Use of plant growth promoting bacteria as an efficient biotechnological tool to enhance the biomass and secondary metabolites production of the industrial crop Pelargonium graveolens L'Hér. under semi-controlled conditions
Introduction
Plant secondary metabolites are a useful array of natural products including essential oils, phenolic acids, flavonoids, alkaloids, tannins among others with increasing industrial interest as pharmaceuticals, bio-agrochemicals, flavouring agents and food additives (Gonçalves and Romano, 2018; Thakur et al., 2019). The accumulation levels of secondary metabolites in plants are generally very low, less than 1 % of dry weight with significant fluctuations depending on endogenous and exogenous factors (Riahi et al., 2013; Thakur et al., 2019). Thus, the industrial exploitation requires high plant biomass yields for the extraction of these high-value bioactive molecules (dos Santos Marques et al., 2018). Consequently, finding efficient practical strategies to increase the contents of high-value secondary metabolites and modulate their composition in addition to plant biomass improvement is required and poses a continuous challenge for researchers worldwide (Yang et al., 2018; Riahi et al., 2019a).
The plant biomass and secondary metabolites components present the main target traits for improvement and selection in aromatic and medicinal crops (Sarrou et al., 2017). The use of non conventional biotechnological tools based on genetic engineering methods or the abundant application of chemical fertilizers and pesticides to ameliorate the plant biomass yields and the production of bioactive molecules of interest is often confronted with ethical issues and oppositions by the consumers given their potential negative impact on human health and on environment (Hussain et al., 2012).
The excessive use of chemical fertilizers to improve the yields and quality of plant species is becoming a serious threat to natural ecosystems and present high negative environmental impact (Wang et al., 2018). The long time applications of chemical fertilizers deteriorate the pH, nutritional status, microbial community and increased heavy metals reactivity in soils (Ning et al., 2017; Lin et al., 2019). Furthermore, the chemical fertilization causes continuous degradation of water resources and have negative incidence on human and animal health (Farhadinejad et al., 2014; Prashar and Shah, 2016).
Innovative biotechnology approaches such as the application of beneficial associations between plants and bacteria called plant growth promoting bacteria were recently proposed as sustainable and environmentally respectful methods which avoids or minimize the use of synthetic fertilizers and pesticides and rely on bio-fertilization (Ibort et al., 2018; Tennakoon et al., 2019). These PGP bacteria have been shown able to increase nutrient uptake, promote plant growth and protection against soil-borne pathogens which present effective and promising alternative biotechnological tools (Pagnani et al., 2018). The use of plant growth promoting bacteria as bio-elicitors to improve crop yields is recognized as a clean and efficient strategy in both in vitro and in vivo plant systems through various mechanisms under normal as well as adverse conditions (Thakur et al., 2019). The application of this strategy to major agronomic species was widely elucidated (Ambreetha et al., 2018; Rozier et al., 2019). However, investigations interested in aromatic and medicinal plants and targeting the impact of these bacteria on the production of secondary metabolites is still limited and is recently in progress (Cappellari et al., 2019).
Pelargonium graveolens L'Hér. (Geraniaceae), well known as rose-scented geranium is a valuable industrial crop commonly cultivated worldwide for its high-value secondary metabolites used as ingredients in high grade perfumery, pharmaceutical and cosmetic industries with increasing demand in the international markets (Shawl et al., 2006). Previous scientific reports interested in rose-scented geranium essential oils and organic extracts showed antioxidant (Cavar and Maksimovic, 2012), anti-inflammatory (Ghanizadeh et al., 2015), antimicrobial (Ben Hsouna and Hamdi, 2012), hypoglycemic (Boukhris et al., 2012), DNA damage protective effects (Boukhris et al., 2015) and therapeutic potential in metabolic diseases (Neagu et al., 2018).
In Tunisia, rose-scented geranium is propagated mainly by stem cuttings and is growing under different bioclimatic stages with both rainfall and irrigated systems. In addition to its ornamental use, this species is used in Tunisian perfume industry and to produce flavouring flower-water used in traditional pastries, as antispasmodic agent and to treat hyperglycemia, headaches and angina (Ghrabi-Gammar et al., 2009; Boukhris et al., 2012, 2015).
Based on the previous considerations, the main aim of the present study is to evaluate the plant growth promoting potentials of three bacterial strains namely Pseudomonas rhizophila S211, Halomonas desertis G11 and Oceanobacillus iheyensis E9 in single, dual and consortium inoculation modalities on transplants of Pelargonium graveolens L'Hér. under semi-controlled conditions. The effects of the inoculations were assessed based on various quantitative growth parameters, the photosynthetic pigments contents and their abilities to enhance the production of industrially valuable essential oils and phenolic secondary metabolites.
