Abstract
With increasing economic and nutritional demands that far outpace the addition of new agricultural areas around the world, biofertilizers are increasingly used to ensure the productivity of existing areas without sacrificing sustainability. This study evaluated the combination of algal extracts of Macrocystis pyrifera (a natural biofertilizer) with the plant growth-promoting bacteria Azospirillum argentinense in terms of their effectiveness in stimulating germination and growth of maize plants under different irrigation conditions. The performance of maize plants inoculated with the algae-bacteria formulation under water stress conditions was evaluated. The variables studied included different germination and growth parameters, such as dry and fresh weight of aerial and root part, total height and aerial and root part. The hormonal profile in maize seedlings was determined. The results related to growth parameters and phytohormone content demonstrate a synergistic effect between algae and bacteria, which means that a bioinoculant could be formulated based on their combination to promote the growth of maize in different climatic conditions and/or or water regimes. Such a product would fit well into current or future environmentally friendly plans for growing maize, aiming to reduce dependence on chemical fertilizers while preserving yield.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data Availability
The datasets generated and/or analysed in the current study are available from the corresponding author at reasonable request.
References
Abdelgawad AM, Hudson SM, Rojas OJ (2014) Antimicrobial wound dressing nanofiber mats from multicomponent (chitosan/silver-NPs/polyvinyl alcohol) systems. Carbohydr Polyms 100:166–178. https://doi.org/10.1016/j.carbpol.2012.12.043
Ahmad R, Khalid M, Naveed M, Shahzad SM, Zahir ZA, Khokhar SN (2008) Comparative efficiency of auxin and its precursor applied through compost for improving growth and yield of maize. Pak J Bot 40:1703–1710
Ali S, Hayat K, Iqbal A, Xie L (2020) Implications of abscisic acid in the drought stress tolerance of plants. Agron 10(9):1323. https://doi.org/10.3390/agronomy10091323
Almanza V, Buschmann AH (2013) The ecological importance of Macrocystis pyrifera (Phaeophyta) forests towards a sustainable management and exploitation of Chilean coastal benthic co-management areas. Int J Environ Sustain Dev 12:341–360. https://doi.org/10.1504/IJESD.2013.056331
Arioli T, Mattner SW, Winberg PC (2015) Applications of seaweed extracts in Australian agriculture: past, present and future. J Appl Phycol 27:2007–2015. https://doi.org/10.1007/s10811-015-0574-9
Bolsa de Cereales (2020) Panorama Agrícola Semanal. (consulted September 23, 2021). http://www.bolsadecereales.org
Borras-Chavez R, Edwards M, Vásquez JA (2012) Testing sustainable management in Northern Chile: harvesting Macrocystis pyrifera (Phaeophyceae, Laminariales). A case study. J Appl Phycol 24:1655–1665
Bottini R, Fulchieri M, Pearce D, Pharis R (1989) Identification of gibberellins A1,A3, and Iso-A3in cultures of A. Lipoferum. Plant Physiol 90:45–47. https://doi.org/10.1104/pp.90.1.45
Campos H, Cooper M, Edmeades GO, Loffler C, Schussler JR, Ibanez M (2006) Changes in drought tolerance in maize associated with fifty years of breeding for yield in the US maize belt. Maydica 51:369
Cassán F, Perrig D, Sgroy V, Masciarelli O, Penna C, Luna V (2009) Azospirillum brasilense Az39 and Bradyrhizobium japonicum E109, inoculated singlyorin combination, promote seed germination and early seedling growth in maize (Zea mays L.) and soybean (Glycine max L). Eur J Soil Biol 45:28–35. https://doi.org/10.1016/j.ejsobi.2008.08.005
Chávez L, González LM (2009) Mecanismos moleculares involucrados en la tolerancia de las plantas a la salinidad. ITEA 105:231–256
Coniglio A, Mora V, Puente M, Cassán F (2019) Azospirillum as biofertilizer for sustainable agriculture: Azospirillum brasilense AZ39 as a model of PGPR and field traceability. Microbial Probiotics for Agricultural systems. Springer, Cham, pp 45–70. https://doi.org/10.1007/978-3-030-17597-9_4
