Plant growth-promoting microorganisms as mitigators of water stress in pastures: a narrative review

Authors

DOI:

https://doi.org/10.33448/rsd-v11i11.34029

Keywords:

Bacteria; Fungi; Mycorrhiza; Co-inoculation; Resilience.

Abstract

Water stress is a reality present in pastoral areas throughout Brazil, and more challengingly in semi-arid regions. These climatic conditions test the tolerance to water stress of the forage species used, which despite their rusticity, markedly decrease their performance in low water availability, which limits the expression of all their productive potential. In this sense, it is important to search for sustainable technologies that help a greater resilience of animal production on pasture and that are beneficial to the environment, such as the use of microorganisms that promote plant growth, which can potentially help these species to tolerate the deleterious effects of water stress. Therefore, the objective of this review was to compile information on the use of plant growth-promoting bacteria, arbuscular mycorrhizal fungi and their co-inoculation with water stress mitigating agents in forage plants. In view of data obtained from research platforms, the effects of inoculations with beneficial soil microorganisms on morphophysiological and productive characteristics of forage plants were addressed and how this symbiosis can potentially help plants to tolerate water stress, in addition to describing the specifics of the tripartite relationship between fungi, bacteria and forage plants. With this review, it was found that the use of microbiological inputs as modulators of species tolerance to drought has potential use, requiring a greater volume of studies to consolidate the technique in a way that strengthens it with a sustainable and resilient alternative of livestock to pasture.

References

Abdul Jaleel, C., Manivannan, P., Kishorekumar, A., Sankar, B., Gopi, R., Somasundaram, R. & Paneerselvam, R. (2007). Alterations in osmoregulation, antioxidante enzymes and indole alkaloid levels in Catharanthus roseus exposed to water deficit. Colloids and Surfaces B: Biointerfaces. 59(2), p.150-157.

Abbaspour, H., Saeidi-sar, S., Afshari, H. & Abdel-Wahhab, M. A. (2012). Tolerance of mycorrhiza infected pistachio (Pistacia vera L.) seedling to drought stress under glasshouse conditions. J. Plant Physiol. 169(7), p.704-709.

Ahemad, M. & Kibret, M. (2014). Mechanisms and applications of plant growth promoting rhizobacteria: current perspective. J. King Saud Univ. Sci. 26(1), p.1–20.

Allen, M. F. (2009). Bidirectional water flows through the soil-fungalplant mycorrhizal continuum. New Phytol. 182(2), p.290-293.

Amiri, R. A., Nikbakht, A. & Etemadi, N. (2015). Alleviation of drought stress on rose geranium [Pelargonium graveolens (L.) Herit.] in terms of antioxidant activity and secondary metabolites by mycorrhizal inoculation. Sci. Hortic. 197, p.373-380.

Ambrósio, L. A., Toledo, L. M. & Demski, J. B. (2018). Operacionalização do conceito de resiliência de forrageiras sob pastoreio rotativo aos distúrbios de mudanças climáticas. Boletim de Indústria Animal. 75, p.1-15.

Aroca, R. (2012). Plant responses to drought stress. From morphological to molecular features, 1-5.

Atul-Nayyar, A.., Hamel, C., Hanson, K., & Germida, J. (2009). The arbuscular mycorrhizal symbiosis links N mineralization to plant demand. Mycorrhiza, 19, p.239-246.

Augé, R. M., Toler, H. D., Sams, C. E., & Nasim. G. (2008). Hydraulic conductance and water potential gradients in squash leaves showing mycorrhiza-induced increases in stomatal conductance. Mycorrhiza, 18, p.115-21.

Augé, R. M. (2004). Arbuscular mycorrhizae and soil/plant water relations. Can. J. Soil Sci. 84, p.373-381.

Bagyaraj, D. J; Sharma, M. P., & Maiti, D. (2015). Phosphorus nutrition of crops through arbuscular mycorrhizal fungi. Curr Sci, 108(7), p.1288–1293.