Section snippets
Bacterial strains and plant material
Three bacterial strains (Pseudomonas rhizophila S211 (S1), Halomonas desertis G11 (S2) and Oceanobacillus iheyensis E9 (S3)) provided by the Laboratory of Biotechnology and Bio-Geo Resources Valorisation LR11ES31 at the Higher Institute of Biotechnology of Sidi Thabet in Tunisia were used in this investigation as bio-elicitors to improve the biomass and secondary metabolites production for the studied plant species. The three selected bacterial strains were isolated, identified and
Effect of bacterial inoculation on the plant growth parameters
After three months of cultivation under greenhouse conditions, the obtained results showed that the applied PGPBs have the capacity to enhance P. graveolens growth. The transplants subjected to single, dual or consortium inoculations exhibited a remarkable visual modification of their roots and aerial parts compared with the non inoculated plants (Fig. 1). Except for the inoculation [P. rhizophila S211 + O. iheyensis E9], the plant height values of the treated plants increased significantly as
Conclusion
Based on this investigation, the inoculation of P. graveolens transplants with three plant growth promoting bacteria with single and mixture modalities under semi-controlled conditions resulted in significant positive effects on the growth related parameters and enhanced the production of phenolic, flavonoid and essential oil metabolites over the control. Significant variations in plant responses depending both on the studied parameter and the used inoculum were observed. The inoculation with
CRediT authorship contribution statement
Leila Riahi: Investigation, Methodology, Formal analysis, Writing - original draft, Writing - review & editing. Hanene Cherif: Investigation, Methodology, Resources, Writing - review & editing. Sahar Miladi: Investigation, Writing - review & editing. Mohamed Neifar: Methodology, Resources, Writing - review & editing. Bilel Bejaoui: Resources, Writing - review & editing. Habib Chouchane: Resources, Writing - review & editing. Ahmed Slaheddine Masmoudi: Resources, Writing - review & editing.
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgments
The authors acknowledge financial support from the Tunisian Ministry of Higher Education and Scientific Research in the ambit of the laboratory project LR11ES31 and the PhosAgro/UNESCO/IUPAC partnership in the ambit of the Green Chemistry for Life project “Development of biofertilizers for a sustainable agriculture in Tunisia”. The authors are also grateful to Dr. Wafa Hassen and Dr. Darine El-Hidri for supplying plant growth promoting bacterial strains.
References (65)
- et al.
PGPR-induced OsASR6 improves plant growth and yield by altering root auxin sensitivity and the xylem structure in transgenic Arabidopsis thaliana
J. Plant Physiol.
(2019) - et al.
Plant-associated Bacillus modulates the expression of auxin-responsive genes of rice and modifies the root architecture
Rhizosphere
(2018) - et al.
Plant growth promoting rhizobacteria (PGPR) confer drought resistance and stimulate biosynthesis of secondary metabolites in pennyroyal (Mentha pulegium L.) under water shortage condition
Sci. Hortic.
(2020) - et al.
Bioprospecting glacial ice for plant growth promoting bacteria
Microbiol. Res.
(2015) - et al.
Chemical composition, biological activities and DNA damage protective effect of Pelargonium graveolens L’Hér. essential oils at different phenological stages
Ind. Crops Prod.
(2015) - et al.
Changes in soil microbial activity, essential oil quantity, and quality of Thai basil as response to biofertilizers and humic acid
J. Clean. Prod.
(2020) - et al.
Inducing phenolic production and volatile organic compounds emission by inoculating Mentha piperita with plant growth-promoting rhizobacteria
Sci. Hortic.
(2017) - et al.
Induction of essential oil production in Mentha x piperita by plant growth promoting bacteria was correlated with an increase in jasmonate and salicylate levels and a higher density of glandular trichomes
Plant Physiol. Biochem.
(2019) - et al.
Colonization and beneficial effects on annual ryegrass by mixed inoculation with plant growth promoting bacteria
Microbiol. Res.
(2017) - et al.
Antioxidant activity of essential oil and aqueous extract of Pelargonium graveolens L’Her
Food Control
(2012)
Plant growth promoting rhizobacteria improve the antioxidant status in Mentha piperita grown under drought stress leading to an enhancement of plant growth and total phenolic content
Ind. Crops Prod.
Proteomics provides insights into biological pathways altered by plant growth promoting bacteria and arbuscular mycorrhiza in sorghum grown in marginal soil
Biochim. Biophys. Acta
Antioxidant activity of some Algerian medicinal plants extracts containing phenolic compounds
Food Chem.
Improvement of biomass and essential oil production of Lippia alba (Mill) N.E. Brown with green manures in sccession
Ind. Crops Prod.
The anti-inflammatory effect of Pelargonium graveolens methanolic extract in acetic acid-induced ulcerative colitis in Rat model
Clin. Ther.
Screening of essential oils from wild-growing plants in Tunisia for their yield and toxicity to the poultry red mite, Dermanyssus gallinae
Ind. Crops Prod.
