Published September 26, 2023 | Version v1
Journal article Open

Efecto de rizobacterias promotoras del crecimiento vegetal en plantas sometidas a estrés hídrico: un enfoque desde la fisiología vegetal

  • 1. Departamento de Microbiología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional. Prol. Carpio y Plan de Ayala s/n. Col. Santo Tomás, Alcaldía Miguel Hidalgo. C.P. 11340. Ciudad de México, México.; Departamento de Unidades de Aprendizaje del Área Básica, Centro de Estudios Científicos y Tecnológicos 16 "Hidalgo", Instituto Politécnico Nacional. Carretera Pachuca-Actopan km 1 + 500. San Agustín Tlaxiaca. C.P. 42162. Hidalgo, México.
  • 2. Departamento de Microbiología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional. Prol. Carpio y Plan de Ayala s/n. Col. Santo Tomás, Alcaldía Miguel Hidalgo. C.P. 11340. Ciudad de México, México.

Description

RESUMEN

La sequía afecta significativamente el estado fisiológico de las plantas y, en consecuencia, la producción agrícola. El cambio climático supone un reto mayor para la agricultura, ya que las proyecciones indican la disminución del agua disponible para los cultivos en varias regiones del mundo. En este sentido, es necesario buscar estrategias que permitan la viabilidad de la producción sin provocar los daños que la agricultura intensiva convencional trae al equilibrio planetario. En este trabajo se abordan, desde un enfoque fisiológico, los impactos que tiene la sequía sobre las plantas y que afectan negativamente su productividad. Asimismo, se revisan los diferentes mecanismos de resistencia que han desarrollado las plantas para enfrentar la falta de agua para así comprender las características que presentan las rizobacterias promotoras del crecimiento vegetal y que, de diversas maneras, refuerzan o inducen resistencia ante el estrés hídrico en las plantas con las que se asocian, convirtiéndolas en una opción de interés para la adaptación de los cultivos ante condiciones de baja disponibilidad de agua. Asimismo, se plantea la importancia de transitar hacia la concepción de los ecosistemas rizosféricos como un sistema complejo y favorecer prácticas agrícolas basadas en el profundo entendimiento de los procesos ecológicos que se llevan a cabo entre el microbioma y la planta para coadyuvar a generar agroecosistemas productivos y resilientes ante los embates del cambio climático, reduciendo las afectaciones al ambiente y la salud humana.

 

ABSTRACT

Drought is a stressor that significantly affects the physiological state of plants and, consequently, agricultural production. Climate change possess a major challenge to agriculture as projections indicate a decrease in water availability for crops in various world regions. Therefore, it is necessary to seek strategies that enable viable production without causing the damage associated with conventional intensified agriculture which disrupts the planetary balance. This review focuses on the physiological impacts of drought on plants which negatively affect productivity. It also examines the different resistance mechanisms that plants have developed to cope with water scarcity, aiming to understand the characteristics of plant growth promoting rhizobacteria. These bacteria, in various ways, reinforce or induce resistance to water stress in the plants they associated with, making them an interesting option for adapting crops to conditions of low water availability.  Additionally, we highlight the importance of viewing rhizospheric ecosystems as complex systems that favor agricultural practices based on a deep understanding of the ecological processes occurring between the microbiome and the plant. The creation of productive and resilient agroecosystems in the face of climate change will likely reduce negative effects on the environment and human health.

Files

4) Jasso-Arreola et al, 2023.pdf

Files (1.6 MB)

Name Size Download all
md5:7a88b225a22eec856565e2a3c2295fb9
1.6 MB Preview Download