Bal, H. B., Nayak, L., Das, S. & Adhya, T. K. Isolation of ACC deaminase producing PGPR from rice rhizosphere and evaluating their plant growth promoting activity under salt stress. Plant and soil. 366, p.93–105.

Barbosa, M. R., Silva, M. M. A., Willadino, L., Ulisses, C. & Camara, T. R. (2014). Geração e desintoxicação enzimática de espécies reativas de oxigênio em plantas. Ciência Rural, Santa Maria, 44(3), p.453-460.

Bauer, J. T., Kleczewski, N. M., Bever, J. D., Clay, K. & Reynolds, H. L. (2012). Nitrogen-fixing bacteria, arbuscular mycorrhizal fungi, and the productivity and structure of prairie grassland communities. Oecologia, v. 170, p.1089–1098.

Bechtaoui, N., Raklami, A., Benidire, L., Tahiri, A.I., Göttfert, M., & Oufdou, K. (2020). Effects of PGPR Co-inoculation on growth, phosphorus nutrition and phosphatase/phytase activities of faba bean under different phosphorus availability conditions. Polish J. Environ. Stud. 29, 1557–1565.

Behrooz, A., Vahdati, K., Rejali, F., Lotfi, M., Sarikhani, S. & Leslie, C. (2019). Arbuscular mycorrhiza and plant growth-promoting bacteria alleviate drought stress in walnut. Hortscience, 54(6): p.1087–1092.

Bellone, C; & Carrizo de Bellone, S. (2012). Interaction of Azospirillum brasilense and Glomus intrarradis in sugar cane roots. Indian J Microbiol, 52(1): p.70–75.

Biró, B., Köves-Péchy, K., Vörös, I., Takács, T., Eggenberger, P. & Strasser, R. J. (2000). Interrelations between Azospirillum and Rhizobium nitrogen-fi xers and arbuscular mycorrhizal fungi in the rhizosphere of alfalfa in sterile, AMF-free or normal soil conditions. Appl Soil Ecol, 15, p.159–168.

Bulegon, L. G., Guimarães, V. F., & Laureth, J. C. U. (2016). Azospirillum brasilense affects the antioxidant activity and leaf pigment content of Urochloa ruziziensis under water stress. Pesquisa Agropecuária Tropical [online]. v.46, n.3, p. 343-349..

Bulegon, L. G., Battistus, A. G., Guimaraes, V. F., Inagaki, A. M., Offemann, L. C., De Souza, A. K. P. & De Oliveira, P. S. R. (2017). Physiological responses of “Urochloa ruziziensis” inoculated with “Azospirillum brasilense” to severe drought and rehydration conditions. Australian Journal of Crop Science, 11(10), p.1283-1289.

Bulegon, L.G., Guimarães, V. F., Cecatto Júnior, R., Battistus, A. G., Inagaki, A. N., & Suss, A. D. (2019). Photosynthetic and Production of Urochloa ruziziensis Inoculated with Azospirillum brasilense under Drought. Journal of Experimental Agriculture International. 38(6). p.1-9.

Butt, Y. N., Fatima, Q., Nasar, S., Ikram, J., & Akram, S. (2017). Drought tolerance in plants: a review. Res. Rev. J. Ecol. Environ. Sci, 5(4), 20-28.

Bhale, U. N., Bansode, S. A., & Singh, S. (2018). Multifactorial role of arbuscular mycorrhizae in agroecosystem. In Fungi and their role in sustainable development: Current perspectives, p. 205-220.

Bhowmik, S. N., & Singh, C. S. (2004). Mass multiplication of AM inoculum: effect of plant growth-promoting rhizobacteria and yeast in rapid culturing of Glomus mosseae. Current Science, 705-709.

Blum, A. (2005). Drought resistance, water-use efficiency, and yield potential—are they compatible, dissonant, or mutually exclusive?. Australian Journal of Agricultural Research, 56(11), 1159-1168.

Carrizo, I. M., Lopez Colomba, E., Tommasino, E., Carloni, E., Bollati, G., & Grunberg, K. (2021). Contrasting adaptive responses to cope with drought stress and recovery in Cenchrus ciliaris L. and their implications for tissue lignification. Physiologia Plantarum, 172(2), 762-779.

