Skip to main content

Advertisement

SpringerLink
Log in

Effect of Azolla filiculoides on Growth, Physiological and Yield Attributes of Maize Grown under Water and Nitrogen Deficiencies

  • Published:
Journal of Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Owing to water scarcity and environmental hazards of synthetic fertilizers, reducing water and chemical N fertilizers is very urgent for sustainable agriculture. Thus, two field experiments were conducted to understand the physiological role of Azolla filiculoides Lam. extract (AE), as a promising biofertilizer, in enhancing growth, physiology, yield, N uptake efficiency (NUpE), N use efficiency (NUE) and irrigation water use efficiency (IWUE) in N-deficient maize plants under full and deficit irrigation. The experimental design was split plot with irrigation treatments as main plots and N treatments including full nitrogen (FN; 285 kg N ha−1), nitrogen deficiency (ND; 190 kg N ha−1) and ND (190 kg N ha−1) + AE (10% w/v) as subplots. At the vegetative stage, deficit irrigation was performed by withholding water from 26 to 56 days after sowing, while N-deficient plants received two-thirds of the total recommended N. N deficiency caused deleterious impacts on growth and yield of maize plants, particularly under deficit irrigation. However, results evidenced the role of Azolla extract, as an efficient biofertilizer, in combination with deficit irrigation in improving NUpE, NUE and IWUE without substantial decreases in grain and stover yields of N-deficient maize plants. Application of Azolla extract improved growth, yield attributes, irrigation water and N use efficiency via enhancing photosynthetic pigments, leaf water status, proline accumulation and N uptake with a reduction in membrane oxidative damage. Overall, the application of Azolla extract is an eco-friendly and cost-effective organic fertilizer to reduce more than 30% of urea fertilizer without affecting grain yield of maize plants.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abd El-Halim AA, Abd El-Razek UA (2014) Effect of different irrigation intervals on water saving, water productivity and grain yield of maize (Zea mays L.) under the double ridge-furrow planting technique. Arch Agron Soil Sci 60:587–596

    Google Scholar 

  • Abrams D, Metcalf D, Hojjatie M (2014) Determination of Kjeldahl nitrogen in fertilizers by AOAC Official MethodSM 97802: effect of copper sulfate as a catalyst. J AOAC Int 97:764–767

    CAS  PubMed  Google Scholar 

  • Ahmad I, Wajid SA, Ahmad A, Cheema MJM, Judge J (2019) Optimizing irrigation and nitrogen requirements for maize through empirical modeling in semi-arid environment. Environ Sci Pollut Res 26:1227–1237

    CAS  Google Scholar 

  • Alandia G, Jacobsen SE, Kyvsgaard NC, Condori B, Liu F (2016) Nitrogen sustains seed yield of quinoa under intermediate drought. J Agro Crop Sci 202:281–291

    CAS  Google Scholar 

  • Aseel DG, Mostafa Y, Riad SA, SA, Hafez EE, (2019) Improvement of nitrogen use efficiency in maize using molecular and physiological approaches. Symbiosis 78:263–274

    CAS  Google Scholar 

  • Bao AK, Wang SM, Wu GQ, Xi JJ, Zhang JL, Wang CM (2009) Overexpression of the Arabidopsis H+-PPase enhanced resistance to salt and drought stress in transgenic alfalfa (Medicago sativa L.). Plant Sci 176:232–240

    CAS  Google Scholar 

  • Bates LS, Waldron RP, Teare ID (1973) Rapid determination of free proline in water stress studies. Plant Soil 39:205–207

    CAS  Google Scholar 

  • Cai H, ChuQ YL, Liu J, Chen X, Chen F, Mi G, Zhang F (2012) Identification of quantitative trait loci for leaf area and chlorophyll content in maize (Zea mays L.) under low nitrogen and low phosphorus supply. Mol Breed 30:251–266

    CAS  Google Scholar 

  • Chai Q, Gan Y, Zhao C, Xu HL, WaskomRM NY, Siddique KHM (2016) Regulated deficit irrigation for crop production under drought stress: a review. Agron Sustain Dev 36:3

