Skip to main content
SpringerLink
Log in

Priming maize seeds with cyanobacteria enhances seed vigour and plant growth in elite maize inbreds

  • Original Article
  • Published:
3 Biotech Aims and scope Submit manuscript

Abstract

Biofilm formation of a nitrogen-fixing cyanobacterium Anabaena torulosa with a beneficial fungus Trichoderma viride (An-Tr) was examined under laboratory conditions. A gradual enhancement in growth over A. torulosa alone was recorded in the biofilm, with 15–20% higher values in nitrogen fixation, IAA and exopolysaccharide production illustrating the synergism among the partners in the biofilm. To investigate the role of such biofilms in priming seed attributes, mesocosm studies using primed seeds of two maize inbred lines (V6, V7) were undertaken. Beneficial effects of biofilm (An-Tr) were recorded, as compared to uninoculated treatment and cyanobacterial consortium (Anabaena–Nostoc; BF 1-4) at both stages (7 and 21 DAS, days after sowing) with a significant increase of more than 20% in seedling attributes, along with 5–15% increment in seed enzyme activities. More than three- to fivefold higher values in nitrogen fixation and C-N mobilizing enzyme activities, and significant increases in leaf chlorophyll, proteins and PEP carboxylase activity were observed with V7-An-Tr biofilm. Cyanobacterial inoculation brought about distinct changes in the soil phospholipid fatty acid profiles (PLFA); particularly, significant changes in those representing eukaryotes and anaerobic bacteria. Principal component analyses illustrated the significant role of dehydrogenase activity and microbial biomass carbon and distinct elicited effects on soil microbial communities, as evidenced by the PLFA. This investigation highlighted the promise of cyanobacteria as valuable priming options to improve mobilization of nutrients at seed stage, modulating the abundance and activities of various soil microbial communities, thereby, enhanced plant growth and vigour 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
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Baudoin E, Benizri E, Guckert A (2003) Impact of artificial root exudates on the bacterial community structure in bulk soil and maize rhizosphere. Soil Biol Biochem 35:1183–1192

    CAS  Google Scholar 

  • Berendsen RL, Pieterse CM, Bakker PA (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486

    CAS  PubMed  Google Scholar 

  • Berman-Frank I, LundgrenFalkowski PP (2003) Nitrogen fixation and photosynthetic oxygen evolution in cyanobacteria. Res Microbiol 154:157–164

    CAS  PubMed  Google Scholar 

  • Bidyarani N, Prasanna R, Babu S, Hossain F (2016) Enhancement of plant growth and yields in Chickpea (Cicer arietinum L.) through novel cyanobacterial and biofilmed inoculants. Microbiol Res 188:97–105

    PubMed  Google Scholar 

  • Buyer JS, Teasdale JR, Roberts DP, Zasada IA, Maul JE (2010) Factors affecting soil microbial community structure in tomato cropping systems. Soil Biol Biochem 42:831–841

    CAS  Google Scholar 

  • Casida LEJ, Klein DA, Santaro T (1964) Soil dehydrogenase activity. Soil Sci 98:371–376

    CAS  Google Scholar 

  • Chand R, Pavithra S (2015) Fertiliser use and imbalance in India. Econ Polit Wkly 50:99

    Google Scholar 

  • Chang WS, Halverson LJ (2003) Reduced water availability influences the dynamics, development, and ultrastructural properties of Pseudomonas putida biofilms. J Bacteriol 185:6199–6204

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen L, Xin X, Zhang J, Redmile-Gordon M, Nie G (2019) Soil characteristics overwhelm cultivar effects on the structure and assembly of root-associated microbiomes of modern maize. Pedosphere 29:360–373

    Google Scholar 

  • Corrales I, Amenós M, Poschenrieder C, Barceló J (2007) Phosphorus efficiency and root exudates in two contrasting tropical maize varieties. J Plant Nutr 30:887–900

    CAS  Google Scholar 

  • Dharmawardene MWN, Haystead A, Stewart WDP (1973) Glutamine synthetase of the nitrogen-fixing alga Anabaena cylindrical. Arch Microbiol 90:281–295

    CAS  Google Scholar 

  • Di Cello F, Bevivino A, Chiarini L, Fani R, Paffetti D, Tabacchioni S, Dalmastri C (1997) Biodiversity of a Burkholderia cepacia population isolated from the maize rhizosphere at different plant growth stages. Appl Environ Microbiol 63:4485–4493

    PubMed  PubMed Central  Google Scholar 

  • Dicko AH, Babana AH, Kassogué A, Fané R, Nantoumé D, Ouattara D, Maiga K, Dao S (2018) A Malian native plant growth promoting Actinomycetes based biofertilizer improves maize growth and yield. Symbiosis 75:267–275

