Abstract
Background and aims
Endophytic bacteria from legume roots and nodules play important roles in regulating plant growth and health. Therefore, the aim is to focus on the community structure and network of pea root endophytes throughout the plant life cycle.
Methods
We collected five edible pea cultivars to study the endophytic bacterial community during the whole developmental period using Illumina sequencing of 16S rRNA gene.
Results
The structure and complexity of root endophytes was significantly affected by the development period and different root endophytes were recruited by peas at different developmental stages. Pea cultivars gave no significant influence on the patterns of root endophytic bacterial community during plant growth. Here, the complexity of root-endophytic bacterial community was the highest at seedling stage and became more and more simple after that. Rhizobium was a dominant root bacteria during the whole developmental stage. The amount of Rhizobium began to accumulate in pea seedling roots, and reached the highest at flowering stage and decreased at the mature stage. The relative abundance of Pseudomonas increased overtime throughout the pea entire life cycle, whereas the amount of Bacteroides decreased overtime.
Conclusions
The pea root and nodule endophytes were dominated by Rhizobium, Pseudomonas and Bacteroides. These findings provide an endophyte-based characterization of the reference stock bacteria detail for the establishment of root endophytic bacteria throughout the plant life cycle. Specially, a proper synthetic microbial community to improve pea yields.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Not applicable.
Code availability
Not applicable.
References
Bai Y, D’Aoust F, Smith DL, Driscoll BT (2002) Isolation of plant-growth-promoting Bacillus strains from soybean root nodules. Can J Microbiol 48:230–238. https://doi.org/10.1139/w02-014
Barberán A, Bates ST, Casamayor EO, Fierer N (2012) Using network analysis to explore co-occurrence patterns in soil microbial communities. ISME J 6:343. https://doi.org/10.1038/ismej.2011.119
Barraza A, Vizuet-de-Rueda JC, Alvarez-Venegas R (2020) Highly diverse root endophyte bacterial community is driven by growth substrate and is plant genotype-independent in common bean (Phaseolus vulgaris L.). PeerJ 8:e9423. https://doi.org/10.7717/peerj.9423
Berendsen RL, Pieterse CM, Bakker PA (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486. https://doi.org/10.1016/j.tplants.2012.04.001
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120. https://doi.org/10.1093/bioinformatics/btu170
Boring LR, Swank WT, Waide JB, Henderson GS (1988) Sources, fates, and impacts of nitrogen inputs to terrestrial ecosystems: review and synthesis. Biogeochemistry 6:119–159. https://doi.org/10.1007/BF00003034
Bulgarelli D, Schlaeppi K, Spaepen S, Van Themaat EVL, Schulze-Lefert P (2013) Structure and functions of the bacterial microbiota of plants. Annu Rev Plant Biol 64:807–838. https://doi.org/10.1146/annurev-arplant-050312-120106
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. https://doi.org/10.1038/nmeth.f.303
Cauwenberghe JV, Michiels J, Honnay O (2015) Effects of local environmental variables and geographical location on the genetic diversity and composition of Rhizobium leguminosarum nodulating Vicia cracca populations. Soil Biol Biochem 90:71–79. https://doi.org/10.1016/j.soilbio.2015.08.001
