Rhizobia inoculation increases pea grain yield: an overview and challenges

Autores

DOI:

https://doi.org/10.14393/BJ-v40n0a2024-67453

Palavras-chave:

Bibliometric analysis, Biological nitrogen fixation, Pisum sativum, Rhizobacteria, Rhizobium.

Resumo

The aim of this study was to evaluate the contribution of inoculation with microorganisms, mainly rhizobia, on pea (Pisum sativum) production using a systematic literature review approach and a comparative analysis of grain yield to provide information to fill gaps in nontraditional regions of cultivation for this legume. A systematic search strategy was implemented, targeting papers published in scientific journals accessible through the Web of Science® (WoS) database spanning from January 1990 to April 2022. The search terms "Pisum sativum," "inoculation," and "strain" were used. The differences between the pea grain yields from plants inoculated with nitrogen-fixing microorganisms and those from noninoculated plants (control) were analyzed using thirteen field-scale studies. Overall, pea inoculation/coinoculation promoted a greater grain yield (3118 ±210 kg ha-1) than noninoculation (2338± 127 kg ha-1), showing the importance of biological nitrogen fixation for legume crop production. In the pursuit of reducing pea production costs, emphasis has been placed on inoculation, highlighting the importance of comprehending the symbiotic relationship between peas and Rhizobium. Furthermore, this research aimed to explore the interaction between Rhizobium and selected microorganisms known to enhance plant growth to identify optimal combinations to boost pea productivity.

Downloads

Não há dados estatísticos.

Referências

AHMAD, E., KHAN, M.S. and ZAIDI, A. ACC deaminase producing Pseudomonas putida strain PSE3 and Rhizobium leguminosarum strain RP2 in synergism improves growth, nodulation and yield of pea grown in alluvial soils. Symbiosis. 2013, 61(2), 93-104. https://doi.org/10.1007/s13199-013-0259-6

AHMED, R., et al. Effect of inoculation methods of Rhizobium on yield attributes, yield and protein content in seed of pea. Journal of Soil and Nature. 2007, 1(3), 30-35.

ALMACA, A., et al. Effects of Rhizobium leguminosarum whey powder and nitrogenous fertilizer treatments on nodulation and yield components of forage pea. Fresenius Environmental Bulletin. 2021, 30(6), 6292-6296.

ANDRADE, D.S., MURPHY, P.J. and GILLER, K.E. The diversity of Phaseolus-nodulating rhizobial populations Is altered by liming of acid Soils planted with Phaseolus vulgaris L. in Brazil. Applied and Environmental Microbiology. 2002a, 68(8), 4025-4034. https://doi.org/10.1128/AEM.68.8.4025-4034.2002

ANDRADE, D.S., MURPHY, P.J. and GILLER, K.E. Effects of liming and legume/cereal cropping on popupations of indigenous rhizobia in an acid Brazilian oxisol. Soil Biology & Biochemistry 2002b, 34, 477-485. https://doi.org/10.1016/S0038-0717(01)00206-1

ARAFA, M.M., EL-BATANONY, N.H. and NOFAL, A.M. Inoculation effect of rhizobial strains on growth, yield and chemical composition of some legume crops in new reclaimed soil. Middle East Journal of Agriculture Research. 2018, 7(2), 352-363.

BALLARD, R.A., et al. Size, symbiotic effectiveness and genetic diversity of field pea rhizobia (Rhizobium leguminosarum bv. viciae) populations in South Australian soils. Soil Biology and Biochemistry. 2004, 36(8), 1347-1355. https://doi.org/10.1016/j.soilbio.2004.04.016

BASHIR, T. and NAZ, S. Plant growth promoting rhizobacteria in combination with plant growth regulators attenuate the effect of drought stress. Pakistan Journal of Botany. 2020, 52(3), 783-793. http://dx.doi.org/10.30848/PJB2020-3(17)

BEGUM, A.A., et al. Inoculation of pea (Pisum sativum L.) by Rhizobium leguminosarum bv. viceae preincubated with naringenin and hesperetin or application of naringenin and hesperetin directly into soil increased pea nodulation under short season conditions. Plant and Soil. 2001, 237(1), 71-80. https://doi.org/10.1023/A:1013328906027