    Google Scholar 

  • Dineshkumar R, Subramanian J, Gopalsamy J, Jayasingam P, Arumugam A, Kannadasan S, Sampathkumar P (2019) The impact of using microalgae as biofertilizer in maize (Zea mays L.). Waste Biomass Valoriz 10:1101–1110

    CAS  Google Scholar 

  • Duncan DB (1955) Multiple range and multiple F tests. Biometrics 11:1–42

    Google Scholar 

  • Filip Z (2002) International approach to assessing soil quality by ecologically-related biological parameters. Agric Ecosyst Environ 88:169–174

    Google Scholar 

  • Frostegard A, Baath E (1996) The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil. Biol Fertil Soils 22:59–65

    Google Scholar 

  • Gupta V, Ratha SK, Sood A, Chaudhary V, Prasanna R (2013) New insights into the biodiversity and applications of cyanobacteria (blue-green algae)—prospects and challenges. Algal Res 2:79–97

    Google Scholar 

  • Hardy R, Burns RC, Holsten RD (1973) Applications of the acetylene-ethylene assay for measurement of nitrogen fixation. Soil Biol Biochem 5:47–81

    CAS  Google Scholar 

  • Hiscox JD, Israelstam GF (1979) A method for the extraction of chlorophyll from leaf tissue without maceration. Can J Bot 57:1332–1334

    CAS  Google Scholar 

  • Jayasinghearachchi HS, Seneviratne G (2004) A Bradyrhizobial-Penicillium spp. biofilm with nitrogenase activity improves N2 fixing symbiosis of soybean. Biol Fertil Soils 40:432–434

    CAS  Google Scholar 

  • Kanchan K, Simranjit K, Ranjan K, Prasanna R, Ramakrishnan B, Singh MC, Hasan M, Shivay YS (2018) Microbial biofilm inoculants benefit growth and yield of chrysanthemum varieties under protected cultivation through enhanced nutrient availability. Plant Biosyst 153:301–316. https://doi.org/10.1080/11263504.2018.1478904

    Article  Google Scholar 

  • Karthikeyan N, Prasanna R, Nain L, Kaushik BD (2007) Evaluating the potential of plant growth promoting cyanobacteria as inoculants for wheat. Eur J Soil Biol 43:23–30

    CAS  Google Scholar 

  • Kaushik BD (1987) Laboratory methods for blue green algae. Associated Publishing Company, New Delhi

    Google Scholar 

  • Krishnan HB, Blanchette JT, Okita TW (1985) Wheat invertases: characterization of cell wall-bound and soluble forms. Plant Physiol 78:241–245

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lowe RH, Evans HJ (1964) Preparation and some properties of a soluble nitrate reductase from Rhizobium japonicum. Biochim Biophys Acta (BBA) 85:377–389

    CAS  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193:265–275

    CAS  Google Scholar 

  • Lugtenberg BJ, Kravchenko LV, Simons M (1999) Tomato seed and root exudate sugars: composition, utilization by Pseudomonas biocontrol strains and role in rhizosphere colonization. Environ Microbiol 1:439–446

    CAS  PubMed  Google Scholar 

  • MacKinney G (1941) Absorption of light by chlorophyll solutions. J Biol Chem 140:315–322

    CAS  Google Scholar 

  • Mandal B, Vlek PLG, Mandal LN (1999) Beneficial effects of blue-green algae and Azolla, excluding supplying nitrogen, on wetland rice fields: a review. Biol Fertil Soils 28:329–342

    CAS  Google Scholar 

  • Manjunath M, Kanchan A, Ranjan K, Venkatachalam S, Prasanna R, Ramakrishnan B, Hossain F, Nain L, Shivay YS, Rai AB, Singh B (2016) Beneficial cyanobacteria and eubacteria synergistically enhance bioavailability of soil nutrients and yield of okra. Heliyon 2:e00066

    PubMed  PubMed Central  Google Scholar 

  • Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 31:426–428

    CAS  Google Scholar 

  • Misra S, Kaushik BD (1989) Growth promoting substances of cyanobacteria. I: Vitamins and their influence on rice plant. Proc Indian Natl Sci Acad 55:295–300

    CAS  Google Scholar 

  • Moshynets OV, Kosakivska IV (2010) Phytosphere ecology: plant-microbial interactions. Part 1. Structure functional characteristic of rhizo-, endo- and phytosphere. Bull Nat Kharkov Agrar Univ 2:19–36

    Google Scholar 

  • Nayak S, Prasanna R, Pabby A, Dominic TK, Singh PK (2004) Effect of urea, blue green algae and Azolla on nitrogen fixation and chlorophyll accumulation in soil under rice. Biol Fertil Soils 40:67–72

