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Potential applicability of a cyanobacterium as a biofertilizer and biopesticide in rice fields

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Abstract

Aims

This study aimed to evaluate the potential applicability of Anabaena variabilis SCAU30 as a biofertilizer and biopesticide in rice fields.

Methods

The effects of A. variabilis SCAU30 inoculation on disease severity, plant growth, rice yield, and soil nutrients were investigated by microchamber, micro-area, and field experiments. The nitrogen fixation ability was estimated by acetylene reduction activity. Hormones were analyzed using liquid chromatography-tandem mass spectrometry.

Results

In microchamber experiments, the control efficacies of A. variabilis SCAU30 against rice sheath blight and bacterial blight were 62.3 ± 8.9% and 45.3 ± 5.6%, respectively. The cell extracts of A. variabilis SCAU30 exhibited high antagonistic effects on corresponding pathogens, whereas volatile compounds only showed inhibition on Xanthomonas oryzae. The results of pond experiments showed that inoculation with A. variabilis SCAU30 could promote the growth of rice plants, increase yield, control diseases, and decrease chemical nitrogen fertilizer input. Moreover, in field experiments, the combined treatment of A. variabilis SCAU30 and 50% topdressing fertilizer increased rice yields by 13.9%–22% compared with the conventional fertilizer treatment. This potentially represents economic gains of 26,753 ~ 38,987 Chinese Yuan ha−1 season−1 if sold as a green food.

Conclusions

The present study suggests that A. variabilis SCAU30 may act as a fertilizer and pesticide in developing green rice in South China.

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Abbreviations

SCAU:

South China Agricultural University

NFC:

nitrogen-fixing cyanobacterium

RSB:

rice sheath blight;

RBB:

rice leaf blight

PDA:

potato dextrose agar

NA:

nutrient agar

Chl a :

chlorophyll a

TN:

total nitrogen

TOC:

total organic carbon

NH4-N:

ammonium nitrogen

AP:

available phosphorus

FW:

fresh weight

DW:

dry weight

SA:

salicylic acid

TZ:

trans-zeatin

TZR:

trans-zeatin riboside

N6:

N6-dimethylallyladenine

IBA:

indole-3-butyric acid

IAM:

indole-3-acetamide

CRD:

completely randomized design

CNY:

Chinese Yuan

References

  • Abdel-Hafez SII, Abo-Elyousr KAM, Abdel-Rahim IR (2015) Fungicidal activity of extracellular products of cyanobacteria against Alternaria porri. Eur J Phycol 50:239–245

    CAS  Google Scholar 

  • Ali MA, Sattar MA, Islam MN, Inubushi K (2014) Integrated effects of organic, inorganic and biological amendments on methane emission, soil quality and rice productivity in irrigated paddy ecosystem of Bangladesh: field study of two consecutive rice growing seasons. Plant Soil 378:239–252

    CAS  Google Scholar 

  • Anahas AMP, Muralitharan G (2015) Isolation and screening of heterocystous cyanobacterial strains for biodiesel production by evaluating the fuel properties from fatty acid methyl ester (FAME) profiles. Bioresour Technol 184:9–17

    CAS  PubMed  Google Scholar 

  • Babu S, Bidyarani N, Chopra P, Monga D, Kumar R, Prasanna R, Kranthi S, Saxena AK (2015) Evaluating microbe-plant interactions and varietal differences for enhancing biocontrol efficacy in root rot disease challenged cotton crop. Eur J Plant Pathol 142:345–362

    CAS  Google Scholar 

  • Badr OAM, El-Shawaf IIS, El-Garhy HAS, Moustafa MMA, Ahmed-Farid OA (2019) Antioxidant activity and phycoremediation ability of four cyanobacterial isolates obtained from a stressed aquatic system. Mol Phylogenet Evol 134:300–310

    CAS  PubMed  Google Scholar 

  • Bakker PAHM, Ran L, Mercado-Blanco J (2014) Rhizobacterial salicylate production provokes headaches! Plant Soil 382:1–16

    CAS  Google Scholar 

  • Bhattacharyya PN, Jha DK (2012) Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World J Microbiol Biotechnol 28:1327–1350

    CAS  PubMed  Google Scholar 

  • Biondi N, Piccardi R, Margheri MC, Rodolfi L, Smith GD, Tredici MR (2004) Evaluation of Nostoc strain ATCC 53789 as a potential source of natural pesticides. Appl Environ Biotechnol 70:3313–3320

