Does inoculation with Rhizobium tropici and nitrogen fertilization increase chickpea production?

Inoculação com Rhizobium tropici e adubação nitrogenada aumentam a produção de grão-de-bico?

Maria Nilfa Almeida Neta Rodinei Facco Pegoraro Regynaldo Arruda Sampaio Cândido Alves da Costa Luiz Arnaldo Fernandes Jessica Mendes Ferreira About the authors

ABSTRACT

Studies related to nitrogen fertilization and biological nitrogen fixation in the increase of chickpea production are considered scarce in tropical regions. This work aimed to evaluate the inoculation with Rhizobium tropici, and nitrogen fertilization, under irrigated tropical conditions, on the development of chickpea in low and high content of soil organic matter (SOM). The experimental design was in randomized blocks, with four replications, in a 2 x 6 factorial scheme. Treatments, consisted of the presence and absence of inoculation with R. tropici, and six N doses (0, 25, 50, 75, 100, and 125 kg ha-1) in the form of urea. The study was divided into two areas with distinct contents of SOM. In the area with the lowest content of SOM (3.55 dag kg-1), the inoculation with R. tropici or the fertilization with 125 kg ha-1 N increased the leaf content of nutrients (N, K, Mg, and P) and grain mass per plant, 100-grain mass, number of pods with two grains, dry mass of leaves, branches, chlorophyll index, and relative agronomic efficiency. Thus, the yield was increased in 65%, compared to the control treatment, recommending the application of 100 to 125 kg ha-1 of N with or without R. tropici. In the area with the highest content of SOM (7.37 dag kg-1), the inoculation with R. tropici provided a higher grain mass per plants, number of pods with one gain, dry mass of leaves, total dry mass, and chlorophyll index; nitrogen fertilization increased the leaf content of N and the chlorophyll index, although neither factor interfered with the yield, and are not recommended. Such results indicate the dependence of the nitrogen fertilization and inoculation with Rhizobium on the natural availability of N in the SOM.

Index terms:
Cicer arietinum L.; N doses; soil organic matter.

RESUMO

Estudos relacionados à adubação nitrogenada e fixação biológica de nitrogênio no aumento da produção de grão-de-bico são considerados escassos em regiões tropicais. Objetivou-se avaliar a inoculação do Rhizobium tropici e doses de N sob condições irrigadas em região tropical nos componentes de produção e desenvolvimento do grão-de-bico, em solos com maior e menor teor de matéria orgânica (MOS). O delineamento foi em blocos ao acaso, com quatro repetições, esquema fatorial 2 x 6, consistindo da presença e ausência da inoculação do R. tropici e seis doses de 0, 25, 50, 75, 100 e 125 kg ha-1 de N na forma de ureia. O estudo foi dividido em duas áreas com distintos teores de matéria orgânica do solo (MOS). Na área com menor teor de MOS (3.55 dag kg-1), a inoculação com R. tropici ou a adubação com 125 kg ha-1 de N aumentaram os teores foliares de nutrientes (N, K, Mg e P) e a massa de grãos por planta, massa de 100 grãos, número de vagens com dois grãos, massa seca de folhas, ramos, índice de clorofila e eficiência agronômica relativa. Com isso, a produtividade foi incrementada em 65%, em comparação ao tratamento testemunha, recomendando-se a aplicação de 100 a 125 kg ha-1 de N com ou sem R. tropici. Na área com maior teor de MOS, a inoculação com R. tropici propiciou maior massa de grãos por plantas, número de vagens com um grão, massa seca de folhas, total e índice de clorofila; a adubação nitrogenada aumentou o teor foliar de N e o índice de clorofila, mas ambos não interferiram na produtividade, não sendo recomendadas. Tais resultados indicam a dependência do manejo da adubação nitrogenada e inoculação com Rhizobium à disponibilidade natural de N na MOS.

Termos para indexação:
Cicer arietinum L.; doses de N; matéria orgânica do solo.

INTRODUCTION

Chickpea (Cicer arietinum L.) is the third most cultivated grain legume in the world, with a production of 14.5 million tons and a mean grain yield of 0.96 t ha-1 (FAO, 2017FOOD AND AGRICULTURE ORGANIZATION OF THE UNITED NATIONS - FAO. FAOSTAT. Food and agriculture data. 2017. Available in:<Available in:http://faostat3. fao.org/faostat-gateway/go/to/home/E >. Access in: JUL.10. 2018.
http://faostat3. fao.org/faostat-gateway...
). India detains 70% of world chickpea production, being the largest consumer of this crop (Icrisat, 2017INTERNATIONAL CROPS RESEARCH INSTITUTE FOR THE SEMI-ARID TROPICS - ICRISAT. Chickpea. 2017. Available in: <Available in: http://exploreit.icrisat.org/profile/Chickpea/232 >.Access in: June, 02, 2019.
http://exploreit.icrisat.org/profile/Chi...
). In Brazil, the development of more productive and adapted cultivars to the local climatic conditions of cultivation has allowed the increase of production. The Brazilian semi-arid region has the potential to obtain grain yields greater than 1,000 kilos per hectare (Pegoraro et al., 2018PEGORARO, R. F. et al. Chickpea production and soil chemical attributes after phosphorus and molybdenum fertilization. Ciência e Agrotecnologia , 42(5):474-483, 2018.; Avelar et al., 2018AVELAR, R. I. S. et al. Production and quality of chickpea seeds in different sowing and harvest periods. Journal of Seed Science, 40(2):155-164, 2018.; Artiaga et al., 2015ARTIAGA, O. P. et al. Avaliação de genótipos de grão de bico em cultivo de sequeiro nas condições de Cerrado. Revista Brasileira Ciências Agrárias, 10(1):102-109, 2015.). In this condition, chickpea presents a higher nutritional demand, especially for elements related to the production of biomass and grains, such as nitrogen.

Nitrogen (N) is the main component of proteins, nucleic acids, chlorophyll, coenzymes, phytohormones, and secondary metabolites, being decisive for plant growth (Marschner, 2012MARSCHNER, P. Marschner’s mineral nutrition of higher plants. Amsterdã, Holanda: 3.ed. Academic press. v.89. 2012, 649p.; Taiz et al., 2017TAIZ, L. et al. Fisiologia e desenvolvimento vegetal. 6.ed. Porto Alegre, Artmed Editora, 2017. 858p.). Given its importance and high mobility in the soil, this element has been studied, aiming at maximizing the use efficiency through management practices that reduce losses and increase its use efficiency by plants. Ismail, Amoursy and Mousa (2017ISMAIL, M. M.; AMOURSY, A. H. M. E. D.; MOUSA, A. E. Effect of organic and inorganic N fertilizeron growth and yield of chickpea (Cicer arietinum L.) grown on sandy soil using 15N tracer. Bangladesh Journal of Botany, 46(1):155-161, 2017.) and Khaitov and Abdiev (2018KHAITOV, B.; ABDIEV, A. Performance of chickpea (Cicer arietinum L.) to bio-fertilizer and nitrogen application in arid condition. Journal of Plant Nutrition , 41(15):1980-1987, 2018.) reported the need to apply 48 and 75 kg ha-1 N for higher grain yield in chickpeas in Bangladesh and Uzbekista, respectively. However, these doses of N vary according to the productive potential of the crop and soil characteristics, such as the organic matter content, responsible for the supply of native N to the plants.