BELIMOV, A., et al. Abscisic acid-utilizing rhizobacteria disturb nitrogen-fixing symbiosis of pea Pisum sativum L., Biological Communications. 2020, 65(4), 283–287. https://doi.org/10.21638/spbu03.2020.401

BOMFIM, C.A., et al. Brief history of biofertilizers in Brazil: from conventional approaches to new biotechnological solutions. Brazilian Journal of Microbiology. 2021, 52(4), 2215-2232. http://dx.doi.org/10.1007/s42770-021-00618-9

BOOPATHI, T., et al. Characterization of IAA production by the mangrove Cyanobacterium Phormidium sp. MI405019 and Its Influence on tobacco seed germination and organogenesis. Journal of Plant Growth Regulation. 2013, 32(4), 758-766. https://doi.org/10.1007/s00344-013-9342-8

BOURION, V., et al. Co-inoculation of a pea core-collection with diverse rhizobial strains shows competitiveness for nodulation and efficiency of nitrogen fixation are distinct traits in the interaction. Frontiers in Plant Science. 2018, 8, 2249. https://doi.org/10.3389/fpls.2017.02249

CHAUDHARI, D., et al. Pea (Pisum sativum L.) plant shapes its rhizosphere microbiome for nutrient uptake and stress amelioration in acidic soils of the North-East Region of India. Frontiers in Microbiology 2020, 11, 968-683. https://doi.org/10.3389/fmicb.2020.00968

CHEMINING'WA, G.N. and VESSEY, J.K. The abundance and efficacy of Rhizobium leguminosarum bv. viciae in cultivated soils of the eastern Canadian prairie. Soil Biology & Biochemistry. 2006, 38(2), 294-302. https://doi.org/10.1016/j.soilbio.2005.05.007

CHOUDHURY, P.R., TANVEER, H. and DIXIT, G.P. Identification and detection of genetic relatedness among important varieties of pea (Pisum sativum L.) grown in India. Genetica. 2007, 130(2), 183-191. https://doi.org/10.1007/s10709-006-9005-9

CLAYTON, G.W., et al. Inoculant formulation and fertilizer nitrogen effects on field pea: Nodulation, N2 fixation and nitrogen partitioning. Canadian Journal of Plant Science 2004, 84(1), 79–88. https://doi.org/10.4141/P02-089

DAHL, W., FOSTER, L.M. and TYLER, R.T. Review of the health benefits of peas (Pisum sativum L.). British Journal of Nutrition. 2012, 108, 3-10. https://doi.org/10.1017/S0007114512000852

DE FREITAS, J.R., GUPTA, V.V.S.R. and GERMIDA, J.J. Influence of Pseudomonas syringae R25 and P. putida R105 on the growth and N2 fixation (acetylene reduction activity) of pea (Pisum sativum L.) and field bean (Phaseolus vulgaris L.). Biology and Fertility of Soils 1993, 16(3), 215-220. https://doi.org/10.1007/BF00361411

DEY, R., et al. Growth promotion and yield enhancement of peanut (Arachis hypogaea L.) by application of plant growth-promoting rhizobacteria. Microbiological Research. 2004, 159(4), 371-394. https://doi.org/10.1016/j.micres.2004.08.004

DREW, E.A., et al. Agronomic and environmental drivers of population size and symbiotic performance of Rhizobium leguminosarum bv. viciae in Mediterranean-type environments. Crop and Pasture Science. 2012, 63(5), 467-477. https://doi.org/10.1071/CP12032

EGAMBERDIYEVA, D. Plant growth promoting properties of rhizobacteria isolated from wheat and pea grown in loamy sand soil. Turkish Journal of Biology. 2008, 32, 9-15.

EJAZ, S., et al. Effects of inoculation of root-associative Azospirillum and Agrobacterium strains on growth, yield and quality of pea (Pisum sativum L.) grown under different nitrogen and phosphorus regimes. Scientia Horticulturae. 2020, 270, 109401. https://doi.org/10.1016/j.scienta.2020.109401

FAO, 2021.FAOSTAT - Food and Agriculture Organization of the United Nations, In: FAOSTAT. Peas, D., World’s Area Harvested and Production Quantity. FAO.