Cortés-Patiño, S., Vargas, C., Álvarez-Flórez, F., Bonilla, R. & Estrada-Bonilla, G. (2021). Potential of Herbaspirillum and Azospirillum Consortium to Promote Growth of Perennial Ryegrass under Water Deficit. Microorganisms, 9(1), p. 1-16.

Chen, W., Meng, P., Feng, H., & Wang, C. (2020). Effects of arbuscular mycorrhizal fungi on growth and physiological performance of Catalpa bungei CA Mey. under drought stress. Forests, 11(10), 1117.

Danneberg, G., Latus, C., Zimmer, W., Hundeshagen, B., Schneider-Poetsch, H. J. & Bothe, H. (1992). Influence of vesicular-arbuscular mycorrhiza on phytohormone balances in maize (Zea mays L.). J Plant Physiol, 141(1): p.33–39.

Dimkpa, C., Weinand, T., & Asch, F. (2009). Plant–rhizobacteria interactions alleviate abiotic stress conditions. Plant, Cell and Environment, Germany, v.32, n.1, p.1682–1694.

Domínguez-Núñez, J. A., Berrocal-Lobo, M., & Albanesi, A. S. (2015). Interaction of Azospirillum and mycorrhiza. In Handbook for Azospirillum, p. 419-432.

Farooq, M., Wahid, A., Kobayashi, N. S. M. A., Fujita, D. B. S. M. A., & Basra, S. M. A. (2009). Plant drought stress: effects, mechanisms and management. Agron. Sustain. Dev. 29, p.185–212.

Farooq, M., Hussain, M., Wahid, A., & Siddique, K. H. M. (2012). Drought stress in plants: an overview. Plant responses to drought stress, p.1-33.

Ferreira, E. P. B., Knupp, A. M., & Martin-Didonet, C. C. G. (2014). Crescimento de cultivares de arroz (Oryza sativa L.) influenciado pela inoculação com bactérias promotoras de crescimento de plantas. Bioscience Journal, Uberlândia, 30(3), p. 655-665.

Fernández-Lizarazo J. C. & Moreno-Fonseca L. P. (2016). Mechanisms for tolerance to water-deficit stress in plants inoculated with arbuscular mycorrhizal fungi. A review. Agron. Colomb. v.34, p.179–189.

Ferrera-Cerrato, R., & Alarcón, A. (2004). Biotecnología de los hongos micorrízicos arbusculares. In Memoria Simposio de Biofertilización (eds). Río Bravo, Tampa, México, p. 1-9.

Fukami, J., Ollero, F. J., De La., Osa, C., Valderrama Fernández, R., Nogueira, M. A., Megías, M. & Hungria, M. (2018). Antioxidant activity and induction of mechanisms of resistance to stresses related to the inoculation with Azospirillum brasilense. Arch Microbiol. 200: p.1191-203.

Fracasso, A., Telò, L., Lanfranco, L., Bonfante, P. & Amaducci, S. (2020). Physiological beneficial effect of Rhizophagus intraradices inoculation on tomato plant yield under water deficit conditions. Agronomy, 10, p.1-21.

Francisco, P. R. M., Bandeira, M. M., Santos, D., Pereira, F. C., & Gonçalves, J. L. G. (2016). Aptidão climática da cultura do feijão comum (Phaseolus vulgaris) para o estado da Paraíba. Revista Brasileira de Climatologia, Paraíba-PB, 19(1), p. 366-378.

Gaiero, J. R., McCall, C. A., Thompson, K. A., Day, N. J., Best, A. S., & Dunfield, K. E. (2013). Inside the root microbiome: bacterial root endophytes and plant growth promotion. American journal of botany, 100(9), 1738-1750.

Gamalero, E., Berta, G., & Glick, B. R. (2009). The use of microorganisms to facilitate the growth of plants in saline soils. In: Khan MS, Zaidi A, Musarrat J (eds) Microbial strategies for crop improvement. Springer, Berlin, p 1–22.