Additional details

References

  • Marshman J, Blay-Palmer A, Landman K. Anthropocene crisis: climate change, pollinators, and food security. Environments 2019; 6: 22. Disponible en: https://doi.org/10.3390/environments6020022
  • Tirado MC, Clarke R, Jaykus LA, McQuatters-Gollop A, Frank JM. Climate change and food safety: a review. Food Res Int 2010; 43: 1745–65. Disponible en: https://doi.org/10.1016/j.foodres.2010.07.003
  • Naciones Unidas. Población. Desafíos Glob n.d. Disponible en: https://www.un.org/es/global-issues/population
  • Naciones Unidas. La Agenda 2030 y los Objetivos de Desarrollo Sostenible: una oportunidad para América Latina y el Caribe. Santiago:(Chile): 2018. Disponible en: https://repositorio.cepal.org/bitstream/handle/11362/40155/24/S1801141_es.pdf
  • Porter JR, Semenov MA. Crop responses to climatic variation. Philos Trans R Soc B-Biological Sci 2005; 360: 2021–35. Disponible en: https://doi.org/10.1098/rstb.2005.1752
  • Ahmad A, Diwan H, Abrol YP. Global climate change, stress and plant productivity. In: Pareek A, Sopory S, Bohnert H, eds. Abiotic Stress Adaptation in Plants; Dordrecht: Springer Netherlands; 2009; 503–21. Disponible en: https://doi.org/10.1007/978-90-481-3112-9_23
  • Rosenzweig C, Strzepek KM, Major DC, Iglesias A, Yates DN, McCluskey A, Hillel D. Water resources for agriculture in a changing climate: international case studies. Glob Environ Chang 2004; 14: 345–60. Disponible en: https://doi.org/10.1016/j.gloenvcha.2004.09.003
  • Schlaeppi K, Bulgarelli D. The plant microbiome at work. Mol Plant-Microbe Interact 2015; 28:212–7. Disponible en: https://doi.org/10.1094/MPMI-10-14-0334-FI
  • Chouhan GK, Verma JP, Jaiswal DK, Mukherjee A, Singh S, de Araujo Pereira AP, Liu H, Abd_Allah EF, Singh BK. Phytomicrobiome for promoting sustainable agriculture and food security: Opportunities, challenges, and solutions. Microbiol Res 2021; 248: 126763. Disponible en: https://doi.org/10.1016/j.micres.2021.126763
  • Fiodor A, Singh S, Pranaw K. The contrivance of plant growth promoting microbes to mitigate climate change impact in agriculture. Microorganisms 2021; 9:1–36. Disponible en: https://doi.org/10.3390/microorganisms9091841
  • Turner TR, James EK, Poole PS. The plant microbiome. Genome Biol 2013; 14:1–10. Disponible en: https://doi.org/10.1186/gb-2013-14-6-209
  • Berendsen RL, Pieterse CMJ, Bakker PAHM. The rhizosphere microbiome and plant health. Trends Plant Sci 2012; 17:478–86. Disponible en: https://doi.org/10.1016/j.tplants.2012.04.001
  • Ahluwalia O, Singh PC, Bhatia R. A review on drought stress in plants: Implications, mitigation and the role of plant growth promoting rhizobacteria. Resour Environ Sustain 2021; 5:100032. Disponible en: https://doi.org/10.1016/j.resenv.2021.100032
  • Ali S, Khan N. Delineation of mechanistic approaches employed by plant growth promoting microorganisms for improving drought stress tolerance in plants. Microbiol Res 2021; 249: 126771. https://doi.org/10.1016/j.micres.2021.126771
  • Gowtham HG, Singh SB, Shilpa N, Aiyaz M, Nataraj K, Udayashankar AC, Amruthesh KN, Murali M, Poczai P, Gafur A, Almalki WH, Sayyed RZ. Insight into recent progress and perspectives in improvement of antioxidant machinery upon PGPR augmentation in plants under drought stress: a review. Antioxidants 2022; 11:1763. Disponible en: https://doi.org/10.3390/antiox11091763
  • Richerson PJ, Boyd R, Bettinger RL. Was agriculture impossible during the Pleistocene but mandatory during the Holocene? A climate change hypothesis. Am Antiq 2001; 66:387–411.Disponible en: https://doi.org/10.2307/2694241
  • Equihua Zamora M, Hernández Huerta A, Pérez Maqueo O, Benítez Badillo G, Ibáñez Bernal S. Cambio global: el Antropoceno. Cienc Ergo-Sum, Rev Científica Multidiscip Prospect 2016; 23:67–75. Disponible en: https://cienciaergosum.uaemex.mx/article/view/8115
  • Lambers H, Chapin FS, Pons TL. Plant physiological ecology. New York, NY: Springer New York; 2008. Disponible en: https://doi.org/10.1007/978-0-387-78341-3
  • Odum EP, Barrett GW. Fundametos de Ecología. 5th ed. México: Cengage Learning; 2006.