The acquisition of N by plants via symbiotic process, either in replacement to mineral fertilization or in association can be cited as practices that can increase the efficiency of N use in agriculture. However, for productive chickpea cultivars, these management data are still scarce. In this crop, the biological fixation of atmospheric N can contribute substantially to reduce the consumption of mineral fertilizers, being able to accumulate from 80 to 120 kg ha-1 N (Laranjo; Alexandre; Oliveira, 2014LARANJO, M.; ALEXANDRE, A.; OLIVEIRA, S. Legume growth-promoting rhizobia: An overview on the Mesorhizobium genus. Microbiological research, 169(1):2-17, 2014.; Nascimento et al., 2016NASCIMENTO, W. M. de et al. Grão-de-bico. Hortaliças Leguminosas. Brasília, DF: Empresa Brasileira de Pesquisa Agropecuária, 89-118p, 2016.; Singh; Singh, 2018SINGH, Z.; SINGH, G. Role of Rhizobium in chickpea (Cicer arietinum) production: A review. Agricultural Reviews, 39(1):31-39, 2018.; Zhang et al., 2020ZHANG, J. et al. Biogeographic distribution of chickpea rhizobia in the world. In: ZHANG, J. et al. Molecular Aspects of Plant Beneficial Microbes in Agriculture. Amsterdã, Holanda: Academic press, 2020, p.235-239.). Singh and Singh (2018SINGH, Z.; SINGH, G. Role of Rhizobium in chickpea (Cicer arietinum) production: A review. Agricultural Reviews, 39(1):31-39, 2018.) report that the chickpea vegetable residues incorporated into the soil have a low C:N ratio, which favors the rapid availability of N to subsequent crops, also favoring the availability of P by increasing the content of soil organic matter (SOM).

The main advantage of biological fixation lies on the natural conversion of atmospheric N2 via reaction at ambient temperature and sub-atmospheric pressure into mineral forms that are absorbable by the plants (Marschner, 2012MARSCHNER, P. Marschner’s mineral nutrition of higher plants. Amsterdã, Holanda: 3.ed. Academic press. v.89. 2012, 649p.; Zhang et al., 2020ZHANG, J. et al. Biogeographic distribution of chickpea rhizobia in the world. In: ZHANG, J. et al. Molecular Aspects of Plant Beneficial Microbes in Agriculture. Amsterdã, Holanda: Academic press, 2020, p.235-239.), whereas in the industrial process for the production of nitrogen fertilizer, greenhouse gases are released, demanding a great amount of non-renewable fossil fuel (Jensen; Carlsson; Hauggaard-Nielsen, 2020JENSEN, E. S.; CARLSSON, G.; HAUGGAARD-NIELSEN, H. Intercropping of grain legumes and cereals improves the use of soil N resources and reduces the requirement for synthetic fertilizer N: A global-scale analysis. Agronomy for Sustainable Development, 40(1):1-9, 2020.).

However, the formation of symbiosis between nodulating bacteria and chickpea cannot supply the nitrogen demand of the crop, requiring complementation via inorganic fertilization (Elias; Herridge, 2014ELIAS, N. V.; HERRIDGE, D. F. Crop-available water and agronomic management, rather than nitrogen supply, primarily determine grain yield of commercial chickpea in northern New South Wales. Crop and Pasture Science, 65(5):442-452, 2014.; Wolde-Meskel et al., 2018WOLDE-MESKEL, E. et al. Additive yield response of chickpea (Cicer arietinum L.) to Rhizobium inoculation and phosphorus fertilizer across mall holder farms in Ethiopia. Agriculture, Ecosystems & Environment, 261:144-152, 2018.). In this context, the response of fertilization on yield depends on factors related to soil and plant, among them the presence of SOM and the productive potential of the cultivar, among others. Soils with a high content of organic matter present greater natural availability of N to plants (Liu et al., 2020LIU, K. et al. Intensifying crop rotations with pulse crops enhances system productivity and soil organic carbon in semi-arid environments. Field Crops Research, 248:107657, 2020.; Camargo et al., 2008CAMARGO, F. A. O. et al. Nitrogênio orgânico do solo. In: SANTOS, G. A. et al. Fundamentos da matéria orgânica do solo: Ecossistemas tropicais e subtropicais. 2ª Ed. Porto Alegre: Metropole, 2008, p.87-97.), interfering with the external demand for nitrogen fertilization and the symbiosis with nodulating bacteria (Marschner, 2012MARSCHNER, P. Marschner’s mineral nutrition of higher plants. Amsterdã, Holanda: 3.ed. Academic press. v.89. 2012, 649p.). Alvarez et al. (2020ALVAREZ, R. et al. Using a nitrogen mineralization index will improve soil productivity rating by artificial neural networks. Archives of Agronomy and Soil Science, 66(4):517-531, 2020.) reported the nitrogen mineralization capacity of organic matter as the main characteristic of the soil responsible for wheat production in the Argentine Pampas.

The elaboration of studies that comprise the ability of the chickpea crop in using the nitrogen from nodulating bacteria and nitrogen fertilization is required for the adequation of the management of this grain legume in tropical regions. In that perspective, this work aimed to evaluate the inoculation with R. tropici, and nitrogen fertilization, under irrigated tropical conditions, on the development of chickpea in low and high content of soil organic matter (SOM).

MATERIAL AND METHODS

The experiments were conducted in the autumn-winter period, in two years of cultivation in 2017 (April to June) and 2018 (March to June), located at the geographic coordinates 16°40’35.96” S and 43°50’55.51” O. The climate of the region is classified as Aw, with a dry winter and a rainy summer (Alvares et al., 2013ALVARES, C. A. et al. Köppen’s climate classification map for Brazil. Meteorologische Zeitschrift, 22(6):711-728, 2013.). The climatic conditions were monitored during the conduction of the studies (Figure 1).

Figure 1:
Rainfall, maximum and minimum temperature during chickpea cultivation for the area with the lowest in 2017 (A) and highest in 2018 (B) content of SOM, according to the data by National Institute of Meteorology (INMET, 2019INSTITUTO NACIONAL DE METEOROLOGIA - INMET, Dados meteorológicos de estações automáticas. 2019. Available in: <Available in: http://www.inmet.gov.br/portal/ >. Access in: December 20, 2019.
http://www.inmet.gov.br/portal/...
).

