Changes in Root Exudates and Root Proteins in Groundnut–Pseudomonas sp. Interaction Contribute to Root Colonization by Bacteria and Defense Response of the Host
- 3 Downloads
Selection and application of rhizobacteria, for improved plant health will benefit from a complete understanding of the plant–bacteria interaction. Root exudates (REs) are known to contain signal molecules that facilitate beneficial association of plants with microbes. We have selected a tentatively identified Pseudomonas sp. (RP2), from 126 groundnut (Arachis hypogaea L.)-associated bacterial isolates that significantly promoted growth of groundnut and also induced resistance against the stem rot pathogen Sclerotium rolfsii. REs were collected from 12 to 24 days grown RP2-bacterized and non-bacterized plants and analyzed through gas chromatography coupled with mass spectrometer. Several organic acids, fatty acids, sugars, hydrocarbons, and alcohols were detected. In the untargeted multivariate analysis of the REs, relative content of eight compounds varied significantly on RP2 bacterization. Among these eight compounds, myristic acid, stearic acid, and palmitic acid, positively influenced the root colonization by RP2. Benzoic acid and salicylic acid, increased in RP2-bacterized REs, showed the highest growth inhibition of S. rolfsii. In root proteomics, 11 differentially expressed proteins were identified by 2D-gel electrophoresis followed by matrix-assisted laser desorption ionization-time of flight. Chitinase, thaumatin-like protein, ascorbate peroxidase, and glutathione S-transferase, known to have a role in plant defense against phytopathogens, were upregulated in RP2 interaction. Similarly, upregulation of enolase in roots is likely to improve plant growth in RP2-bacterized groundnut. We conclude that colonization of groundnut roots by RP2 resulted in exudation of metabolites that facilitated root colonization, suppressed fungal growth, promoted plant growth, and also increased the expression of defense-related proteins in the roots.
KeywordsGroundnut Pseudomonas sp. PGPR Root exudates Root proteins Antifungal
We thank Department of Biotechnology (DBT), Government of India (GoI) for financial support under project No: BT/PR4175/AGR/21/350/2011 dated 01.03.2012. SA thanks Council of Scientific and Industrial Research, GoI for Senior research fellowship. TSR acknowledges financial support from Dr. D. S. Kothari postdoctoral fellowship scheme (BSR/BL/16-17/0344). We also thank the Department of Science and Technology (DST), GoI, Funds for Infrastructure in Science and Technology, Level II support (DST-FIST level II), and Special Assistance Programme-UGC (SAP-UGC) to the Department of Plant Sciences, School of Life Sciences. The authors are grateful to Groundnut division, International Crops Research Institute for the Semi-Arid Tropics, Hyderabad, for providing Arachis hypogaea L. seeds and Dr. Vincent Vadez, Principal Scientist, Division of Crop Physiology, ICRISAT, Hyderabad, for allowing the use of WinRHIZO Pro 5.0 root analyzer facility.
ARP designed the experiment. SA isolated and screened groundnut PGPR, and analyzed REs by GC-MS. TSR carried out root proteomics using 2DE. ARP, SA, and TSR analyzed the data and wrote the manuscript.
Compliance with Ethical Standards
Conflict of interest
The authors declare no conflict of interest.