  • Salehi-Lisar SY, Bakhshayeshan-Agdam H. Drought stress tolerance in plants, vol 1: physiology and biochemistry. In: Hossain M, Wani S, Bhattacharjee S, Burritt D, Tran LS, eds. Drought stress tolerance in plants, Vol 1: physiology and biochemistry; Springer, Cham; 2016; 1–16. Disponible en: https://doi.org/10.1007/978-3-319-28899-4_1
  • Cuervo-Robayo AP, Ureta C, Gómez-Albores MA, Meneses-Mosquera AK, Téllez-Valdés O, Martínez-Meyer E. One hundred years of climate change in Mexico. PLoS One 2020; 15:1–19. Disponible en: https://doi.org/10.1371/journal.pone.0209808
  • SEMARNAT. México: Tercer informe bienal de actualización ante la Convención Marco de las Naciones Unidas sobre el cambio climático. Ciudad de México 2022. Disponible en: https://www.gob.mx/cms/uploads/attachment/file/747507/158_2022_Mexico_3er_BUR.pdf
  • Monterroso A, Conde C. Exposure to climate and climate change in Mexico. Geomatics, Nat Hazards Risk 2015; 6: 272–88. Disponible en : https://doi.org/10.1080/19475705.2013.847867
  • Donatti CI, Harvey CA, Martinez-Rodriguez MR, Vignola R, Rodriguez CM. Vulnerability of smallholder farmers to climate change in Central America and Mexico: current knowledge and research gaps. Clim Dev 2019; 11: 264–86. Disponible en: https://doi.org/10.1080/17565529.2018.1442796
  • Farooq M, Hussain M, Wahid A, Siddique KHM. Drought stress in plants: an overview. In: Aroca R, ed. Plant responses to drought stress; Berlin, Heidelberg: Springer Berlin Heidelberg; 2012; 1–33. Disponible en: https://doi.org/10.1007/978-3-642-32653-0_1
  • Sharma-Natu P, Ghildiyal MC. Potential targets for improving photosynthesis and crop yield. Curr Sci 2005; 88: 1918–28. Disponible en: https://www.jstor.org/stable/24110618
  • Kathpalia R, Bhatla SC. Plant water relations. In: Bhatla S, Lal M, eds. Plant physiology, development and metabolism; Singapore: Springer Singapore; 2018; 3–36. Disponible en: https://doi.org/10.1007/978-981-13-2023-1_1
  • Daszkowska-Golec A, Szarejko I. Open or close the gate - Stomata action under the control of phytohormones in drought stress conditions. Front Plant Sci 2013; 4: 1–16. Disponible en: https://doi.org/10.3389/fpls.2013.00138
  • Morgan PW, Drew MC. Ethylene and plant responses to abiotic stress. Physiol Plant 1997; 100:620–30. Disponible en: https://doi.org/10.1111/j.1399-3054.1997.tb03068.x
  • Wilkinson S, Davies WJ. Drought, ozone, ABA and ethylene: new insights from cell to plant to community. Plant, Cell Environ 2010; 33: 510–25. Disponible en: https://doi.org/10.1111/j.1365-3040.2009.02052.x
  • Farooq M, Wahid A, Kobayashi N, Fujita D, Basra SMA. Plant drought stress: effects, mechanisms and management. In: Lichtfouse E, Navarrete M, Debaeke P, Souchère V, Alberola C, eds. Sustainable agriculture; Dordrecht: Springer Netherlands; 2009; 153–88. Disponible en: https://doi.org/10.1007/978-90-481-2666-8_12
  • Aroca R. Plant responses to drought stress. From morphological to molecular features. Granada: Springer; 2013. Disponible en: https://doi.org/10.1007/978-3-642-32653-0
  • Vilagrosa A, Chirino E, Peguero-Pina JJ, Barigah TS, Cochard H, Gil-Pelegrín E. Xylem cavitation and embolism in plants living in water-limited ecosystems. In: Aroca R, ed. Plant responses to drought stress. From morphological to molecular features; Berlin, Heidelberg: Springer Berlin Heidelberg; 2013; 63–109. Disponible en: https://doi.org/10.1007/978-3-642-32653-0_3
  • FAO. Uso de la tierra en la agricultura según las cifras. Aliment y Agric Sostenibles 2020. Disponible en: https://www.fao.org/sustainability/news/detail/es/c/1279267/
  • Jogawat A, Yadav B, Chhaya, Lakra N, Singh AK, Narayan OP. Crosstalk between phytohormones and secondary metabolites in the drought stress tolerance of crop plants: a review. Physiol Plant 2021; 172: 1106–32. Disponible en: https://doi.org/10.1111/ppl.13328
  • Kohli A, Sreenivasulu N, Lakshmanan P, Kumar PP. The phytohormone crosstalk paradigm takes center stage in understanding how plants respond to abiotic stresses. Plant Cell Rep 2013; 32: 945–57. Disponible en: https://doi.org/10.1007/s00299-013-1461-y