FERHI, J., et al. Potential of the physiological response of pea plants (Pisum sativum L.) to iron deficiency (direct or lime- induced). Bioscience Journal. 2017, 33(5), 1208–1218. https://doi.org/10.14393/BJ-v33n5a2017-36988

FESENKO, A.N., et al. Selection of Rhizobium leguminosarum bv. viceae strains for inoculation of Pisum sativum L. cultivars: Analysis of symbiotic efficiency and nodulation competitiveness. Plant and Soil. 1995, 172(2), 189-198. https://doi.org/10.1007/BF00011321

GALLOWAY, J.N., et al. Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science (New York, N.Y.). 2008, 320(5878), 889-892. https://doi.org/10.1126/science.1136674

GAO, C., et al. The integration of bio and organic fertilizers improve plant growth, grain yield, quality and metabolism of hybrid maize (Zea mays L.). Agronomy. 2020, 10(3), 319. https://doi.org/doi:10.3390/agronomy10030319

GAVILANES, F.Z., et al. Co-inoculation of Anabaena cylindrica with Azospirillum brasilense increases grain yield of maize hybrids. Rhizosphere. 2020, 15, 100224. https://doi.org/10.1016/j.rhisph.2020.100224

GAYATHRI, M., et al. Phytohormones and free volatile fatty acids from cyanobacterial biomass wet extract (BWE) elicit plant growth promotion. Algal Research. 2017, 26, 56-64. https://doi.org/10.1016/j.algal.2017.06.022

GENEVA, M., et al. The effect of inoculation of pea plants with mycorrhizal fungi and Rhizobium on nitrogen and phosphorus assimilation. Plant, Soil and Environment 2006, 52, 435-440. https://doi.org/10.17221/3463-PSECitation:Geneva

GUPTA, A., et al. Comparative evaluation of different salt-tolerant plant growth-promoting bacterial isolates in mitigating the induced adverse effect of salinity in Pisum sativum. Biointerface Research in Applied Chemistry. 2021, 11, 13141-13154. https://doi.org/1033263/BRIAC11513114113154

HACHANA, A., et al. Patterns for Pea-Rhizobium symbiosis efficiency response to pedological and varietal variations in Tunisia. Rhizosphere. 2021, 17, 100304. https://doi.org/10.1016/j.rhisph.2020.100304

HARRIER, L. and WATSON, C., 2003. The role of arbuscular mycorrhizal fungi in sustainable cropping systems. In: Sparks, D.L. (Ed.), Advances in Agronomy Elsevier Science, Academic Press, San Diego, California, pp. 185–225.

HE, Y., et al. Symbiotic effectiveness of pea-rhizobia associations and the implications for farming systems in the western Loess Plateau, China African Journal of Biotechnology. 2011, 10(18), 3540-3548. https://doi.org/10.5897/AJB10.1568

HERRIDGE, D.F., PEOPLES, M.B. and BODDEY, R.M. Global inputs of biological nitrogen fixation in agricultural systems. Plant and Soil. 2008, 311(1), 1-18. https://doi.org/10.1007/s11104-008-9668-3

HÖFLICH, G. and RUPPEL, S. Growth stimulation of pea after inoculation with associative bacteria. Microbiology Research 1994, 149(1), 99-104. https://doi.org/10.1016/S0944-5013(11)80149-7

HORÁCIO, E.H., et al. Co-inoculation of rhizobia, azospirilla and cyanobacteria for increasing common bean production. Semina Ciências Agrárias. 2020, 41(5), 2015-2028. https://doi.org/10.5433/1679-0359.2020v41n5Supl1p2015

HUANG, J., et al. Efficacy of starter N fertilizer and rhizobia inoculant in dry pea (Pisum sativum Linn.) production in a semi-arid temperate environment. Soil Science and Plant Nutrition. 2017, 63(3), 248-253. https://doi.org/10.1080/00380768.2017.1315834

HUSSAIN, A., et al. Plant-growth-promoting Bacillus and Paenibacillus species improve the nutritional status of Triticum aestivum L., PLOS ONE. 2020, 15(12), e0241130. https://doi.org/10.1371/journal.pone.0241130

HWANG, S.F., et al. Decrease in incidence of Pythium damping-off of field pea by seed treatment with Bacillus spp. and metalaxyl. Journal of Plant Diseases and Protection. 1996, 103, 31–41.

