Skip to main content

Advertisement

Log in

ACC deaminase positive Enterobacter-mediated mitigation of salinity stress, and plant growth promotion of Cajanus cajan: a lab to field study

  • Research Article
  • Published:
Physiology and Molecular Biology of Plants Aims and scope Submit manuscript

Abstract

Salinity is a major abiotic stress that negatively impacts plant health and soil microbiota. ACC (1-aminocyclopropane carboxylic acid) deaminase producing microorganisms act as natural stress busters that protect plants from different kinds of stresses. The study focused on the isolation of potent, indigenous, multi-trait ACC deaminase producers. The shortlisted ACC deaminase producers were checked for their ability to promote growth of Cajanus cajan, and mitigate stress under laboratory conditions followed by validation of their potency in naturally saline field conditions. Physiological stress markers were assessed to evaluate the impact of salinity in plants treated with ACC deaminase producer, compared to controls. Further, the contribution of ACC deaminase in stress mitigation was demonstrated by using a chemical inhibitor for ethylene biosynthesis. This study presents a polyphasic approach, transitioning from the rhizospheric soil to the laboratory to validation in the field, and puts forth a promising eco-friendly alternative for sustainable agriculture.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Aamir M, Aslam A, Khan MY, Usman M (2013) Co-inoculation with Rhizobium and plant growth promoting rhizobacteria (PGPR) for inducing salinity tolerance in mung bean under field condition of semi-arid climate. Asian J Agric Biol 1:7–12

    Google Scholar 

  • Anand G, Bisaria VS, Sharma S (2020) Impact of abiotic stressors on native rhizospheric bacterial community of Cajanus cajan. J Basic Microbiol 60:4–13

    Article  CAS  PubMed  Google Scholar 

  • Andreae WA, Ysselstein VMWH (1959) Studies on 3-indoleacetic acid metabolism. v. effect of calcium ions on 3-indoleacetic acid uptake and metabolism by pea roots. Plant Physiol 35:220–224

    Article  Google Scholar 

  • Bang C, Dagan T, Deines P, Dubilier N, Duschl WJ, Fraune S et al (2018) Metaorganisms in extreme environments: do microbes play a role in organismal adaptation? Zoology 127:1–19

    Article  PubMed  Google Scholar 

  • Barillot CDC, Sarde CO, Bert V, Tarnaud E, Cochet N (2013) A standardized method for the sampling of rhizosphere and rhizoplan soil bacteria associated to a herbaceous root system. Ann Microbiol 63:471–476

    Article  CAS  Google Scholar 

  • Barnawal D, Bharti N, Maji D, Chanotiya CS, Kalra A (2012) 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase-containing rhizobacteria protect Ocimum sanctum plants during waterlogging stress via reduced ethylene generation. Plant Physiol Biochem 58:227–235

    Article  CAS  PubMed  Google Scholar 

  • Bates L, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  • Bharucha UD, Patel KC, Trivedi UB (2013) In vitro screening of isolates for its plant growth promoting activities from the rhizosphere of alfalfa (Medicago sativa). J Microbiol Biotech Res 3:79–88

    Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Cappuccino JC, Sherman N (1992) Microbiology: a laboratory manual, 3rd edn. Benjamin Cummings Publication Co., New York

    Google Scholar 

  • Chandra D, Srivastava R, Gupta VV, Franco CM, Sharma AK (2019) Evaluation of ACC-deaminase-producing rhizobacteria to alleviate water-stress impacts in wheat (Triticum aestivum L.) plants. Can J Microbiol 65:387–403

    Article  CAS  PubMed  Google Scholar 

  • Claussen W (2005) Proline as a measure of stress in tomato plants. Plant Sci 168:241–248

    Article  CAS  Google Scholar 

  • Dobereiner J (1988) Isolation and identification of aerobic nitrogen fixing bacteria from soil and plants. In: Alef K, Nanniperi P (eds) Nitrogen fixation with non-legumes. Springer, Dordrecht, pp 207–212

    Google Scholar 

  • Etesami H, Hosseini HM, Alikhani HA (2014) Bacterial biosynthesis of 1-aminocyclopropane-1-caboxylate (ACC) deaminase, a useful trait to elongation and endophytic colonization of the roots of rice under constant flooded conditions. Physiol Mol Biol Plants 20:425–434

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Glick BR (2014) Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol Res 169:30–39

    Article  CAS  PubMed  Google Scholar 

  • Goicoechea N, Merino S, Sánchez-Díaz M (2005) Arbuscular mycorrhizal fungi can contribute to maintain antioxidant and carbon metabolism in nodules of Anthyllis cytisoides L. subjected to drought. J Plant Physiol 162:27–35

    Article  CAS  PubMed  Google Scholar 

  • Gordon SA, Weber RP (1951) Colorimetric estimation of indoleacetic acid. Plant Physiol 26:192–195

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gupta R, Bru D, Bisaria VS, Philippot L, Sharma S (2012) Responses of Cajanus cajan and rhizospheric N-cycling communities to bioinoculants. Plant Soil 358:143–154