    CAS  Google Scholar 

  • Chen H, Wang S, Zhang Q (2002) New gene for bacterial blight resistance in rice located on chromosome 12 identified from Minghui 63, an elite restorer line. Phytopathology 92:750–754

    CAS  PubMed  Google Scholar 

  • De Caire GZ, De Cano MS, De Mule MCZ, De Halperin DR (1990) Antimycotic products from the cyanobacterium Nostoc muscorum against Rhizoctonia solani. Phyton 51:1–4

    Google Scholar 

  • Dubey AK, Rai AK (1995) Application of algal biofertilizers (Aulosira fertilissima var. tenuis and Anabaena doliolum Bhardwaja) for sustained paddy cultivation in northern India. Isr J Plant Sci 43:41–51

    Google Scholar 

  • Gao Z, Zhang B, Liu H, Han J, Zhang Y (2017) Identification of endophytic Bacillus velezensis ZSY-1 strain and antifungal activity of its volatile compounds against Alternaria solani and Botrytis cinereal. Biol Control 105:27–39

    Google Scholar 

  • Hashtroudi MS, Ghassempour A, Riahi H, Shariatmadari Z, Khanjir M (2013) Endogenous auxins in plant growth-promoting cyanobacteria—Anabaena vaginicola and Nostoc calcicola. J Appl Phycol 25:379–386

    CAS  Google Scholar 

  • He HZ, Li YJ, Chen TF, Huang XL, Guo Q, Li SF, Yu TH, Li HS (2013) Butachlor induces some physiological and biochemical changes in a rice field biofertilizer cyanobacterium. Pestic Biochem Phys 105:224–230

    CAS  Google Scholar 

  • Hoagland DR, Arnon DI (1938) The water culture method for growing plants without soil. Calif. Agr Exp Sta Circ 347:1–39

    CAS  Google Scholar 

  • Hussain A, Hamayun M, Shah ST (2013) Root colonization and phytostimulation by phytohormones producing entophytic Nostoc sp. AH-12. Curr Microbiol 67:624–630

    CAS  PubMed  Google Scholar 

  • Kulik MM (1995) The potential for using cyanobacteria (blue-green algae) and algae in the cyanobacterial control of plant pathogenic bacteria and fungi. Eur J Plant Path 101:585–599

    Google Scholar 

  • Li SH (1981) Studies on the nitrogen-fixing blue-green algae as biofertilizer in the late rice crop. Acta Hydrobiol Sin 7:417–423 (in Chinese)

    Google Scholar 

  • Mącik M, Gryta A, Frąc M (2020) Chapter two - biofertilizers in agriculture: an overview on concepts, strategies and effects on soil microorganisms. In: Donald L. Sparks (ed) advances in agronomy. Elsevier, pp 162:31–87

    Google Scholar 

  • Mian MH, Stewart WDP (1985) Fate of nitrogen applied as Azolla and blue-green algae (cyanobacteria) in waterlogged rice soils: a 15N tracer study. Plant Soil 83:363–370

    CAS  Google Scholar 

  • Ministry of Agriculture of the People's Republic of China (2010) Method for determination of ammonium nitrogen, available phosphorus and rapidly-available potassium in acid soil - universal extract-colorimetric method: NY/T 1849–2010. Beijing. (In Chinese)

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco cultures. Physiol Plant 15:473–493

    CAS  Google Scholar 

  • Nilsson M, Bhattacharya J, Rai AN, Mariscal V (2002) Colonization of roots of rice (Oryza sativa) by symbiotic Nostoc strains. New Phytol 156:517–525

    CAS  PubMed  Google Scholar 

  • Obreht Z, Kerby NW, Gantar M, Rowell P (1993) Effects of root-associated N2-fixing cyanobacteria on the growth and nitrogen content of wheat (Triticum vulgare L.) seedlings. Biol Fert Soils 15:68–72

    CAS  Google Scholar 

  • Onofrejová L, Vašíčková J, Klejdus B, Misurcová L, Krácmar S, Kopecký J, Vacek J (2010) Bioactive phenols in algae: the application of pressurized liquid and solid-phase extraction techniques. J Pharmaceut Biomed 51:464–470

    Google Scholar 

  • Padaria JC, Tarafdar A, Raipuria R, Lone SA, Gahlot P, Shakil NA, Kumar J (2016) Identification of phenazine-1-carboxylic acid gene (phc CD) from Bacillus pumilus MTCC7615 and its role in antagonism against Rhizoctonia solani. J Basic Microbiol 56:999–1008