    Google Scholar 

  • Chen JW, Yang ZQ, Zhou P, Hai MR, TangTX LYL, An TX (2013) Biomass accumulation and partitioning, photosynthesis, and photosynthetic induction in field-grown maize (Zea mays L.) under low- and high-nitrogen conditions. Acta Physiol Plant 35:95–105

    CAS  Google Scholar 

  • DaMatta FM, Loos RA, Silva EA, LoureiroME DC (2002) Effects of soil water deficit and nitrogen nutrition on water relations and photosynthesis of pot-grown Coffea canephora Pierre. Trees 16:555–558

    CAS  Google Scholar 

  • Das K, Roychoudhury A (2014) Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Front Environ Sci 2:53

    Google Scholar 

  • deBever A, Ndakidemi PA, Laubscher CP (2013) Effects of different combinations of Hoagland’s solution and Azolla filiculoides on photosynthesis and chlorophyll content in Beta vulgaris subsp. cycla ‘fordhook giant’ grown in hydroponic cultures. Afr J Biotechnol 12:2006–2012

    Google Scholar 

  • deVries S, deVries J, Teschke H, von Dahlen JK, Rose LE, Gould SB (2018) Jasmonic and salicylic acid response in the fern Azolla filiculoides and its cyanobiont. Plant Cell Environ 41:2530–2548

    PubMed  Google Scholar 

  • El Saadawi W, Darwish MH (1997) Azollaceae, a new family for the flora of Egypt. Taeckholmia 17:91–100

    Google Scholar 

  • Ganie AH, Ahmad A, Yousuf PY, Pandey R, Ahmad S, Aref IM, Iqbal M (2017) Nitrogen-regulated changes in total amino acid profile of maize genotypes having contrasting response to nitrogen deficit. Protoplasma 254:2143–2153

    CAS  PubMed  Google Scholar 

  • Ge T, Sui F, Bai L, Tong C, Sun N (2012) Effects of water stress on growth, biomass partitioning, and water-use efficiency in summer maize (Zea mays L.) throughout the growth cycle. Acta Physiol Plant 34:1043–1053

    Google Scholar 

  • Gheysari M, Sadeghi SH, Loescher HW, Amiri S, Zareian MJ, Majidi MM, Asgarinia P, Payero JO (2017) Comparison of deficit irrigation management strategies on root, plant growth and biomass productivity of silage maize. Agric Water Manag 182:126–138

    Google Scholar 

  • Gonzalez-Dugo V, Durand JL, Gastal F (2010) Water deficit and nitrogen nutrition of crops: A review. Agron Sustain Dev 30:529–544

    CAS  Google Scholar 

  • Hammad HM, Farhad W, Abbas F, Fahad S, Saeed S, Nasim W, Bakhat HF (2017) Maize plant nitrogen uptake dynamics at limited irrigation water and nitrogen. Environ Sci Pollut Res 24:2549–2557

    CAS  Google Scholar 

  • Hou H, Han Z, Yang Y, Abudu S, Cai H, Li Z (2020) Soil CO2 emissions from summer maize fields under deficit irrigation. Environ Sci Pollution Res 27:4442–4449

    CAS  Google Scholar 

  • Kang S, Shi W, Zhang J (2000) An improved water-use efficiency for maize grown under regulated deficit irrigation. Field Crops Res 67:207–214

    Google Scholar 

  • Kasmaei LS, Yasrebi J, Zarei M, Ronaghi A, Ghasemi R, Saharkhiz MJ, Ahmadabadi Z, Schnug E (2019) Influence of plant growth promoting rhizobacteria, compost, and biochar of Azolla on rosemary (RosmarinusOfficinalis L.) growth and some soil quality indicators in a calcareous soil. Commun Soil Sci Plan 50:119–131

    Google Scholar 

  • Khalili M, Naghavi MR, Aboughadareh AP, Rad HN (2013) Effects of drought stress on yield and yield components in maize cultivars (Zea mays L.). Int J Agron Plant Prod 4:809–812

