, NY: Springer), 137–167.
Öpik, M., and Moora, M. (2012). Missing nodes and links in mycorrhizal networks.
New Phytol.194, 304–306. doi: 10.1111/j.1469-8137.2012.04121.x
Ortas, I. (2012). The effect of mycorrhizal fungal inoculation on plant yield, nutrient uptake and inoculation effectiveness under long-term field conditions. Field Crop. Res. 125, 35–48. doi: 10.1016/j.fcr.2011.
08.005
Pellegrino, E., Bedini, S., Avio, L., Bonari, E., and Giovannetti, M. (2011). Field inoculation effectiveness of native and exotic arbuscular mycorrhizal fungi in a Mediterranean agricultural soil. Soil Biol. Biochem. 43, 367–376. doi:
10.1007/s00572-014-0600-9
Pellegrino, E., Turrini, A., Gamper, H. A., Cafa, G., Bonari, E., Young, J. P. W., et al.
(2012). Establishment, persistence and effectiveness of arbuscular mycorrhizal fungal inoculants in the field revealed using molecular genetic tracing and measurement of yield components.New Phytol.94, 810–822.
Phillips, J., and Hayman, D. (1970). Improved producers for clearing roots and vesicular arbuscular mycorrhizal fungi for rapid assessment of infection.Trans.
Br. Mycol. Soc.55, 158–160. doi: 10.1016/S0007-1536(70)80110-3
Plenchette, C., Fortin, J. A., and Furlan, V. (1983). Growth responses of several plant species to mycorrhizae in a soil of moderate P-fertility:
mycorrhizal dependency under field conditions.Plant Soil70, 199–209. doi:
10.1007/BF02374780
Rillig, M. C. (2004). Arbuscular mycorrhizae, glomalin, and soil aggregation.Can.
J. Soil. Sci.84, 355–363. doi: 10.4141/S04-003
Romero, C. C., and Bago, A. (2010). Inoculante Aséptico de Micorrización y Procedimientos de Aplicación en Condiciones In Vitro y Ex Vitro. Patent WO 2007/014974
Sarruge, J. R., and Haag, H. P. (1974).Analises Químicas em Plantas. Piracicaba:
Escola Superior de Agricultura Luiz de Queiroz.
Schroeder, M. S., and Janos, D. P. (2005). Plant growth, phosphorus nutrition, and root morphological responses to arbuscular mycorrhizas,
phosphorus fertilization, and intraspecific density.Mycorrhiza15, 203–221. doi:
10.1007/s00572-004-0324-3
Smith, S. E., and Smith, F. A. (2011). Mycorrhizas in plant nutrition and growth:
new paradigms from cellular to ecosystem scales.Annu. Rev. Plant. Biol.62, 227–250. doi: 10.1146/annurev-arplant-042110-103846
Smith, S. E., Smith, F. A., and Jakobsen, I. (2003). Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses.Plant Physiol.133, 16–20. doi: 10.1104/pp.103.024380
Taffouo, V. D., Ngwene, B., Akoa, A., and Franken, P. (2013). Influence of phosphorus application and arbuscular mycorrhizal inoculation on growth, foliar nitrogen mobilization, and phosphorus partitioning in cowpea plants.
Mycorrhiza24, 361–368. doi: 10.1007/s00572-013-0544-5
Thompson, J. P., Seymour, N. P., and Clewett, T. G. (2012). Stunted cotton (Gossypium hirsutumL.) fully recovers biomass and yield of seed cotton after delayed root inoculation with spores of an arbuscular mycorrhizal fungus (Glomus mosseae).Australas. Plant Pathol.41, 431–437. doi: 10.1007/s13313- 012-0137-3
Tilman, D., Cassman, K. G., Matson, P. A., Naylor, R., and Polasky, S. (2002).
Agricultural sustainability and intensive production practices. Nature 418, 671–677. doi: 10.1038/nature01014
Verbruggen, E., van der Heijden, M. G. A., Rillig, M. C., and Kiers, T. (2013).
Mycorrhizal fungal establishment in agricultural soils: factors determining inoculation success. New Phytol. 197, 1104–1109. doi: 10.1111/j.1469- 8137.2012.04348.x
Xie, X., Wenga, B. D., Cai, B., Dong, Y., and Yan, C. (2014). Effects of arbuscular mycorrhizal inoculation and phosphorus supply on the growth and nutrient uptake of Kandelia obovata seedlings in autoclaved soil. Appl. Soil Ecol. 75, 162–171. doi: 10.1016/j.apsoil.2013.
