Skip to main content

Advertisement

Log in

A Consortium of Three Plant Growth-Promoting Rhizobacterium Strains Acclimates Lycopersicon esculentum and Confers a Better Tolerance to Chilling Stress

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

Abstract

Using beneficial microorganisms has emerged as a potential new solution to induce resistance to biotic and abiotic stress tolerance in several plant species. BBS is a consortium of three plant growth-promoting rhizobacterium (PGPR) strains (Bacillus cereus AR156, B. subtilis SM21, and Serratia sp. XY21) we screened for soil-borne disease control and registered as a biofertilizer that was recently found to be resistant to the adverse environment. The present study examines the effect of BBS on chilling (4 °C) tolerance in tomato seedlings and its mechanism. After 7 days of chilling treatment and 1 week recovery at normal 28 °C, BBS-treated tomato plants had a survival rate of 92.59 %, on average six times more than control plants (15.56 %). Compared with the control, the BBS treatment stimulated faster and higher accumulations of MDA and H2O2 as chilling stress started, which initiated mechanisms to efficiently attenuate the chilling-induced injury. Besides, in relation to the control, the significantly higher transcription of CBF1 in BBS treatment may lead to stress-related gene induction. These findings suggested that BBS acclimated tomato seedlings and induced tolerance to chilling by promoting soluble sugar, proline, and osmotin accumulation, enhancing the antioxidant defense system, and stimulating CBF transcription factors to activate stress-related genes. This is the first time that PGPR-induced acclimation has been shown to protect tomato plants against low-temperature stress.

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
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Agnieszka KM, Pascal R, Tadeusz R (2008) The organ-dependent abundance of a Solanum lipid transfer protein is up-regulated upon osmotic constraints and associated with cold acclimation ability. J Exp Bot 59:2191–2203

    Article  CAS  Google Scholar 

  • Ait Barka E, Nowak J, Clément C (2006) Enhancement of chilling resistance of inoculated grapevine plantlets with a plant growth-promoting rhizobacterium, Burkholderia phytofirmans strain PsJN. Appl Environ Microbiol 72:7246–7252

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Badawi GH, Yamauchi E, Shimada E, Sasaki R, Kawano N, Tanaka K, Tanaka K (2004) Enhanced tolerance to salt stress and water deficit by overexpressing superoxide dismutase in tobacco (Nicotiana tabacum) chloroplasts. Plant Sci 166:919–928

    Article  CAS  Google Scholar 

  • Beck EH, Heim R, Hansen J (2004) Plant resistance to cold stress: mechanisms and environmental signals triggering frost hardening and dehardening. J Biosci 29:449–459

    Article  PubMed  Google Scholar 

  • Chen WP, Li PH (2002) Membrane stabilization by abscisic acid under cold aids proline in alleviating chilling injury in maize (Zea mays L.) cultured cells. Plant Cell Environ 25:955–962

    Article  CAS  Google Scholar 

  • Dimkpa C, Weinand T, Asch F (2009) Plant–rhizobacteria interactions alleviate abiotic stress conditions. Plant Cell Environ 32:1682–1694

    Article  PubMed  CAS  Google Scholar 

  • Ding S, Huang CL, Sheng HM, Song CL, Li YB, An LZ (2011) Effect of inoculation with the endophyte Clavibacter sp. strain Enf12 on chilling tolerance in Chorispora bungeana. Physiol Plant 141:141–151

    Article  PubMed  CAS  Google Scholar 

  • Dobrá J, Vanková R, Havlová M, Burman AJ, Libus J, Storchová H (2011) Tobacco leaves and roots differ in the expression of proline metabolism-related genes in the course of drought stress and subsequent recovery. J Plant Physiol 168:1588–1597

    Article  PubMed  CAS  Google Scholar 

  • Fernandez O, Theocharis A, Bordiec S, Feil R, Jacquens L, Clément C, Fontaine F, Ait Barka E (2012a) Burkholderia phytofirmans PsJN acclimates grapevine to cold by modulating carbohydrate metabolism. Mol Plant Microbe Interact 25:496–504

    Article  PubMed  CAS  Google Scholar 

  • Fernandez O, Vandesteene L, Feil R, Baillieul F, Lunn JE, Clément C (2012b) Trehalose metabolism is activated upon chilling in grapevine and might participate in Burkholderia phytofirmans induced chilling tolerance. Planta 236:355–369

    Article  PubMed  CAS  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930

    Article  PubMed  CAS  Google Scholar 

  • Gilmour SJ, Sebolt AM, Salazar MP, Everard JD, Thomashow MF (2000) Overexpression of the Arabidopsis CBF3 transcriptional activator mimics multiple biochemical changes associated with cold acclimation. Plant Physiol 124:1854–1865