  • Salvi P, Manna M, Kaur H, Thakur T, Gandass N, Bhatt D. Phytohormone signaling and crosstalk in regulating drought stress response in plants. Plant Cell Rep 2021; 40:1305–29. Disponible en: https://doi.org/10.1007/s00299-021-02683-8
  • Rock CD, Sun X. Crosstalk between ABA and auxin signaling pathways in roots of Arabidopsis thaliana (L.) Heynh. Planta 2005; 222:98–106. Disponible en: https://doi.org/10.1007/s00425-005-1521-9
  • Gowtham HG, Duraivadivel P, Ayusman S, Sayani D, Gholap SL, Niranjana SR, et al. ABA analogue produced by Bacillus marisflavi modulates the physiological response of Brassica juncea L. under drought stress. Appl Soil Ecol 2021; 159:103845. Disponible en: https://doi.org/10.1016/j.apsoil.2020.103845
  • Salomon MV, Bottini R, de Souza Filho GA, Cohen AC, Moreno D, Gil M, Piccoli P. Bacteria isolated from roots and rhizosphere of Vitis vinifera retard water losses, induce abscisic acid accumulation and synthesis of defense-related terpenes in in vitro cultured grapevine. Physiol Plant 2014; 151: 359–74. Disponible en: https://doi.org/10.1111/ppl.12117
  • Cohen AC, Bottini R, Pontin M, Berli FJ, Moreno D, Boccanlandro H, Travaglia CN, Piccoli PN. Azospirillum brasilense ameliorates the response of Arabidopsis thaliana to drought mainly via enhancement of ABA levels. Physiol Plant 2015; 153:79–90. Disponible en: https://doi.org/10.1111/ppl.12221
  • Zhang Y, Li Y, Hassan MJ, Li Z, Peng Y. Indole-3-acetic acid improves drought tolerance of white clover via activating auxin, abscisic acid and jasmonic acid related genes and inhibiting senescence genes. BMC Plant Biol 2020; 20: 1–12. Disponible en: https://doi.org/10.1186/s12870-020-02354-y
  • Du H, Wu N, Chang Y, Li X, Xiao J, Xiong L. Carotenoid deficiency impairs ABA and IAA biosynthesis and differentially affects drought and cold tolerance in rice. Plant Mol Biol 2013; 83: 475–88. Disponible en: https://doi.org/10.1007/s11103-013-0103-7
  • Zhang H, Kim M-S, Krishnamachari V, Payton P, Sun Y, Grimson M, Farag MA, Ryu C, Allen R, Melo IS, Paré PW. Rhizobacterial volatile emissions regulate auxin homeostasis and cell expansion in Arabidopsis. Planta 2007; 226: 839–51. Disponible en: https://doi.org/10.1007/s00425-007-0530-2
  • Spaepen S, Vanderleyden J. Auxin and plant-microbe interactions. Cold Spring Harb Perspect Biol 2011; 3: a001438–a001438. Disponible en: https://doi.org/10.1101/cshperspect.a001438
  • Yousef NMH. Capability of plant growth-promoting rhizobacteria (PGPR) for producing indole acetic acid (IAA) under extreme conditions. Eur J Biol Res 2018; 8:174–82. Disponible en: http://journals.tmkarpinski.com/index.php/ejbr/article/view/78
  • Uzma M, Iqbal A, Hasnain S. Drought tolerance induction and growth promotion by indole acetic acid producing Pseudomonas aeruginosa in Vigna radiata. PLoS One 2022; 17:1–21. Disponible en: https://doi.org/10.1371/journal.pone.0262932
  • Li W, Herrera-Estrella L, Tran LSP. The Yin-Yang of cytokinin homeostasis and drought acclimation/adaptation. Trends Plant Sci 2016; 21:548–50. Disponible en: https://doi.org/10.1016/j.tplants.2016.05.006
  • Rivero RM, Kojima M, Gepstein A, Sakakibara H, Mittler R, Gepstein S, et al. Delayed leaf senescence induces extreme drought tolerance in a flowering plant. Proc Natl Acad Sci 2007; 104:19631–6. https://doi.org/10.1073/pnas.0709453104
  • Sarafraz-Ardakani M-R, Khavari-Nejad R-A, Moradi F, Najafi F. Abscisic acid and cytokinin-induced osmotic and antioxidant regulation in two drought-tolerant and drought-sensitive cultivars of wheat during grain filling under water deficit in field conditions. Not Sci Biol 2014; 6:354–62. Disponible en: https://doi.org/10.15835/nsb639301
  • Arkhipova TN, Prinsen E, Veselov SU, Martinenko E V., Melentiev AI, Kudoyarova GR. Cytokinin producing bacteria enhance plant growth in drying soil. Plant Soil 2007; 292:305–15. Disponible en: https://doi.org/10.1007/s11104-007-9233-5
  • Liu F, Xing S, Ma H, Du Z, Ma B. Cytokinin-producing, plant growth-promoting rhizobacteria that confer resistance to drought stress in Platycladus orientalis container seedlings. Appl Microbiol Biotechnol 2013; 97:9155–64. Disponible en: https://doi.org/10.1007/s00253-013-5193-2