    Article  CAS  Google Scholar 

  • Hamdia MA, Shaddad MAK, Doaa MM (2004) Mechanism of salt tolerance and interactive effect of Azospirillum brasilense inoculation on maize cultivars grown under salt stress conditions. Plant Growth Regul 44:165–174

    Article  CAS  Google Scholar 

  • Hass D, Defago G (2005) Biological control of soil-born pathogen by fluorescent pseudomonads. Nat Rev Microbiol 3:369–372

    Google Scholar 

  • Hodges DM, Delong JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acid reactive-substances assay for estimating lipid peroxidation in plant tissue containing anthocyanin and other interfering compounds. Planta 207:604–611

    Article  CAS  Google Scholar 

  • Jamil A, Riaz S, Ashraf M, Foolad MR (2011) Gene expression profiling of plants under salt stress. Crit Rev Plant Sci 30:435–458

    Article  Google Scholar 

  • Kang SM, Shahzad R, Bilal S, Khan AL, Park Y-G, Lee K-E, et al. (2019) Indole-3-acetic-acid and ACC deaminase producing Leclercia adecarboxylata MO1 improves Solanum lycopersicum L. growth and salinity stress tolerance by endogenous secondary metabolites regulation. BMC Microbiol 19:80

  • Kiani MZ, Sultan T, Ali A, Rizvi ZF (2016) Application of ACC-deaminase containing PGPR improves sunflower yield under natural salinity stress. Pak J Bot 48:53–56

    CAS  Google Scholar 

  • Kruasuwan W, Thamchaipenet A (2018) 1-Aminocyclopropane-1-carboxylate (ACC) deaminase-producing endophytic diazotrophic Enterobacter sp. EN-21 modulates salt–stress response in sugarcane. J Plant Growth Regul 37:849–858

    Article  CAS  Google Scholar 

  • Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, New York, pp 115–175

    Google Scholar 

  • Lorck H (1948) Production of hydrocyanic acid by bacteria. Physiol Plant 1:142–146

    Article  CAS  Google Scholar 

  • Madhaiyan M, Poonguzhali S, Ryu J, Sa T (2006) Regulation of ethylene levels in canola (Brassica campestris) by 1-aminocyclopropane-1-carboxylate deaminase-containing Methylobacterium fujisawaense. Planta 224:268–278

    Article  CAS  PubMed  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  CAS  PubMed  Google Scholar 

  • Nadeem SM, Zahir ZA, Naveed M, Arshad M (2009) Rhizobacteria containing ACC-deaminase confer salt tolerance in maize grown on salt-affected fields. Can J Microbiol 55:1302–1309

    Article  CAS  PubMed  Google Scholar 

  • Nautiyal CS (1999) An efficient microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS Micobiol Lett 170:265–270

    Article  CAS  Google Scholar 

  • Naylor D, Coleman-Derr D (2018) Drought stress and root-associated bacterial communities. Front Plant Sci 8:2223

    Article  PubMed  PubMed Central  Google Scholar 

  • Nishiguchi MK, Doukakis P, Egan M, Kizirian D, Phillips A, Prendini L et al (2002) DNA isolation procedures. In: DeSalle R, Giribet G, Wheeler W (eds) Methods and tools in biosciences and medicine: techniques in molecular systematics and evolution. Verlag, Basel, pp 249–287

    Google Scholar 

  • Nordstedt NP, Jones ML (2020) Isolation of rhizosphere bacteria that improve quality and water stress tolerance in greenhouse ornamentals. Front Plant Sci 11:826

    Article  PubMed  PubMed Central  Google Scholar 

  • Oliveira CA, Alves VMC, Marriel IE, Gomes EA, Scotti MR, Carneiro NP et al (2009) Phosphate solubilizing microorganisms isolated from rhizosphere of maize cultivated in an oxisol of the Brazilian Cerrado Biome. Soil Biol Biochem 41:1782–1787

    Article  CAS  Google Scholar 

  • Palaniyandi SA, Damodharan K, Yang SH, Suh JW (2014) Streptomyces sp. strain PGPA39 alleviates salt stress and promotes growth of ‘Micro Tom’tomato plants. J Appl Microbiol 117:766–773

    Article  CAS  PubMed  Google Scholar 

  • Penrose DM, Glick BR (2003) Technical focus methods for isolating and characterizing ACC deaminase-containing plant growth-promoting rhizobacteria. Physiol Plant 118:10–15

    Article  CAS  PubMed  Google Scholar 

  • Qiao G, Wen XP, Yu LF, Ji XB (2011) The enhancement of drought tolerance for pigeon pea inoculated by arbuscular mycorrhizae fungi. Plant Soil Environ 57:541–546

    Article  Google Scholar 

  • Saikia J, Sarma RK, Dhandia R, Yadav A, Bharali R, Gupta VK et al (2018) Alleviation of drought stress in pulse crops with ACC deaminase producing rhizobacteria isolated from acidic soil of Northeast India. Sci Rep 8:3560

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sarkar A, Ghosh PK, Pramanik K, Mitra S, Soren T, Pandey S et al (2018) A halotolerant Enterobacter sp. displaying ACC deaminase activity promotes rice seedling growth under salt stress. Res Microbiol 169:20–32

