The effects of Pseudomonas strains isolated from Achnatherum inebrians on plant growth: A genomic perspective.


Journal

Environmental microbiology reports
ISSN: 1758-2229
Titre abrégé: Environ Microbiol Rep
Pays: United States
ID NLM: 101499207

Informations de publication

Date de publication:
Oct 2024
Historique:
received: 02 04 2024
accepted: 29 08 2024
medline: 13 10 2024
pubmed: 13 10 2024
entrez: 10 10 2024
Statut: ppublish

Résumé

Achnatherum inebrians is a perennial grass widely distributed in northwest China. Nearly all wild A. inebrians plants are infected by Epichloë endophytes. In this study, bacteria from the phyllosphere were isolated from leaves of both endophyte-free and endophyte-infected A. inebrians and sequenced for identification. Pseudomonas, comprising 48.12% of the culturable bacterial communities, was the most dominant bacterial genus. Thirty-four strains from 12 Pseudomonas species were used to inoculate A. inebrians seeds and plants. Results indicated that Epichloë significantly increased the diversity and richness index of the phyllosphere. Pseudomonas Sp1, Sp3, Sp5 and Sp7 had a significantly positive effect on plant growth and photosynthesis, whereas Sp10, Sp11 and Sp12 had a significantly negative effect. Whole-genome and pan-genome analysis suggested that the variability in the effects of Pseudomonas on A. inebrians was related to differences in genome composition and genomic islands.

Identifiants

pubmed: 39387603
doi: 10.1111/1758-2229.70011
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e70011

Subventions

Organisme : Fundamental Research Funds for the Central Universities, Lanzhou University
ID : jbky-2022-ey21
Organisme : National Natural Science Foundation of China
ID : 31772665
Organisme : National Natural Science Foundation of China
ID : 32061123004
Organisme : Gansu Provincial Science and Technology Major Projects
ID : 23ZDNA009

Informations de copyright

© 2024 The Author(s). Environmental Microbiology Reports published by John Wiley & Sons Ltd.

