Abstract
Microbial volatile organic compounds (mVOCs) play important roles in inter- and intra-kingdom interactions, and they are also important as signal molecules in physiological processes acting either as plant growth-promoting or negatively modulating plant development. We investigated the effects of mVOCs emitted by PGPR vs non-PGPR from avocado trees (Persea americana) on growth of Arabidopsis thaliana seedlings. Chemical diversity of mVOCs was determined by SPME–GC–MS; selected compounds were screened in dose–response experiments in A. thaliana transgenic lines. We found that plant growth parameters were affected depending on inoculum concentration. Twenty-six compounds were identified in PGPR and non-PGPR with eight of them not previously reported. The VOCs signatures were differential between those groups. 4-methyl-2-pentanone, 1-nonanol, 2-phenyl-2-propanol and ethyl isovalerate modified primary root architecture influencing the expression of auxin- and JA-responsive genes, and cell division. Lateral root formation was regulated by 4-methyl-2-pentanone, 3-methyl-1-butanol, 1-nonanol and ethyl isovalerate suggesting a participation via JA signalling. Our study revealed the differential emission of volatiles by PGPR vs non-PGPR from avocado trees and provides a general view about the mechanisms by which those volatiles influence plant growth and development. Rhizobacteria strains and mVOCs here reported are promising for improvement the growth and productivity of avocado crop.
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Acknowledgements
We thank the Consejo Nacional de Ciencia y Tecnología (CONACYT) for the grants no. PDCPN-2015-882, FORDECyT-PRONACES 292399 and the Asociación de Productores y Empacadores Exportadores de Aguacate de México A.C. (APEAM) for the grant no. 42002. R.G.B thanks APEAM for his postdoctoral fellowship. We thank M. Sc. Diana Yuridia López Ley and M. Sc. Nut Liahut Guin for their technical support in volatiles dose-dependent experiments, providing and maintaining of bacteria strains, and isolation of DNA and amplification of 16S rRNA gene.
Funding
This work was financed by grants from the Asociación de Productores y Empacadores Exportadores de Aguacate de México A.C. (APEAM)-Instituto de Ecología A.C. (INECOL) (grant no. 42002); Consejo Nacional de Ciencia y Tecnología (CONACYT, México, grants PDCPN-2015–882 and FORDECYT-PRONACES 292399).
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R.G.B., D.D. and R.O.C. conceived and designed the experiments; R.G.B. performed experiments; R.G.B. and R.O.C. analyzed the data; G.C. and R.O.C. contributed reagents/materials/analysis tools; R.G.B. and R.O.C. wrote the paper; R.G.B, D.D., R.O.C. and G.C. reviewed and edited the paper. G.C. and R.O.C. applied for funding. J.M.T., E.R.C. and A.L.K.M. provided reagents, material and technical support for GC–MS analysis.
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Fig. S1
Representative images of shoot and root growth of Arabidopsis seedlings in response to avocado rhizobacteria volatiles exposure. Seven-day-old A. thaliana seedlings were co-inoculated with 20 µL of liquid culture of (a) PGPR and (b) non-PGPR strains, containing either 1x104, 1x106 and 1x108 total CFU, or 20 µL of LB medium (0 µM). All assays were performed in triplicates. At least 10 transgenic seedlings were analyzed with a Leica S8 APO stereoscopic microscope. Shoot and root system images were captured with a Sony Cyber-shot DSC-S75 digital camera adapted to the microscope. Scale bar = 500 µm. (PNG 24658 KB)
Fig. S2
Typical total ion chromatograms (TICs) of VOCs detected in the headscape of Petri dishes from PGPR and non-PGPR strains from avocado rhizosphere. Eight sterilized sedes of A. thaliana were germinated and grown in one half of the plate. After seven days, A. thaliana seedlings were co-inoculated in the second compartment with 20 μL of the selected bacterial strains. All assays were performed in triplicates. Seven days after inoculation, SPME fibers were introduced and kept for 2 hours into the headspace of Petri plates. The captured volatiles were analyzed by GC-MS, which was performed independently for A. thaliana-bacteria co-culture, and for plant and bacteria grown alone, and for culture media. (PNG 4688 KB)
Fig. S3
Fig. S3 Effect of selected pure VOCs on Arabidopsis biomass parameters. Six compounds were selected for growth promotion assays: 2-phenyl-2-propanol, ethyl isovalerate, 1-nonanol, 3-octanone, 3-methyl-1-butanol and 4-methyl-2-pentanone. The pure VOCs were screened at three different concentrations: 25, 50 and 100 µM. In vitro plant growth-promotion assays were performed by using seven-days-old A. thaliana seedlings, which were exposed to 25 µL of each different dilution of the standard compounds (dissolved in water), and 25 µL of only water as negative control applied to a sterile filter paper (diameter of 1.85 cm) in the other side of the two-compartment plate. The experiments were performed in triplicate. After seven days of individual mVOC exposition, (a) shoot fresh weight and (b) root fresh weight were measured. Data points represent mean of eight seedlings (three replicates) ± SD (n=24). Dashed red line indicates control average. Different letters indicate statistical difference at P<0.05. (PNG 914 KB)
Fig. S4
Representative images of shoot and root growth of Arabidopsis seedlings in response to pure VOCs treatment. Seven days-old A. thaliana seedlings were exposed to three different concentrations (25, 50 and 100 µM) of the six pure compounds selected: a) 4-Methyl-2-pentanone, b) 3-Methyl-1-butanol, c) 3-Octanone, d) 1-Nonanol, e) 2-Phenyl-2-propanol, f) Ethyl isovalerate. All assays were performed in triplicates. After seven days of mVOCs exposition, at least 10 transgenic seedlings were analyzed with a stereoscopic microscope. Shoot and root system images were captured with a digital camera adapted to the microscope. Scale bar = 500 µm. (PNG 21797 KB)
Fig. S5
GUS activity detected in shoot and lateral roots of DR5::uidA and PRZ1::uidAPRZ1::uidA transgenic lines in a dose-response volatile assays. Expression of (a) DR5::uidA and (b) PRZ1::uidA gene constructs was evaluated in response to exposure of transgenic lines at three different concentrations (25, 50 and 100 µM) of each of the six pure compounds (2-phenyl-2-propanol, ethyl isovalerate, 1-nonanol, 3-octanone, 3-methyl-1-butanol and 4-methyl-2-pentanone) selected for this experiment. The experiments were performed by triplicate. After seven days of individual mVOC exposition, A. thaliana seedlings expressing the uidA reporter gene were incubated at 37 °C in GUS reaction buffer (0.5 mg/mL of 5-bromo-4-chloro-3-indolyl-β-D-glucuronide in 100 mM sodium phosphate, pH 7) overnight. The stained seedlings were cleared and photographed. Photographs are representative of at least eighteen stained seedlings. Scale bar = 500 µm. (PNG 10493 KB)
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Gamboa-Becerra, R., Desgarennes, D., Molina-Torres, J. et al. Plant growth-promoting and non-promoting rhizobacteria from avocado trees differentially emit volatiles that influence growth of Arabidopsis thaliana. Protoplasma 259, 835–854 (2022). https://doi.org/10.1007/s00709-021-01705-2
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DOI: https://doi.org/10.1007/s00709-021-01705-2