    Article  CAS  PubMed  Google Scholar 

  • Saxena KB, Nadarajan N (2010) Prospects of pigeon pea hybrids in Indian agriculture. Electron J Plant Breed 1:1107–1117

    Google Scholar 

  • Schwarz D, Grosch R (2003) Influence of nutrient solution concentration and a root pathogen (Pythium aphanidermatum) on tomato root growth and morphology. Sci Hort 97:109–120

    Article  CAS  Google Scholar 

  • Schwyn B, Neilands JB (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160:47–56

    Article  CAS  PubMed  Google Scholar 

  • Shaharoona B, Arshad M, Khalid A (2007) Differential response of etiolated pea seedlings to inoculation with rhizobacteria capable of utilizing 1-aminocyclopropane-1-carboxylate or l-methionine. J Microbiol 45:15–20

    CAS  PubMed  Google Scholar 

  • Singh RP, Jha PN (2016a) The multifarious PGPR Serratia marcescens CDP-13 augments induced systemic resistance and enhanced salinity tolerance of wheat (Triticum aestivum L.). PloS ONE 11:e0155026

  • Singh RP, Jha PN (2016b) Mitigation of salt stress in wheat plant (Triticum aestivum) by ACC deaminase bacterium Enterobacter sp. SBP-6 isolated from Sorghum bicolor. Acta Physiol Plant 38:110

  • Sood G, Kaushal R, Chauhan A, Gupta S (2018) Effect of conjoint application of indigenous PGPR and chemical fertilizers on productivity of maize (Zea mays L.) under mid hills of Himachal Pradesh. J Plant Nutr 41:297–303

    Article  CAS  Google Scholar 

  • Stromberger ME, Abduelafez I, Byrne P, Elamari AA, Manter DK, Weir T (2017) Genotype-specific enrichment of 1-aminocyclopropane-1-carboxylic acid deaminase-positive bacteria in winter wheat rhizospheres. Soil Sci Soc Am J 81:796–805

    Article  CAS  Google Scholar 

  • Taiz L, Zeiger E (2002) Plant physiology, 3rd edn. Sinauer Associates, Sunderland

    Google Scholar 

  • Timmusk S, Paalme V, Pavlicek T, Bergquist J, Vangala A, Danilas T et al. (2011) Bacterial distribution in the rhizosphere of wild barley under contrasting microclimates. PLoS ONE 6:e17968

  • Ullah A, Akbar A, Luo Q, Khan AH, Manghwar H, Shaban M et al (2019) Microbiome diversity in cotton rhizosphere under normal and drought conditions. Microbiol Ecol 77:429–439

    Article  CAS  Google Scholar 

  • Win KT, Tanaka F, Okazaki K, Ohwaki Y (2018) The ACC deaminase expressing endophyte Pseudomonas spp. enhances NaCl stress tolerance by reducing stress-related ethylene production, resulting in improved growth, photosynthetic performance, and ionic balance in tomato plants. Plant Physiol Biochem 127:599–607

    Article  CAS  PubMed  Google Scholar 

  • Yaish MW, Al-Lawati A, Jana GA, Vishwas Patankar H, Glick BR (2016) Impact of soil salinity on the structure of the bacterial endophytic community identified from the roots of Caliph Medic (Medicago truncatula). PLoS ONE 11:e0159007

  • Yan N, Marschner P, Cao W, Zuo C, Qin W (2015) Influence of salinity and water content on soil microorganisms. Int Soil Water Cons Res 3:316–323

    Article  Google Scholar 

  • Zarei T, Moradi A, Kazemeini SA, Akhgar A, Rahi AA (2020) The role of ACC deaminase producing bacteria in improving sweet corn (Zea mays L. var saccharata) productivity under limited availability of irrigation water. Sci Rep 10:20361

Download references

Funding

The work was supported by Science and Engineering Research Board, Department of Science and Technology, Govt. of India (Grant No. YSS/2015/001437) granted to SS. GA wishes to acknowledge his fellowship from IIT Delhi. AB wishes to acknowledge her fellowship from Science and Engineering Research Board, Department of Science and Technology, Government of India (PDF/2018/001905).

Author information

Authors and Affiliations

Authors

Contributions

GA and SS conceptualized the study, SS acquired financial support, GA and SS designed the experiments, GA, VLS, SD and AB performed the experiments and compiled the data, SS supervised the work, GA wrote the original draft, AB and SS reviewed and edited the manuscript, all authors approved the manuscript.

Corresponding author

Correspondence to Shilpi Sharma.

Ethics declarations

Conflict of interest

The authors declared that they have no conflict of interest.

Additional information

Publisher's Note

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

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file 1 (DOCX 8935 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Anand, G., Bhattacharjee, A., Shrivas, V.L. et al. ACC deaminase positive Enterobacter-mediated mitigation of salinity stress, and plant growth promotion of Cajanus cajan: a lab to field study. Physiol Mol Biol Plants 27, 1547–1557 (2021). https://doi.org/10.1007/s12298-021-01031-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12298-021-01031-0

Keywords

Navigation