Abstract
The cultivation of high-quality upland rice, which is known to be drought tolerant and widely adaptable, can help solve the challenges of food and water shortages for the world’s rising populations, so it is of great significance to sustainable agricultural development. Certain microbial agents can further enhance plant drought resistance, such as the endophytic bacteria that live in plant seeds without causing infection, making them a vital resource that can improve upland rice cultivation and yield. In this study, high-throughput sequencing technology based on the Illumina MiSeq platform was used to investigate the structure and diversity of endophytic bacterial communities in the seeds of 12 upland rice varieties from different areas in Yunnan Province, China. The results showed that 39 endophytic operational taxonomic units (OTUs) were found to coexist in all samples. At the phylum level, the dominant phyla in the 12 seed samples were Proteobacteria (66.92–99.98%). At the genus level, Pantoea (9.75–99.24%), Pseudomonas (0.11–37.24%), Curtobacterium (0.01–19.90%), Microbacterium (0.01–14.95%), Methylobacterium (0.40–5.86%), Agrobacterium (0.01–4.53%), Sphingomonas (0.04–1.56%), Aurantimonas (0.01–1.45%) and Rhodococcus (0.11–1.09%) were found to be the dominant genera coexisting in all the tested upland rice seeds tested, representing the core microbiota in upland rice seeds. Furthermore, correlation analysis showed that upland rice habitat environmental factors, such as climate, precipitation and altitude, exert significant effects on the composition and diversity of the endophytic bacterial communities in the upland rice seeds. The findings of this study contribute significantly to understanding the relationship between upland rice and its endophytic bacteria, which can be developed to enhance drought tolerance and yield in this important crop.
Data Availability
All data generated or analyzed during this study are included in this published article and its supplementary information files.
Abbreviations
- OTU:
-
Operational Taxonomic Units
- PCoA:
-
Principal Coordinates Analysis
- RDA:
-
Redundancy Analysis
References
Ansary WR, Prince FRK, Haque E, Sultana F, West HM, Rahman M, Mondol AM, Akanda AM, Rahman M, Clarke ML, Islam T (2018) Endophytic Bacillus spp. from medicinal plants inhibit mycelial growth of Sclerotinia sclerotiorum and promote plant growth. Z Naturforsch c, J Biosci 73:247–256
Cherif-Silini H, Thissera B, Bouket AC, Saadaoui N, Silini A, Eshelli M, Alenezi FN, Vallat A, Luptakova L, Yahiaoui B, Cherrad S, Vacher S, Rateb ME, Belbahri L (2019) Durum wheat stress tolerance induced by endophyte Pantoea agglomerans with genes contributing to plant functions and secondary metabolite arsenal. Int J Mol Sci 20:3989
Chouhan GK, Verma JP, Jaiswal DK, Mukherjee A, Singh S, de Araujo Pereira AP, Liu H, Abd Allah EF, Singh BK (2021) Phytomicrobiome for promoting sustainable agriculture and food security: opportunities, challenges, and solutions. Microbiol Res 248:126763
Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ, Kulam-Syed-Mohideen AS, McGarrell DM, Marsh T, Garrity GM, Tiedje JM (2009) The ribosomal database project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37:D141–D145
Domergue JB, Abadie C, Limami A, Way D, Tcherkez G (2019) Seed quality and carbon primary metabolism. Plant Cell Environ 42:2776–2788
Egamberdieva D, Wirth S, Alqarawi AA, Abd Allah EF (2015) Salt tolerant Methylobacterium mesophilicum showed viable colonization abilities in the plant rhizosphere. Saudi J Biol Sci 22:585–590
García-Fontana C, Vilchez JI, Manzanera M (2020) Proteome comparison between natural desiccation-tolerant plants and drought-protected Caspicum annuum plants by Microbacterium sp. 3J1. Front Microbiol 11:1537
Khan MIR, Palakolanu SR, Chopra P, Rajurkar AB, Gupta R, Iqbal N, Maheshwari C (2021) Improving drought tolerance in rice: Ensuring food security through multi-dimensional approaches. Physiol Plant 172:645–668
Liu Y, Xu PP, Yang FZ, Li M, Yan H, Li N, Zhang X, Wang W (2019) Composition and diversity of endophytic bacterial community in seeds of super hybrid rice ‘Shenliangyou 5814’ (Oryza sativa L.) and its parental lines. Plant Growth Regul 87:257–266
Luo Y, Zhou M, Zhao Q, Wang F, Gao J, Sheng H, An L (2020) Complete genome sequence of Sphingomonas sp. Cra20, a drought resistant and plant growth promoting rhizobacteria. Genomics 112:3648–3657
Luziatelli F, Ficca AG, Cardarelli M, Melini F, Cavalieri A, Ruzzi M (2020) Genome sequencing of Pantoea agglomerans C1 provides insights into molecular and genetic mechanisms of plant growth-promotion and tolerance to heavy metals. Microorganisms 8:153
Mohamad OAA, Li L, Ma JB, Hatab S, Xu L, Guo JW, Rasulov BA, Liu YH, Hedlund BP, Li WJ (2018) Evaluation of the antimicrobial activity of endophytic bacterial populations from Chinese traditional medicinal plant licorice and characterization of the bioactive secondary metabolites produced by Bacillus atrophaeus against Verticillium dahliae. Front Microbiol 9:924