Both soils were classified as Haplic Cambisols (IUSS, 2015INTERNATIONAL UNION OF SOIL SCIENCE WORKING - IUSS, World Reference Base for Soil Resources (WRB).2015. Available in: < Available in: https://www.iuss.org/world-of-soils/ >. Access in: October 12. 2019.
https://www.iuss.org/world-of-soils/...
) with a medium texture. Before the implantation of the crop, soil samples were collected at a 0-20 cm depth for chemical characterization. In the area with the lowest content of SOM (in 2017), the following values were verified: organic matter: 3.55 dag kg-1; pH(H2O): 7.6; 10 mg kg-1 N-NO3 -; 10 mg kg-1 N-NH4 +; 1.67 mg kg-1 total N; 7.56 mg dm-3 P (Mehlich 1); 177 mg dm-3 K (Mehlich 1); 7.5 cmolc dm-3 Ca; 1.92 cmolc dm-3 Mg, 0.0 cmolc dm-3 Al (KCl); 0.85cmolc dm-3 H+Al; 9.87cmolc dm-3 SB; 9.87 cmolc dm-3 CEC (effective); 92% base saturation; 11.14 cmolc dm-3 CEC (potential); this soil was cultivated for approximately ten years with fruit species and annual crops. In the area with the highest content of SOM (in 2018), the following chemical characteristics were obtained: 7.37 dag kg-1 organic matter; pH (H2O): 5.5; 60 mg kg-1 N-NO3 -; 20 mg kg-1 N-NH4 +; 2.17 mg kg-1 total N; 2.93 mg dm-3 P (Mehlich 1); 76 mg dm-3 K (Mehlich 1); 7.3 cmolc dm-3 Ca; 3.46 cmolc dm-3 Mg; 0.04 cmolc dm-3 Al (KCl); 3.95 cmolc dm-3 H+Al; 10.96 cmolc dm-3 SB; 11 cmolc dm-3 CEC (effective); 73% base saturation (V%); 14.92 cmolc dm-3 CEC (potential), and the soil laid fallow for ten years. These soils showed favorable chemical conditions for the cultivation of chickpea, however, in the area with the lowest SOM content, the pH was considered above of the appropriate range (5.5 to 6.5) recommended by Nascimento et al. (2016NASCIMENTO, W. M. de et al. Grão-de-bico. Hortaliças Leguminosas. Brasília, DF: Empresa Brasileira de Pesquisa Agropecuária, 89-118p, 2016.).

Both studies, the experiments were performed under randomized blocks design, with four replications, in a 2 x 6 factorial scheme. The first factor was represented by either the absence or presence of Rhizobium tropici SEMIA 4077, in the form of a commercial peat-based product in a 2:1 ratio (peat:inoculum), at a concentration of 1 x 109 UFC per gram. The second factor consisted of six N doses (0, 25, 50, 75, 100 and 125 kg ha-1), in the form of urea (45% N), applied thirty days after emergence (DAE) and incorporated.

Soil preparation was performed by plowing and harrowing in both areas. The chickpea cultivar used was the ‘Aleppo’, with grains of the Kabuli type, of semi-erect growth, and with adaptability to the semiarid region of Minas Gerais (Nascimento et al., 2014NASCIMENTO, W. M. et al. BRS Aleppo: grão-de-bico. Maior tolerância a fungos de solo. Brasília; Anápolis: Embrapa Hortaliças, Boletim Técnico. 4p. 2014.). The sowing was performed in the planting furrow, with two seeds spaced every 0.10 m, and the thinning was performed after emergence to obtain ten plants per linear meter, spaced 0.50 m between rows. The plots consisted of four rows of 2 m long and 2 m wide, totaling 4 m2 of area, with 2 m2 of usable area.

Base fertilization, at sowing, was performed with the application of 110 kg ha-1 P2O5 (single superphosphate) and 20 kg ha-1 K2O (potassium chloride) in the planting furrow, using the soil analysis described above to recommended fertilization (highest technological level-NT4) in bean cultivation, according to Chagas et al. (1999CHAGAS, J. M. et al. Feijão. In: RIBEIRO, A. C. et al. (Ed.) Recomendações para o uso de corretivos e fertilizantes em Minas Gerais: 5ª aproximação. Viçosa, MG: Comissão de Fertilidade do Solo do Estado de Minas Gerais, 1999. p.306-307.).The topdressing with nitrogen fertilization was performed close to the sowing row (approximately 5 cm far from the plants), at thirty DAE. At 30 and 50 DAE, in all plots, the following micronutrients were supplied via foliar application: B, Mo, Cu, Fe, and Zn, at the ratio of 0.2% boric acid (0.34 g L-1 B), 0.2% sodium molybdate (0.3 g L-1 Mo), 0.2% copper sulfate (0.26 g L-1of Cu), 0.2% ferrous sulfate (0.38 g L-1 Fe), and 0.2% zinc sulfate (0.40 g L-1 B), respectively (Nascimento et al., 2016NASCIMENTO, W. M. de et al. Grão-de-bico. Hortaliças Leguminosas. Brasília, DF: Empresa Brasileira de Pesquisa Agropecuária, 89-118p, 2016.).

Phytosanitary treatments and irrigation were performed according to the need of the crop and the technical recommendations for the crop in the region (Nascimento et al., 2016NASCIMENTO, W. M. de et al. Grão-de-bico. Hortaliças Leguminosas. Brasília, DF: Empresa Brasileira de Pesquisa Agropecuária, 89-118p, 2016.). Irrigation was performed by micro-sprinklers in 2017 and with a conventional sprinkler systemin 2018, with an irrigation shift of four days. The manual control of weeds was performed whenever necessary. Plant health treatments and irrigation were carried out according to crop needs and technical recommendations for the crop in the region, as indicated by Nascimento (2016). A micro-spray irrigation system was used, with irrigation frequency of every four days.

At flowering, which occurred at 70 DAE, the total chlorophyll content was performed using a chlorophyll meter (SPAD-502) through twenty measurements on the main leaflets of the central plants of each useful plot. At this moment, the collection of twenty leaflets was also performed, which were stored and taken to a forced-air circulation oven at 65 °C until reaching constant mass. Afterward, the leaflets were ground in a Wiley mill with a 02 mm mesh, homogenized, and sampled for the determination of the N contents, according to the Kjeldahl method (Bataglia et al., 1983BATAGLIA, O. C. et al. Methods of chemical analysis of plants. Campinas: Instituto Agronômico, 1983. 48p.), and P, K, Ca, Mg, and Na, determined by nitric-perchloric digestion (Tedesco; Volkweiss; Bohnen, 1995TEDESCO, M. J.; VOLKWEISS, S. J.; BOHNEN, H. Análise de solo, plantas e outros materiais. Porto Alegre: UFRGS, 1995. 188p.).

At the end of the crop cycle (100 DAE), the following variables were evaluated in the ten central plants of each plot: plant height (cm), dry mass weight (g per plant) of botanic structure: leaves (LDM), branches (BDM), and total (TDM), as well as the 100-grain mass (G100), grains per plant (GP), number of pods with one grain (NP1), two grains (NP2), and total (NPT), yield in kg ha-1, harvest index (HI) in % ((seed weight/shoot biomass) x 100) and agronomic efficiency, expressed by the following Equation 1:

A E = Y t a Y t i D T a (1)

In which:

AE = Agronomic efficiency in kg of grains per kg of nutrient applied

Yta = Yield of the treatment fertilized with N (kg ha-1)

Yti = Yield of the control treatment (kg ha-1)

DTa = Dose in the treatment fertilized with N (kg ha-1)

The data were subjected to analysis of variance. Afterward, according to the significance (p≤0.05), the t-test was used for the qualitative factors, and the adjustments with regression models were performed for the quantitative factors, selected based on the significance of the regression coefficients and the potential to explain the biological phenomenon. Statistical analyses were performed using R software (R Development Core Team, 2013R DEVELOPMENT CORE TEAM. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria: 2013. Available in: <Available in: http://www.r-project.org >. Access in: February15. 2020.
http://www.r-project.org...
). For the main production components (G100, GP, TDM, and NPT) and the yield, the grouping analysis was also performed (dendrograms) using the un weighted pair-group average method (UPGMA) and distance metric of the Euclidean distance (non-standardized), as proposed by Klikocka and Tatarczak (2015KLIKOCKA, H.; TATARCZAK, A. The use of cluster analysis to evaluate yield and yield components of spring barley in a two-variable field experiment. International Journal of Agriculture and Statistical Science, 11(1):35-42, 2015.) for the evaluation of production components in field experiments.