11.009
Conflict of Interest Statement: The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Copyright © 2016 Cely, de Oliveira, de Freitas, de Luca, Barazetti, dos Santos, Gionco, Garcia, Prete and Andrade. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
Edited by:
Mohamed Hijri, Université de Montréal, Canada
Reviewed by:
Raffaella Balestrini, National Research Council, Italy Christian Staehelin, Sun Yat-sen University, China
*Correspondence:
Galdino Andrade [email protected]
Specialty section:
This article was submitted to Plant Biotic Interactions, a section of the journal Frontiers in Plant Science
Received:27 June 2016 Accepted:31 October 2016 Published:22 November 2016 Citation:
Cely MVT, Siviero MA, Emiliano J, Spago FR, Freitas VF, Barazetti AR, Goya ET, Lamberti GdS, dos Santos IMO, De Oliveira AG and Andrade G (2016) Inoculation of Schizolobium parahyba with Mycorrhizal Fungi and Plant Growth-Promoting Rhizobacteria Increases Wood Yield under Field Conditions. Front. Plant Sci. 7:1708.
doi: 10.3389/fpls.2016.01708
Inoculation of Schizolobium
parahyba with Mycorrhizal Fungi and Plant Growth-Promoting
Rhizobacteria Increases Wood Yield under Field Conditions
Martha V. T. Cely1, Marco A. Siviero2, Janaina Emiliano1, Flávia R. Spago1,
Vanessa F. Freitas1, André R. Barazetti1, Erika T. Goya1, Gustavo de Souza Lamberti1, Igor M. O. dos Santos1, Admilton G. De Oliveira1and Galdino Andrade1*
1Laboratório de Ecologia Microbiana, Departamento de Microbiologia, Universidade Estadual de Londrina, Londrina, Brazil,
2Grupo Arboris-Manejo Florestal, Dom Eliseu, Brazil
Schizolobium parahyba var. amazonicum (Huber ex Ducke) occurs naturally in the Brazilian Amazon. Currently, it is being planted extensively because of its fast growth and excellent use in forestry. Consequently, there is great interest in new strategies to increase wood production. The interaction between soil microorganisms and plants, specifically in the roots, provides essential nutrients for plant growth. These interactions can have growth-promoting effects. In this way, this study assessed the effect of the inoculation with arbuscular mycorrhizal fungi (AMF) and plant growth-promoting rhizobacteria (PGPR) on growth ofS. parahybavar.amazonicumunder field conditions.
We used two native species of arbuscular mycorrhizal fungi,Claroideoglomus etunicatum (Ce), andAcaulosporasp. (Ac); two native strains ofRhizobiumsp. (Rh1 and Rh2); and a non-native strain ofBurkholderiasp. Different combinations of microorganisms were supplemented with chemical fertilizers (doses D1 and D2) in two planting methods, seed sowing and seedling planting. In seed sowing, the results showed that treatments with Ce/Rh1/Fertilizer D2 and Ac/No PGPR/Fertilizer D2 increased wood yield. In seedling planting, two combinations (Ac/Rh2/Fertilizer D1 and Ac/Rh1/Fertilizer D1) were more effective in increasing seedling growth. In these experiments, inoculation with AMF and PGPR increased wood yield by about 20% compared to the application of fertilizer alone.
Keywords: microorganism interaction, reforestation, Amazon forest, Schizolobium parahyba, mycorrhizal inoculant
INTRODUCTION
The negative impacts of agro-industrial development and wood exploitation in native forest areas have encouraged the development of projects focused on reforestation with homogeneous stands or intercropped species of rapid growth and high commercial value. These strategies are directed at degraded areas with the objective of forest restoration or wood production. The family Leguminosae is one of the most representative in terms of number and frequency of plant species in the Amazon region of Brazil (Silva et al., 1988). Some tree species (nodulating and non-nodulating)
Ducke), belonging to the family Leguminosae and subfamily Caesalpinioideae, is a non-nodulating species native to the Amazon. It is considered an ecologically and economically important species due to its significant wood potential; its commercial potential has been exploited since the 1970s. Today, it is the native species most planted in the Brazilian states of Amazonia, Pará, Maranhão, and Rondonia, covering 87,901 ha (ABRAF, 2012). Due to its fast growth, S. parahyba var.
amazonicum can reach an annual wood yield of 30 m3 ha−1 year−1 with 6 years of age (Carvalho, 2007). Moreover, it is considered an important species for carbon sequestration because it produces high levels of biomass in a short period of time (Siviero et al., 2008). The quality of its wood is suitable for furniture and plywood production.