Contesto C, Miles S, Mantelin S, Zancarini A, Desbrosses G, Varoquaux F, Touraine B (2010) The auxin-signaling pathway is required for the lateral root response of Arabidopsis to the rhizobacterium Phyllobacterium brassicacearum. Planta 232:1455–1470. https://doi.org/10.1007/s00425-010-1264-0
Creus C, Graziano M, Casanovas E, Pereyra A, Simontacchi M, Puntarulo S, Barassi C, Lamattina L (2005) Nitric oxide is involved in the Azospirillum brasilense-induced lateral root formation in tomato. Planta 221:297–303. https://doi.org/10.1007/s00425-005-1523-7
Dar TA, Uddin M, Khan MMA, Hakeem KR, Jaleel H (2015) Jasmonates counter plant stress: a review. Env Exp Bot 115:49–57. https://doi.org/10.1016/j.envexpbot.2015.02.010
Das PP, Singh KR, Nagpure G, Mansoori A, Singh RP, Ghazi IA, Singh J (2022) Plant-soil-microbes: a tripartite interaction for nutrient acquisition and better plant growth for sustainable agricultural practices. Environ Res 214:113821. https://doi.org/10.1016/j.envres.2022.113821
Di Rienzo F, Debarnot U, Daligault S, Saruco E, Delpuech C, Doyon J, Guillot A (2016) Online and offline performance gains following motor imagery practice: a comprehensive review of behavioral and neuroimaging studies. Front Hum Neurosci 10:315. https://doi.org/10.3389/fnhum.2016.00315
Dimkpa C, Weinand T, Asch F (2009) Plant-rhizobacteria interactions alleviate abiotic stress conditions. Plant Cell Environ 32:1682–1694. https://doi.org/10.1111/j.1365-3040.2009.02028
Dodd IC, Pérez-Alfocea F (2012) Microbial amelioration of crops salinity stress. J Exp Bot 63:3415–3428. https://doi.org/10.1093/jxb/ers033
Dodd IC, Tan LP, He J (2003) Do increases in xylem sap pH and/or ABA concentration mediate stomatal closure following nitrate deprivation? J Exp Bot 54:1281–1288. https://doi.org/10.1093/jxb/erg122
Eyras MC, Defosse GE, Dellatorre F (2008) Seaweed compost as an amendment for horticultural soils in Patagonia, Argentina. Compost Sci Util 16:119–124. https://doi.org/10.1080/1065657X.2008.10702366
Fahad S, Nie L, Chen Y, Wu C, Xiong D, Saud S, Huang J (2015) Crop plant hormones and environmental stress. Sustain Agric Rev 371–400. https://doi.org/10.1007/978-3-319-09132-7_10
FAO (2018) Food and Agricultural Organization of the United Nations. Statistics of farming production Maize Available in http://www.fao.org/faostat/
Forchetti G, Masciarelli O, Alemano S, Alvarez D, Abdala G (2010) Native bacteria from sunflower roots produce salicylic acid and improve seedling growth under water deficit stress. Curr Microbiol 61:485–493. https://doi.org/10.1007/s00284-010-9642-1
Helman Y, Burdman S, Okon Y (2012) Plant growth promotion by rhizosphere bacteria through direct effects. Beneficial microorganisms in multicellular life forms. Springer, Berlin, Heidelberg, pp 89–103. https://doi.org/10.1007/978-3-642-21680-0_6
Ilyas M, Nisar M, Khan N, Hazrat A, Khan AH, Hayat K, Ullah A (2021) Drought tolerance strategies in plants: a mechanistic approach. J Plant Growth Reg 40:926–944. https://doi.org/10.1007/s00344-020-10174-5
Iparraguirre J, Llanes A, Masciarelli O, Zocolo GJ, Villasuso AL, Luna V (2023) Formulation technology: Macrocystis pyrifera extract is a suitable support/medium for Azospirillum brasilense. Algal Res 69:102916. https://doi.org/10.1016/j.algal.2022.102916
ISTA (2006) International rules for seed testing. Edition 2006. The International Seed Testing Association (ISTA), Bassersdorf, CH-Switzerland
Jaleel CA, Manivannan P, Wahid A, Farooq M, Al-Juburi HJ, Somasundaram R, Panneerselvam R (2008) Drought stress in plants: a review on morphological characteristics and pigments composition. Int J Agr Biol 11:100–105
Kamara AY, Menkir A, Badu-Apraku B, Ibikunle O (2003) The influence of drought stress on growth, yield and yield components of selected maize genotypes. J Agri Sci 141(1):43–50. https://doi.org/10.1017/S0021859603003423