RESULTS AND DISCUSSION

Plant development and nutrient contents -area with the lowest content of SOM.

The plant characteristics were not influenced by the interaction between inoculation and doses of N. The inoculation with R. tropici did not interfere with the CI, Height, G100, NP1, TNP, and HI features (Table 1), which obtained the following means: 45, 102 cm, 29 g, 28, and 39, respectively. These means were similar to those obtained by Pegoraro et al. (2018PEGORARO, R. F. et al. Chickpea production and soil chemical attributes after phosphorus and molybdenum fertilization. Ciência e Agrotecnologia , 42(5):474-483, 2018.) after phosphate fertilization and inoculation with R. tropici in the chickpea cultivar ‘Aleppo’. However, the height obtained in the present study was considered superior to that described by Artiaga et al. (2015ARTIAGA, O. P. et al. Avaliação de genótipos de grão de bico em cultivo de sequeiro nas condições de Cerrado. Revista Brasileira Ciências Agrárias, 10(1):102-109, 2015.). These authors observed heights from 33 to 66 cm when evaluating thirteen chickpea genotypes of distinct origins and two commercial cultivars, ‘Cícero’ and ‘IAC Marrocos’, in dry land farming conditions.

The inoculation with R. tropici increased the NP2, GP, LDM, BDM, TDM, and the Yield by 40, 32, 25, 19, 21, and 33%, respectively, compared to the absence of inoculation (Table 1). The increase in shoot biomass and yield (Table 1) by the inoculation with R. tropici was justified by several possible positive effects on phytohormones production, nutrient absorption and increased photosynthetic activity of the plant. R. tropici in the roots, through the nitrogenase enzyme complex, catalyzes the reduction reaction of atmospheric N2 in the plants into NH3 +, which is converted into organic forms (amides or ureides) released in the xylem and transported to the shoot part, where they are catabolized into ammonium (NH4 +) by the plants (Taiz et al., 2017TAIZ, L. et al. Fisiologia e desenvolvimento vegetal. 6.ed. Porto Alegre, Artmed Editora, 2017. 858p.). Gopalakrishnan et al. (2018GOPALAKRISHNAN, S. et al. Influence of diazotrophic bacteria on nodulation, nitrogen fixation, growth promotion and yield traits in five cultivars of chickpea. Biocatalysis and Aricultural Biotechnology, 15:35-42, 2018.), studying three diazotrophic bacteria (native to India) in chickpea inoculation, also observed an increase in the number of nodules, as well as a higher dry mass of shoot and root.

Table 1:
Chlorophyll index (CI), height (H), 100-mass grain (G100), grain mass per plant (GP), number of pods with one grain (NP1), two grains (NP2), and total (TNP), dry mass of leaves (LDM), branches (BDM), and total dry mass (TDM), yield, harvest index (HI),agronomic efficiency (AE), leaf contents of nitrogen (N), potassium (K), calcium (Ca), magnesium (Mg), sodium (Na), and phosphorus (P) of the chickpea cultivar Aleppo with and without inoculation with R. tropici.

The production of phytohormones and the greater availability of nutrients in plants that form a symbiosis with nitrogen-fixing bacteria also improved their growth and yield (Singh; Singh, 2018SINGH, Z.; SINGH, G. Role of Rhizobium in chickpea (Cicer arietinum) production: A review. Agricultural Reviews, 39(1):31-39, 2018.; Laranjo; Alexandre; Oliveira, 2014LARANJO, M.; ALEXANDRE, A.; OLIVEIRA, S. Legume growth-promoting rhizobia: An overview on the Mesorhizobium genus. Microbiological research, 169(1):2-17, 2014.; Marschner, 2012MARSCHNER, P. Marschner’s mineral nutrition of higher plants. Amsterdã, Holanda: 3.ed. Academic press. v.89. 2012, 649p.). This phenomenon may have occurred with the chickpea inoculated with R. tropici.

The inoculation of R. tropici it may also have favored the growth and grain yield of chickpeas by stimulating the photosynthetic activity of plants. Beneficial effects have been reported by enhanced growth and development of photosynthetic organs and the rate of photosynthates accumulation (Moinuddin et al., 2014MOINUDDIN, D. T. et al. Use of N and P biofertilizers together with phosphorus fertilizer Improves growth and physiological attributes of chickpea. Global Journal of Agriculture and Agricultural Sciences, 2(3):168-174. 2014.).Thus, nodulating plants may have greater photosynthetic activity due to the increased demand for carbon compounds consumed by the symbiotic bacteria for N2 fixation (Kaschuk et al., 2012KASCHUK, G. et al. Photosynthetic adaptation of soybean due to varying effectiveness of N2 fixation by two distinct Bradyrhizobium japonicum strains. Environmental and Experimental Botany, 76:1-6, 2012.), this metabolic alteration may favor plant growth and grain yield in legumes.

The agronomic efficiency was increased by 66 % in the treatment with R. tropici (Table 1), which indicates a positive effect of inoculation on chickpea production, even after the application of N doses. In Ethiopia, through which Wolde-Meskel et al. (2018)WOLDE-MESKEL, E. et al. Additive yield response of chickpea (Cicer arietinum L.) to Rhizobium inoculation and phosphorus fertilizer across mall holder farms in Ethiopia. Agriculture, Ecosystems & Environment, 261:144-152, 2018. obtained a positive response of the inoculation with Mesorhizobium ciceri on chickpea yield (2.0 t ha-1), compared to the control treatment (1.6 t ha-1) without inoculation. Emphasizing the importance of the inoculation with nodulating bacteria in chickpea in order to obtain higher profitability and quality of grains (Gopalakrishnan et al., 2018GOPALAKRISHNAN, S. et al. Influence of diazotrophic bacteria on nodulation, nitrogen fixation, growth promotion and yield traits in five cultivars of chickpea. Biocatalysis and Aricultural Biotechnology, 15:35-42, 2018.; Zhang et al., 2020ZHANG, J. et al. Biogeographic distribution of chickpea rhizobia in the world. In: ZHANG, J. et al. Molecular Aspects of Plant Beneficial Microbes in Agriculture. Amsterdã, Holanda: Academic press, 2020, p.235-239.).