    CAS  Google Scholar 

  • Neumann G, Römheld V (2001) The release of root exudates as affected by the plant’s physiological status. In: Pinton R, Varini Z, Nannipieri P (eds) The rhizosphere. Biochemistry and organic substances at the soil–plant interface. Marcel Dekker, New York, pp 41–93

    Google Scholar 

  • Noirot-Gros MF, Shinde S, Larsen PE, Zerbs S, Korajczyk P, Kemner KM, Noirot PH (2018) Dynamics of aspen roots colonization by pseudomonads reveals strain-specific and mycorrhizal-specific patterns of biofilm formation. Front Microbiol. https://doi.org/10.3389/fmicb.2018.00853

    Article  PubMed  PubMed Central  Google Scholar 

  • Nunan N, Morgan MA, Herlihy M (1998) Ultraviolet absorbance (280 nm) of compounds released from soil during chloroform fumigation as an estimate of the microbial biomass. Soil Biol Biochem 30:1599–1603

    CAS  Google Scholar 

  • O'Toole GA (2011) Microtiter dish biofilm formation assay. JoVE 47:1–2

    Google Scholar 

  • Pandey S, Gupta S, Ramawat N (2019) Unravelling the potential of microbes isolated from rhizospheric soil of chickpea (Cicer arietinum) as plant growth promoter. 3 Biotech 9(7):277

    PubMed  Google Scholar 

  • Patten CL, Glick BR (2002) Role of Pseudomonas putida indole acetic acid in development of the host plant root system. Appl Environ Microbiol 68:3795–3801

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pedurand P, Reynaud PA (1987) Do cyanobacteria enhance germination and growth of rice? Plant Soil 101:235–240

    Google Scholar 

  • Prasanna R, Bidyarani N, Babu S, Hossain F, Shivay YS, Nain L (2015) Cyanobacterial inoculation elicits plant defense response and enhanced Zn mobilization in maize hybrids. Cogent Food Agric 1:998507

    Google Scholar 

  • Prasanna R, Jaiswal P, Nayak S, Sood A, Kaushik BD (2009) Cyanobacterial diversity in the rhizosphere of rice and its ecological significance. Indian J Microbiol 49:89–97

    CAS  PubMed  PubMed Central  Google Scholar 

  • Prasanna R, Kanchan A, Ramakrishnan B, Ranjan K, Venkatachalam S, Hossain F, Shivay YS, Krishnan P, Nain L (2016) 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, Kumar A, Babu S, Chawla G, Chaudhary V, Singh S, Gupta V, Nain L, Saxena AK (2013) Deciphering the biochemical spectrum of novel cyanobacterium-based biofilms for use as inoculants. Biol Agric Hortic 29:145–158

    Google Scholar 

  • Quesada E, Béjar V, Calvo C (1993) Exopolysaccharide production by Volcaniella eurihalina. Experientia 49:1037–1041

    CAS  Google Scholar 

  • Rahman K, Zhang D (2018) Effects of fertilizer broadcasting on the excessive use of inorganic fertilizers and environmental sustainability. Sustainability 10:759

    Google Scholar 

  • Ramsey PW, Rillig MC, Feris KP, Holben WE, Gannon JE (2006) Choice of methods for soil microbial community analysis: PLFA maximizes power compared to CLPP and PCR-based approaches. Pedobiologia 50:275–280

    CAS  Google Scholar 

  • Rana A, Joshi M, Prasanna R, Shivay YS, Nain L (2012) Biofortification of wheat through inoculation of plant growth promoting rhizobacteria and cyanobacteria. Eur J Soil Biol 50:118–126

    CAS  Google Scholar 

  • Ranjan K, Priya H, Ramakrishnan B, Prasanna R, Venkatachalam S, Thapa S, Tiwari R, Nain L, Singh R, Shivay YS (2016) Cyanobacterial inoculation modifies the rhizosphere microbiome of rice planted to a tropical alluvial soil. Appl soil ecol 108:195–203

    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 

  • Ringelberg DB, Sutton S, White DC (1997) Biomass, bioactivity and biodiversity: microbial ecology of the deep subsurface: analysis of ester-linked phospholipid fatty acids. FEMS Microbiol Rev 20:371–377

    CAS  Google Scholar 

  • Rudrappa T, Biedrzycki ML, Bais HP (2008) Causes and consequences of plant-associated biofilms. FEMS Microbiol Ecol 64:153–166

    CAS  PubMed  Google Scholar 

  • Schmidt JE, Gaudin AC (2018) What is the agronomic potential of biofertilizers for maize? A meta-analysis. FEMS Microbiol Ecol 94:fiy094

    Google Scholar 

  • Seneviratne G, Weerasekara ML, Seneviratne KA, Zavahir JS, Kecskés ML, Kennedy IR (2010) Importance of biofilm formation in plant growth promoting rhizobacterial action. In: Maheshwari D (ed) Plant growth and health promoting bacteria. Springer, Berlin, Heidelberg, pp 81–95

