Accessibility / Report Error

Occurrence of symbiotic fungi and rhizospheric phosphate solubilization in weeds

Ocorrência de fungos simbiontes e solubilização rizosférica de fosfato em plantas daninhas

Abstracts

Studies on the ecology of the organisms involved in the production process are necessary for the development of sustainable agriculture, and sustainability is currently closely linked to the profitability of production. The objective of this study was to verify the occurrence of arbuscular mycorrhizal fungi in weeds infesting Brazilian crops and to evaluate the inorganic phosphate solubilization potential of the associated microbiota. A total of 36 weed species were evaluated for the occurrence of mycorrhizae; of these, 11 were selected to evaluate their potential for total and relative phosphate solubilization. All of the species demonstrated mycorrhizal colonization, including a member of the Brassicaceae family, which is usually assumed to be non-mycorrhizal. In most of the species, morphological types of arbuscular and coiled hyphae were observed, with the coiled hyphae being the most common in the grasses. Dark septate endophytic fungi were observed in most of the plants. The weeds presented different potentials for P solubilization in the rhizosphere; Amaranthus retroflexus, Bidens pilosa and Leonotis nepetaefolia showed high values of relative phosphate solubilization. This is the first report on the mycorrhizae and phosphate solubilization activity in weeds in Brazil.

arbuscular mycorrhiza; dark septate endophytes; Sinapis arvensis L.; microbial biomass; phosphate solubilizers


Estudos sobre a ecologia de organismos envolvidos no processo de produção são necessários para o desenvolvimento de uma agricultura sustentável, e hoje, a sustentabilidade está intimamente ligada à rentabilidade de produção. Objetivou-se com este trabalho verificar a ocorrência de fungos micorrízicos arbusculares em plantas daninhas de lavouras brasileiras e avaliar o potencial de solubilização de fosfato inorgânico da microbiota associada. 36 espécies de plantas daninhas foram avaliadas quanto à ocorrência de micorrizas, e 11 foram selecionadas para avaliação do potencial de solubilização total e relativa de fosfato. Todas as espécies apresentaram colonização por micorrizas, inclusive um exemplar da família Brassicaceae, geralmente enquadrada como não micorrizada. Na maioria das espécies, os tipos morfológicos de arbúsculos e enovelados de hifas foram observados, sendo os enovelados mais comuns entre as gramíneas. Fungos endofíticos do tipo dark septate foram visualizados na maioria das plantas. As plantas daninhas apresentaram distintos potenciais de solubilização de P na rizosfera. Amaranthus retroflexus, Bidens pilosa e Leonotis nepetaefolia apresentaram elevados valores de solubilização relativa de fosfato. Este é o primeiro relato de micorrizas e da atividade de solubilização de fosfato em plantas daninhas no Brasil.

micorriza arbuscular; endofíticos dark septate; Sinapis arvensis L.; biomassa microbiana; solubilizadores de fosfato


AGRICULTURAL MICROBIOLOGY

Occurrence of symbiotic fungi and rhizospheric phosphate solubilization in weeds

Ocorrência de fungos simbiontes e solubilização rizosférica de fosfato em plantas daninhas

Edson Aparecido dos SantosI, * * Author for correspondence. E-mail: edsonapsant@yahoo.com.br ; Lino Roberto FerreiraII; Maurício Dutra CostaII; Marliane de Cássia Soares da SilvaII; Marcelo Rodrigues dos ReisII; André Cabral FrançaIII

IUniversidade Estadual Paulista, Via de Acesso Prof. Paulo Donato Castellane, s/n, Jaboticabal, São Paulo, Brazil

IIUniversidade Federal de Viçosa, Viçosa, Minas Gerais, Brazil

IIIUniversidade Federal dos Vales do Jequitinhonha e Mucuri, Diamantina, Minas Gerais, Brazil