    CAS  PubMed  Google Scholar 

  • Peng D, Li SD, Wang JX, Chen CJ, Zhou MG (2014) Integrated biological and chemical control of rice sheath blight by Bacillus subtilis NJ-18 and Jinggangmycin. Pest Manag Sci 70:258–263

    CAS  PubMed  Google Scholar 

  • Pereira I, Ortega R, Barrientos L, Moya M, Reyes G, Kramm V (2009) Development of a biofertilizer based on filamentous nitrogen-fixing cyanobacteria for rice crops in Chile. J Appl Phycol 21:135–144

    Google Scholar 

  • Prasad B, Eizenga GC (2008) Rice sheath blight disease resistance identified in Oryza spp. accessions. Plant Dis 92:1503–1509

    CAS  PubMed  Google Scholar 

  • Prasanna R, Adak A, Verma S, Bidyarani N, Babu S, Pal M, Shivay YS, Nain L (2015a) Cyanobacterial inoculation in rice grown under flooded and SRI modes of cultivation elicits differential effects on plant growth and nutrient dynamics. Ecol Eng 84:532–541

    Google Scholar 

  • Prasanna R, Babu S, Bidyarani N, Kumar A, Triveni S, Monga D, Mukherjee AK, Kranthi S, Gokte-Narkhedkar N, Adak A (2015b) Prospecting cyanobacteria-fortified composts as plant growth promoting and biocontrol agents in cotton. Exp Agr 51:42–65

    Google Scholar 

  • Prasanna R, Chaudhary V, Gupta V, Babu S, Kumar A, Singh R, Shivay YS, Nain L (2013) Cyanobacteria mediated plant growth promotion and bioprotection against Fusarium wilt in tomato‌. Eur J Plant Pathol 136:337–353

    Google Scholar 

  • Prasanna R, Kanchan A, Ramakrishnan B, Ranjan K, Venkatachalam S, Hossain F, Shivay YS, Krishnan P, Nain L (2016a) Cyanobacteria-based bioinoculants influence growth and yields by modulating the microbial communities favourably in the rhizospheres of maize hybrids. Eur J Soil Biol 75:15–23

    Google Scholar 

  • Prasanna R, Ramakrishnan B, Ranjan K, Venkatachalam S, Kanchan A, Solanki P, Monga D, Shivay YS, Kranthi S (2016b) Microbial inoculants with multifaceted traits suppress Rhizoctonia populations and promote plant growth in cotton. J Phytopathol 164:1030–1042

    CAS  Google Scholar 

  • Renuka N, Guldhe A, Prasanna R, Singh P, Bux F (2018) Microalgae as multi-functional options in modern agriculture: current trends, prospects and challenges. Biotechnol Adv 36:1255–1273

    CAS  PubMed  Google Scholar 

  • Righini H, Baraldi E, García FY, Martel QA, Roberti R (2019) Different antifungal activity of Anabaena sp., Ecklonia sp., and Jania sp. against Botrytis cinerea. Mar Drugs 17:299. https://doi.org/10.3390/md17050299

    Article  CAS  PubMed Central  Google Scholar 

  • Righini H, Somma A, Cetrullo S, D’Adamo S, Flamigni F, Quintana AM, Roberti R (2020) Inhibitory activity of aqueous extracts from Anabaena minutissima, Ecklonia maxima and Jania adhaerens on the cucumber powdery mildew pathogen in vitro and in vivo. J Appl Phycol 32:3363–3375

    CAS  Google Scholar 

  • Rippka R, Deruells J, Waterbury JB, Herdman M, Stanier RY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61

    Google Scholar 

  • Roberti R, Galletti S, Burzi PL, Righinia H, Cetrulloc S, Perezd C (2015) Induction of defence responses in zucchini (Cucurbita pepo) by Anabaena sp. water extract‌. Biol Control 82:61–68

    CAS  Google Scholar 

  • Rush MC, Hoff JJ, Mcllrath WO (1976) A uniform disease rating system for rice disease in the United States. Proc 16th Rice tech working group. Lake Charles, Louisana, p 64

    Google Scholar 

  • Saikia K, Bora LC (2021) Exploring actinomycetes and endophytes of rice ecosystem for induction of disease resistance against bacterial blight of rice. Eur J Plant Pathol 159:67–79