The choice of plant species that are used for restoration and wood production in degraded lands represents a great challenge, because these species need to be able to survive under conditions of low soil fertility. These restrictive factors for plant growth can be attenuated by the action of efficient soil microorganisms such as plant growth-promoting rhizobacteria (PGPR) and arbuscular mycorrhizal fungi (AMF;Chaer et al., 2011). The microbial community in the soil plays an important role in the sustainability of plant communities (Andrade, 2004).
The interaction between microorganisms and plants, specifically in the roots, provides for important nutritional requirements of plants and also the microorganisms associated with them. Thus, as the roots directly affect the surrounding microbial populations, the microorganisms present in the rhizosphere can also influence plant growth (Giri et al., 2005).
PGPR are microorganisms that colonize the rhizosphere and promote plant growth. Among them, the N-fixing bacteria (NFB) such asRhizobium species can establish symbiosis with leguminous plant species, resulting in a beneficial interaction for plant growth. Some diazotrophic bacteria can help plant nutrition through biological fixation of N2 or production of phytohormones (Vessey, 2003). AMF, associated with plant roots, increase the uptake of soil inorganic nutrients, mainly P (Neumann and George, 2010). In addition, other benefits related to AMF are the stabilization of soil aggregates (Rillig, 2004), increasing resistance to water stress (Garg and Chandel, 2010) and protection against pathogens (Jung et al., 2012). In the mycorrhizosphere, the soil surrounding the roots and fungal hyphae (Artursson et al., 2006), AMF can interact with PGPR bacterial species, as well as with endophytic bacteria. Some belong to the genus Burkholderia (Bianciotto and Bonfante, 2002). These interactions can provide potential benefits for plant development. The inoculation of compatible combinations of PGPR and AMF in forest and agricultural systems may result in a significant increase in plant growth (Biró et al., 2000;
Nadeem et al., 2014; Hashem et al., 2016). Many studies (Marques et al., 2001; Valdenegro et al., 2001; Patreze and Cordeiro, 2004) have demonstrated the synergistic effect of the inoculation of Rhizobium and AMF in promoting nodulated legume tree
S. parahybavar.amazonicumis a non-nodulating legume, and Rhizobium bacteria may promote plant growth in this species in two ways. Some authors suggest that non-nodulating species of the family Leguminoseae can profit from N fixed by root- associated bacteria (rhizosphere bacteria or endophytes) like nodulating species (Bryan et al., 1996; Van Sambeek et al., 2007).
On the other hand, it can be assumed that theRhizobiumact as plant growth-promoting bacteria in the rhizosphere and release phytohormones (Mehboob et al., 2012).
The use of growth-promoting microorganisms inS. parahyba var. amazonicum was assessed by Siviero et al. (2008), who showed that this species displays a positive response to inoculation with AMF in combination with N-fixing bacteria isolated from another plant species (exogenous, i.e., non-native bacteria). The authors observed differences between planting methods (seeds or seedlings) in inoculated plants. In the planting method with seeds, only AMF (Glomus intrarradices) inoculation increased biomass and wood production. In the planting method with seedlings, the dual inoculation of AMF (Glomus clarum) and PGPR (LEM6 or Rhi1Rhizobiumstrains) was more effective.
In this work, the authors suggested that the selection of native microorganisms is very important to obtain the best results in the field.
Our hypothesis was that the inoculation with indigenous microorganisms is more effective in promoting plant growth of S. parahybavar.amazonicum, and that the presence of inoculum would help plant roots to be more effective in using the chemical fertilizer applied. Therefore, this study assessed the effect on wood production, comparing inoculation with two indigenous AMF (Claroideoglomus etunicatumandAcaulosporasp.) isolated from S. parahyba var. amazonicum roots in interaction with three bacterial strains (two indigenousRhizobiumspp. and one exogenous Burkholderia sp.). The inoculation with different combinations of microorganisms and the addition of chemical fertilizer was investigated using a completely randomized block experiment. The effect of these factors on S. parahyba var.
amazonicumgrowth was determinedin situover 2 years.