    Google Scholar 

  • Khomami AM, Padasht MN, Lahiji AA, Mahtab F (2019) Reuse of peanut shells and Azolla mixes as a peat alternative in growth medium of Dieffenbachia amoena ‘tropic snow’. Int J Recycl Org Waste Agric 8:151–157

    Google Scholar 

  • Kimani SM, Bimantara PO, Hattori S, Tawaraya K, Sudo S, Cheng W (2020) Azolla incorporation and dual cropping influences CH4 and N2O emissions from flooded paddy ecosystems. Soil Sci Plant Nutr. https://doi.org/10.1080/00380768.2019.1705736

    Article  Google Scholar 

  • Kirda C, Topcu S, Kaman H, Ulger AC, Yazici A, Cetin M, Derici MR (2005) Grain yield response and N-fertiliser recovery of maize under deficit irrigation. Field Crops Res 93:132–141

    Google Scholar 

  • Kollah B, Patra AK, Mohanty SR (2016) Aquatic microphylla Azolla: a perspective paradigm for sustainable agriculture, environment and global climate change. Environ Sci Pollut Res 23:4358–4369

    CAS  Google Scholar 

  • Li X, Kang S, Zhang X, Li F, Lu H (2018) Deficit irrigation provokes more pronounced responses of maize photosynthesis and water productivity to elevated CO2. Agric Water Manag 195:71–83

    Google Scholar 

  • Lichtenthaler HK, Verbeek L (1973) Inhibition of carotenoid synthesis during nitrogen deficiency. Planta 112:265–271

    CAS  PubMed  Google Scholar 

  • Ma N, Dong L, Lü W, Lü J, Meng O, Liu P (2020) Transcriptome analysis of maize seedling roots in response to nitrogen-, phosphorus-, and potassium deficiency. Plant Soil. https://doi.org/10.1007/s11104-019-04385-3

    Article  Google Scholar 

  • Maham SG, Rahimi A, Smith DL (2018) Environmental assessment of the essential oils produced from dragonhead (Dracocephalum moldavica L.) inconventional and organic farms with different irrigation rates. J Clean Prod 204:1070–1086

    Google Scholar 

  • Maham SG, Rahimi A, Subramanian S, Smith DL (2020) The environmental impacts of organic greenhouse tomato production based on the nitrogen-fixing plant (Azolla). J Clean Prod 245:118679

    CAS  Google Scholar 

  • Malyan SK, Bhatia A, Kumar SS, Fagodiya RK, Pugazhendhi A, Duc PA (2019) Mitigation of greenhouse gas intensity by supplementing with Azolla and moderating the dose of nitrogen fertilizer. Biocatal Agric Biotechnol 20:101266

    Google Scholar 

  • Mananze SE, Pôças I, Cunha M (2018) Maize leaf area estimation in different growth stages based on allometric descriptors. Afr J Agric Res 13:202–209

    Google Scholar 

  • Masclaux-Daubresse C, Daniel-Vedele F, Dechorgnat J, Chardon F, Gaufichon L, Suzuki A (2010) Nitrogen uptake, assimilation and remobilization in plants: challenges for sustainable and productive agriculture. Ann Bot 105:1141–1157

    PubMed  PubMed Central  Google Scholar 

  • Maswada HF, Abd El-Kader NIK (2016) Redox halopriming: a promising strategy for inducing salt tolerance in bread wheat. J Agron Crop Sci 202:37–50

    CAS  Google Scholar 

  • Maswada HF, Abd El-Razek UA, El-Sheshtawy AA, Elzaawely AA (2018) Morpho-physiological and yield responses to exogenous moringa leaf extract and salicylic acid in maize (Zea mays L.) under water stress conditions. Arch Agron Soil Sci 64:994–1010

    CAS  Google Scholar 

  • Meise P, Seddig S, Uptmoor R, Ordon F, Schum A (2018) Impact of nitrogen supply on leaf water relations and physiological traits in a set of potato (Solanum tuberosum L.) cultivars under drought stress. J Agro Crop Sci 204:359–374