  • Abdel-Kader DZ. Drought and gibberellic acid-dependent oxidative stress: effect on antioxidant defense system in two lettuce cultivars. Pakistan J Biol Sci 2001; 4:1138–43. Disponible en: https://scialert.net/abstract/?doi=pjbs.2001.1138.1143
  • Kang SM, Radhakrishnan R, Khan AL, Kim MJ, Park JM, Kim BR, Shin D, Lee I. Gibberellin secreting rhizobacterium, Pseudomonas putida H-2-3 modulates the hormonal and stress physiology of soybean to improve the plant growth under saline and drought conditions. Plant Physiol Biochem 2014; 84: 115–24. Disponible en: https://doi.org/10.1016/j.plaphy.2014.09.001
  • Wang KL-C, Li H, Ecker JR. Ethylene biosynthesis and signaling networks. Plant Cell 2002; 14: S131–51. Disponble en : https://doi.org/10.1105/tpc.001768
  • Johnson PR, Ecker JR. The ethylene gas signal transduction pathway: a molecular perspective. Annu Rev Genet 1998; 32:227–54. Disponible en: https://doi.org/10.1146/annurev.genet.32.1.227
  • Houben M, Van de Poel B. 1-aminocyclopropane-1-carboxylic acid oxidase (ACO): the enzyme that makes the plant hormone ethylene. Front Plant Sci 2019; 10: 1–15. Disponible en: https://doi.org/10.3389/fpls.2019.00695
  • Glick BR. Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol Res 2014; 169: 30–9. Disponible en: https://doi.org/10.1016/j.micres.2013.09.009
  • Sapre S, Gontia-Mishra I, Tiwari S. ACC deaminase-producing bacteria: a key player in alleviating abiotic stresses in plants. In: Kumar A, Meena VS, eds. Plant Growth Promoting Rhizobacteria for Agricultural Sustainability; Singapore: Springer Singapore; 2019; 267–91. Disponible en: https://doi.org/10.1007/978-981-13-7553-8_14
  • Murali M, Singh SB, Gowtham HG, Shilpa N, Prasad M, Aiyaz M, Amruthesh K. Induction of drought tolerance in Pennisetum glaucum by ACC deaminase producing PGPR- Bacillus amyloliquefaciens through antioxidant defense system. Microbiol Res 2021; 253:126891. Disponible en: https://doi.org/10.1016/j.micres.2021.126891
  • Gupta A, Rai S, Bano A, Sharma S, Kumar M, Binsuwaidan R, Khan M, Upadhyay T, Alshammari N, Saeed M, Pathak N. ACC Deaminase produced by PGPR mitigates the adverse effect of osmotic and salinity stresses in Pisum sativum through modulating the antioxidants activities. Plants 2022; 11: 3419. Disponible en: https://doi.org/10.3390/plants11243419
  • Timmusk S, Abd El-Daim IA, Copolovici L, Tanilas T, Kännaste A, Behers L, Nevo E, Seisenbaeva G, Stenström E, Niinemets Ü. Drought-tolerance of wheat improved by rhizosphere bacteria from harsh environments: enhanced biomass production and reduced emissions of stress volatiles. PLoS One 2014; 9: e96086. Disponible en: https://doi.org/10.1371/journal.pone.0096086
  • Gowtham HG, S. BS, M. M, N. S, Prasad M, Aiyaz M, Amruthesh KN, Niranjana SR. Induction of drought tolerance in tomato upon the application of ACC deaminase producing plant growth promoting rhizobacterium Bacillus subtilis Rhizo SF 48. Microbiol Res 2020; 234: 126422. Disponible en: https://doi.org/10.1016/j.micres.2020.126422
  • Danish S, Zafar-Ul-Hye M, Hussain S, Riaz M, Qayyum MF. Mitigation of drought stress in maize through inoculation with drought tolerant ACC deaminase containing PGPR under axenic conditions. Pakistan J Bot 2020; 52:49–60. Disponible en: https://doi.org/10.30848/PJB2020-1(7)
  • Zafar-ul-Hye M, Danish S, Abbas M, Ahmad M, Munir TM. ACC Deaminase producing PGPR Bacillus amyloliquefaciens and Agrobacterium fabrum along with biochar improve wheat productivity under drought stress. Agronomy 2019; 9:343. Disponible en: https://doi.org/10.3390/agronomy9070343
  • Arshad M, Shaharoona B, Mahmood T. Inoculation with Pseudomonas spp. containing ACC-deaminase partially eliminates the effects of drought stress on growth, yield, and ripening of pea (Pisum sativum L.). Pedosphere 2008; 18:611–20. Disponible en: https://doi.org/10.1016/S1002-0160(08)60055-7
  • Tiwari S, Prasad V, Chauhan PS, Lata C. Bacillus amyloliquefaciens confers tolerance to various abiotic stresses and modulates plant response to phytohormones through osmoprotection and gene expression regulation in rice. Front Plant Sci 2017; 8:1–13. Disponible en: https://doi.org/10.3389/fpls.2017.01510