Chen J, Xu D, Chao L, Liu H, Bao Y (2020) Microbial assemblages associated with the rhizosphere and endosphere of an herbage, Leymus chinensis. Microb Biotechnol 13:1390–1402. https://doi.org/10.1111/1751-7915.13558
Cousin R (1997) Peas (Pisum sativum L.). Field Crop Res 53:111–130. https://doi.org/10.1016/S0378-4290(97)00026-9
Dhariwal A, Chong J, Habib S, King IL, Agellon LB, Xia J (2017) MicrobiomeAnalyst: a web-based tool for comprehensive statistical, visual and meta-analysis of microbiome data. Nucleic Acids Res 45:W180–W188. https://doi.org/10.1093/nar/gkx295
Dudeja SS, Giri R, Saini R, Suneja-Madan P, Kothe E (2012) Interaction of endophytic microbes with legumes. J Basic Microb 52:248–260. https://doi.org/10.1002/jobm.201100063
Edwards J, Johnson C, Santos-Medellín C, Lurie E, Podishetty NK, Bhatnagar S, Eisen JA, Sundaresan V (2015) Structure, variation, and assembly of the root-associated microbiomes of rice. Proc Natl Acad Sci U S A 112:E911–E920. https://doi.org/10.1073/pnas.1414592112
Faust K, Raes J (2012) Microbial interactions: from networks to models. Nat Rev Microbiol 10:538–550. https://doi.org/10.1038/nrmicro2832
Gaiero JR, Mccall CA, Thompson KA, Day NJ, Best AS, Dunfield KE (2013) Inside the root microbiome: bacterial root endophytes and plant growth promotion. Am J Bot 100:1738–1750. https://doi.org/10.3732/ajb.1200572
Galloway JN, Dentener FJ, Capone DG, Boyer EW, Howarth RW, Seitzinger SP, Asner GP, Cleveland CC, Green PA, Holland EA, Karl DM, Michaels AF, Popter JH, Townsend AR, Vorosmarty CJ (2004) Nitrogen cycles: past, present, and future. Biogeochemistry 70:153–226. https://doi.org/10.1007/s10533-004-0370-0
Gao J, Sun P, Wang X, Lv FY, Mao X, Sun J (2017) Rhizobium wenxiniae sp. nov., an endophytic bacterium isolated from maize root. Int J Syst Evol Microbiol 67: 2798–2803. https://doi.org/10.1099/ijsem.0.002025
Gupta G, Panwar J, Jha PN (2013) Natural occurrence of Pseudomonas aeruginosa, a dominant cultivable diazotrophic endophytic bacterium colonizing Pennisetum glaucum (L.) R. Br. Appl Soil Ecol 64:252–261. https://doi.org/10.1016/j.apsoil.2012.12.016
Hoflich G, Wiehe W, Hecht-Buchholz C (1995) Rhizosphere colonization of different growth promoting Pseudomonas and Rhizobium bacteria. Microbiol Res 150:139–147. https://doi.org/10.1016/S0944-5013(11)80048-0
Hyungmin R, Victor VE, Nicholas W, Doty SL, Soo-Hyung K (2018) Salicaceae endophytes modulate stomatal behavior and increase water use efficiency in rice. Front Plant Sci 9:188. https://doi.org/10.3389/fpls.2018.00188
Jiang Y, Li S, Li R, Zhang J, Liu Y, Lv L, Zhu H, Wu W, Li W (2017) Plant cultivars imprint the rhizosphere bacterial community composition and association networks. Soil Biol Biochem 109:145–155. https://doi.org/10.1016/j.soilbio.2017.02.010
Kwak MJ, Kong HG, Choi K, Kwon SK, Kim JF (2018) Rhizosphere microbiome structure alters to enable wilt resistance in tomato. Nat Biotech 36:1100–1109. https://doi.org/10.1038/nbt.4232
Laranjo M, Alexandre A, Oliveira S (2014) Legume growth-promoting rhizobia: an overview on the Mesorhizobium genus. Microbiol Res 169:2–17. https://doi.org/10.1016/j.micres.2013.09.012
Leo VO, Dirk VEJ (2008) Effects of plant genotype and growth stage on the structure of bacterial communities associated with potato (Solanum tuberosum L.). FEMS Microbiol Ecol 64:283–296. https://doi.org/10.1111/j.1574-6941.2008.00469.x
Li M, Li Y, Chen WF, Sui XH, Li Y, Li Y, Wang ET, Chen WX (2012) Genetic diversity, community structure and distribution of rhizobia in the root nodules of Caragana spp. from arid and semi-arid alkaline deserts, in the north of China. Syst Appl Microbiol 35:239–245. https://doi.org/10.1016/j.syapm.2012.02.004