    CAS  Google Scholar 

  • Shao Y, Chen Z, Xiao H, Zhu Z, Li B (2019) Integrating environmental parameters and economic benefits to analyze the ecological agriculture (EA) application in the mountain rice paddy system of Chongqing, China. Environ Sci Eur 31:22. https://doi.org/10.1186/s12302-019-0204-2

    Article  CAS  Google Scholar 

  • Singh DP, Prabha R, Yandigeri MS, Arora DK (2011) Cyanobacteria-mediated phenylpropanoids and phytohormones in rice (Oryza sativa) enhance plant growth and stress tolerance. Anton Leeuw 100:557–568

    CAS  Google Scholar 

  • Singh JS, Kumar A, Rai AN, Singh DP (2016) Cyanobacteria: a precious bio-resource in agriculture, ecosystem, and environmental sustainability. Front Microbiol 7:529. https://doi.org/10.3389/fmicb.2016.00529

    Article  PubMed  PubMed Central  Google Scholar 

  • Steward WD, Fitzgerald GP, Burris RH (1967) In situ studies on N2-fixation using the acetylene reduction technique. PNAS 58:2071–2078

    Google Scholar 

  • Tirol A, Roger PA, Wntanabe I (1982) Fate of nitrogen from a blue-green alga in a flooded rice soil. Soil Sci Pl Nutr 28:559–569

    CAS  Google Scholar 

  • Tiwari KR, Sitaula BK, Bajracharya RM, Borresen T (2010) Effects of soil and crop management practices on yields, income and nutrients losses from upland farming systems in the middle mountains region of Nepal. Nutr Cycl Agroecosyst 86:241–253

    CAS  Google Scholar 

  • Triveni S, Prasanna R, Kumar A, Bidyarani N, Singh R, Saxena AK (2015) Evaluating the promise of Trichoderma and Anabaena based biofilms as multifunctional agents in Macrophomina phaseolina-infected cotton crop. Biocontrol Sci Tech 25:656–670

    Google Scholar 

  • Vlot AC, Dempsey DA, Klessig DF (2009) Salicylic acid, a multifaceted hormone to combat disease. Annu Rev Phytopathol 47:177–206

    CAS  Google Scholar 

  • Wang FF, Wang YH, Cai ZC, Chen X (2020) Environmental losses and driving forces of nitrogen flow in two agricultural towns of Hebei province during 1997–2017. Environ Pollut 264:114636. https://doi.org/10.1016/j.envpol.2020.114636

    Article  CAS  PubMed  Google Scholar 

  • Wenz J, Davis JG, Storteboom H (2019) Influence of light on endogenous phytohormone concentrations of a nitrogen-fixing Anabaena sp. cyanobacterium culture in open raceways for use as fertilizer for horticultural crops. J Appl Phycol 31:3371–3384

    CAS  Google Scholar 

  • Wilson JT, Eskew DL, Habte M (1980) Recovery of nitrogen by rice from blue-green algae added in a flooded soil. Soil Sci Soc Am J 44:1330–1331

    CAS  Google Scholar 

  • Xie S, Zang H, Wu H, Uddin RF, Gao X (2018) Antibacterial effects of volatiles produced by Bacillus strain D13 against Xanthomonas oryzae pv. oryzae. Mol Plant Pathol 19:49–58

    CAS  PubMed  Google Scholar 

  • Zhou YW, Bao JQ, Zhang DH, Li Y, Li HS, He HZ (2020) Effect of heterocystous nitrogen-fixing cyanobacteria against rice sheath blight and the underlying mechanism. Appl Soil Ecol 153:103580. https://doi.org/10.1016/j.apsoil.2020.103580

    Article  Google Scholar 

  • Zulpa G, Zaccaro MC, Boccazzi F, Parada JL, Storni M (2003) Bioactivity of intra and extracellular substances from cyanobacteria and lactic acid bacteria on “wood blue stain” fungi. Biol Control 27:345–348

    Google Scholar 

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Acknowledgments

This work was supported by the Public Welfare Science and Technology Research Project of Zhongshan City (2018B1013 and 2019B2004), the Science and Technology Planning Project of Qingyuan City (2019DZX005), the Science and Technology Planning Project of Guangdong Province, China (2019B030301007), and the Open Foundation of Integrative Microbiology Research Centre of South China Agricultural University (IM20170301).

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Correspondence to Hongzhi He.

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Bao, J., Zhuo, C., Zhang, D. et al. Potential applicability of a cyanobacterium as a biofertilizer and biopesticide in rice fields. Plant Soil 463, 97–112 (2021). https://doi.org/10.1007/s11104-021-04899-9

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