Goswami, D., P, S., Vaghela, H., Dhandhukia, P., & Thakker, J. (2015). Describing Paenibacillus mucilaginosus strain N3 as an efficient plant growth promoting rhizobacteria (PGPR). Cogent Food & Agriculture, 1(1), p.1-13.

Glick, B. R. (2004). Bacterial ACC deaminase and the alleviation of plant stress. Adv Appl Microbiol, 56, p.291–312.

Glick, B. R. (2014). Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiológical Research, 169(1), p.30-39.

Glick, B. R. (2012). "Plant Growth-Promoting Bacteria: Mechanisms and Applications", Scientifica, vol.2012, p.1-15.

Guimarães, G. S., Rondina, A. B. L., Santos, M. S., Nogueira, M. A., & Hungria, M. (2022). Pointing Out Opportunities to Increase Grassland Pastures Productivity via Microbial Inoculants: Attending the Society’s Demands for Meat Production with Sustainability. Agronomy, 12(8), 1-23.

Guirra, B. S., Silva, J. A., Leal, C. C. P., Torres, S. B., Da Silva, J. E. S. B., Guirra, K. S., & Pereira, K. T. O. (2022). Growth and metabolism of Pityrocarpa moniliformis Benth. seedlings under water deficit. Ciência Florestal, 32(2), p.923-938.

Hungria, M., Campo, R. J., Souza, E. M. E., Pedrosa, F. O. (2010). Inoculation with selected strains of Azospirillum brasilense and A. lipoferum improves yields of maize and wheat in Brazil. Plant and Soil, v.331, p.413-425.

Hungria, M., Rondina, A. B. L., Nunes, A. L. P., Araújo, R. S., Nogueira, N. A. (2021). Seed and leaf-spray inoculation of PGPR in brachiarias (Urochloa spp.) as an economic and environmental opportunity to improve plant growth, forage yield and nutrient status. Plant Soil, 463, p.171–186.

Stocker, T. (Ed.). (2014). Climate change 2013: the physical science basis: Working Group I contribution to the Fifth assessment report of the Intergovernmental Panel on Climate Change. Cambridge university press.

Jaderlund, L., Arthurson, V., Granhall, U., Jansson, J. K. (2008). Specific interactions between arbuscular mycorrhizal fungi and plant growth-promoting bacteria: as revealed by different combinations. FEMS Microbiol Lett, 287, p.174–80.

Jakobsen, I., Abbott, L. K., Robson, A. D. (1992). External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium subterraneum L. New Phytologist, 120, p.371-380.

Jeffries, P., Gianinazzi, S., Perotto, S., Turnau, K. & Barea, J. (2003). The contribution of arbuscular mycorrhizal fungi in sustainable maintenance of plant health and soil fertility. Biol Fertil Soils, 37, p.1–16.

Jiang, S., Zhang, D., Wang, L., Pan, J., Liu, Y., Kong, X., Zhou, Y. & Li D. (2013). A maize calcium-dependent protein kinase gene, ZmCPK4, positively regulated abscisic acid signaling and enhanced drought stress tolerance in transgenic Arabidopsis. Plant Physiol. Biochem. 71, p.112–120.

Jiang, F., Zhang, L., Zhou, J., George, T. S. & Feng, G. (2021). Arbuscular mycorrhizal fungi enhance mineralisation of organic phosphorus by carrying bacteria along their extraradical hyphae. New Phytol, 230: p.304-315.

Kaushal, M. & WANI, S. P. (2016). Plant-growth-promoting rhizobacteria: drought stress alleviators to ameliorate crop production in drylands. Ann. Microbiol. 66, p.35–42.

Kiani, S. P., Talia, P., Maury, P., Grieu, P., Heinz, R., Perrault, A., Nishinakamasu, V., Hopp, E., Gentzbittel, L., Paniego, N. & Sarrafi, A. (2007). Genetic analysis of plant water status and osmotic adjustment in recombinant inbred lines of sunflower under two water treatments. Plant Science, 172(4), p.773-787.