ABSTRACT

Studies on the ecology of the organisms involved in the production process are necessary for the development of sustainable agriculture, and sustainability is currently closely linked to the profitability of production. The objective of this study was to verify the occurrence of arbuscular mycorrhizal fungi in weeds infesting Brazilian crops and to evaluate the inorganic phosphate solubilization potential of the associated microbiota. A total of 36 weed species were evaluated for the occurrence of mycorrhizae; of these, 11 were selected to evaluate their potential for total and relative phosphate solubilization. All of the species demonstrated mycorrhizal colonization, including a member of the Brassicaceae family, which is usually assumed to be non-mycorrhizal. In most of the species, morphological types of arbuscular and coiled hyphae were observed, with the coiled hyphae being the most common in the grasses. Dark septate endophytic fungi were observed in most of the plants. The weeds presented different potentials for P solubilization in the rhizosphere; Amaranthus retroflexus, Bidens pilosa and Leonotis nepetaefolia showed high values of relative phosphate solubilization. This is the first report on the mycorrhizae and phosphate solubilization activity in weeds in Brazil.

Keywords: arbuscular mycorrhiza, dark septate endophytes, Sinapis arvensis L., microbial biomass, phosphate solubilizers.

RESUMO

Estudos sobre a ecologia de organismos envolvidos no processo de produção são necessários para o desenvolvimento de uma agricultura sustentável, e hoje, a sustentabilidade está intimamente ligada à rentabilidade de produção. Objetivou-se com este trabalho verificar a ocorrência de fungos micorrízicos arbusculares em plantas daninhas de lavouras brasileiras e avaliar o potencial de solubilização de fosfato inorgânico da microbiota associada. 36 espécies de plantas daninhas foram avaliadas quanto à ocorrência de micorrizas, e 11 foram selecionadas para avaliação do potencial de solubilização total e relativa de fosfato. Todas as espécies apresentaram colonização por micorrizas, inclusive um exemplar da família Brassicaceae, geralmente enquadrada como não micorrizada. Na maioria das espécies, os tipos morfológicos de arbúsculos e enovelados de hifas foram observados, sendo os enovelados mais comuns entre as gramíneas. Fungos endofíticos do tipo dark septate foram visualizados na maioria das plantas. As plantas daninhas apresentaram distintos potenciais de solubilização de P na rizosfera. Amaranthus retroflexus, Bidens pilosa e Leonotis nepetaefolia apresentaram elevados valores de solubilização relativa de fosfato. Este é o primeiro relato de micorrizas e da atividade de solubilização de fosfato em plantas daninhas no Brasil.

Palavras-chave: micorriza arbuscular, endofíticos dark septate, Sinapis arvensis L., biomassa microbiana, solubilizadores de fosfato.

Introduction

Agricultural ecosystem sustainability is as desirable as high productivity and profitability. According to Kitamura (2003), the future of agriculture demands innovations in conventional intensive practices and, consequently, more responsibility with regard to the environment. However, sustainable techniques in agricultural production must be based on studies on the ecology of the populations involved. It is noteworthy that crops suffer interference from many organisms and that greater importance has been given to weeds, which present a high aggressiveness that is often conditioned by the high soil-use capacity (RADOSEVICH et al., 1997). This fact has attracted special interest with regard to the many processes occurring at the soil/root interface, and many of these processes are unknown due to the intense participation of several edaphic organisms, other than plants, in competition (ASAEDA et al., 2011; LI et al., 2007).

In respect of crops, weed competitive advantage in the field may result from the interaction with different groups of soil microorganisms (REINHART; CALLAWAY, 2006). The interaction between plants and two groups of fungi, Arbuscular Mycorrhizal Fungi (AMFs) and Dark Septate Endophytes (DSEs), provide more efficient use of the available resources in plants (ZAK et al., 2003). AMFs provide plants with a higher absorption of nutrients and water and protection against pathogens and toxic elements in the soil (HERRMAN et al., 2004). AMFs are strongly affected by their host plants, and this association has been classified as vital in the structuring among plant species (WARDLE, 2002). Although many attributes of DSEs are similar to those of mycorrhizae, their function has not yet been clarified and demands further study (LINGFEI et al., 2005). Detmann et al. (2008) report a high frequency of DSEs in the plants of the Brazilian savannah, revealing the adaptive character of these fungi to adverse conditions.