Références

Angiuoli, S.V. & Salzberg, S.L. (2011) Mugsy: fast multiple alignment of closely related whole genomes. Bioinformatics, 27, 334–342.
Backer, R., Rokem, J.S., llangumaran, G., Lamont, J., Praslickova, D., Ricci, E. et al. (2018) Plant growth‐promoting rhizobacteria: context, mechanisms of action, and roadmap to commercialization of biostimulants for sustainable agriculture. Frontiers in Plant Science, 90, 1437.
Bastías, D.A., Bustos, L.B., Jáuregui, R., Barrera, A., Acuña‐Rodríguez, I.S., Molina‐Montenegro, M.A. et al. (2021) Epichloë fungal endophytes influence seed‐associated bacterial communities. Frontiers in Microbiology, 12, 795354.
Chen, J., Liu, Y., Liu, M., Guo, W., Wang, Y., He, Q. et al. (2023) Pangenome analysis reveals genomic variations associated with domestication traits in broomcorn millet. Nature Genetics, 55, 2243–2254.
Chen, N., He, R.L., Chai, Q. et al. (2016) Transcriptomic analyses giving insights into molecular regulation mechanisms involved in cold tolerance by Epichloë endophyte in seed germination of Achnatherum inebrians. Plant Growth Regulation, 80, 367–375.
Chen, Y.M., Guo, Y.E., Xie, X.M., Wang, Z., Miao, L., Yang, Z. et al. (2023) Pangenome‐based trajectories of intracellular gene transfers in Poaceae unveil high cumulation in Triticeae. Plant Physiology, 193, 578–594.
Cheng, H.Y., Concepcion, G.T., Feng, X.W., Zhang, H. & Li, H. (2020) Haplotype‐resolved de novo assembly using phased assembly graphs with hifiasm. Nature Methods, 18, 170–175.
Chiappero, J., Cappellari, L.D., Alderete, L.G.S., Palermo, T.B. & Banchio, E. (2019) Plant growth promoting rhizobacteria improve the antioxidant status in Mentha piperita grown under drought stress leading to an enhancement of plant growth and total phenolic content. Industrial Crops and Products, 139, 111553.
Christensen, M.J., Bennett, R.J., Ansari, H.A., Koga, H., Johnson, R.D., Bryan, G.T. et al. (2008) Epichloë endophytes grow by intercalary hyphal extension in elongating grass leaves. Fungal Genetics & Biology, 45, 84–93.
Claire, B. & Brinkman, F.S.L. (2018) Improved genomic Island predictions with IslandPath‐DIMOB. Bioinformatics, 13, 13.
Cui, X.L., Zhang, X.X., Shi, L.L., Christensen, M.J., Nan, Z. & Xia, C. (2022) Effects of Epichloë endophyte and transgenerational effects on physiology of Achnatherum inebrians under drought stress. Agriculture, 12, 761.
Delcher, A.L., Phillippy, A., Carlton, J. & Salzberg, S.L. (2002) Fast algorithms for large‐scale genome alignment and comparison. Nucleic Acids Research, 30, 2478–2483.
Dimkic, I., Janakiev, T., Petrovic, M., Degrassi, G. & Fira, D. (2022) Plant‐associated Bacillus and Pseudomonas antimicrobial activities in plant disease suppression via biological control mechanisms—a review. Physiological and Molecular Plant Pathology, 117, 101754.
Ding, W., Baumdicker, F. & Neher, R.A. (2018) PanX: pan‐genome analysis and exploration. Nucleic Acids Research, 46, e5.
Dumas, E., Christina, B.E., Vandenbogaert, M., Rodríguez de la Vega, R.C., Thiberge, J.M., Caro, V. et al. (2016) Mycobacterial pan‐genome analysis suggests important role of plasmids in the radiation of type VII secretion systems. Genome Biology and Evolution, 8, 387–402.
Elbersen, W.W. & West, C.P. (1996) Growth and water relations of field‐grown tall fescue as influenced by drought and endophytes. Grass and Forage Science, 51, 333–342.
Fatichi, S., Leuzinger, S. & Körner, C. (2014) Moving beyond photosynthesis: from carbon source to sink‐driven vegetation modeling. New Phytologist, 201, 1086–1095.
Feng, H.C., Fu, R.X., Luo, J.Y., Hou, X., Gao, K., Su, L. et al. (2023) Listening to plant's Esperanto via root exudates: reprogramming the functional expression of plant growth‐promoting rhizobacteria. New Phytologist, 239, 2307–2319.
Freschi, L., Vincent, A.T., Jeukens, J., Emond‐Rheault, J.G., Kukavica‐Ibrulj, I., Dupont, M.J. et al. (2019) The Pseudomonas aeruginosa pan‐genome provides new insights on its population structure, horizontal gene transfer, and pathogenicity. Genome Biology and Evolution, 11, 109–120.
Garrido‐Sanz, D., Čaušević, S., Vacheron, J., Heiman, C.M., Sentchilo, V., van der Meer, J.R. et al. (2023) Changes in structure and assembly of a species‐rich soil natural community with contrasting nutrient availability upon establishment of a plant‐beneficial pseudomonas in the wheat rhizosphere. Microbiome, 11, 214.
Gibbs, R.A. & Hayes, C.R. (1988) The use of R2A medium and the spread plate method for the enumeration of heterotrophic bacteria in drinking water. Letters in Applied Microbiology, 6, 19–21.
Gomila, M., Peña, A., Mulet, M., Lalucat, J. & García‐Valdés, E. (2015) Phylogenomics and systematics in Pseudomonas. Frontiers in Microbiology, 6, 214.
Guzman, M.M., Valenzuela, J.L., Sanchez, A. & Romero, L. (1992) Physiological ternary groups in horticultural plants. 2. Macronutrients. Agrochimica, 36, 34–52.
He, A.L., Niu, S.Q., Zhao, Q., Li, Y.S., Gou, J.Y., Gao, H.J. et al. (2018) Induced salt tolerance of Perennial ryegrass by a novel bacterium strain from the rhizosphere of a desert shrub Haloxylon ammodendron. International Journal of Molecular Sciences, 19, 469.
Jiao, H.W., Xu, W.H., Chen, W.J., Hu, Y., Tian, R. & Wang, Z. (2022) Complete genome sequence data of Bacillus altitudinis LZP02, a bacterium from the rice rhizosphere, for studying the promotion of plant growth. Molecular Plant‐Microbe Interactions, 35, 368–438.