Kpomblekou, A. K., Tabatabai, M. A. (1994). Effect of organic acids on release of phosphorus from phosphate rocks. Soil Science, 158, p.442-453.

Kumar, A. & Verma, J. P. (2018). Does plant—Microbe interaction confer stress tolerance in plants: A review?. Microbiológical Research, 207, p.41–52.

Lau, J. A. & Lennon, J. T. (2011). Evolutionary ecology of plant–microbe interactions: soil microbial structure alters selection on plant traits. New Phytol, 192, p.215–24.

Lawlor, D. W. & Cornic, G. (2002). Photosynthetic carbon assimilation and associated metabolism in relation to water deficits in higher plants. Plant, Cell Environ, 25: p.275–294.

Leite, R. D. C., dos Santos, J. G., Silva, E. L., Alves, C. R., Hungria, M., Leite, R. D. C., & dos Santos, A. C. (2018). Productivity increase, reduction of nitrogen fertiliser use and drought-stress mitigation by inoculation of Marandu grass (Urochloa brizantha) with Azospirillum brasilense. Crop and Pasture Science, 70(1), p.61-67.

Lemaire, G. (2001). Ecophysiology of grasslands: dynamic aspects of forage plant populations in grazed swards. In: International Grassland Congress. São Paulo: SBZ, p.29-37.

Levy, A., Merritt, A. J., Mayo, M. J., Chang, B. J., Abbott, L. K., & Inglis, T. J. (2009). Association between Burkholderia species and arbuscular mycorrhizal fungus spores in soil. Soil Biology and Biochemistry, 41(8), p.1757-1759.

Li, Y., Ye, W., Wang, M., & Yan, X. (2009). Climate change and drought: a risk assessment of crop-yield impacts. Climate research, 39(1), p.31-46.

Li, T., Lin, G., Zhang, X., Chen, Y., Zhang, S., & Chen, B. (2014). Relative importance of an arbuscular mycorrhizal fungus (Rhizophagus intraradices) and root hairs in plant drought tolerance. Mycorrhiza, 24(8), p.595-602.

Lima, J. B. M. P., Rodríguez, N. M., Martha Júnior, G. B., Guimarães Júnior, R., Vilela, L., Graça, D. S., & Saliba, E. O. S. (2012). Suplementação de novilhos Nelore sob pastejo, no período de transição águas-seca. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 64, 943-952.

Magalhães, A. J., Alves, J. M. B., Silva, E. M. D., Nunes, F. T., Barbosa, A. C. B., Santos, A. C. S. D., & Sombra, S. S. (2020). Verânicos no Brasil: Observações e Modelagens (CMIP5). Revista Brasileira de Meteorologia, 34, 597-626.

Mamédio, D., Cecato, U., Sanches, R., da Silva, S. M. D. S., da Silva, D. R., & Rodrigues, V. O. (2020). Bactérias promotoras do crescimento de plantas contribuem para a maior persistência das pastagens tropicais em déficit hídrico? Uma revisão. Research, Society and Development, 9(8),p.1-30.

Maranhão, S. R., Pompeu, R. C. F. F., Souza, H. A., Araújo, R. A., Fontinele, R.G. & Cândido, M. J. D. (2019). Morphophysiology of buffel grass grown under diferent water supplies in the dry and dry-rainy seasons. Revista Brasileira de Engenharia Agrícola e Ambiental, 23(8), p.566-571.

Marengo, J. A., Torres, R. R., & Alves, L. M. (2017). Drought in Northeast Brazil—past, present, and future. Theoretical and Applied Climatology, 129(3), p.1189-1200.

Marulanda, A., Azcon, R., & Ruiz‐Lozano, J. M. (2003). Contribution of six arbuscular mycorrhizal fungal isolates to water uptake by Lactuca sativa plants under drought stress. Physiologia Plantarum, 119(4), p.526-533.