JAUHRI, K.S., BHATNAGAR, R.S. and ISWARAN, V. Associative effect of inoculation of different strains of Azotobacter and homologous rhizobium on the yield of moong (Vigna radiata), soybean (Glycine max) and pea (Pisum sativum). Plant and Soil. 1979, 53(1), 105-108. https://doi.org/10.1007/BF02181884

JULIÃO, A.K.S., et al. Do biofertilizers affect nodulation ability and pod production in peanut genotypes?, Anais da Academia Brasileira de Ciencias. 2022, 94(2), e20201163. https://doi.org/10.1590/0001-3765202220201163

KHALIFA, A.Y.Z. and ALMALKI, M.A. Isolation and characterization of an endophytic bacterium, Bacillus megaterium BMN1, associated with root-nodules of Medicago sativa L. growing in Al-Ahsaa region, Saudi Arabia. Annals of Microbiology. 2015, 65(2), 1017-1026. https://doi.org/10.1007/s13213-014-0946-4

KHALIFA, A.Y.Z., et al. Characterization of the plant growth promoting bacterium, Enterobacter cloacae MSR1, isolated from roots of non-nodulating Medicago sativa. Saudi Journal of Biological Sciences. 2016, 23(1), 79-86. https://doi.org/10.1016/j.sjbs.2015.06.008

KING, E.B. and PARKE, J.L. Biocontrol of Aphanomyces root rot and Pythium damping-off by Pseudomonas cepacia AMMD on four pea cultivars. Plant Disease. 1993, 77(12), 1185-1188. https://doi.org/10.1094/PD-77-1185

KUMAR, A., SURI, V.K. and CHOUDHARY, A.K. Influence of inorganic phosphorus, vam fungi, and irrigation regimes on crop productivity and phosphorus transformations in okra (Abelmoschus esculentus L.)–Pea (Pisum sativum L.) cropping System in an acid Alfisol. Communications in Soil Science and Plant Analysis. 2014, 45(7), 953-967. https://doi.org/10.1080/00103624.2013.874025

KUMAR, B.S.D., BERGGREN, I. and MÅRTENSSON, A. Potential for improving pea production by co-inoculation with fluorescent Pseudomonas and Rhizobium. Plant and Soil. 2001, 229(1), 25-34. https://doi.org/10.1023/A:1004896118286

KUTCHER, H., et al. Rhizobium inoculant and seed-applied fungicide effects on field pea production. Canadian Journal of Plant Science 2002, 82(4), 645-661.

LIBERATI, A., et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. PLOS Medicine. 2009, 6(7), e1000100. https://doi.org/10.1371/journal.pmed.1000100

LIRA JUNIOR, M.d.A., et al. Effect of root temperature on nodule development of bean, lentil and pea. Soil Biology & Biochemistry. 2005, 37(2), 235-239. https://doi.org/10.1016/j.soilbio.2004.07.032

LUGTENBERG, B. and KAMILOVA, F. Plant-Growth-Promoting Rhizobacteria. Annual Review of Microbiology. 2009, 63(1), 541-556. https://doi.org/10.1146/annurev.micro.62.081307.162918

MABROUK, Y., et al. The potential of Rhizobium strains for biological control of Orobanche crenata. Biologia, Bratislava. 2007, 62(2), 139-143. https://doi.org/10.2478/s11756-007-0021-8

MÄDER, P., et al. Inoculation of root microorganisms for sustainable wheat–rice and wheat–black gram rotations in India. Soil Biology & Biochemistry. 2011, 43(3), 609-619. https://doi.org/10.1016/j.soilbio.2010.11.031

MESFIN, S., et al. Mineral Fertilizer Demand for Optimum Biological Nitrogen Fixation and Yield Potentials of Legumes in Northern Ethiopia. Sustainability. 2020, 12(16), 6449. https://doi.org/10.3390/su12166449

MISHRA, P.K., et al. Coinoculation of Rhizobium leguminosarum-pr1 with a cold tolerant Pseudomonas sp. improves iron acquisition, nutrient uptake and growth of field pea (Pisum sativum L.). Journal of Plant Nutrition. 2012, 35(2), 243-256. https://doi.org/10.1080/01904167.2012.636127

MISHRA, P.K., et al. Coinoculation of Bacillus thuringeinsis-KR1 with Rhizobium leguminosarum enhances plant growth and nodulation of pea (Pisum sativum L.) and lentil (Lens culinaris L.). World Journal of Microbiology and Biotechnology. 2009, 25(5), 753-761. https://doi.org/10.1007/s11274-009-9963-z

MORENO-CHIRINOS, Z.E., et al. Eficiencia en la nodulación por rizobios nativos, procedentes de nódulos de Pisum sativum "arveja" colectados de diferentes Departamentos del Perú. Scientia Agropecuaria. 2016, 7(3), 165-172.