Two morphological types of symbiosis between AMFs and plants have been distinguished-Arum and Paris-as first described by Gallaud (1905). The former is characterized by the distribution of hyphae throughout the cortex, extracellularly, spreading along the apoplast, and the formation of arbuscules. In contrast, the Paris-type is characterized by the extensive development of intracellular mycelia, forming coils that may or may not be interspersed with arbuscular hyphae. Yamato (2004) showed the importance of defining the main factor acting on their morphologies, as the functional differences between the two groups are not known with certainty.

In the rhizosphere environment, a portion of the microbial biomass excretes organic acids that dissolve rock phosphate or phosphate precipitated in the soil with Al, Ca, and Fe by the chelation of the cations that accompany the phosphate anion, thus releasing P (KUCEY, 1983). The activity of these phosphate-solubilizing microorganisms is affected by the soil management and vegetation (NAHAS et al., 1994; SOUCHIE et al., 2005). Thus, Reis et al. (2008) proposed the use of a quotient to evaluate the efficiency of the phosphate-solubilization activity per microbial biomass unit, defined as the relative inorganic phosphate solubilization (RIPS). The quotient is calculated by dividing the amount of inorganic P released by the units of microbial biomass in the rhizosphere. The RIPS allows the identification of plants that host microbiota that are more efficient in promoting phosphate solubilization in the rhizosphere.

The elucidation of these symbiotic associations and their role in the interactions of competition between weeds and crops may contribute to the development of more sustainable management practices. Thus, the present work aimed to (1) verify whether arbuscular mycorrhizal fungi and dark septate endophytic fungi are present in weeds and (2) determine whether the rhizosphere microbiota of the evaluated weeds presented differences in their microbial phosphate-solubilization potential.

Material and methods

In January and February of 2009, we collected 36 species of plants belonging to 14 botanical families, which are considered weeds for the most important Brazilian agricultural crops. The plants were collected during full flowering, which is considered to be the stage when increased symbiotic activity occurs (SMITH; READ, 1997). The 0.8 ha collection site, 650 meters above sea level, was located in the city of Viçosa, Minas Gerais State, Brazil, at lat 20º 46' 00" S and long 42º 52' 04" W. This site had not been subjected to the application of pesticides in the six years prior to the collection. A square shovel was used to collect the plants to preserve the soil mass adhered to the roots, and the sample was placed in 5.0 L buckets and transported to the laboratory for botanical identification. At least three plants per species were collected when found isolated, i.e., without the interference of other plants.

After the botanical identification, the roots were separated from the soil and washed in running water. The samples of roots were grouped according to their species and sectioned into fragments of 1.0 to 2.0 cm. A sample of 1.0 g of the fragments was preserved in formaldehyde:ethanol:acetic acid (FAA) solution with a 5:90:5 ratio. The fragments were washed and clarified with 10% KOH and subjected to trypan blue staining. The observation of fungal structures was performed according to Giovannetti and Mosse (1980). The root fragments were observed in Petri dishes using a binocular stereoscope with a magnification of 40x. Thus, the most characteristic fragments were selected for the preparation of slides for observation using an optical microscope (Olympus BX50). The fungal structures were photographed with a Qcolor 3 Olympus digital camera using the QCapture Pro 6.0.0.412 software system. The presence of mycorrhizae was assessed by the observation of their structures, such as arbuscules, vesicles, spores and hyphae, and the occurrence of DSEs was determined by the observation of microesclerotia.

According to phytosociological relevance in the area, 11 of the species were selected for the evaluation of the phosphate-solubilization potential of the rhizosphere microbiota and were used to determine the microbial biomass carbon in compliance with Mueller-Dombois and Ellenberg (1974). To estimate the solubilization potential, 1.0 g of rhizosphere soil (fresh weight) was transferred to a test tube containing NBRIP liquid medium, pH 6.8-7.0, composed of the following (g L-1): glucose, 10; Ca3(PO4)2, 5; MgCl2.6H2O, 0.5; MgSO4.7H2O, 0,25; KCl, 0.2; and (NH4)2SO4, 0.1 (NAUTIYAL, 1999). After the incubation of the samples for 15 days at 27ºC, the liquid phase was centrifuged at 5,008 x g for 20 minutes, and the quantity of inorganic P was determined in the supernatant by the colorimetric method of vitamin C, according to Braga and Defelipo (1974).