    CAS  Google Scholar 

  • Mi G, Chen F, Zhang F (2008) Physiological and genetic mechanisms for nitrogen-use efficiency in maize. J Crop Sci Biotech 10:57–63

    Google Scholar 

  • Mishra DJ, Singh R, Mishra UK, Shahi SK (2013) Role of bio-fertilizer in organic agriculture: A review. Res J Recent Sci 2:39–41

    CAS  Google Scholar 

  • Moll RH, Kamprath EJ, Jackson WA (1982) Analysis and interpretation of factors which contribute to efficiency of nitrogen utilization. Agron J 74:562–564

    Google Scholar 

  • Ouda S, Zohry A, Noreldin T (2020) Deficit Irrigation: A remedy for water scarcity. Springer Nature Switzerland AG. https://doi.org/10.1007/978-3-030-35586-9

  • Oyekunle M, Badu-Apraku B (2014) Genetic analysis of grain yield and other traits of early-maturing maize inbreds under drought and well-watered conditions. J Agro Crop Sci 200:92–107

    CAS  Google Scholar 

  • Partey ST, Thevathasan NV, Zougmore RB, Preziosi RF (2018) Improving maize production through nitrogen supply from ten rarely-used organic resources in Ghana. Agroforest Syst 92:375–387

    Google Scholar 

  • Peever TL, Higgins VJ (1989) Electrolyte leakage, lipoxygenase, and lipid peroxidation induced in tomato leaf tissue by specific and nonspecific elicitors from Cladosporium fulvum. Plant Physiol 90:867–875

    CAS  PubMed  PubMed Central  Google Scholar 

  • Petruccelli R, Bati CB, Carlozzi P, Padovani G, Vignozzi N, Bartolini G (2015) Use of Azolla as a growing medium component in the nursery production of olive trees. Int J Basic Appl Sci 4:333–339

    CAS  Google Scholar 

  • Razavipour T, Moghaddam SS, Doaei S, Noorhosseini SA, Damalas CA (2018) Azolla (Azolla filiculoides) compost improves grain yield of rice (Oryza sativa L.) under different irrigation regimes. Agric Water Manag 209:1–10

    Google Scholar 

  • Ripley BS, Kiguli LN, Barker NP (2003) Azolla filiculoides as a biofertilizer of wheat under dry-land soil conditions. S Afr J Bot 69:295–300

    Google Scholar 

  • Rodríguez-Merino A, Fernández-Zamudio R, García-Murillo P, Muñoz J (2019) Climatic niche shift during Azolla filiculoides invasion and its potential distribution under future scenarios. Plants 8:424

    PubMed Central  Google Scholar 

  • Roy DC, Pakhira MC, Bera S (2016) A review on biology, cultivation and utilization of Azolla. Adv Life Sci 5:11–15

    Google Scholar 

  • Salisbury FB (1996) Units, symbols and terminology for plant physiology: a reference for presentation of research results in the plant sciences. Oxford University Press, New York

    Google Scholar 

  • Sánchez E, Garcia PC, López-Lefebre LR, Rivero RM, Ruiz JM, Romero L (2002) Proline metabolism in response to nitrogen deficiency in French bean plants (Phaseolus vulgaris L. cv Strike). Plant Growth Regul 36:261–265

    Google Scholar 

  • Shaltout KH, El-Komi TM, Eid EM (2012) Seasonal variation in the phytomass, chemical composition and nutritional value of Azolla filiculoides Lam. along the water courses in the Nile Delta. Egypt Feddes Repert 123:37–49

    Google Scholar 

  • Sharifi P, Shorafa M, Mohammadi MH (2019) Comparison of the effect of cow manure, vermicompost, and Azolla on safflower growth in a saline-sodic soil. Commun Soil Sci Plan 50:1417–1424

    CAS  Google Scholar 

  • Sinclair TR, Vadez V (2002) Physiological traits for crop yield improvement in low N and P environments. Plant Soil 245:1–15