Miyauchi, M. Y. H., Lima, D. S., Nogueira, M. A., Lovato, G. M., Murate, L. S., Cruz, M. F., Ferreira, J. M., Zangaro, W. & Andrade, G. (2008). Interactions between diazotrophic bacteria and mycorrhizal fungus in maize genotypes. Scientia Agricola, 65, p.525-531.

Miransari, M., Bahrami, H. A., Rejali, F., & Malakouti, M. J. (2008). Using arbuscular mycorrhiza to alleviate the stress of soil compaction on wheat (Triticum aestivum L.) growth. Soil biology and biochemistry, 40(5), p.1197-1206.

Nadeem, S. M., Ahmad, M., Zahir, Z. A., Javaid, A., & Ashraf, M. (2014). The role of mycorrhizae and plant growth promoting rhizobacteria (PGPR) in improving crop productivity under stressful environments. Biotechnol. Adv. 32, p.429–448..

Naing, A. H., & Kim, C. K. (2021). Abiotic stress‐induced anthocyanins in plants: Their role in tolerance to abiotic stresses. Physiologia Plantarum, 172(3), p.1711-1723.

Neilands, J. B. (1981). Iron adsorption and transport in microorganisms. Annu Rev Nut, 1, p.27–46.

Odokonyero, K., Acuna, T. B., Cardoso, J. A., Jimenéz, J. D. L. C., & Rao, I. M. (2017). Effect of endophyte association with Brachiaria species on shoot and root morpho-physiological responses under drought stress. Journal of Plant Biochemistry and Physiology, 5(1), 1-10.

Ozkur, O., Ozdemir, F., Bor, M. & Turkan, I. (2009). Physiochemical and antioxidant responses of the perennial xerophyte Capparis ovata Desf. to drought. Environ Exp Bot, 66, p.487–492.

Paula, M. A.., Reis, V. M. & Döbereiner, J. (1991). Interations of Glomus clarum with A. dizotrophicus in infection of sweet potato, sugar cane, sweet sorghum. Biology and Fertility of Soils, 11, p.111-115.

Pimentel, R. M., Bayão, G. F. G., Lelis, D. L., Cardoso, A. J. da S., Saldarriaga, F. V., Melo, C. C. V. & Souza, F. B. M. V. (2016). Ecofisiologia de plantas forrageiras. PUBVET, 10(9), p.666-679.

Porto, E. M. V., Amaro, H. T. R., Alves, D. D., Andrade, W. R., Rufino, L. D. A. & Gomes, V. M. (2022). O capim Andropogon. Informe agropecuário, Belo horizonte, 43(317), p. 26-36.

Raimam, M. P., Albino, U., Cruz, M. F., Lovato, G. M., Spago, F., Ferracin, T. P., Lima D. S., Goulart, T., Bernardi, C. M., Miyauchi, M., Nogueira, M. A. & Andrade, G. (2007). Interaction among free-living N-fixing bacteria isolated from Drosera villosa var. villosa and AM fungi (Glomus clarum) in rice (Oryza sativa). Applied Soil Ecology, 35(1), p.25-34.

Reis, R. A., Ruggieri, A. C., Oliveira, A. A., Azenha, M. V. (2011). Manejo da pastagem, diferimento, e estratégias de suplementação na engorda de bovinos no pasto. In.: X Congresso sobre Manejo e Nutrição de Bovinos. Anais... Campo Grande, 2011.

Revillini, D., Gehring, C. A., & Johnson, N. C. (2011). The role of locally adapted mycorrhizas and rhizobacteria in plant—soil feedback systems. Functional Ecology, 30(7), p.1086–1098.

Rodriguez, H., Gonzalez, T., Goire, I. & Bashan, Y. (2004). Gluconic acid production and phosphate solubilization by the plant growth-promoting bacterium Azospirillum spp. Naturwissenschaften, 91, p.552–555.

Rouseaux, R. R., Cañizares, P. J. C. & Pedroso, J. F. R. (2020). Biofertilization with Azospirillum brasilense and Rhizoglomus irregulare and reduction of nitrogen fertilization in Urochloa hybrid cv. Mulatto II. Cuban Journal of Agricultural Science, v.54, n.4, p.611-620.