To estimate the microbial biomass, the method described by Vance et al. (1987), as modified by Islam and Weil (1998), was used. The relative solubilization quotient was determined by dividing the value of the solubilized P by the microbial biomass.

Where appropriate, experiments were performed with four replicates. The data were subjected to an analysis of variance, and the means were grouped by Scott-Knott test at a 5% probability.

Results and discussion

The colonization by arbuscular mycorrhizal fungi was observed for all 36 species, as characterized by the presence of vesicles, hyphae, arbuscules, hyphal coils and fungal spores. Moreover, auxiliary vesicles in the roots of Eupatorium urticaefolium and the spores of Panicum maximum were observed. Hyphal coils were more frequently observed in the root system of the species evaluated, compared to arbuscules, which were not observed among the grasses. In Sinapis arvensis L., a species of the Brassicaceae family, vesicles, hyphae, arbuscules and Arum-type mycorrhizal colonization were observed. The presence of DSEs was observed in 33% of the analyzed plant species, belonging to the following families: Amaranthaceae, Asteraceae, Convolvulaceae, Labiatae, Malvaceae, Solanaceae and Verbenaceae (Figure 1 and Table 1).


According to Smith and Smith (1997), the Arum arbuscular mycorrhizae are found in most angiosperms, whereas the Paris type is prevalent in gymnosperms. Environmental factors, such as temperature, light intensity and soil moisture, also determine the morphological type of the arbuscular mycorrhizae (CAVAGNARO et al., 2001). The results of Yamato and Iwasaki (2002) showed that the Arum type prevails in pioneer herbaceous plants and that the Paris-type occurs more frequently in herbaceous understory plants. In the present work, the Arum type was not observed in the grasses and only the botanic classification probably defined the colonization type, as the plants were found in the same environment.

In the literature, it has been reported that mycorrhizal association is rare or absent in certain botanical families, such as Brassicaceae, Proteaceae and Cyperaceae (LAMONT, 2003; SOUZA et al., 2006). However, the presence of arbuscular mycorrhizae in plants of the Proteaceae family in soil with high contents of nickel and low contents of phosphorus indicates that the botanical factor alone does not determine colonization (BOULET; LAMBERS, 2005). Similarly, Regvar et al. (2003) report the presence of hyphae, vesicles, coils and arbuscules in the roots of Thlaspi praecox, Thlaspi caerulescens and Thlaspi montanum, which belong to the Brassicaceae family. Carneiro et al. (2001) highlight mycorrhizal colonization in Brassicaceae (Brassica sp.) after the inoculation of spores or only by natural mycorrhizal colonization in an environment contaminated with heavy metals, indicating the importance of the environment in the process of the colonization of plants by AMFs. In the present work, the occurrence of AMFs associated with the roots of S. arvensis L. is reported for the first time under Brazilian conditions, which indicates the need of a more comprehensive survey on the occurrence of arbuscular mycorrhizae in weeds grouped in botanical families that are considered, thus far, to be non-mycorrhizal.

More than 600 plant species can associate with dark, septate, endophytic fungi, and their occurrence is related to abiotic factors, such as low humidity in the environment and the day length (BARROW; AALTONEN, 2001). Li and Guan (2007) reported a close relationship between DSEs and AMFs, suggesting competition or even cooperation between them. Confirming the association of the studied weeds with EDS, the biggest difficulty in the presentation of our results can be explained by the presence of certain components in the cell walls of those fungi that hinder their visualization in some plant species (BARROW; AALTONEN, 2001).

The evaluation of the plant's ability to solubilize phosphorus in the soil demonstrated that Bidens pilosa, Amaranthus retroflexus and Leonotis nepetaefolia presented higher potentials for solubilizing phosphate when compared to the other weed species (Figure 2). However, it must be stressed that, for all of the other species evaluated, the solubilization potential values were higher in the rhizosphere soil compared with the non-rhizosphere soil (Figure 2). L. nepetaefolia, B. pilosa, and A. retroflexus presented the best phosphate-solubilization potential (Figure 3) in relation to the rhizosphere biomass (relative solubilization).