Kapoor D, Bhardwaj S, Landi M, Sharma A, Ramakrishnan M, Sharma A (2020) The impact of drought in plant metabolism: how to exploit tolerance mechanisms to increase crop production. Appl Sci 10:5692. https://doi.org/10.3390/app10165692
Khan W, Rayirath U, Subramanian S, Jithesh M, Rayorath P, Hodges D, Critchley A, Craigie J, Norrie J, Prithiviraj B (2009) Seaweed extracts as biostimulants of Plant Growth and Development. J Plant Growth Regul 28:386–399. https://doi.org/10.1007/s00344-009-9103-x
Khan N, Bano A, Ali S, Babar M (2020) Crosstalk amongst phytohormones from plants and PGPR under biotic and abiotic stresses. Plant Growth Reg 90(2):189–203. https://doi.org/10.1007/s10725-020-00571-x
Lafitte HR, Yongsheng G, Ya S, Li ZK (2007) Whole plant responses, key processes, and adaptation to drought stress: the case of rice. J Exp Bot 58:169–175. https://doi.org/10.1093/jxb/erl101
Li SM, Zheng HX, Zhang XS, Sui N (2021) Cytokinins as central regulators during plant growth and stress response. Plant Cell Rep 40:271–282. https://doi.org/10.1007/s00299-020-02612-1
Liu H, Wang X, Zhang X, Zhang L, Li Y, Huang G (2017) Evaluation on the responses of maize (Zea mays L.) growth, yield and water use efficiency to drip irrigation water under mulch condition in the Hetao irrigation District of China. Agric Water Manag 179:144–157. https://doi.org/10.1016/j.agwat.2016.05.031
Llanes A, Andrade A, Alemano S, Luna V (2016) Alterations of endogenous hormonal levels in plants under drought and salinity. Am J Plant Sci 7:1357–1371. https://doi.org/10.4236/ajps.2016.79129
Malhotra M, Srivastava S (2009) Stress-responsive indole-3-acetic acid biosynthesis by Azospirillum brasilense SM and its ability to modulate plant growth. Eur J Soil Biol 45:73–80. https://doi.org/10.1016/j.ejsobi.2008.05.006
Mercau JL, Otegui ME (2014) A modeling approach to explore water management strategies for late-sown maize and double-cropped wheat-maize in the rainfed Pampas region of Argentina. Practical Appl Agricultural Syst Models Optimize Use Ltd Water 351–374. https://doi.org/10.2134/advagricsystmodel5.c13
Miller RJ, Lafferty KD, Lamy T, Kui L, Rassweiler A, Reed DC (2018) Giant kelp, Macrocystis pyrifera, increases faunal diversity through physical engineering. Proceedings of the Royal Society B: Biological Sciences, 285, 20172571. https://doi.org/10.1098/rspb.2017.2571
Minhas PS, Ramos TB, Ben-Gal A, Pereira LS (2020) Coping with salinity in irrigated agriculture: crop evapotranspiration and water management issues. Agric Water Manag 227:105832. https://doi.org/10.1016/j.agwat.2019.105832
Nemeskéri E, Helyes L (2019) Physiological responses of selected vegetable crop species to water stress. Agronomy 9:447. https://doi.org/10.3390/agronomy9080447
Okon Y, Labandera-González C (1994) Agronomic applications of Azospirillum: an evaluation of 20 years worldwide field inoculation. Soil Biol Biochem 26:1591–1601. https://doi.org/10.1016/0038-0717(94)90311-5
Pandey P, Ramegowda V, Senthil-Kumar M (2015) Shared and unique responses of plants to multiple individual stresses and stress combinations: physiological and molecular mechanisms. Front Plant Sci 6:1–14. https://doi.org/10.3389/fpls.2015.00723
Perrig D, Boiero ML, Masciarelli OA, Penna C, Ruiz OA, Cassán FD, Luna MV (2007) Plant-growth-promoting compounds produced by two agronomically important strains of Azospirillum brasilense, and implications for inoculant formulation. App Microbiol Biotech 75:1143–1150. https://doi.org/10.1007/s00253-007-0909-9
Rahdari P, Hoseini SM (2012) Drought stress: a review. Int JAgron Plant Prod 3:443–446
Rampino P, Pataleo S, Gerardi C, Mita G, Perrotta C (2006) Drought stress response in wheat: physiological and molecular analysis of resistant and sensitive genotypes. Plant Cell Env 29:2143–2152. https://doi.org/10.1111/j.1365-3040.2006.01588.x
Rehman FU, Kalsoom M, Adnan M, Toor M, Zulfiqar A (2020) Plant growth promoting rhizobacteria and their mechanisms involved in agricultural crop production: a review. SunText Rev Biotechnol 1:1–6. https://doi.org/10.51737/2766-5097.2020.010