Roth, M. T. P., Resende, F. D., Oliveira, I. M., Fernandes, R. M., Custódio, L., & Siqueira, G. R. (2017). Does supplementation during previous phase influence performance during the growing and finishing phase in Nellore cattle?. Livestock Science, 204, p.122-128.

Ruiz-Lozano, J. M., Porcel, R., Bárzana, G., Azcón, R., & Aroca, R. (2012). Contribution of arbuscular mycorrhizal symbiosis to plant drought tolerance: state of the art. Plant responses to drought stress, p.335-362.

Ruíz-Sánchez, M,. Armada, E., Munoz, Y., Salamone, I. E., Aroca, R., Ruíz-Lozano, J. M. & Azcón, R. (2011). Azospirillum and arbuscular mycorrhizal colonization enhance rice growth and physiological traits under well-watered and drought conditions. J Plant Physiol, 168, p.1031–1037.

Sadava, D., Heller, H. C., Orians, G. H., Purves, W. K., Hillis, D. M. (2009). Vida: a ciência da biologia. V.2: Evolução, Diversidade e Ecologia. Porto Alegre: Artmed.

Santos, N. L., Azenha, M. V., Souza, F. H. M., Reis, F. A. & Ruggieri, A. C. (2011). Fatores ambientais e de manejo na qualidade de pastos tropicais. enciclopédia biosfera, Centro Científico Conhecer - Goiânia, 7(13), 531-549.

Serkedjieva, J. (2011). Antioxidant effects of plant polyphenols: a case study of a polyphenol-rich extract from Geranium sanguineum L. Reactive oxygen species and antioxidants in higher plants, 13, p.275-293.

Serraj, R. & Sinclair, T. R. (2002). Osmolyte accumulation: can it really help increase crop yield under drought conditions? Plant, Cell & Environment, 25, p.333-341.

Siddiqui, Z. S., Shahid, H., Cho, J. I., Park, S. H., Ryu, T. H. & Park, S. C. (2016). Physiological responses of two halophytic grass species under drought stress environment. Acta Botanica Croatica, 75, p.31–38.

Sikes, B. A. (2010). When do arbuscular mycorrhizal fungi protect plant roots from pathogens? Plant Signal Behav, 5, p.763–765.

Silvana, V. M., Carlos, F. J., Lucía, A. C., Natalia, A., & Marta, C. (2020). Colonization dynamics of arbuscular mycorrhizal fungi (AMF) in Ilex paraguariensis crops: Seasonality and influence of management practices. Journal of King Saud University-Science, 32(1), p.183-188.

Souza, R. D., Ambrosini, A., & Passaglia, L. M. (2015). Plant growth-promoting bacteria as inoculants in agricultural soils. Genetics and molecular biology, 38, 401-419.

Shaffique, S., Khan, M. A., Imran, M., Kang, S. M., Park, Y. S., Wani, S. H., & Lee, I. J. (2022). Research Progress in the Field of Microbial Mitigation of Drought Stress in Plants. Frontiers in Plant Science, 13.

Taiz, L., Zeiger, E., Møller, I. M., & Murphy, A. (2017). Fisiologia e desenvolvimento vegetal. Porto Alegre. 6 ed. Artmed Editora. 888p.

Toljander, J. F., Artursson, V., Paul, L. R., Jansson, J. K., & Finlay, R. D. (2006). Attachment of different soil bacteria to arbuscular mycorrhizal fungal extraradical hyphae is determined by hyphal vitality and fungal species. FEMS Microbiology Letters, 254(1), p.34-40.

Tyagi, J.., Varma, A.; & Pudake, R. N. (2017). Evaluation of comparative effects of arbuscular mycorrhiza (Rhizophagus intraradices) and endophyte (Piriformospora indica) association with finger millet (Eleusine coracana) under drought stress. European Journal of Soil Biology, 81, p.1-10.