Weeds have different capacities for nutrient absorption, depending on the availability of the elements; soils with high phosphorus contents favor weeds, to the detriment of crops (TOMASO, 1995). Part of this nutrient-absorption capacity is due to the presence of microorganisms associated with the rhizosphere. Santos et al. (2012) reported that the accumulation of macronutrients, mainly phosphorus, was impaired in B. pilosa in a fumigated substrate using an assay to assess the accumulation of macro- and micronutrients in the tissues of several weeds after substrate fumigation. The fumigation may have inhibited the growth of microorganisms in the substrate, thus hindering the absorption of nutrients by B. pilosa. Therefore, it can be inferred that plants with a high phosphate-solubilization potential due to the association with soil microorganisms should be considered for use in integrated pest management programs in crops, as they operate more efficiently in nutrient cycling, especially phosphorus cycling, which is a limiting element in tropical-soil agriculture.

Ronchi et al. (2003) compared the extraction of phosphorus by coffee plants and Bidens pilosa and found that this weed (B. pilosa) extracted ten times more phosphorus from the soil than the coffee crop. Our present results suggest a significant contribution of the rhizosphere microbiota to the supply of phosphorus for weeds and in their competitive potential with relation to cultivated plants. However, because mycorrhizal fungi do not colonize all weed species, some weeds may have their activity affected by the presence of mycorrhizae. This fact is evidenced in a study by Rinaudo et al. (2010) who found that the species Amaranthus retroflexus, Chenopodium album, Digitaria sanguinalis, Echinochloa crus-galli, Setaria viridis and Sinapis arvensis are hindered by the presence of Glomus mosseae, Glomus coronatum and Glomus intraradices mycorrhizal fungi.

The relative solubilization index allows inferences about the intrinsic characteristics of a species in relation to other species. In this work, L. nepetaefolia, B. pilosa and A. retroflexus presented associated microbiota that promoted higher values of phosphate-solubilization potential, suggesting better plant development and the higher accumulation of phosphorus.

Conclusion

All of the evaluated species presented colonization by arbuscular mycorrhizal fungi, a symbiosis that has advantages for weeds, including the better access to nutrients, water and protection against soil-borne pathogens. Under Brazilian conditions, these associations have not been previously documented. Furthermore, a greater ability to extract phosphorus and a greater efficiency in competing with the crops for soil resources was verified in the weeds that had higher potentials of microbial phosphate solubilization.

Acknowledgements

The authors would like to thank the National Council for Scientific and Technological Development for their financial support.

Received on October 17, 2011.

Accepted on February 4, 2012.