  • Trivedi P, Leach JE, Tringe SG, Sa T, Singh BK. Plant–microbiome interactions: from community assembly to plant health. Nat Rev Microbiol 2020; 18: 607–21. Disponible en: https://doi.org/10.1038/s41579-020-0412-1
  • Etesami H, Adl SM. Plant growth-promoting rhizobacteria (PGPR) and their action mechanisms in availability of nutrients to plants. In: Kumar M, Kumar V, Prasad R, eds. Phyto-Microbiome in Stress Regulation; Singapore: Springer, Singapore; 2020; 147–203. Disponible en: https://doi.org/10.1007/978-981-15-2576-6_9
  • D'Oria A, Courbet G, Billiot B, Jing L, Pluchon S, Arkoun M, Maillard A, Paysant-Le Roux C, Trouverie J, Etienne P, Diquélou S, Ourry A. Drought specifically downregulates mineral nutrition: Plant ionomic content and associated gene expression. Plant Direct 2022; 6: 1–19. Disponible en: https://doi.org/10.1002/pld3.402
  • Ciríaco da Silva E, Custódio Nogueira RJ, Almeida da Silva M, Bandeira de Albuquerque M. Drought stress and plant nutrition. Plant Stress 2011; 5:32–41. Disponible en: http://globalsciencebooks.info/Online/GSBOnline/images/2011/PS_5SI1/PS_5(SI1)32-41o.pdf
  • Stanhill G. Water use efficiency. Adv Agron 1986; 39: 53–85. Disponible en: https://doi.org/10.1016/S0065-2113(08)60465-4
  • Raymond NS, Gómez-Muñoz B, van der Bom FJT, Nybroe O, Jensen LS, Müller-Stöver DS, Oberson A, Richardson AE. Phosphate-solubilising microorganisms for improved crop productivity: a critical assessment. New Phytol 2021; 229:1268–77. Disponible en: https://doi.org/10.1111/nph.16924
  • Kour D, Rana KL, Yadav N, Yadav AN, Kumar A, Meena VS, Singh B, Chauhan V, Dhaliwal H, Saxena AK. Rhizospheric microbiomes: biodiversity, mechanisms of plant growth promotion, and biotechnological applications for sustainable agriculture. In: Kumar A, Meena VS, eds. Plant growth promoting rhizobacteria for agricultural sustainability; Singapore: Springer Singapore; 2019; 19–65. Disponible en : https://doi.org/10.1007/978-981-13-7553-8_2
  • Aguado-Santacruz GA, Moreno-Gómez B, Jiménez-Francisco B, García-Moya E, Preciado-Ortiz RE. Impacto de los sideróforos microbianos y fitosideróforos en la asimilación de hierro por las plantas: una síntesis. Rev Fitotec Mex 2012; 35:9–21. Disponible en: https://doi.org/10.35196/rfm.2012.1.9
  • Jin CW, Li GX, Yu XH, Zheng SJ. Plant Fe status affects the composition of siderophore-secreting microbes in the rhizosphere. Ann Bot 2010; 105:835–41. Disponible en: https://doi.org/10.1093/aob/mcq071
  • Singh M, Kumar J, Singh S, Singh VP, Prasad SM. Roles of osmoprotectants in improving salinity and drought tolerance in plants: a review. Rev Environ Sci Bio/Technology 2015; 14:407–26. Disponible en: https://doi.org/10.1007/s11157-015-9372-8
  • Barnawal D, Bharti N, Pandey SS, Pandey A, Chanotiya CS, Kalra A. Plant growth-promoting rhizobacteria enhance wheat salt and drought stress tolerance by altering endogenous phytohormone levels and TaCTR1/TaDREB2 expression. Physiol Plant 2017; 161: 502–14. Dispinible en: https://doi.org/10.1111/ppl.12614
  • Saha I, Datta S, Biswas D. Exploring the role of bacterial extracellular polymeric substances for sustainable development in agriculture. Curr Microbiol 2020; 77: 3224–39. Disponible en: https://doi.org/10.1007/s00284-020-02169-y
  • Naseem H, Ahsan M, Shahid MA, Khan N. Exopolysaccharides producing rhizobacteria and their role in plant growth and drought tolerance. J Basic Microbiol 2018; 58: 1009–22. Disponible en: https://doi.org/10.1002/jobm.201800309
  • Cruz de Carvalho MH. Drought stress and reactive oxygen species: Production, scavenging and signaling. Plant Signal Behav 2008; 3: 156–65. Disponible en: https://doi.org/10.4161/psb.3.3.5536
  • Nadarajah KK. Ros homeostasis in abiotic stress tolerance in plants. Int J Mol Sci 2020; 21: 1–29. Disponible en: https://doi.org/10.3390/ijms21155208
  • Mittler R. Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 2002; 7: 405–10. Disponible en: https://doi.org/10.1016/S1360-1385(02)02312-9
  • Sarma RK, Saikia R. Alleviation of drought stress in mung bean by strain Pseudomonas aeruginosa GGRJ21. Plant Soil 2014; 377: 111–26. Disponible en: https://doi.org/10.1007/s11104-013-1981-9