Liu F, Hewezi T, Lebeis SL, Pantalone V, Grewal PS, Staton ME (2019) Soil indigenous microbiome and plant genotypes cooperatively modify soybean rhizosphere microbiome assembly. BMC Microbiol 19:201–219. https://doi.org/10.1186/s12866-019-1572-x
Matsumoto H, Fan X, Wang Y, Kusstatscher P, Duan J, Wu S, Chen S, Qiao K, Wang Y, Ma B, Zhu G, Hashidoko Y, Berg G, Cernava T, Wang M (2021) Bacterial seed endophyte shapes disease resistance in rice. Nat Plants 7:60–72. https://doi.org/10.1038/s41477-020-00826-5
Miliute I, Buzaite O, Baniulis D, Stanys V (2015) Bacterial endophytes in agricultural crops and their role in stress tolerance: a review. Zemdirbyste 102:465–478 http://www.zemdirbyste-agriculture.lt/1024_str60/
Mus F, Crook MB, Garcia K, Garcia Costas A, Geddes BA, Kouri ED, Paramasivan P, Ryu MH, Oldroyd GED, Poole PS, Udvardi MK, Voigt CA, Ané JM, Peters JW (2016) Symbiotic nitrogen fixation and the challenges to its extension to nonlegumes. Appl Environ Microb 82:3698–3710 https://aem.asm.org/content/82/13/3698
Nossa CW, Oberdorf WE, Yang L, Aas JA, Paster BJ, Desantis TZ (2010) Design of 16S rRNA gene primers for 454 pyrosequencing of the human foregut microbiome. World J Gastroentero 16:4135–4144. https://doi.org/10.3748/wjg.v16.i33.4135
Pérez-Jaramillo JE, Mendes R, Raaijmakers JM (2016) Impact of plant domestication on rhizosphere microbiome assembly and functions. Plant Mol Biol 90:635–644. https://doi.org/10.1007/s11103-015-0337-7
Polivkova M, Suman J, Strejcek M, Kracmarova M, Hradilova M, Filipova A, Cajthaml T, Macek T, Uhlik O (2018) Diversity of root-associated microbial populations of Tamarix parviflora cultivated under various conditions. Appl Soil Ecol 125:264–272. https://doi.org/10.1016/j.apsoil.2018.02.002
Rafal Z, James EK, Simon K, Yasuyuki K, Nadieh DJ, Jensen DB, Madsen LH, Simona R, Mcdowell JM (2015) A legume genetic framework controls infection of nodules by symbiotic and endophytic bacteria. PLoS Genet 11:e1005280. https://doi.org/10.1371/journal.pgen.1005280
Reiter B, Pfeifer U, Schwab H, Sessitsch A (2002) Response of endophytic bacterial communities in potato plants to infection with Erwinia carotovora subsp. atroseptica. Appl Environ Microb 68:2261–2268 https://aem.asm.org/content/68/5/2261
Remigi P, Zhu J, Young JPW, Masson-Boivin C (2016) Symbiosis within symbiosis: evolving nitrogen-fixing legume symbionts. Trends Microbiol 24:63–75. https://doi.org/10.1016/j.tim.2015.10.007
Reyon D, Tsai SQ, Khayter C, Foden JA, Sander JD, Joung JK (2012) FLASH assembly of TALENs for high-throughput genome editing. Nat Biotechnol 30:460–465. https://doi.org/10.1038/nbt.2170
Rivas R, Velázquez E, Willems A, Vizcaíno N, Subba-Rao NS, Mateos PF, Gillis M, Dazzo FB, Martínez-Molina E (2002) A new species of Devosia that forms a unique nitrogen-fixing root-nodule symbiosis with the aquatic legume Neptunia natans (L.f.) druce. Appl Environ Microb 68:5217–5222. https://doi.org/10.1128/AEM.68.11.5217-5222.2002
Rognes T, Flouri T, Nichols B, Quince C, Mahe F (2016) VSEARCH: a versatile open source tool for metagenomics. Peer J 4:e2584. https://doi.org/10.7717/peerj.2584
Sánchez AC, Gutiérrez RT, Santana RC, Urrutia AR, Fauvart M, Michiels J, Vanderleyden J (2014) Effects of co-inoculation of native Rhizobium and Pseudomonas strains on growth parameters and yield of two contrasting Phaseolus vulgaris L. genotypes under Cuban soil conditions. Eur J Soil Biol 62:105–112. https://doi.org/10.1016/j.ejsobi.2014.03.004