License information: This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

  • ASAEDA, T.; RASHID, M. D.; KOTAGIRI, S.; UCHIDA, T. The role of soil characteristics in the succession of two herbaceous lianas in a modified river floodplain. River Research and Applications, v. 27, n. 5, p. 591-601, 2011.
  • BARROW, J. R.; AALTONEN, R. E. Evaluation of the internal colonization of Atriplex canescens (Pursh) Nutt. roots by dark septate fungi and the influence of host physiological activity. Mycorrhiza, v. 11, n. 4, p. 199-205, 2001.
  • BOULET, F. M.; LAMBERS, H. Characterisation of arbuscular mycorrhizal fungi colonisation in cluster roots of Hakea verrucosa F. Muell (Proteaceae), and its effect on growth and nutrient acquisition in ultramafic soil. Plant and Soil, v. 269, n. 1, p. 357-367, 2005.
  • BRAGA, J. M.; DEFELIPO, B. V. Determinação espectrofotométrica de fósforo em extratos de solos e plantas. Revista Ceres, v. 6, n. 4, p. 73-85, 1974.
  • CARNEIRO, M. A. C.; SIQUEIRA, J. O.; MOREIRA, F. M. S. Estabelecimento de plantas herbáceas em solo com contaminação de metais pesados e inoculação de fungos micorrízicos arbusculares. Pesquisa Agropecuária Brasileira, v. 36, n. 12, p. 1443-1452, 2001.
  • CAVAGNARO, T. R.; SMITH, F. A.; LORIMER, M. F.; HASKARD, K. A.; AYLING, S. M.; SMITH, S. E. Quantitative development of Paris-type arbuscular mycorrhizas formed between Asphodelus fistulosus and Glomus coronatum New Phytologist, v. 149, n. 1, p. 105-113, 2001.
  • DETMANN, K.; DELGADO, M. N.; REBELLO, V. P. A.; LEITE, T. S.; AZEVEDO, A. A.; KASUYA, M. C. M.; ALMEIDA, A. M. Comparação de métodos para a observação de fungos micorrízicos arbusculares e endofíticos do tipo dark septate em espécies nativas de Cerrado. Revista Brasileira de Ciência do Solo, v. 32, n. 5, p. 1883-1890, 2008.
  • GALLAUD, I. Études sur les mycorrhizes endotrophes. Revue Générale de Botanique, v. 17, n. 1, p. 5-50, 1905.
  • GIOVANNETTI, M.; MOSSE, B. An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytollogist, v. 84, n. 3, p. 489-500, 1980.
  • HERRMAN, S.; OELMMULLER, R.; BUSCOT, F. Manipulation of the onset of ectomycorrhyza formation by indole-3-acetic acid, activated charcoal or relative humidity in the association between oak micronuttines and Piloderma croceum influence on plant development and photosynthesis. Journal of Plant Physiology, v. 161, n. 5, p. 509-517, 2004.
  • ISLAM, K. R.; WEIL, R. R. Microwave irradiation of soil four routine measurement of microbial biomass carbon. Biology and Fertility of Soils, v. 27, n. 4, p. 408-416, 1998.
  • KITAMURA, P. C. Agricultura Sustentável no Brasil: avanços e Perspectivas. Ciência e Ambiente, v. 27, n. 1, p. 7-28, 2003.
  • KUCEY, R. M. N. Phosphate-solubilizing bacteria and fungi in various cultivated and virgin Alberta soils. Canadian Journal of Soil Science, v. 63, n. 4, p. 671-678, 1983.
  • LAMONT, B. B. Structure, ecology and physiology of root clusters - a review. Plant and Soil, v. 248, n. 1-2, p. 1-19, 2003.
  • LI, A. R.; GUAN, K. Y. Mycorrhizal and dark septate endophytic fungi of pedicularis species from Northwest of Yunnan Province, China. Mycorrhiza, v. 17, n. 2, p. 103-110, 2007.
  • LI, L. F.; ZHANG, Y.; ZHAO, Z. W. Arbuscular mycorrhizal colonization and spore density across different land-use types in a hot and arid ecosystem, Southwest China. Journal of Plant Nutrition and Soil Science, v. 170, n. 3, p. 419-425, 2007.
  • LINGFEI, L.; ANNA, Y.; ZHIWEI, Z. Seasonality of arbuscular mycorrhizal symbiosis and dark septate endophytes in a grassland site in southwest China. FEMS Microbiol Ecology, v. 54, n. 3, p. 367-373, 2005.
  • MUELLER-DOMBOIS, D.; ELLENBERG, H. A. Aims and methods of vegetation ecology New York: John Wiley, 1974.