The inoculation with R. tropici increased the leaf content of Na (19 %) and reduced the content of N by 17 %, but interfered with the contents of K, Ca, and Mg, compared to the absence of the inoculant (Table 1). The higher biomass production in the shoot part of the inoculated plants possibly provided a dilution effect of N in the plant tissue compared to the absence of inoculation, as demonstrated by Marles (2017MARLES, R. J. Mineral nutrient composition of vegetables, fruits and grains: The context of reports of apparent historical declines. Journal of Food Composition and Analysis, 56:93-103, 2017.). The increase in carbohydrate production is not proportionally followed by the content of minerals, that is, the nutrient contents of the plant may decrease without causing a lower grain yield (Marles, 2017MARLES, R. J. Mineral nutrient composition of vegetables, fruits and grains: The context of reports of apparent historical declines. Journal of Food Composition and Analysis, 56:93-103, 2017.; Briat et al., 2020BRIAT, J. F. et al. Reappraisal of the central role of soil nutrient availability in nutrient management in light of recent advances in plant nutrition at crop and molecular levels. European Journal of Agronomy, 116:e126069, 2020.).

The N doses increased the chlorophyll index (Figure 2B), obtaining an increment of 0.06 in the CLO for each kilogram of N added, indicating a potential increase of growth and production of cultivated plants. Increases in the chlorophyll content favor the photosynthetic rates at low light intensities, resulting in a healthy plant with a higher yield (Joshi et al., 2019JOSHI, D. et al. Impacts of bioinoculants Pseudomonas jesenii MP1 and Rhodococcus qingshengii S10107 on chickpea (Cicer arietinum L.) yield and soil nitrogen status. Pedosphere, 29(3):388-399, 2019.; Gu et al., 2017GU, J. et al. Photosynthetic properties and potentials for improvement of photosynthesis in pale green leaf rice under high light conditions. Frontiers in Plant Science, 8:1082, 2017.). Higher doses of N also incremented the G100 and NP2 (Figure 2C, 2E). Each kilogram of N added contributed to the increase of 0.03 g in the 100-grain mass and 0.22 pods with two grains.

Figure 2:
Height(A), chlorophyll index (B), 100-grain mass(C), dry mass of leaves, branches, grains, and total dry mass (D), number of pads with one, two, and total grains (E), yield (F), harvest index (G), and agronomic efficiency (H) of chickpea under N doses.

The height, NP1, and NPT were not influenced by the increment in the doses of N (Figure 2A and 2E). The dose of 125 kg ha-1of N incremented the dry mass of leaves, branches, grains, and the total dry mass (Figure 2D), with 7, 23, 10, and 36 g per plant, respectively. The application of 125 kg ha-1 N with or without R. tropici provided the maximum production values of 2.09 t ha-1 grains (Figure 2F). These results indicate a greater importance of the factor doses of N for the increase of grain production in soil with lower content of organic matter, and that the application of higher doses of N can minimize the positive effect of nodulating bacteria in the production of chickpea. This yield was considered superior to the world average of 0.96 t ha-1 (FAO, 2017), and close to the 2.71 t ha-1 obtained by Pegoraro et al. (2018PEGORARO, R. F. et al. Chickpea production and soil chemical attributes after phosphorus and molybdenum fertilization. Ciência e Agrotecnologia , 42(5):474-483, 2018.) in the northern region of Minas Gerais.

The recommended dose of 125 kg ha-1 N for maximum grain production was considered high compared to studies carried out in other countries, but it is similar when compared to recommendations made for other leguminous crops in Brazil, such as beans, where the doses vary from 40 to 120 kg ha-1, according to the technological level adopted. Ismail, Amoursy and Mousa (2017ISMAIL, M. M.; AMOURSY, A. H. M. E. D.; MOUSA, A. E. Effect of organic and inorganic N fertilizeron growth and yield of chickpea (Cicer arietinum L.) grown on sandy soil using 15N tracer. Bangladesh Journal of Botany, 46(1):155-161, 2017.) and Khaitov and Abdiev (2018KHAITOV, B.; ABDIEV, A. Performance of chickpea (Cicer arietinum L.) to bio-fertilizer and nitrogen application in arid condition. Journal of Plant Nutrition , 41(15):1980-1987, 2018.) reported the need to apply 48 and 75 kg ha-1 N for higher grain yield in chickpeas in Bangladesh and Uzbekista, respectively. While, Rani and Krishna (2016RANI, B. S.; KRISHNA, T. G. Response of chickpea (Cicer arietinum L.) varieties to nitrogen on a calcareous vertisols. Indian Journal of Agricultural Research, 50(3):278-281, 2016.) found no difference in grain yield using doses of 20, 30 and 40 kg ha-1 N in India. The greater need for nitrogen fertilization observed in this crop (Figure 2F) may be related to the lower natural availability of nitrogen in the soil, as described in the material and methods.

The leaf contents of N, P (with inoculation), K, and Mg were incremented with the growing doses of N (Figure 3A, 3B, and 3C). The maximum contents of these nutrients corresponded to 41.45; 5.25; 23.60, and 4.40 g kg-1, respectively, at the dose of 125 kg ha-1 N. With that, it is suggested that a synergistic effect of nitrogen fertilization with urea in the absorption of these macronutrients by chickpea plants is suggested (Briat et al., 2020BRIAT, J. F. et al. Reappraisal of the central role of soil nutrient availability in nutrient management in light of recent advances in plant nutrition at crop and molecular levels. European Journal of Agronomy, 116:e126069, 2020.). However, nitrogen fertilization did not interfere with the contents of Ca, with a mean of 8.42 g kg-1 (Figure 3B), and reduced the leaf contents of Na in the treatment with R. tropici (Figure 3D). Indicating the attenuation of sodium in the plant caused by inoculation (Abdiev et al., 2019ABDIEV, A. et al. Growth, nutrient uptake and yield parameters of chickpea (Cicer arietinum L.) enhance by Rhizobium and Azotobacter inoculations in saline soil. Journal of Plant Nutrition, 42(20):2703-2714, 2019.).

Figure 3:
Contents of nitrogen (A), potassium, calcium, magnesium (B), phosphorus (C), and sodium (D) of chickpea under N doses.

The content of P was influenced by the interaction between inoculation versus doses of N, being lower on the leaves of the inoculated plants, and at the doses 0, 25, and 50 kg ha-1 N (Figure 3C). However, the highest content of P was obtained in the presence of R. tropici at the dose of 125 kg ha-1 N (Figure 3C). The performance of nodulation and N2 fixation depends on the properties of the soil and the nutrients that it contains (Briat et al., 2020BRIAT, J. F. et al. Reappraisal of the central role of soil nutrient availability in nutrient management in light of recent advances in plant nutrition at crop and molecular levels. European Journal of Agronomy, 116:e126069, 2020.), especially those nutrients with direct involvement in the structure and metabolic function of the microbial cell (Marschner, 2012MARSCHNER, P. Marschner’s mineral nutrition of higher plants. Amsterdã, Holanda: 3.ed. Academic press. v.89. 2012, 649p.). P is demanded in larger amounts by plants that associate with bacteria since there is greater ATP production for the action of the nitrogenase enzyme and the development of nodules. In the condition of greater availability of N and the presence of R. tropici, the photosynthetic activity of the plants may have been stimulated, due to the increased demand for carbon compounds consumed by the symbiotic bacteria for N2 fixation (Kaschuk et al., 2012KASCHUK, G. et al. Photosynthetic adaptation of soybean due to varying effectiveness of N2 fixation by two distinct Bradyrhizobium japonicum strains. Environmental and Experimental Botany, 76:1-6, 2012.), stimulating the absorption of P by the plants and the grain yield in chickpea. The higher is nodulation the higher is the allocation of P in the roots of the plants (Kuang et al., 2005KUANG, R. B. et al. Phosphorus and nitrogen interactions in field-grown soybean as related to genetic attributes of root morphological and nodular traits. Journal of Integrative Plant Biology, 47(5):549-559, 2005.; Valentine; Kleinert; Benedito, 2017VALENTINE, A. J.; KLEINERT, A.; BENEDITO, V. A. Adaptive strategies for nitrogen metabolism in phosphate deficient legume nodules. Plant Science, 256:46-52, 2017.). This can explain the lower leaf contents of P after the inoculation with R. tropici, at the lowest N doses (Figure 3C).