MUNIZ, A., et al. Symbiotic efficiency of pea (Pisum sativum) rhizobia association under field conditions. African Journal of Agricultural Research. 2017, 12(32), 2582-2585. https://doi.org/10.5897/AJAR2017.12257

MUTCH, L.A. and YOUNG, J.P.W. Diversity and specificity of Rhizobium leguminosarum biovar viciae on wild and cultivated legumes. Molecular Ecology. 2004, 13(8), 2435-2444. https://doi.org/10.1111/j.1365-294X.2004.02259.x

OONO, R., ANDERSON, C.G. and DENISON, R.F. Failure to fix nitrogen by non-reproductive symbiotic rhizobia triggers host sanctions that reduce fitness of their reproductive clonemates. Proceedings of the Royal Society B: Biological Sciences. 2011, 278(1718), 2698-2703. https://doi.org/10.1098/rspb.2010.2193

OSMAN, M.E.H., et al. Effect of two species of cyanobacteria as biofertilizers on some metabolic activities, growth, and yield of pea plant. Biology and Fertility of Soils 2010, 46(8), 861-875. https://doi.org/10.1007/s00374-010-0491-7

PARIHAR, M., et al. A consortium of arbuscular mycorrizal fungi improves nutrient uptake, biochemical response, nodulation and growth of the pea (Pisum sativum L.) under salt stress. Rhizosphere. 2020a, 15, 100235. https://doi.org/10.1016/j.rhisph.2020.100235

PARIHAR, M., et al. The effect of arbuscular mycorrhizal fungi inoculation in mitigating salt stress of pea (Pisum sativum L.). Communications in Soil Science and Plant Analysis. 2020b, 51(11), 1545-1559. https://doi.org/10.1080/00103624.2020.1784917

PEOPLES, M., et al. The contributions of nitrogen-fixing crop legumes to the productivity of agricultural systems. Symbiosis. 2009, 48(1-3), 1-17. https://doi.org/10.1007/bf03179980

PRASANNA, R., et al. Prospecting cyanobacteria-fortified composts as plant growth promoting and biocontrol agents in cotton. Experimental Agriculture 2014a, 51(1), 42-65. https://doi.org/10.1017/S0014479714000143

PRASANNA, R., et al. Evaluating the establishment and agronomic proficiency of cyanobacterial consortia as organic options in wheat–rice cropping sequence. Experimental Agriculture 2013, 49(3), 416-434. https://doi.org/10.1017/S001447971200107X

PRASANNA, R., et al. Evaluating the efficacy of cyanobacterial formulations and biofilmed inoculants for leguminous crops. Archives of Agronomy and Soil Science. 2014b, 60(3), 349-366. https://doi.org/10.1080/03650340.2013.792407

RABBANI, M.G., et al. Effects of Rhizobium inoculant, nitrogen, phosphorus and molybdenum on nodulation, yield and seed protein in pea. Korean Journal of Crop Science 2005, 50(2), 112-119.

RAHI, P., et al. Rhizobium indicum sp. nov., isolated from root nodules of pea (Pisum sativum) cultivated in the Indian trans-Himalayas. Systematic and Applied Microbiology. 2020, 43(5), 126-127. https://doi.org/10.1016/j.syapm.2020.126127

RANA, A., et al. Biofortification of wheat through inoculation of plant growth promoting rhizobacteria and cyanobacteria. European Journal of Soil Biology. 2012, 50, 118-126. https://doi.org/10.1016/j.ejsobi.2012.01.005

RAPČAN, I., et al. Reaction of garden pea (Pisum sativum L.) to inoculation and nitrogen fertilization in Eastern Croatia Journal of Central European Agriculture. 2017, 18(4), 889-901. https://doi.org/10.5513/jcea.v18i4.5920

RATINAUD, P., 2008.IRAMUTEQ: Interface de R pour les analyses multidimensionnelles de textes et de questionnaires [Computer software].