  • NAHAS, E.; CENTURION, J. F.; ASSIS, L. C. Microrganismos solubilizadores de fosfato e produtores de fosfatases de vários solos. Revista Brasileira de Ciência do Solo, v. 18, n. 3, p. 43-48, 1994.
  • NAUTIYAL, C. S. An efficient microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS Microbiology Letters, v. 170, n. 1, p. 265-270, 1999.
  • RADOSEVICH, S.; HOLT, J.; GHERS, A. C. Weed ecology: implications for management. 2nd ed. New York: Wiley, 1997.
  • REGVAR, M.; VOGEL, K.; IRGEL, N.; WRABER, T.; HILDEBRANDT, U.; WILDE, P.; BOTHE, H. Colonization of pennycresses (Thlaspi spp.) of the Brassicaceae by arbuscular mycorrhizal fungi. Journal of Plant Physiology, v. 160, n. 6, p. 615-662, 2003.
  • REINHART, K. O.; CALLAWAY, R. M. Soil biota and invasive plants. New Phytologist, v. 170, n. 3, p. 445-457, 2006.
  • REIS, M. R.; SILVA, A. A.; GUIMARÃES, A. A.; COSTA, M. D.; MASSENSSINI, A. M.; FERREIRA, E. A. Ação de herbicidas sobre microrganismos solubilizadores de fosfato inorgânico em solo rizosférico de cana-de-açúcar. Planta Daninha, v. 26, n. 2, p. 333-341, 2008.
  • RINAUDO, V.; BÀRBERI, B.; GIOVANNETTI, M.; VAN DER HEIJDEN, M. G. A. Mycorrhizal fungi suppress aggressive agricultural weeds. Plant Soil, v. 333, n. 1-2, p. 7-20, 2010.
  • RONCHI, C. P.; TERRA, A. A.; SILVA, A. A.; FERREIRA, L. R. Acúmulo de nutrientes pelo cafeeiro sob interferência de plantas daninhas. Planta Daninha, v. 21, n. 2, p. 219-227, 2003.
  • SANTOS, E. A.; FERREIRA, L. R.; COSTA, M. D.; SANTOS, J. B.; SILVA, M. C. S.; ASPIAZU, I. The effects of soil fumigation on the growth and mineral nutrition of weeds and crops. Acta Scientiarum. Agronomy, v.34, n.2, p.207-212, 2012.
  • SMITH, S. E.; READ, D. J. Mycorrhizal symbiosis London: Academic Press, 1997.
  • SMITH, F. A.; SMITH, S. E. Structural diversity in (vesicular)-arbuscular mycorrhizal symbioses. Tansley Review No. 96. New Phytologist, v. 137, n. 3, p. 373-388, 1997.
  • SOUCHIE, E. L.; AZCÓN, R.; BAREA, J. M.; SAGGIN-JÚNIOR, O. J.; SILVA, E. M. R. Phosphate solubilization in solid and liquid media by soil bacteria and fungi. Pesquisa Agropecuária Brasileira, v. 40, n. 11, p. 1149-1152, 2005.
  • SOUZA, V. C.; SILVA, A. R.; CARDOSO, G. D.; BARRETO, A. F. Estudos sobre fungos micorrízicos. Revista Brasileira de Engenharia Agrícola e Ambiental, v. 10, n. 3, p. 612-618, 2006.
  • TOMASO, J. M. Approaches for improving crop competitiveness through the manipulation of fertilization strategies. Weed Science, v. 43, n. 3, p. 491-497, 1995.
  • VANCE, E. D.; BROOKES, P. C.; JENKINSON, D. S. An extraction method for measuring soil microbial biomass C. Soil Biology Biochemistry, v. 19, n. 6, p. 703-707, 1987.
  • WARDLE, D. A. Communities and ecosystems: linking aboveground and belowground components. Princeton: Princeton University Press, 2002.
  • YAMATO, M. Morphological types of arbuscular fungi in roots of weeds on vacant land. Mycorrhiza, v. 14, n. 2, p. 127-131, 2004.
  • YAMATO, M.; IWASAKI, M. Morphological types of arbuscular mycorrhizal fungi in roots of forest floor plants. Mycorrhiza, v. 12, n. 2, p. 291-296, 2002.
  • ZAK, D. R.; HOLMES, W. E.; WHITE, D. C.; PEACOCK, A. D.; TILMAN, D. Plant diversity, soil microbial communities, and ecosystem function: are there any links? Ecology, v. 84, n. 8, p. 2042-2050, 2003.
  • *
    Author for correspondence. E-mail:
  • Publication Dates

    • Publication in this collection
      21 Jan 2013
    • Date of issue
      Mar 2013

    History

    • Received
      17 Oct 2011
    • Accepted
      04 Feb 2012
    Editora da Universidade Estadual de Maringá - EDUEM Av. Colombo, 5790, bloco 40, 87020-900 - Maringá PR/ Brasil, Tel.: (55 44) 3011-4253, Fax: (55 44) 3011-1392 - Maringá - PR - Brazil
    E-mail: actaagron@uem.br