    CAS  Google Scholar 

  • Singh P, Jaiswal S, Sheokand S, Duhan S (2018) Morpho-physiological and oxidative responses of nitrogen and phosphorus deficiency in wheat (Triticum aestivum L.). Ind J Agric Res 52:40–45

    Google Scholar 

  • Stirk WA, van Staden J (2003) Occurrence of cytokinin-like compounds in two aquatic ferns and their exudates. Environ Exp Bot 49:77–85

    CAS  Google Scholar 

  • Wang Y, Janz B, Engedal T, de Neergaard A (2017) Effect of irrigation regimes and nitrogen rates on water use efficiency and nitrogen uptake in maize. Agric Water Manag 179:271–276

    Google Scholar 

  • Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physiol 144:307–313

    CAS  Google Scholar 

  • Yang G, Rhodes D, Joly RJ (1996) Effect of high temperature on membrane stability and chlorophyll fluorescence in glycinebetaine-containing maize lines. Aust J Plant Physiol 23:431–443

    Google Scholar 

  • Yang LP, Dong S, Zhang J, Zhao B (2019a) Effects of fertilizer type and rate on summer maize grain yield and ammonia volatilization loss in northern China. J Soil Sediment 19:2200–2211

    CAS  Google Scholar 

  • Yang Z, Wang Z, Yang C, Yang Z, Li H, Wu Y (2019b) Physiological responses and small RNAs changes in maize under nitrogen deficiency and resupply. Genes Genom 41:1183–1194

    CAS  Google Scholar 

  • Yao Y, Zhang M, TianY ZM, Zeng K, Zhang B, Zhao M, Yin B (2018) Azolla biofertilizer for improving low nitrogen use efficiency in an intensive rice cropping system. Field Crops Res 216:158–164

    Google Scholar 

  • Zhang J, Blackmer AM, Blackmer TM, Kyveryga PM, Ellsworth JW (2007a) Nitrogen deficiency and recovery in sustainable corn production as revealed by leaf chlorophyll measurements. Agron Sustain Dev 27:313–319

    CAS  Google Scholar 

  • Zhang LX, Li SX, Zhang H, Liang ZS (2007b) Nitrogen rates and water stress effects on production, lipid peroxidation and antioxidative enzyme activities in two maize (Zea mays L.) genotypes. J Agro Crop Sci 193:387–397

    CAS  Google Scholar 

  • Zhang LX, Li SX, Liang ZS (2009) Differential plant growth and osmotic effects of two maize (Zea mays L.) cultivars to exogenous glycinebetaine application under drought stress. Plant Growth Regul 58:297–309

    CAS  Google Scholar 

Download references

Acknowledgements

The authors extend their appreciation to the Deanship of Scientific Research at King Khalid University for funding this work through Program of Research Groups under grant number (R.G.P 2/28/40).

Author information

Authors and Affiliations

  1. Department of Agricultural Botany, Faculty of Agriculture, Tanta University, Tanta, Egypt

    Hanafey F. Maswada

  2. Department of Agronomy, Faculty of Agriculture, Tanta University, Tanta, Egypt

    Usama A. Abd El-Razek

  3. Department of Environment and Bio-Agriculture, Faculty of Agriculture, Al-Azhar University, Cairo, Egypt

    Abdel-Nasser A. El-Sheshtawy

  4. Business Administration Department, Community College, King Khalid University, Abha, Kingdom of Saudi Arabia

    Yasser S. A. Mazrou

Authors
  1. Hanafey F. Maswada
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Usama A. Abd El-Razek
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Abdel-Nasser A. El-Sheshtawy
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yasser S. A. Mazrou
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hanafey F. Maswada.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Research Involving Human and Animal Participants

This article does not contain any studies with human participants (or animals) performed by any of the authors.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Maswada, H.F., Abd El-Razek, U.A., El-Sheshtawy, AN.A. et al. Effect of Azolla filiculoides on Growth, Physiological and Yield Attributes of Maize Grown under Water and Nitrogen Deficiencies. J Plant Growth Regul 40, 558–573 (2021). https://doi.org/10.1007/s00344-020-10120-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-020-10120-5

Keywords

Search

Navigation