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Guo JH, Xue QY, Liu HX (2009) ‘Shu Dekang’ as a brand name. Trademark Office of The State Administration for Industry & Commerce of the People’s Republic of China. Patent application number 7823197

  • Harare ZS (2012) Black frost destroys citrus, horticulture. http://www.thezimbabwean.co/business/agriculture/50828/black-frost-destroys-citrus-horticulture.html. Accessed 11 Mar 2015

  • Islama F, Yasmeen T, Ali Q, Ali S, Arif MS, Hussain S, Rizvi H (2014) Influence of Pseudomonas aeruginosa as PGPR on oxidative stress tolerance in wheat under Zn stress. Ecotoxicol Environ Saf 104:285–293

    Article  CAS  Google Scholar 

  • Jaglo KR, Kleff S, Amundsen KL, Zhang X, Haake V, Zhang JZ, Deits T, Thomashow MF (2001) Components of the Arabidopsis C-repeat/dehydration-responsive element binding factor cold-response pathway are conserved in Brassica napus and other plant species. Plant Physiol 127:910–917

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Janská A, Maršík P, Zelenková S, Ovesná J (2010) Cold stress and acclimation-what is important for metabolic adjustment? Plant Biol 12:395–405

    Article  PubMed  CAS  Google Scholar 

  • Knight MR, Knight H (2012) Low-temperature perception leading to gene expression and cold tolerance in higher plants. New Phytol 195:737–751

    Article  PubMed  CAS  Google Scholar 

  • Krasensky J, Jonak C (2012) Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. J Exp Bot 63:1593–1608

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Li F, Wu QY, Sun YL, Wang LY, Yang XH, Meng QW (2010) Overexpression of chloroplastic monodehydroascorbate reductase enhanced tolerance to temperature and methyl viologen-mediated oxidative stresses. Physiol Plant 139:421–434

    PubMed  CAS  Google Scholar 

  • Liu H, Ouyang B, Zhang J, Wang T, Li H, Zhang Y, Yu C, Ye Z (2012) Differential modulation of photosynthesis, signaling, and transcriptional regulation between tolerant and sensitive tomato genotypes under cold stress. PLoS One 7:e50785

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Lucas JA, García-Cristobal J, Bonilla A, Ramos B, Gutierrez-Manero J (2014) Beneficial rhizobacteria from rice rhizosphere confers high protection against biotic and abiotic stress inducing systemic resistance in rice seedlings. Plant Physiol Biochem 82:44–53

    Article  PubMed  CAS  Google Scholar 

  • BBC News (2011) Cold snap hits Mexico maize crop. http://www.bbc.co.uk/news/world-latin-america-12437862. Accessed 11 Mar 2015

  • Niu DD, Liu HX, Jiang CH, Wang YP, Wang QY, Jin HL, Guo JH (2011) The plant growth-promoting rhizobacterium Bacillus cereus AR156 induces systemic resistance in Arabidopsis thaliana by simultaneously activating salicylate- and jasmonate/ethylene-dependent signaling pathways. Mol Plant Microbe Interact 24:533–542

    Article  PubMed  CAS  Google Scholar 

  • Niu DD, Wang CJ, Guo YH, Jiang CH, Zhang WZ, Wang YP, Guo JH (2012) The plant growth-promoting rhizobacterium Bacillus cereus AR156 induces resistance in tomato with induction and priming of defence response. Biocontrol Sci Technol 22:991–1004

    Article  Google Scholar 

  • Patade VY, Khatri D, Kumari M, Grover A, Mohan Gupta S, Ahmed Z (2013) Cold tolerance in transgenic tomato (Solanum lycopersicum L.) is associated with modulation in transcript abundance of stress responsive genes. Springerplus 2:117

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Patton AJ, Cunningham SM, Volenec JJ, Reicher ZJ (2007) Differences in freeze tolerance of zoysiagrasses: II. Carbohydrate and proline accumulation. Crop Sci 47:2170–2181

    Article  CAS  Google Scholar 

  • Pinhero RG, Rao MV, Paliyath G, Murr DP, Fletcher RA (1997) Changes in activities of antioxidant enzymes and their relationship to genetic and paclobutrazol-induced chilling tolerance of maize seedlings. Plant Physiol 114:695–704

    PubMed Central  PubMed  CAS  Google Scholar 

  • Prasad TK, Anderson MD, Stewart CR (1994) Acclimation, hydrogen peroxide, and abscisic acid protect mitochondria against irreversible chilling injury in maize seedlings. Plant Physiol 105:619–627