Through the unweighted pair-group average method (UPGMA) it was possible to identify three classes of fertilization response: 100 and 125 kg ha-1 N (high response), 75 and 25 kg ha-1 N (average response), and 50 and 0 kg ha-1 N (low response). The height of the Y-axis for each group identifies this amplitude (Figure 4A). The three grouped classes complement the analysis of variance (Figure 2) for relating the highest productions of total and grain dry mass, 100-grain mass, and yield, with the 100 and 125 kg ha-1 N. In the multivariate analysis, with the data reorganized in matrices (Figure 4B), it was also possible to identify the strong positive relationship (above 0.8) of the highest doses (100 and 125 kg ha-1 N), and the negative relationship (inferior a -0.7) of the lowest doses (50 and 0 kg ha-1) with these components of production and yield.

Figure 4:
Dendrograms with multivariate analysis of A (UPGMA method) and B groupings (multivariate cluster analysis) for the main chickpea production components (G100 - 100-grain mass, DMT- total dry mass, GP-grain dry mass, NPT- total number of pods, and - yield) after fertilization with doses of N: D0 (0 kg ha-1), D25 (25 kg ha-1), D50 (50 kg ha-1), D75 (75 kg ha-1), D100 (100 kg ha-1), and 125 (125 kg ha-1).

Plant development and nutrient contents -area with the highest content of SOM

There was no interaction between the inoculation factors and doses of N for all evaluated characteristics. Isolated effect of the inoculation with R. tropici increased the GP, NP1, DML, and DMT (Table 2) by 27.07, 26.78, 20.93%, and 16.26%, respectively, compared to the absence of inoculation. Reinforcing the greater effect of R. tropici on the production of grain mass per plant. The higher content of organic matter in the soil may have increased the bacterial population, contributing to the symbiosis of R. tropici with the roots favoring the performance of these characteristics of chickpeas. However, this effect was limited, as inoculation did not interfere with the CI, Height, G100, NPT, BDM, and Yield (Table 2). Indicating the greater natural capacity of this soil to provide adequate conditions for grain yield.

Table 2:
Chlorophyll index (CI), height (H), 100-grain mass (G100), grain mass per plant (GP), number of pods with one grain (NP1), total number of pods (TNP), dry mass of leaves (LDM), branches (BDM), total dry mass (TDM), yield, harvest index (HI), agronomic efficiency (AE), and leaf contents of nitrogen (N), phosphorus (P), potassium (K), calcium (Ca), magnesium (Mg), and sodium (Na) of the chickpea cultivar ‘Aleppo’ with and without inoculation with R. tropici (RIZ).

The absence of inoculation with R. tropici provided the highest leaf contents of N (9 %), P (11%), and Ca (15%) (Table 2). Contrarily to what was verified by Abdiev et al. (2019ABDIEV, A. et al. Growth, nutrient uptake and yield parameters of chickpea (Cicer arietinum L.) enhance by Rhizobium and Azotobacter inoculations in saline soil. Journal of Plant Nutrition, 42(20):2703-2714, 2019.) with chickpea, with the highest contents of N, P, and K on roots and leaves when in the presence of inoculation.

The addition of N doses increased the chlorophyll index and the content of N in the chickpea leaves, with means of 51 and 48 g kg-1, respectively, at the 125 kg ha-1 N (Figure 5B, 5J), and it did not change the height, G100,GP, and the leaf contents of P, K, Ca, and Mg (Figure 5A, 5C, 5Dand 5J).The higher chlorophyll production and absorption of N at the highest doses applied did not imply directly on greater plant growth and G100, indicating the luxury absorption of N by the chickpea, besides the adequate supply of native N to the plants, at the lowest doses applied. This indicates a greater capacity of this soil with a higher SOM content in providing native N for chickpeas. Ciclot et al. (2017CLIVOT, H. et al. Quantifying in situ and modeling net nitrogen mineralization from soil organic matter in arable cropping systems. Soil Biology and Biochemistry, 111:44-59. 2017.) report that the SOM nitrogen mineralization rate in the arable layer (0.30 m) ranges from 0.13 to 1.10 kg ha-1 day-1 N in soils in France. These authors describe a positive correlation between the mineralization rate and the SOM content, indicating a substantial increase in the availability of N for plants in soils with a higher SOM content. In tropical soils it is believed that these rates are higher, however, if we consider the mineralization of 1 kg ha-1 day-1 N it would be possible to supply the demand for chickpeas in the soil with higher SOM content.

Figure 5:
Height (A), chlorophyll index (B), 100-grain mass (C), dry mass of leaves, branches, seeds, and total dry mass (D), number of pods with one, two, and total grains (E), yield (F), harvest index (G), agronomic efficiency (H), leaf content of N (I), and leaf contents of phosphorus, potassium, calcium, magnesium, and sodium (J) of chickpea under N doses.

The mean chickpea yield after the application of N doses corresponded to 1.78 t ha-1 (Figure 5F), which is above those obtained in other countries, such as India (0.91 t ha-1), Uzbekistan (1.46 t ha-1), Ethiopia (1.67 t ha-1), and Australia (1.22 t ha-1) (FAO, 2017FOOD AND AGRICULTURE ORGANIZATION OF THE UNITED NATIONS - FAO. FAOSTAT. Food and agriculture data. 2017. Available in:<Available in:http://faostat3. fao.org/faostat-gateway/go/to/home/E >. Access in: JUL.10. 2018.
http://faostat3. fao.org/faostat-gateway...
). According to Rani and Krishna (2016RANI, B. S.; KRISHNA, T. G. Response of chickpea (Cicer arietinum L.) varieties to nitrogen on a calcareous vertisols. Indian Journal of Agricultural Research, 50(3):278-281, 2016.), in India, the application of N doses (20, 30,and 40 kg ha-1) did not interfere with grain yield, which reinforces the ability of these plants in using native N in the soil or provided via symbiosis. Soares et al. (2016SOARES, B. L. et al. Agronomic and economic efficiency of common-bean inoculation with rhizobia and mineral nitrogen fertilization. Revista Brasileira de Ciência do Solo, 40:e0150235, 2016.), studying the cultivation of common beans, reported that 20 kg ha-1 of N at sowing favored root growth and higher nodulation when compared to superior doses, suggesting that lower N doses can favor the initial development of vegetable species.

