Pre-colonization of PGPR triggers rhizosphere microbiota succession associated with crop yield enhancement
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Plant growth-promoting rhizobacteria (PGPR) substantially improve plant growth and health, but their effects on the succession of rhizosphere microbiota throughout the growth period triggered by pre-inoculation have not yet been considered.
Pepper seedlings cultured from a bio-nursery substrate containing Bacillus velezensis NJAU-Z9 and ordinary nursery substrate were used in this study to evaluate the effects of pre-colonization of a PGPR strain at the seedling stage on yield enhancement. To elucidate the underlying mechanisms involved in the rhizosphere microbiota succession during the whole growth period and their association with yield enhancement, high-throughput sequencing combined with qPCR was conducted.
The results showed that, compared to the control without inoculation, pre-inoculation led to a steady yield enhancement in two-season field trials, as well as higher rhizosphere bacterial richness (Chao1) and diversity (Shannon-Wiener). The plant growth stage as the first driving factor, followed by pre-colonization drove the variations of the rhizosphere microbial community composition according to multivariate regression tree analysis and principal coordinate analysis. Variance partitioning analysis (VPA) and Mantel test results showed that the previous plant growth period induced variations in the fungal and bacterial communities at the next stage. Compared to the seedling and flowering stages, the mature-stage microbial community showed a higher degree of explanation of yield enhancement. Additionally, pre-inoculation led to distinctive rhizosphere microbiota succession compared to the control, due to alteration of the initial community. The heat map analysis showed that the rhizosphere microbiota was related to crop yield. In addition to Bacillus velezensis NJAU-Z9, which showed stable abundance in the pepper rhizosphere, stable higher relative abundance of the bacterial genera Sphingomonas, Sphingopyxis, Bradyrhizobium, Chitinophaga, Dyadobacter, Streptomyces, Lysobacter, Pseudomonas and Rhizomicrobium, and the fungal genera Cladorrhinum, Cladosporium and Aspergillus throughout the growth period induced by pre-colonization was associated with yield enhancement.
Overall, we conclude that pre-colonization with PGPR changed the initial rhizosphere microbiota and that the plant was triggered to further select distinctive microbes to form unique rhizosphere microbial consortia at the later growth stages, which resulted in plant growth promotion.
KeywordsSweet pepper Plant growth-promoting rhizobacteria (PGPR) Pre-colonization Crop yield enhancement Rhizosphere microbiota
This research was supported by the National Key Basic Research Program of China (2015CB150506), the Fundamental Research Funds for the Central Universities (KYZ201871 and KJQN201746), the Priority Academic Program Development of the Jiangsu Higher Education Institutions (PAPD), the 111 project (B12009), the Top-notch Academic Programs Project of the Jiangsu Higher Education Institution (PPZY2015A061), the Innovative Research Team Development Plan of the Ministry of Education of China (IRT_17R56), and the China Scholarship Council (award to Rong Li for 1 year’s abroad study).
- Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B Methodol 57:289–300Google Scholar
- Chaney RL, Munns JB, Cathey HM (1980) Effectiveness of digested sewage sludge compost in supplying nutrients for soilless potting media. J Am Soc Hortic Sci 105:485–492Google Scholar
- De'Ath G (2002) Multivariate regression trees: a new technique for modeling species–environment relationships. Ecology 83:1105–1117Google Scholar
- Duineveld BM, Kowalchuk GA, Keijzer A, Elsas JDV, Veen JAV (2001) Analysis of bacterial communities in the rhizosphere of chrysanthemum via denaturing gradient gel electrophoresis of PCR-amplified 16S rRNA as well as DNA fragments coding for 16S rRNA. Appl Environ Microbiol 67:172–178CrossRefGoogle Scholar
- Gopalakrishnan S, Srinivas V, Alekhya G, Prakash B (2015) Effect of plant growth-promoting Streptomyces sp. on growth promotion and grain yield in chickpea (Cicer arietinum L). Biotech 5:799–806Google Scholar
- Lasudee K, Tokuyama S, Lumyong S, Pathom-Aree W (2016) Mycorrhizal spores associated Lysobacter soli and its plant growth promoting activity. Chiang Mai J Sci 44:94–101Google Scholar
- Liu H, Chen D, Zhang R, Hang X, Li R, Shen Q (2016) Amino acids hydrolyzed from animal carcasses are a good additive for the production of bio-organic fertilizer. Front Microbiol 7:1290Google Scholar
- Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2013) Vegan: Community Ecology Package. URL http://CRAN.R-project.org/package=vegan, R package version 2.0-10. Accessed 2 Sept 2014
- Pan S, Liu C, Huang F, Yalan LI, Tang H, Yang T (2016) Influence of root exudates on efficiency of rhizosphere microbial degradation under PAHs stress. Journal of Chengdu University 35:86–89Google Scholar
- Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406Google Scholar
- Shcherbakova EN, Shcherbakov AV, Andronov EE, Gonchar LN, Kalenskaya SM, Chebotar VK (2017) Combined pre-seed treatment with microbial inoculants and Mo nanoparticles changes composition of root exudates and rhizosphere microbiome structure of chickpea (Cicer arietinum L.) plants. Symbiosis 73:57–69CrossRefGoogle Scholar
- Shen Z, Penton CR, Lv N, Xue C, Yuan X, Ruan Y, Li R, Shen Q (2017) Banana fusarium wilt disease incidence is influenced by shifts of soil microbial communities under different monoculture spans. Microb Ecol 75:1–12Google Scholar
- Smalla K, Wieland G, Buchner A, Zock A, Parzy J, Kaiser S, Roskot N, Heuer H, Berg G (2001) Bulk and rhizosphere soil bacterial communities studied by denaturing gradient gel electrophoresis: plant-dependent enrichment and seasonal shifts revealed. Appl Environ Microbiol 67:4742–4751CrossRefGoogle Scholar
- Thiery BCA, Sharif B, Dossou GF, Helmut B (2015) Cotton fertilization using PGPR Bacillus amyloliquefaciens FZB42 and compost: impact on insect density and cotton yield in North Benin, West Africa. Cogent Food Agric 1(1). https://doi.org/10.1080/23311932.2015.1063829
- Toju H, Peay KG, Yamamichi M, Narisawa K, Hiruma K, Naito K, Fukuda S, Ushio M, Nakaoka S, Onoda Y, Yoshida K, Schlaeppi K, Bai Y, Sugiura R, Ichihashi Y, Minamisawa K, Kiers ET (2018) Core microbiomes for sustainable agroecosystems. Nature Plants 4:247–257Google Scholar
- Weller DM (1984) Distribution of a take-all suppressive strain of Pseudomonas fluorescens on seminal roots of winter wheat. Appl Environ Microbiol 48:897–899Google Scholar
- White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR protocols: a guide to methods and applications 18:315–322Google Scholar
- Zhang Y, Wen CY, Zhao MQ, Zhang M, Gao Q, Li R, Shen QR (2015) Isolation of plant growth promoting rhizobacteria from pepper and development of bio-nursery substrates. J Nanjing Agric Univ 6:950–957Google Scholar