  • Hayat S, Hayat Q, Alyemeni MN, Wani AS, Pichtel J, Ahmad A. Role of proline under changing environments: a review. Plant Signal Behav 2012; 7: 1456–66. Disponible en: https://doi.org/10.4161/psb.21949
  • Shetty P, Atallah MT, Shetty K. Enhancement of total phenolic, L-DOPA and proline contents in germinating fava bean (Vicia faba) in response to bacterial elicitors. Food Biotechnol 2001; 15: 47–67. Disponible en: https://doi.org/10.1081/FBT-100103894
  • Agami R, Medani RA, Abd El-Mola IA, Taha RS. Exogenous application with plant growth promoting rhizobacteria (PGPR) or proline induces stress tolerance in basil plants (Ocimum basilicum L.) exposed to water stress. Int J Environ Agric Res 2016; 2: 78–92. Disponible en: https://issuu.com/ijoear-environmentalandagriculturer/docs/ijoear-may-2016-10/1
  • Nasrin S, Saha S, Begum HH, Samad R. Impacts of drought stress on growth, protein, proline, pigment content and antioxidant enzyme activities in rice (Oryza sativa L. var. BRRI dhan-24). Dhaka Univ J Biol Sci 2020; 29:117–23. Disponible en: https://doi.org/10.3329/dujbs.v29i1.46537
  • Ortiz-Covarrubias Y, Dhliwayo T, Palacios-Rojas N, Ndhlela T, Magorokosho C, Aguilar-Rincón VH, Cruz-Morales A, Trachsel S. Effects of drought and low nitrogen stress on provitamin a carotenoid content of biofortified maize hybrids. Crop Sci 2019; 59:2521–32. Disponible en: https://doi.org/10.2135/cropsci2019.02.0100
  • Yasmin H, Nosheen A, Naz R, Bano A, Keyani R. L -tryptophan-assisted PGPR-mediated induction of drought tolerance in maize (Zea mays L.). J Plant Interact 2017; 12:567–78. Disponible en: https://doi.org/10.1080/17429145.2017.1402212
  • Arif I, Batool M, Schenk PM. Plant microbiome engineering: expected benefits for improved crop growth and resilience. Trends Biotechnol 2020; 38: 1385–96. Disponible en: https://doi.org/10.1016/j.tibtech.2020.04.015
  • Bitas V, Kim HS, Bennett JW, Kang S. Sniffing on microbes: Diverse roles of microbial volatile organic compounds in plant health. Mol Plant-Microbe Interact 2013; 26:835–43. Disponible en: https://doi.org/10.1094/MPMI-10-12-0249-CR
  • Yuan JS, Himanen SJ, Holopainen JK, Chen F, Stewart CN. Smelling global climate change: mitigation of function for plant volatile organic compounds. Trends Ecol Evol 2009; 24:323–31. Disponible en: https://doi.org/10.1016/j.tree.2009.01.012
  • Dudareva N, Klempien A, Muhlemann JK, Kaplan I. Biosynthesis, function and metabolic engineering of plant volatile organic compounds. New Phytol 2013; 198: 16–32. Disponible en: https://doi.org/10.1111/nph.12145
  • Cho SM, Kang BR, Han SH, Anderson AJ, Park J, Lee Y, Cho B, Yang K, Ryu C, Kim Y. 2R,3R-Butanediol, a bacterial volatile produced by Pseudomonas chlororaphis O6, is involved in induction of systemic tolerance to drought in Arabidopsis thaliana. Mol Plant-Microbe Interact 2008; 21:1067–75. Disponible en: https://doi.org/10.1094/MPMI-21-8-1067
  • Ortiz-Castro R, Díaz-Pérez C, Martínez-Trujillo M, del Río RE, Campos-García J, López-Bucio J. Transkingdom signaling based on bacterial cyclodipeptides with auxin activity in plants. Proc Natl Acad Sci 2011; 108:7253–8. Disponible en : https://doi.org/10.1073/pnas.1006740108
  • Gutiérrez-Luna FM, López-Bucio J, Altamirano-Hernández J, Valencia-Cantero E, de la Cruz HR, Macías-Rodríguez L. Plant growth-promoting rhizobacteria modulate root-system architecture in Arabidopsis thaliana through volatile organic compound emission. Symbiosis 2010; 51: 75–83. Disponible en: https://doi.org/10.1007/s13199-010-0066-2
  • Aloni R, Aloni E, Langhans M, Ullrich CI. Role of cytokinin and auxin in shaping root architecture: Regulating vascular differentiation, lateral root initiation, root apical dominance and root gravitropism. Ann Bot 2006; 97: 883–93. Disponible en: https://doi.org/10.1093/aob/mcl027
  • Grover M, Bodhankar S, Sharma A, Sharma P, Singh J, Nain L. PGPR mediated alterations in root traits: way toward sustainable crop production. Front Sustain Food Syst 2021; 4:1–28. Disponible en: https://doi.org/10.3389/fsufs.2020.618230