The N doses did not increment the harvest index (IC) and the agronomic efficiency (EA), and their means corresponded to 28.34 % and 5.04, respectively (Figure 5G and 5H), indicating that 28.34 % of the biomass accumulated in the shoot part was converted into grains. The IC and the EA refer to the ability of the plant to produce grains according to its growth and availability of nutrients via fertilization. In this context, the inexistence of alterations in grain production after the use of the highest N doses was observed, corroborating with the condition of adequate nutritional supply in the plant at lower N doses. The highest agronomic efficiency occurs when higher productions are obtained at lower N doses (Leal et al., 2019LEAL, F. T. et al. Use efficiency and responsivity to nitrogen of common bean cultivars. Ciência e Agrotecnologia, 43:e004919, 2019.).

In this study, the application of Rhizobium spp. and the N doses did not interfere with grain production, possibly as a consequence of the high natural soil fertility especially associated with the high content of mineral N, total N (NT), and soil organic matter, attributes that contribute to biological activity, providing greater availability of mineral N in the soil solution and higher diversity of nodulating bacteria in the soil (Marschner, 2012MARSCHNER, P. Marschner’s mineral nutrition of higher plants. Amsterdã, Holanda: 3.ed. Academic press. v.89. 2012, 649p.).

In this condition, there is a higher amount of mineral and organic N in the labile fraction of the soil, converted into ammonium and nitrate, released by the action of decomposing microorganisms (Liu et al., 2020LIU, K. et al. Intensifying crop rotations with pulse crops enhances system productivity and soil organic carbon in semi-arid environments. Field Crops Research, 248:107657, 2020.; Camargo et al., 2008CAMARGO, F. A. O. et al. Nitrogênio orgânico do solo. In: SANTOS, G. A. et al. Fundamentos da matéria orgânica do solo: Ecossistemas tropicais e subtropicais. 2ª Ed. Porto Alegre: Metropole, 2008, p.87-97.). Elias and Herridge (2014ELIAS, N. V.; HERRIDGE, D. F. Crop-available water and agronomic management, rather than nitrogen supply, primarily determine grain yield of commercial chickpea in northern New South Wales. Crop and Pasture Science, 65(5):442-452, 2014.), in an assessment on chickpea cultivation in Australia, observed a low efficiency of this vegetable species in forming a symbiosis with native nitrogen-fixing bacteria the first years of cultivation, although this phenomenon was minimized after the use of inoculants with a greater populational abundance of Rhizobium, reinforcing the importance of the fixation of atmospheric N in increasing chickpea production and the subsequent crops.

In the analysis of the unweighted pair group method (UPGMA), it was possible to observe isolated behaviors, with a higher amplitude, at the doses of125 and 0 kg ha-1 N for the production components (Figure 6A). The 0 kg ha-1 N was responsible for the obtainment of higher positive relationships (above 1.0) with the DMT, NPT, and GP, whereas the 125 kg ha-1 dose was responsible for a negative relationship (below -1.0) with the yield and production components (Figure 6B), characterizing the adequate supply of N for chickpea production at the lowest dose used.

Figure 6:
Dendrograms with multivariate analysis of A (UPGMA method) and B groupings (multivariate cluster analysis) for the main chickpea production components (G100-100-grain mass, DMT- total dry mass, GP- grain dry mass, NPT- total number of pod sand- yield) after fertilization with doses of N: D0 (0 kg ha-1), D25 (25 kg ha-1), D50 (50 kg ha-1), D75 (75 kg ha-1), D100 (100 kg ha-1), and 125 (125 kg ha-1).

In summary, this study obtained a positive effect of the inoculation with Rhizobium and nitrogen fertilization in the increase of chickpea production in the soil with lower natural availability of N, whereas in soils with a higher content of organic matter the production responses are less expressive, which can be attributed to the high mineralization ability of the organic fraction of the soil due to the tropical conditions of cultivation.

CONCLUSIONS

In the soil with the lowest content of organic matter, the inoculation with R. tropici increases the biomass of the shoot part and the chickpea yield and does not interfere with the IC. In this condition, the application of 100 to 125 kg ha-1 N provides the maximum yield of 2.09 t ha-1 and the relative chickpea agronomic efficiency of 21.6%. In the soil with the highest contents of organic matter, the inoculation with R. tropici increased the biomass of the shoot part and does not interfere with chickpea yield. Likewise, the N doses increase the chlorophyll index but do not interfere with the remaining production components and chickpea yield.

ACKNOWLEDGEMENTS

The authors thank the Foundation for Research Support of the State of Minas Gerais (FAPEMIG), the Brazilian National Council for Scientific and Technological Development (CNPq), the Pro-Rectory Research of Universidade Federal de Minas Gerais (PRPq -UFMG), and the Brazilian Coordination for the Improvement of Higher Education Personnel (CAPES; Financial Code 001) for financial support to this research project and grating of scholarships