    Google Scholar 

  • Singh B, Ryan J (2015) Managing fertilizers to enhance soil health. International Fertilizer Industry Association, Paris

    Google Scholar 

  • Thapa S, Bharti A, Prasanna R (2017) Algal biofilms and their biotechnological significance. In: Rastogi RP, Madamwar D, Pandey A (eds) Algal green chemistry. Elsevier, Amsterdam, pp 285–303. https://doi.org/10.1016/B978-0-444-63784-0.00014-X

    Chapter  Google Scholar 

  • Velmourougane K, Prasanna R, Saxena AK (2017) Agriculturally important microbial biofilms: present status and future prospects. J Basic Microbiol 57:548–573

    PubMed  Google Scholar 

  • Venkataraman GS (1981) Blue-green algae for rice production—a manual for its promotion. FAO Soils Bull (FAO) 46:1–99

    Google Scholar 

  • Verma R, Chourasia SK, Jha MN (2011) Population dynamics and identification of efficient strains of Azospirillum in maize ecosystems of Bihar (India). 3 Biotech 1(4):247–253

    PubMed  PubMed Central  Google Scholar 

  • Walker TS, Bais HP, Déziel E, Schweizer HP, Rahme LG, Fall R, Vivanco JM (2004) Pseudomonas aeruginosa-plant root interactions. Pathogenicity, biofilm formation, and root exudation. Plant Physiol 134:320–331

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wright SF, Upadhyaya A (1996) Extraction of an abundant and unusual protein from soil and comparison with hyphal protein of arbuscular mycorrhizal fungi. Soil Sci 161:575–586

    CAS  Google Scholar 

  • Wu MX, Wedding RT (1985) Diurnal regulation of phosphoenolpyruvate carboxylase from Crassula. Plant Physiol 77:667–675

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zelles L (1999) Fatty acid patterns of phospholipids and lipopolysaccharides in the characterization of microbial communities in soil: a review. Biol Fertil Soils 29:111–129

    CAS  Google Scholar 

Download references

Acknowledgements

The authors are thankful to the Division of Microbiology, Post Graduate School and Director, ICAR-IARI (New Delhi, India) for providing necessary facilities towards the Ph.D. program of the first author, who also is grateful to SKRAU, Bikaner, for deputation on study leave. This study was supported partially by the grants from the ICAR-Network Project on Microorganisms ‘Application of Microorganisms in Agriculture and Allied Sectors’ (AMAAS) granted by Indian Council of Agricultural Research (ICAR), New Delhi to RP. The authors are also thankful to Mr. Gulab Singh for his help in the soil analyses and Mr. Suresh Kumar, Division of Agricultural Economics, ICAR-IARI, New Delhi for assisting in the statistical analyses. Funding was provided by National Bureau of Agriculturally Important Microorganisms (T12/22).

Author information

Authors and Affiliations

  1. Division of Microbiology, ICAR-Indian Agricultural Research Institute (IARI), New Delhi, 110012, India

    Vikas Sharma, Radha Prasanna & Lata Nain

  2. Maize Genetics Section, Division of Genetics, ICAR-Indian Agricultural Research Institute, New Delhi, 110012, India

    Firoz Hossain & Vignesh Muthusamy

  3. Division of Soil Science and Agricultural Chemistry, ICAR-Indian Agricultural Research Institute, New Delhi, 110012, India

    Shrila Das

  4. Division of Agronomy, ICAR-Indian Agricultural Research Institute, New Delhi, 110012, India

    Yashbir Singh Shivay

  5. National Phytotron Facility, ICAR-Indian Agricultural Research Institute, New Delhi, 110012, India

    Arun Kumar

Authors
  1. Vikas Sharma
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Radha Prasanna
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Firoz Hossain
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Vignesh Muthusamy
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Lata Nain
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Shrila Das
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yashbir Singh Shivay
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Arun Kumar
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

VS conducted the experiments, recorded the scientific data. RP outlined the hypothesis, designed, assisted in the execution of experiments, and facilitated lab resources, including instrumentation and chemicals to VS. RP and VS interpreted the data and wrote the final manuscript. FH and VM provided plant material and guided in the establishment of experiments. LN and SD provided facilities and expertise for analyses. YSS facilitated the nutrient analyses and its interpretation. AK assisted in the arrangements for experimental setup and its maintenance.

Corresponding author

Correspondence to Radha Prasanna.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest and no competing financial interests.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOC 73 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sharma, V., Prasanna, R., Hossain, F. et al. Priming maize seeds with cyanobacteria enhances seed vigour and plant growth in elite maize inbreds. 3 Biotech 10, 154 (2020). https://doi.org/10.1007/s13205-020-2141-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s13205-020-2141-6

Keywords

Search

Navigation