Turner TR, Ramakrishnan K, Walshaw J, Heavens D, Alston M, Swarbreck D, Osbourn A, Grant A, Poole PS (2013) Comparative metatranscriptomics reveals kingdom level changes in the rhizosphere microbiome of plants. ISME J 7:2248–2258. https://doi.org/10.1038/ismej.2013.119
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 https://aem.asm.org/content/73/16/5261
Wang Y, Li H, Li J, Li X (2017) The diversity and co-occurrence patterns of diazotrophs in the steppes of Inner Mongolia. Catena 157:130–138. https://doi.org/10.1016/j.catena.2017.05.006
Wang H, Gu CT, Liu XF, Yang CW, Li WB, Wang SD (2020a) Impact of soybean nodulation phenotypes and nitrogen fertilizer levels on the rhizosphere bacterial community. Front Microbiol 11:750. https://doi.org/10.3389/fmicb.2020.00750
Wang D, Sun T, Zhao S, Pan L, Liu H, Tian X (2020b) Physiological change alters endophytic bacteria community in clubroot of tumorous stem mustard infected by Plasmodiophora brassicae. BMC Microbiol 20:244–253 https://www.researchsquare.com/article/rs-28394/v1
Yan J, Yan H, Liu L, Chen WF, Zhang XX, Verástegui-Valdés MM, Wang ET, Han XZ (2017) Rhizobium hidalgonense sp. nov., a nodule endophytic bacterium of Phaseolus vulgaris in acid soil. Arch Microbiol 199: 97–104. https://doi.org/10.1007/s00203-016-1281-x
Yu X, Yang J, Wang E, Li B, Yuan H (2015) Effects of growth stage and fulvic acid on the diversity and dynamics of endophytic bacterial community in Stevia rebaudiana Bertoni leaves. Front Microbiol 6:867. https://doi.org/10.3389/fmicb.2015.00867
Zhang B, Du N, Li Y, Shi P, Wei G (2018a) Distinct biogeographic patterns of rhizobia and non-rhizobial endophytes associated with soybean nodules across China. Sci Total Environ 643:569–578. https://doi.org/10.1016/j.scitotenv.2018.06.240
Zhang J, Zhang N, Liu YX, Zhang X, Hu B, Qin Y, Xu H, Wang H, Guo X, Qian J, Wang W, Zhang P, Jin T, Chu C, Bai Y (2018b) Root microbiota shift in rice correlates with resident time in the field and developmental stage. Sci China Life Sci 61:613–621. https://doi.org/10.1007/s11427-018-9284-4
Zipfel C, Oldroyd GED (2017) Plant signalling in symbiosis and immunity. Nature 543:328–336. https://doi.org/10.1038/nature22009
Acknowledgements
This research was supported by the China Agriculture Research System (No. CARS-08), Presidential Foundation of the QINGDAO Academy of Agriculture Sciences, the Qingdao Municipal Project for Science and Technology in Public Benefit (No. 14-2-3-35-nsh).
Author information
Authors and Affiliations
Contributions
XL, QW, XZ, JH, LL, WC, HL, YW and JW performed the experiments; XL, QW and CM analyzed the data; XZ and JH contributed materials; QL planned and designed the research; XL, QW and QL wrote an initial version of the manuscript that was read and revised by all authors.
Corresponding author
Ethics declarations
Ethics approval
Not applicable.
Consent to participate
The authors declare consent to participate.
Consent for publication
The authors declare consent for publication.
Conflict of interest
The authors declare no competing interests.
Additional information
Responsible Editor: Anna Maria Pirttila.
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
ESM 1
(DOCX 128 kb)
Rights and permissions
About this article
Cite this article
Lv, X., Wang, Q., Zhang, X. et al. Community structure and associated networks of endophytic bacteria in pea roots throughout plant life cycle. Plant Soil 468, 225–238 (2021). https://doi.org/10.1007/s11104-021-05124-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-021-05124-3