Pang Z, Zhao Y, Xu P, Yu D (2020a) Microbial diversity of upland rice roots and their influence on rice growth and drought tolerance. Microorganisms 8:1329
Pang Z, Xu P, Yu D (2020b) Environmental adaptation of the root microbiome in two rice ecotypes. Microbiol Res 241:126588
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glockner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590-596
Rangjaroen C, Lumyong S, Sloan WT, Sungthong R (2019) Herbicide-tolerant endophytic bacteria of rice plants as the biopriming agents for fertility recovery and disease suppression of unhealthy rice seeds. Bmc Plant Biol 19:580
Santoyo G (2021) How plants recruit their microbiome? J Adv Res, New insights into beneficial interactions. https://doi.org/10.1016/j.jare.2021.11.020
Schloss PD, Gevers D, Westcott SL (2011) Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies. PLoS ONE 6:e27310
Ullah A, Nisar M, Ali H, Hazrat A, Hayat K, Keerio AA, Ihsan M, Laiq M, Ullah S, Fahad S, Khan A, Khan AH, Akbar A, Yang X (2019) Drought tolerance improvement in plants: an endophytic bacterial approach. Appl Microbiol Biotechnol 103:7385–7397
Vandenkoornhuyse P, Quaiser A, Duhamel M, Le Van A, Dufresne A (2015) The importance of the microbiome of the plant holobiont. New Phytol 206:1196–1206
Walitang DI, Kim CG, Jeon S, Kang Y, Sa T (2018) Conservation and transmission of seed bacterial endophytes across generations following crossbreeding and repeated inbreeding of rice at different geographic locations. MicrobiologyOpen 8:e00662
Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267
Wang S, Ouyang L, Ju X, Zhang L, Zhang Q, Li Y (2014) Survey of plant drought-resistance promoting bacteria from Populus euphratica tree living in arid area. Indian J Microbiol 54:419–426
Wang ZW, Ji YL, Chen YG (2015) Studies and biological significances of plant endophytes. Microbiology China 42:349–363
Wang Z, Zhu Y, Li N, Liu H, Zheng H, Wang W, Liu Y (2021a) High-throughput sequencing-based analysis of the composition and diversity of endophytic bacterial community in seeds of saline-alkali tolerant rice. Microbiol Res 250:126794
Wang Z, Zhu Y, Jing R, Wu X, Li N, Liu H, Zhang X, Wang W, Liu Y (2021b) High-throughput sequencing-based analysis of the composition and diversity of endophytic bacterial community in seeds of upland rice. Arch Microbiol 203:609–620
White JR, Nagarajan N, Pop M (2009) Statistical methods for detecting differentially abundant features in clinical metagenomic samples. PLoS Comput Biol 5:e1000352
White JF, Kingsley KL, Zhang Q, Verma R, Obi N, Dvinskikh S, Elmore MT, Verma SK, Gond SK, Kowalski KP (2019) Review: Endophytic microbes and their potential applications in crop management. Pest Manag Sci 75:2558–2565
Wilson D (1995) Endophyte: the evolution of a term, and clarification of its use and definition. Oikos 73:274–276
Zhang L, Li M, Li Q, Chen C, Qu M, Li M, Wang Y, Shen X (2018a) The catabolite repressor/activator Cra is a bridge connecting carbon metabolism and host colonization in the plant drought resistance-promoting bacterium Pantoea alhagi LTYR-11Z. Appl Environ Microbiol 84:e00054-e118
Zhang J, Zhang C, Yang J, Zhang R, Gao J, Zhao X, Zhao J, Zhao D, Zhang X (2018b) Insights into endophytic bacterial community structures of seeds among various Oryza sativa L. rice genotypes. J Plant Growth Regul 38:1–10
Zhang L, Zhang W, Li Q, Cui R, Wang Z, Wang Y, Zhang YZ, Ding W, Shen X (2020) Deciphering the root endosphere microbiome of the desert plant Alhagi sparsifolia for drought resistance-promoting bacteria. Appl Environ Microbiol 86:e02863-e2919
Acknowledgements
We would like to thank the research team of Prof. Huajun Zheng of Shanghai-MOST Key Laboratory of Health and Disease Genomics of Chinese National Human Genome Center at Shanghai for its platform and technical support in high-throughput sequencing and Bioinformatics analysis.
Funding
The research was supported by the National foreign expert Program of China (No. QN2021105002L), the Open Research Fund of Key Laboratory of Microbial Resources Collection and Preservation, Ministry of Agriculture and Rural Affairs (MRCP-2018–5), the Fundamental Research Funds for the Central Universities (No. FRF-TP-20-044A2; FRF-MP-20–39) and the Open Research Fund of State Key Laboratory of Hybrid Rice (Hunan Hybrid Rice Research Center) (No. 2017KF04).
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WZS and ZYQ designed and participated in all experimental procedures, performed data analysis, and drafted the manuscript. LN participated in the plant samples cultivation. WWP and LY supervised the study and critically revised the manuscript. All authors read and approved the final manuscript.
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Wang, Z., Zhu, Y., Li, N. et al. Composition and Diversity of Endophytic Bacterial Communities in the Seeds of Upland Rice Resources from Different Origin Habitats in China. J Plant Growth Regul 42, 2433–2442 (2023). https://doi.org/10.1007/s00344-022-10714-1
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DOI: https://doi.org/10.1007/s00344-022-10714-1