- Dutta S, Rani TS, Podile AR (2013) Root exudate-induced alterations in Bacillus cereus cell wall contribute to root colonization and plant growth promotion. PLoS ONE 8:1–12Google Scholar
- Garcia-Cristobal J, Garcia-Villaraco A, Ramos B, Gutierrez-Manero J, Lucas JA (2015) Priming of pathogenesis related-proteins and enzymes related to oxidative stress by plant growth promoting rhizobacteria on rice plants upon abiotic and biotic stress challenge. J Plant Physiol 188:72–79CrossRefGoogle Scholar
- George E, Kumar SN, Jacob J, Bommasani B, Lankalapalli RS, Morang P, Kumar BSD (2015) Characterization of the bioactive metabolites from a plant growth-promoting rhizobacteria and their exploitation as antimicrobial and plant growth-promoting agents. Appl Biochem Biotechnol 176:529–546CrossRefGoogle Scholar
- Gómez-Lama Cabanás C, Legarda G, Ruano-Rosa D, Pizarro-Tobías P, Valverde-Corredor A, Niqui JL, Triviño JC, Roca A, Mercado-Blanco J (2018) Indigenous Pseudomonas spp. strains from the olive (Olea europaea L.) rhizosphere as effective biocontrol agents against Verticillium dahliae: from the host roots to the bacterial genomes. Front Microbiol 277:1–19Google Scholar
- Gupta G, Parihar SS, Ahirwar NK, Snehi SK, Singh V (2015) Plant Growth Promoting Rhizobacteria (PGPR): current and future prospects for development of sustainable agriculture. J Microb Biochem Technol 7:96–102Google Scholar
- Han HS, Lee KD (2005a) Plant growth promoting rhizobacteria effect on antioxidant status, photosynthesis, mineral uptake and growth of lettuce under soil salinity. Res J Agri Biol Sci 1:210–215Google Scholar
- Han HS, Lee KD (2005b) Physiological responses of soybean-inoculation of Bradyrhizobium japonicum with PGPR in saline soil conditions. Res J Agri Biol Sci 1:216–221Google Scholar
- Kandasamy S, Loganathan K, Muthuraj R, Duraisamy S, Seetharaman S, Thiruvengadam R, Ponnusamy B, Ramasamy S (2009) Understanding the molecular basis of plant growth promotional effect of Pseudomonas fluorescens on rice through protein profiling. Proteome Sci 8:1–8Google Scholar
- Maina S, Emongor Q, Sharma K (2010) Surface sterilant effect on the regeneration efficiency from cotyledon explants of groundnut (Arachis hypogea L.) varieties adapted to eastern and Southern Africa. Afr J Biotechnol 9:2866–2871Google Scholar
- Mostafa H, Amir G (2012) Effects of water stress and inoculation with plant growth promoting rhizobacteria (PGPR) on antioxidant status and photosynthetic pigments in basil (Ocimum basilicum L.). J Saudi Society of Agri Sci 98:57–61Google Scholar
- Neumann G, Bott S, Ohler MA, Mock HP, Lippmann R, Grosch R, Smalla K (2014) Root exudation and root development of lettuce (Lactuca sativa L. cv. Tizian) as affected by different soils. Trends Plant Sci 5:1–6Google Scholar
- Pérez-Flores P, Valencia-Cantero E, Altamirano-Hernández J, Pelagio-Flores R, López-Bucio J, García-Juárez P, Macías-Rodríguez L (2017) Bacillus methylotrophicus M4-96 isolated from maize (Zea mays) rhizoplane increases growth and auxin content in Arabidopsis thaliana via emission of volatiles. Protoplasma 254:2201–2213CrossRefGoogle Scholar
- Podile AR, Kishore GK (2002) Biological control of peanut diseases. In: Gnanamanickam SS (ed) Biological control of crop diseases, CRC Press, New York, pp 131–160Google Scholar
- Sanchez L, Weidmann S, Brechenmacher L, Batoux M, Tuinen DV, Lemanceau P, Gianinazzi S, Gianinazzi-Pearson V (2004) Common gene expression in Medicago truncatula roots in response to Pseudomonas fluorescens colonization, mycorrhiza development and nodulation. New Phytol 161:855–863CrossRefGoogle Scholar
- Sayyed RZ, Gangurde NS, Patel PR, Joshi SA, Chincholkar SB (2010) Siderophore production by Alcaligenes faecalis and its application for growth promotion in Arachis hypogaea. Indian J Biotechnol 9:302–307Google Scholar
- Sherathia D, Dey R, Thomas M, Dalsania T, Savsani K, Pal KK (2016) Biochemical and molecular characterization of DAPG-producing plant growth promoting rhizobacteria (PGPR) of groundnut (Arachis hypogaea L.). Legume Res 39:614–622Google Scholar
- Sujitha A, Bhaskara Reddy BV, Sivaprasad Y, Prathyusha M, Murali Krishna T, Vijay Krishna Kumar K, Raja Reddy K (2013) Characterisation, genetic diversity and antagonistic potential of 2,4-diacetylphloroglucinol producing Pseudomonas fluorescens isolates in groundnut-based cropping systems of Andhra Pradesh, India. Arch Phytopathology Plant Protect 46:1966–1977CrossRefGoogle Scholar
- Yeole RD, Dube HC (2000) Siderophore-mediated antibiosis of rhizobacterial fluorescent Pseudomonads against certain soil-borne fungal plant pathogens. J Mycol Plant Pathol 30:335–338Google Scholar
- Yuan J, Zhang N, Huang Q, Raza W, Li R, Vivanco JM (2015) Organic acids from root exudates of banana help root colonization of PGPR strain Bacillus amyloliquefaciens NJN-6. Sci Rep 5:1–8Google Scholar