REFERENCES

  • ABDIEV, A. et al. Growth, nutrient uptake and yield parameters of chickpea (Cicer arietinum L.) enhance by Rhizobium and Azotobacter inoculations in saline soil. Journal of Plant Nutrition, 42(20):2703-2714, 2019.
  • ALVARES, C. A. et al. Köppen’s climate classification map for Brazil. Meteorologische Zeitschrift, 22(6):711-728, 2013.
  • ALVAREZ, R. et al. Using a nitrogen mineralization index will improve soil productivity rating by artificial neural networks. Archives of Agronomy and Soil Science, 66(4):517-531, 2020.
  • ARTIAGA, O. P. et al. Avaliação de genótipos de grão de bico em cultivo de sequeiro nas condições de Cerrado. Revista Brasileira Ciências Agrárias, 10(1):102-109, 2015.
  • AVELAR, R. I. S. et al. Production and quality of chickpea seeds in different sowing and harvest periods. Journal of Seed Science, 40(2):155-164, 2018.
  • BATAGLIA, O. C. et al. Methods of chemical analysis of plants. Campinas: Instituto Agronômico, 1983. 48p.
  • BRIAT, J. F. et al. Reappraisal of the central role of soil nutrient availability in nutrient management in light of recent advances in plant nutrition at crop and molecular levels. European Journal of Agronomy, 116:e126069, 2020.
  • CAMARGO, F. A. O. et al. Nitrogênio orgânico do solo. In: SANTOS, G. A. et al. Fundamentos da matéria orgânica do solo: Ecossistemas tropicais e subtropicais. 2ª Ed. Porto Alegre: Metropole, 2008, p.87-97.
  • CHAGAS, J. M. et al. Feijão. In: RIBEIRO, A. C. et al. (Ed.) Recomendações para o uso de corretivos e fertilizantes em Minas Gerais: 5ª aproximação. Viçosa, MG: Comissão de Fertilidade do Solo do Estado de Minas Gerais, 1999. p.306-307.
  • CLIVOT, H. et al. Quantifying in situ and modeling net nitrogen mineralization from soil organic matter in arable cropping systems. Soil Biology and Biochemistry, 111:44-59. 2017.
  • ELIAS, N. V.; HERRIDGE, D. F. Crop-available water and agronomic management, rather than nitrogen supply, primarily determine grain yield of commercial chickpea in northern New South Wales. Crop and Pasture Science, 65(5):442-452, 2014.
  • FOOD AND AGRICULTURE ORGANIZATION OF THE UNITED NATIONS - FAO. FAOSTAT. Food and agriculture data. 2017. Available in:<Available in:http://faostat3. fao.org/faostat-gateway/go/to/home/E >. Access in: JUL.10. 2018.
    » http://faostat3. fao.org/faostat-gateway/go/to/home/E
  • GOPALAKRISHNAN, S. et al. Influence of diazotrophic bacteria on nodulation, nitrogen fixation, growth promotion and yield traits in five cultivars of chickpea. Biocatalysis and Aricultural Biotechnology, 15:35-42, 2018.
  • GU, J. et al. Photosynthetic properties and potentials for improvement of photosynthesis in pale green leaf rice under high light conditions. Frontiers in Plant Science, 8:1082, 2017.
  • INSTITUTO NACIONAL DE METEOROLOGIA - INMET, Dados meteorológicos de estações automáticas. 2019. Available in: <Available in: http://www.inmet.gov.br/portal/ >. Access in: December 20, 2019.
    » http://www.inmet.gov.br/portal/
  • INTERNATIONAL CROPS RESEARCH INSTITUTE FOR THE SEMI-ARID TROPICS - ICRISAT. Chickpea. 2017. Available in: <Available in: http://exploreit.icrisat.org/profile/Chickpea/232 >.Access in: June, 02, 2019.
    » http://exploreit.icrisat.org/profile/Chickpea/232
  • INTERNATIONAL UNION OF SOIL SCIENCE WORKING - IUSS, World Reference Base for Soil Resources (WRB).2015. Available in: < Available in: https://www.iuss.org/world-of-soils/ >. Access in: October 12. 2019.
    » https://www.iuss.org/world-of-soils/
  • ISMAIL, M. M.; AMOURSY, A. H. M. E. D.; MOUSA, A. E. Effect of organic and inorganic N fertilizeron growth and yield of chickpea (Cicer arietinum L.) grown on sandy soil using 15N tracer. Bangladesh Journal of Botany, 46(1):155-161, 2017.
  • JENSEN, E. S.; CARLSSON, G.; HAUGGAARD-NIELSEN, H. Intercropping of grain legumes and cereals improves the use of soil N resources and reduces the requirement for synthetic fertilizer N: A global-scale analysis. Agronomy for Sustainable Development, 40(1):1-9, 2020.
  • JOSHI, D. et al. Impacts of bioinoculants Pseudomonas jesenii MP1 and Rhodococcus qingshengii S10107 on chickpea (Cicer arietinum L.) yield and soil nitrogen status. Pedosphere, 29(3):388-399, 2019.
  • KHAITOV, B.; ABDIEV, A. Performance of chickpea (Cicer arietinum L.) to bio-fertilizer and nitrogen application in arid condition. Journal of Plant Nutrition , 41(15):1980-1987, 2018.
  • KASCHUK, G. et al. Photosynthetic adaptation of soybean due to varying effectiveness of N2 fixation by two distinct Bradyrhizobium japonicum strains. Environmental and Experimental Botany, 76:1-6, 2012.
  • KLIKOCKA, H.; TATARCZAK, A. The use of cluster analysis to evaluate yield and yield components of spring barley in a two-variable field experiment. International Journal of Agriculture and Statistical Science, 11(1):35-42, 2015.
  • KUANG, R. B. et al. Phosphorus and nitrogen interactions in field-grown soybean as related to genetic attributes of root morphological and nodular traits. Journal of Integrative Plant Biology, 47(5):549-559, 2005.
  • LARANJO, M.; ALEXANDRE, A.; OLIVEIRA, S. Legume growth-promoting rhizobia: An overview on the Mesorhizobium genus. Microbiological research, 169(1):2-17, 2014.
  • LEAL, F. T. et al. Use efficiency and responsivity to nitrogen of common bean cultivars. Ciência e Agrotecnologia, 43:e004919, 2019.
  • LIU, K. et al. Intensifying crop rotations with pulse crops enhances system productivity and soil organic carbon in semi-arid environments. Field Crops Research, 248:107657, 2020.
  • MARLES, R. J. Mineral nutrient composition of vegetables, fruits and grains: The context of reports of apparent historical declines. Journal of Food Composition and Analysis, 56:93-103, 2017.
  • MARSCHNER, P. Marschner’s mineral nutrition of higher plants. Amsterdã, Holanda: 3.ed. Academic press. v.89. 2012, 649p.
  • MOINUDDIN, D. T. et al. Use of N and P biofertilizers together with phosphorus fertilizer Improves growth and physiological attributes of chickpea. Global Journal of Agriculture and Agricultural Sciences, 2(3):168-174. 2014.
  • NASCIMENTO, W. M. et al. BRS Aleppo: grão-de-bico. Maior tolerância a fungos de solo. Brasília; Anápolis: Embrapa Hortaliças, Boletim Técnico. 4p. 2014.
  • NASCIMENTO, W. M. de et al. Grão-de-bico. Hortaliças Leguminosas. Brasília, DF: Empresa Brasileira de Pesquisa Agropecuária, 89-118p, 2016.
  • PEGORARO, R. F. et al. Chickpea production and soil chemical attributes after phosphorus and molybdenum fertilization. Ciência e Agrotecnologia , 42(5):474-483, 2018.
  • RANI, B. S.; KRISHNA, T. G. Response of chickpea (Cicer arietinum L.) varieties to nitrogen on a calcareous vertisols. Indian Journal of Agricultural Research, 50(3):278-281, 2016.
  • R DEVELOPMENT CORE TEAM. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria: 2013. Available in: <Available in: http://www.r-project.org >. Access in: February15. 2020.
    » http://www.r-project.org
  • SINGH, Z.; SINGH, G. Role of Rhizobium in chickpea (Cicer arietinum) production: A review. Agricultural Reviews, 39(1):31-39, 2018.
  • SOARES, B. L. et al. Agronomic and economic efficiency of common-bean inoculation with rhizobia and mineral nitrogen fertilization. Revista Brasileira de Ciência do Solo, 40:e0150235, 2016.
  • TAIZ, L. et al. Fisiologia e desenvolvimento vegetal. 6.ed. Porto Alegre, Artmed Editora, 2017. 858p.
  • TEDESCO, M. J.; VOLKWEISS, S. J.; BOHNEN, H. Análise de solo, plantas e outros materiais. Porto Alegre: UFRGS, 1995. 188p.
  • VALENTINE, A. J.; KLEINERT, A.; BENEDITO, V. A. Adaptive strategies for nitrogen metabolism in phosphate deficient legume nodules. Plant Science, 256:46-52, 2017.
  • WOLDE-MESKEL, E. et al. Additive yield response of chickpea (Cicer arietinum L.) to Rhizobium inoculation and phosphorus fertilizer across mall holder farms in Ethiopia. Agriculture, Ecosystems & Environment, 261:144-152, 2018.
  • ZHANG, J. et al. Biogeographic distribution of chickpea rhizobia in the world. In: ZHANG, J. et al. Molecular Aspects of Plant Beneficial Microbes in Agriculture. Amsterdã, Holanda: Academic press, 2020, p.235-239.

Publication Dates

  • Publication in this collection
    24 Aug 2020
  • Date of issue
    2020

History

  • Received
    06 June 2020
  • Accepted
    17 July 2020
Editora da UFLA Editora da UFLA, Caixa Postal 3037 - 37200-900 - Lavras - MG - Brasil, Telefone: 35 3829-1115 - Lavras - MG - Brazil
E-mail: revista.ca.editora@ufla.br