Sakakibara H (2010) Cytokinin biosynthesis and metabolism. En: Plant hormones: biosynthesis, signal transduction, action. Davies PJ (ed) Dordrecht: Springer pp. 95–114. https://doi.org/10.1007/978-1-4020-2686-7_5
Samarah NH (2005) Effects of drought stress on growth and yield of barley. Agron Sustain Develop 25:145–149
Sathya A, Vijayabharath R, Gopalakrishnan S (2017) Plant growth-promoting actinobacteria: a new strategy for enhancing sustainable production and protection of grain legumes. Biotech 7:1–10. https://doi.org/10.1007/s13205-017-0736-3
Seleiman MF, Al-Suhaibani N, Ali N, Akmal M, Alotaibi M, Refay Y, Battaglia ML (2021) Drought stress impacts on plants and different approaches to alleviate its adverse effects. Plants 10:259. https://doi.org/10.3390/plants10020259
Seo JS, Joo J, Kim MJ, Kim YK, Nahm BH, Song SI, Choi YD (2011) OsbHLH148, a basic helix-loop‐helix protein, interacts with OsJAZ proteins in a jasmonate signaling pathway leading to drought tolerance in rice. Plant J 65:907–921. https://doi.org/10.1111/j.1365-313X.2010.04477.x
Shukla S, Zhao C, Shukla D (2019) Dewetting controls plant hormone perception and initiation of drought resistance signaling. Structure 27:692–702. https://doi.org/10.1016/j.str.2018.12.005
Sreenivasulu N, Radchuk V, Alawady A, Borisjuk L, Weier D, Staroske N, Weschke W (2010) De-regulation of abscisic acid contents causes abnormal endosperm development in the barley mutant seg8. Plant J 64:589–603. https://doi.org/10.1111/j.1365-313X.2010.04350.x
Stajković-Srbinović O, Delić DU, Kuzmanović DJ, Protić NAA, Rasulić N, Knežević-Vukčević JELENA (2014) Growth and nutrient uptake in oat and barley plants as affected by rhizobacteria. Rom Biotechnol Lett 19:9429–9436
Strzelczyk E, Kampert M, Li C (1994) Cytokinin-like substance and ethylene production by Azospirillum in media with different carbon sources. Microbiol Res 149:55–60. https://doi.org/10.1016/S0944-5013(11)80136-9
Tien T, Gaskins M, Hubbell D (1979) Plant growth substances produced by Azospirillum brasilense and their effect on the growth of Pearl Millet (Pennisetum americanum). Appl Environ Microbiol 37:1016–1024. https://doi.org/10.1128/aem.37.5.1016-1024.1979
Ullah A, Manghwar H, Shaban M, Khan AH, Akbar A, Al U, Fahad S (2018) Phytohormones enhanced drought tolerance in plants: a coping strategy. Environ Sci Pollution Res 25:33103–33118. https://doi.org/10.1007/s11356-018-3364-5
Van Loon LC (2007) Plant responses to plant growth-promoting rhizobacteria. New perspectives and approaches in plant growth-promoting Rhizobacteria research. Springer, Dordrecht, pp 243–254. https://doi.org/10.1007/978-1-4020-6776-1_2
Yang Y, Lun Z, Xia G, Zheng F, He M, Chen Q (2015) Non-precious alloy encapsulated in nitrogen-doped graphene layers derived from MOFs as an active and durable hydrogen evolution reaction catalyst. Energy Environ Sci 8:3563–3571. https://doi.org/10.1039/C5EE02460A
Funding
This work was partially supported by Secretaría de Ciencia y Técnica de la Universidad Nacional de Río Cuarto, UNRC, Fondo para la Investigación Científica y Técnica (PICT -START UP, Res. N 1408/12), ALV and AL are Career Researchers of CONICET. JI is a CONICET fellowship holder.
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Julia Iparraguirre; Oscar Masciarelli contributed to the hormonal data collection and analysis. The first draft of the manuscript was written by Julia Iparraguirre and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Consent for Publication
The authors affirm that human research participants provided informed consent for publication of this manuscript.
Conflict of Interest
The authors have no conflicts of interest to declare.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Iparraguirre, J., Masciarelli, O., Villasuso, A.L. et al. Macrocystis pyrifera Alga Extracts Combined with Azospirillum argentinense Improve Growth and Hormonal Responses in Zea mays Plants under Drought Stress. J Soil Sci Plant Nutr (2024). https://doi.org/10.1007/s42729-024-01745-6
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s42729-024-01745-6