  • Mantelin S, Touraine B. Plant growth-promoting bacteria and nitrate availability: impacts on root development and nitrate uptake. J Exp Bot 2004; 55: 27–34. Disponible en: https://doi.org/10.1093/jxb/erh010
  • Liu Y, Chen L, Zhang N, Li Z, Zhang G, Xu Y, et al. Plant-microbe communication enhances auxin biosynthesis by a root-associated bacterium, Bacillus amyloliquefaciens SQR9. Mol Plant-Microbe Interact 2016; 29:324–30. Disponible en: https://doi.org/10.1094/MPMI-10-15-0239-R
  • Ambreetha S, Balachandar D. Rhizobacteria-mediated root architectural improvement: a hidden potential for agricultural sustainability. In: Kumar A, Meena VS, eds. Plant Growth Promoting Rhizobacteria for Agricultural Sustainability; Singapore: Springer Singapore; 2019; 111–28. Disponible en: https://doi.org/10.1007/978-981-13-7553-8_6
  • Cohen AC, Travaglia CN, Bottini R, Piccoli PN. Participation of abscisic acid and gibberellins produced by endophytic Azospirillum in the alleviation of drought effects in maize. Botany 2009; 87: 455–62. Disponible en: https://doi.org/10.1139/B09-023
  • Khan N, Bano A, Babar MA. Metabolic and physiological changes induced by plant growth regulators and plant growth promoting rhizobacteria and their impact on drought tolerance in Cicer arietinum L. PLoS One 2019; 14:1–22. Disponible en: https://doi.org/10.1371/journal.pone.0213040
  • Chiappero J, Cappellari L del R, Sosa Alderete LG, Palermo TB, Banchio E. Plant growth promoting rhizobacteria improve the antioxidant status in Mentha piperita grown under drought stress leading to an enhancement of plant growth and total phenolic content. Ind Crops Prod 2019; 139: 111553. Disponible en: https://doi.org/10.1016/j.indcrop.2019.111553
  • Kang S-M, Khan AL, Hamayun M, Hussain J, Joo G-J, You Y-H, et al. Gibberellin-producing Promicromonospora sp. SE188 improves Solanum lycopersicum plant growth and influences endogenous plant hormones. J Microbiol 2012; 50:902–9. Disponible en: https://doi.org/10.1007/s12275-012-2273-4
  • Belimov AA, Dodd IC, Hontzeas N, Theobald JC, Safronova VI, Davies WJ. Rhizosphere bacteria containing 1‐aminocyclopropane‐1‐carboxylate deaminase increase yield of plants grown in drying soil via both local and systemic hormone signalling. New Phytol 2009; 181: 413–23. Disponible en: https://doi.org/10.1111/j.1469-8137.2008.02657.x
  • Cho S-M, Kang BR, Kim YC. Transcriptome analysis of induced systemic drought tolerance elicited by Pseudomonas chlororaphis O6 in Arabidopsis thaliana. Plant Pathol J 2013; 29:209–20. Disponible en: https://doi.org/10.5423/PPJ.SI.07.2012.0103
  • Saikia J, Sarma RK, Dhandia R, Yadav A, Bharali R, Gupta VK, et al. Alleviation of drought stress in pulse crops with ACC deaminase producing rhizobacteria isolated from acidic soil of Northeast India. Sci Rep 2018; 8: 1–17. Disponible en: https://doi.org/10.1038/s41598-018-21921-w
  • Prakasa Rao EVS, Puttana K. Nitrates, agriculture and environment. Curr Sci 2000; 79: 1163–8. Disponible en: https://www.jstor.org/stable/24105267
  • Campbell BM, Beare DJ, Bennett EM, Hall-Spencer JM, Ingram JSI, Jaramillo F, et al. Agriculture production as a major driver of the Earth system exceeding planetary boundaries. Ecol Soc 2017; 22:art8. Disponible en: https://doi.org/10.5751/ES-09595-220408
  • Gliessman SR. Agroecology: the ecology of sustainable food systems. 3rd ed. Florida, EEUU: CRC Press; 2014. Disponible en: https://doi.org/10.1201/b17881
  • Ling N, Zhu C, Xue C, Chen H, Duan Y, Peng C, et al. Insight into how organic amendments can shape the soil microbiome in long-term field experiments as revealed by network analysis. Soil Biol Biochem 2016; 99:137–49. Disponible en: https://doi.org/10.1016/j.soilbio.2016.05.005
  • van der Heijden MGA, Hartmann M. Networking in the plant microbiome. PLoS Biol 2016; 14:1–9. Disponible en: https://doi.org/10.1371/journal.pbio.1002378
  • Longepierre M, Widmer F, Keller T, Weisskopf P, Colombi T, Six J, et al. Limited resilience of the soil microbiome to mechanical compaction within four growing seasons of agricultural management. ISME Commun 2021; 1:44. Disponible en: https://doi.org/10.1038/s43705-021-00046-8