    PubMed Central  PubMed  CAS  Google Scholar 

  • Ruelland E, Vaultier MN, Zachowski A, Hurry V (2009) Cold signalling and cold acclimation in plants. Adv Bot Res 49:35–150

    Article  CAS  Google Scholar 

  • Sasaki K, Kim MH, Imai R (2007) Arabidopsis COLD SHOCK DOMAIN PROTEIN2 is a RNA chaperone that is regulated by cold and developmental signals. Biochem Biophys Res Commun 364:633–638

    Article  PubMed  CAS  Google Scholar 

  • Shou HX, Bordallo P, Fan JB, Yeakley JM, Bibikova M, Sheen J, Wang K (2004) Expression of an active tobacco mitogen-activated protein kinase kinase kinase enhances freezing tolerance in transgenic maize. Proc Natl Acad Sci USA 101:3298–3303

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Stevens R, Page D, Gouble B, Garchery C, Zamir D, Causse M (2008) Tomato fruit ascorbic acid content is linked with monodehydroascorbate reductase activity and tolerance to chilling stress. Plant Cell Environ 31:1086–1096

    Article  PubMed  CAS  Google Scholar 

  • Stockinger EJ, Gilmour SJ, Thomashow MF (1997) Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proc Natl Acad Sci USA 94:1035–1040

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Su LT, Li JW, Liu DQ, Zhai Y, Zhang HJ, Li XW, Zhang QL, Wang Y, Wang QY (2014) A novel MYB transcription factor, GmMYBJ1, from soybean confers drought and cold tolerance in Arabidopsis thaliana. Gene 538:46–55

    Article  PubMed  CAS  Google Scholar 

  • Theocharis A, Bordiec S, Fernandez O, Paquis S, Dhondt-Cordelier S, Baillieul F, Clément C, Ait Barka E (2012) Burkholderia phytofirmans PsJN primes Vitis vinifera L. and confers a better tolerance to low non-freezing temperatures. Mol Plant Microbe Interact 25:241–249

    Article  PubMed  CAS  Google Scholar 

  • Thomashow MF (2010) Molecular basis of plant cold acclimation: Insights gained from studying the CBF cold response pathway. Plant Physiol 154:571–577

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Venema JH, Linger P, van Heusden AW, van Hasselt PR, Bruggemann W (2005) The inheritance of chilling tolerance in tomato (Lycopersicon spp.). Plant Biol 7:118–130

    Article  PubMed  CAS  Google Scholar 

  • Wang WJ, Chen YZ, Liu MQ, Lu CF (2008) Effects of cold hardening on compatible solutes and antioxidant enzyme activities related to freezing tolerance in Ammopiptanthus mongolicus seedlings. For Stud China 10:101–106

    Article  CAS  Google Scholar 

  • Wang CJ, Yang W, Wang C, Gu C, Niu DD, Liu HX, Wang YP, Guo JH (2012) Induction of drought tolerance in cucumber plants by a consortium of three plant growth-promoting rhizobacterium strains. PLoS One 7:e52565

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Yang J, Kloepper JW, Ryu CM (2009) Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci 14:1–4

    Article  PubMed  CAS  Google Scholar 

  • Zhang X, Fowler SG, Cheng H, Lou Y, Rhee SY, Stockinger EJ, Thomashow MF (2004) Freezing-sensitive tomato has a functional CBF cold response pathway, but a CBF regulon that differs from that of freezing-tolerant Arabidopsis. Plant J 39:905–919

    Article  PubMed  CAS  Google Scholar 

  • Zhang W, Zhuang Z, Zheng L, Wang Y, Guo JH (2010) Effects of biopesticide against root-knot nematodes in bitter melon. China: plant bacteria disease and biocontrol. 365

  • Zheng Y, Liu HX, Guo JH (2011) Effects of biopesticide ‘SHUDEKANG’ against banana wilt. Jiangsu Agri Sci 39(2):199–201

    Google Scholar 

  • Zhuang ZG, Zheng L, Zhang WZ, Li SM, Guo JH (2010) Effects of biopesticide‘SHUDEKANG’ against root-knot nematodes in cucumber under field conditions in Huai’an city. China: plant bacteria disease and biocontrol. 372–377

Download references

Acknowledgments

This work was supported by the National Natural Science Foundation of China (31171809) and the Natural Science Foundation of Jiangsu Province (BK20131319).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jian-Hua Guo.

Electronic Supplementary Material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 15 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, C., Wang, C., Gao, YL. et al. A Consortium of Three Plant Growth-Promoting Rhizobacterium Strains Acclimates Lycopersicon esculentum and Confers a Better Tolerance to Chilling Stress. J Plant Growth Regul 35, 54–64 (2016). https://doi.org/10.1007/s00344-015-9506-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-015-9506-9

Keywords

Navigation