Tommasino, E., Colomba, E. L., Carrizo, M., Grunberg, K., Quiroga, M., Carloni, E., Griffa, S. Ribotta, A. & Luna, C. (2018). Individual and combined effects of drought and heat on antioxidant parameters and growth performance in Buffel grass (Cenchrus ciliaris L.) genotypes. South African Journal of Botany, 119, 104-111.

Videira, S. S., de Oliveira, D. M., de Morais, R. F., Borges, W. L., Baldani, V. L. D., & Baldani, J. I. (2012). Genetic diversity and plant growth promoting traits of diazotrophic bacteria isolated from two Pennisetum purpureum Schum. genotypes grown in the field. Plant and Soil, 356(1), p.51-66.

Villarreal, T. C., Medina, M. E., Ulloa, S. M., Darwin, R. O., Bangeppagari, M., Selvaraj, T., & Sikandar, I. M. (2016). Effect of Arbuscular mycorrhizal fungi (AMF) and Azospirillum on growth and nutrition of banana plantlets during acclimatization phase. Journal of Applied Pharmaceutical Science, 6(06), p.131-138.

Vosgerau, D. S. A. R. & Romanowski, J. P. (2014). Estudos de revisão: implicações conceituais e metodológicas. Diálogo Educacional, 14 (41), 165-189.

Wang, Y., Brown, H. N., Crowley, D. E., & Szaniszlo, P. J. (1993). Evidence for direct utilization of a siderophore, ferrioxamine B, in axenically grown cucumber. Plant, Cell & Environment, 16(5), 579-585.

Wang, H., & Yamauchi, A. (2006). Growth and functions of roots under abiotic stress in soil. In: Huang B (ed) Plant–environment interactions, 3rd edn. CRC Press, New York, p. 271–320.

Walker, B., Holling, C. S., Carpenter, S. R., & Kinzig, A. (2004). Resilience, adaptability and transformability in social–ecological systems. Ecology and society, 9(2).

Wu, Q. S., Xia, R. X., & Zou, Y. N. (2008). Improved soil structure and citrus growth after inoculation with three arbuscular mycorrhizal fungi under drought stress. European journal of soil biology, 44(1), 122-128.

Wright, S. F. (2005). Management of arbuscular mycorrhizal fungi. Roots and soil management: interactions between roots and the soil, 48, 181-197.

Yamane, K., Hayakawa, K., Kawasaki, M., Taniguchi, M., & Miyake, H. (2003). Bundle sheath chloroplasts of rice are more sensitive to drought stress than mesophyll chloroplasts. Journal of plant physiology, 160(11), 1319-1327.

Yang, Y., Chen, Y., & Li, W. (2008). Arbuscular mycorrhizal fungi infection in desert riparian forest and its environmental implications: A case study in the lower reach of Tarim River. Progress in Natural Science, 18(8), 983-991.

Yang, C. W., Xu, H. H., Wang, L. L., Liu, J., Shi, D. C., & Wang, D. L. (2009). Comparative effects of salt-stress and alkalistress on the growth, photosynthesis, solute accumulation, and ion balance of barley plants. Photosynthetica, 47(1), p.79-86.

Zhongqun, H., Chaoxing, H., Zhang, Z., Zhirong, Z. & Wang, H. (2007). Changes of antioxidative enzymes and cell membrane osmosis in tomato colonized by arbuscular Mycorrhizae under NaCl stress. Colloids Surf., B. Biointerfaces. 59(2), p.128-133.

Published

31/08/2022

How to Cite

PORTO, E. M. V.; TEIXEIRA, F. A. .; FRIES, D. D.; JARDIM, R. R. .; AMARO, H. T. R. .; SANTOS FILHO, J. R. dos .; SANTOS, J. P. dos; JESUS, F. M. de .; SILVA, H. S. .; VIEIRA, T. M. Plant growth-promoting microorganisms as mitigators of water stress in pastures: a narrative review. Research, Society and Development, [S. l.], v. 11, n. 11, p. e514111134029, 2022. DOI: 10.33448/rsd-v11i11.34029. Disponível em: https://www.rsdjournal.org/index.php/rsd/article/view/34029. Acesso em: 26 apr. 2024.

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Section

Review Article