Current approaches toward production of secondary plant metabolites
J. Pharm. Bioallied Sci.
Proteomic analysis reveals that tomato interaction with plant growth promoting bacteria is highly determined by ethylene perception
J. Plant Physiol.
Effects of plant growth-promoting bacteria isolated from copper tailings on plants in sterilized and non-sterilized tailings
Chemosphere
Optimization of harvest regime and post-harvest handling in geranium production to maximize essential oil yield in Rwanda
Ind. Crops Prod.
Genome analysis provides insights into crude oil degradation and biosurfactant production by extremely halotolerant Halomonas desertis G11 isolated from Chott El-Djerid salt-lake in Tunisian desert
Genomics
Impacts of chemical fertilizer reduction and organic amendments supplementation on soil nutrient, enzyme activity and heavy metal content
J. Integr. Agric.
Plant growth-promoting rhizobacteria (PGPR) in Cannabis sativa ‘Finola’ cultivation: an alternative fertilization strategy to improve plant growth and quality characteristics
Ind. Crops Prod.
Characterization of culturable bacteria isolated from hot springs for plant growth promoting traits and effect on tomato (Lycopersicon esculentum) seedling
C. R. Biologies
Phytochemistry, antioxidant and antimicrobial activities of the essential oils of Mentha rotundifolia L. in Tunisia
Ind. Crops Prod.
Genetic resources of Tunisian Artemisia arborescens L. (Asteraceae), pattern of volatile metabolites concentration and bioactivity and implication for conservation
Biochem. Syst. Ecol.
Biopriming of maize germination by the plant growth-promoting rhizobacterium Azospirillum lipoferum CRT1
J. Plant Physiol.
Evaluating the potential of combined inoculation of Trichoderma harzianum and Brevibacterium halotolerans for increased growth and oil yield in Mentha arvensis under greenhouse and field conditions
Ind. Crops Prod.
Rhizobacteria and plant symbiosis in heavy metal uptake and its implications for soil bioremediation
New Biotechnol.
Tea yield maintained in PGPR inoculated field plants despite significant reduction in fertilizer application
Rhizosphere
Improving production of plant secondary metabolites through biotic and abiotic elicitation
J. Appl. Res. Med. Aromat. Plants
What could promote farmers to replace chemical fertilizers with organic fertilizers?
J. Clean. Prod.
Cited by (32)
Azotobacter chroococcum inoculation under low drought stress condition improves Trachyspermum ammi seeds' essential oil bioactivity
2022, Biochemical Systematics and EcologyCitation Excerpt :It has been claimed that ajwain seed oil contains numerous bioactive chemicals, including thymol, o-cymene, isobornyl isobutyrate, myrcene, verbenene, silphine, α -pineene, p-cymene, and thymyl acetate (Lee et al., 2020; Abdullah et al., 2020). It has been reported that the increase in the plant's secondary metabolite production could be possible through the use of drought as well as the application of other environmental stressors (Riahi et al., 2020; Karimi et al., 2019b). Differing levels of drought stress lead to the generation of reactive oxygen species (ROS), which in turn causes enzyme inhibition, peroxidation of lipids, enhancement of the programmed cell death pathway, and damage to nucleic acids (Perillo et al., 2020).
Efficient nutrient management for rose scented geranium (Pelargonium graveolens L′Herit ex Ait)
2022, Journal of Applied Research on Medicinal and Aromatic PlantsCitation Excerpt :Root inoculated bio agents can positively help in nutrient uptake in ivy geranium as observed by Ghaziani and Fakouri (2016). Inoculation of plant growth promoting bacteria (PGPR’s) in rose geranium significantly increased fresh herb yield and secondary metabolite production (Riahi et al., 2020). Results of a previous study indicates that the total fresh herb and essential oil production in geranium significantly influenced by the combined application of organic manures and chemical fertilizers (Verma et al., 2014).
Harnessing intercellular signals to engineer the soil microbiome
2022, Natural Product ReportsFungal endophytes from medicinal plant Bletilla striata (Thunb.) Reichb. F. promote the host plant growth and phenolic accumulation
2021, South African Journal of BotanyCitation Excerpt :However, the accumulation levels of secondary metabolites in medicinal plants are generally low and cannot satisfy the increasing demand of the market (Thakur et al., 2019). The production of natural products requires high biomass yields of medicinal plants for the extraction of these high-value bioactive molecules (Riahi et al., 2020). Endophytic fungi are the fungi that live in healthy plant tissues for part or all of their lives without causing obvious symptoms of infection in host plants (Bamisile et al., 2018; Tymon et al., 2020).
Variability of qualitative and quantitative secondary metabolites traits among wild genetic resources of Lavandula stoechas L.
2021, Biochemical Systematics and EcologyCitation Excerpt :The obtained results corroborate previous reports which highlighted a significant variation of plant phenolic contents and profiling according to geographical origins (Stefanucci et al., 2018). However, the accumulation of phenolic phytochemicals in plant species vary according to various factors including edaphic and growth conditions (Riahi et al., 2020). The essential oil and phenolic components were subjected to principal component analysis (PCA) and hierarchical cluster analysis (HCA).