RÍOS-RUIZ, W.F., et al. Inoculation of bacterial consortium increases rice yield (Oryza sativa L.) reducing applications of nitrogen fertilizer in San Martin region, Peru. Rhizosphere. 2020, 14, 100200. https://doi.org/10.1016/j.rhisph.2020.100200

SHABAAN, M., et al. Role of plant growth promoting rhizobacteria in the alleviation of lead toxicity to Pisum sativum L., International journal of phytoremediation. 2021, 23(8), 837-845. https://doi.org/10.1080/15226514.2020.1859988

SINGH, S., et al. Plant growth promoting rhizobacteria from heavy metal contaminated soil promote growth attributes of Pisum sativum L., Biocatalysis and Agricultural Biotechnology. 2019, 17, 665-671. https://doi.org/10.1016/j.bcab.2019.01.035

SLATTERY, J.F., PEARCE, D.J. and SLATTERY, W.J. Effects of resident rhizobial communities and soil type on the effective nodulation of pulse legumes. Soil Biology & Biochemistry. 2004, 36(8), 1339-1346. https://doi.org/10.1016/j.soilbio.2004.04.015

SMÝKAL, P., et al. Phylogeny, phylogeography and genetic diversity of the Pisum genus. Plant Genetic Resources 2011, 9(1), 4-0. https://doi.org/10.1017/s147926211000033x

SOUSA, J.X.d., et al. The Bradyrhizobium uaiense strain UFLA 03-164T enhanced yield performance of cowpea in soils with low or high phosphorus content. Bioscience Journal. 2022, 38, e38065. https://doi.org/10.14393/BJ-v38n0a2022-54182

SUPRONIENE, S., et al. Selection of Rhizobium strains for inoculation of Lithuanian Pisum sativum breeding lines. Symbiosis. 2021, 83(2), 193-208. https://doi.org/10.1007/s13199-021-00747-7

TENA, W., WOLDE-MESKEL, E. and WALLEY, F. Symbiotic efficiency of native and exotic Rhizobium strains nodulating lentil (Lens culinaris Medik.) in soils of Southern Ethiopia. Agronomy. 2016, 6(1), 11. https://doi.org/10.3390/agronomy6010011

TORONTO, C. and REMINGTON, R., 2020. A step-by-step guide to conducting an integrative review. Springer.

UHER, D., et al. Importance of winter pea cv. Maksimirski rani in milk production on family farms. Mljekarstvo. 2010, 60(1), 37-49.

UYANÖZ, R. and KARACA, Ü. Effects of different salt concentrations and Rhizobium inoculation (native and Rhizobium tropici CIAT899) on growth of dry bean (Phaseolus vulgaris L.). European Journal of Soil Biology 2011, 47(6), 387-391. https://doi.org/10.1016/j.ejsobi.2011.07.007

VOISIN, A.-S., et al. Using an ecophysiological analysis to dissect genetic variability and to propose an ideotype for nitrogen nutrition in pea. Annals of Botany. 2007, 100(7), 1525-1536. https://doi.org/10.1093/aob/mcm241

WANG, H., et al. Suppression of important pea diseases by bacterial antagonists. BioControl. 2003, 48(4), 447-460. https://doi.org/10.1023/A:1024794809751

YOLCU, H., et al. Effects of plant growth-promoting rhizobacteria on some morphologic characteristics, yield and quality contents of Hungarian vetch. Turkish Journal of Field Crops. 2012, 17(2), 208-214. https://dergipark.org.tr/en/pub/tjfc/issue/17123/179072

ZAFAR, M., et al. Effect of plant growth-promoting rhizobacteria on growth, nodulation and nutrient accumulation of lentil under controlled conditions. Pedosphere. 2012, 22(6), 848-859. https://doi.org/10.1016/S1002-0160(12)60071-X

Downloads

Publicado

2024-07-18

Como Citar

VALENCIA, H.A.M., AMARAL, H.F., NASSAR, J.M. e ANDRADE, D.S., 2024. Rhizobia inoculation increases pea grain yield: an overview and challenges. Bioscience Journal [online], vol. 40, pp. e40034. [Accessed22 dezembro 2024]. DOI 10.14393/BJ-v40n0a2024-67453. Available from: https://seer.ufu.br/index.php/biosciencejournal/article/view/67453.

Edição

Seção

Ciências Agrárias