Ju, Y.W., Kou, M.Z., Zhong, R., Christensen, M.J. & Zhang, X. (2021) Alleviating salt stress on seedings using plant growth promoting rhizobacteria isolated from the rhizosphere soil of Achnatherum inebrians infected with Epichloë gansuensis endophyte. Plant and Soil, 465, 349–366.
Ju, Y.W., Zhong, R., Christensen, M.J. & Zhang, X. (2020) Effects of Epichloë gansuensis endophyte on the root and rhizosphere soil bacteria of Achnatherum inebrians under different moisture conditions. Frontiers in Microbiology, 11, 747.
Kanehisa, M., Goto, S., Kawashima, S., Okuno, Y. & Hattori, M. (2004) The KEGG resource for deciphering the genome. Nucleic Acids Research, 32, 277–280.
Kim, J., Choi, O. & Kim, W.I. (2015) First report of sheath brown rot of rice caused by Pseudomonas fuscovaginae in Korea. Plant Disease, 99, 1033.
Kou, M.Z., Bastías, D.A., Christensen, M.J., Zhong, R., Nan, Z.B. & Zhang, X.X. (2021) The plant salicylic acid signalling pathway regulates the infection of a biotrophic pathogen in grasses associated with an Epichloë endophyte. Journal of Fungi, 7, 633.
Krzywinski, M., Schein, J., Birol, I., Connors, J., Gascoyne, R., Horsman, D. et al. (2009) Circos: an information aesthetic for comparative genomics. Genome Research, 19, 1639–1645.
Kumar, V.P., Rajpoot, A., Srivastav, A., Okuno, Y. & Hattori, M. (2018) Phylogenetic relationship and molecular dating of Indian pangolin (Manis crassicaudata) with other extant pangolin species based on complete cytochrome b mitochondrial gene. Mitochondrial DNA Part A DNA Mapping, Sequencing, and Analysis, 29, 1276–1283.
Li, L., Stoeckert, C.J. & Roos, D.S. (2003) OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Research, 13, 2178–2189.
Li, P., Yuan, W.F., Huang, Y.T.M., Zhang, C., Ni, C., Lin, Q. et al. (2022) Complete genome sequence of Pseudomonas stutzeri S116 owning bifunctional catalysis provides insights into affecting performance of microbial fuel cells. BMC Microbiology, 22, 137.
Liang, J.J., Gao, G.Y., Zhong, R., Liu, B., Christensen, M.J., Ju, Y. et al. (2023) The effect of Epichloë gansuensis endophyte on seed‐borne microbes and seed metabolites in Achnatherum inebrians. Microbiology Spectrum, 11, e01350‐22.
Liang, Y., Wang, H.C., Li, C.J., Nan, Z. & Li, F. (2017) Effects of feeding drunken horse grass infected with Epichloë gansuensis endophyte on animal performance, clinical symptoms and physiological parameters in sheep. BMC Veterinary Research, 13, 223.
Licciardello, G., Strano, C.P., Bertani, I., Bella, P., Fiore, A., Fogliano, V. et al. (2012) N‐acyl‐homoserine‐lactone quorum sensing in tomato phytopathogenic Pseudomonas spp. is involved in the regulation of lipodepsipeptide production. Journal of Biotechnology, 159, 274–282.
Liu, B.W., Ju, Y.W., Xia, C., Zhong, R., Christensen, M.J., Zhang, X. et al. (2022) The effect of Epichloë endophyte on phyllosphere microbes and leaf metabolites in Achnatherum inebrians. iScience, 25, 104144.
Liu, J.P., Xu, W.F., Zhang, Q., Liao, W., Li, L., Chen, S. et al. (2024) OsPHR2‐mediated recruitment of Pseudomondaceae enhances rice phosphorus uptake. Plant Communications, 5, 100930. Available from: https://doi.org/10.1016/j.xplc.2024.100930
Lugtenberg, B. & Kamilova, F. (2009) Plant‐growth‐promoting rhizobacteria. Annual Review of Microbiology, 63, 541–556.
Malinowski, D.P., Leuchtmann, A., Schmidt, D. & Nösberger, J. (1997) Symbiosis with Neotyphodium uncinatum endophyte may increase the competitive ability of meadow fescue. Agronomy Journal, 89, 833–839.
Manzur, M.E., Garello, F.A., Omacini, M., Schnyder, H., Sutka, M.R. & García‐Parisi, P.A. (2022) Endophytic fungi and drought tolerance: ecophysiological adjustment in shoot and root of an annual mesophytic host grass. Functional Plant Biology, 49, 272–282.
Marchi, M., Boutin, M., Gazengel, K., Rispe, C., Gauthier, J.P., Guillerm‐Erckelboudt, A.Y. et al. (2013) Genomic analysis of the biocontrol strain Pseudomonas fluorescens Pf 29Arp with evidence of T3SS and T6SS gene expression on plant roots. Environmental Microbiology Reports, 5, 393–403.
Melnyk, R.A., Hossain, S.S. & Haney, C.H. (2019) Convergent gain and loss of genomic islands drive lifestyle changes in plant‐associated Pseudomonas. ISME Journal, 13, 157–1588.
Nan, Z.B. & Li, C.J. (2000) Neotyphodium in native grasses in China and observations on endophyte/host interactions. Proceedings of the 4th international Neotyphodium/grass interactions symposium soest, pp. 41–50.
Nan, Z.B., Wang, Y.R., Fu, H., Guo, Z.F., Li, C.J., Chen, N., et al. (2021) Stress tolerance biology of native plants. China Science Publiching & Media Ltd. (CSPM). (In Chinese).
Nelson, D.V. & Sommers, L.E. (1982) Total carbon, organic carbon, and organic matter. In: Sparks, D.L. (Ed.) Methods of soil analysis. Part 2: chemical and microbiological properties. Madison, WI: Soil Science Society of America, pp. 961–1010.
Nguyen, L.T., Schmidt, H.A., Von Haeseler, A. & Minh, B.Q. (2015) IQ‐TREE: a fast and effective stochastic algorithm for estimating maximum‐likelihood phylogenies. Molecular Biology and Evolution, 32, 268–274.
Nguyen, M., Ekstrom, A., Li, X. & Yin, Y. (2015) HGT‐Finder: a new tool for horizontal gene transfer finding and application to Aspergillus genomes. Toxins, 7, 4035–4053.
Nissinen, R., Helander, M., Kumar, M. & Saikkonen, K. (2019) Heritable Epichloë symbiosis shapes fungal but not bacterial communities of plant leaves. Scientific Reports, 9, 5253.
Pan, F.J., Zhang, W., Liu, S.J., Li, D. & Wang, K. (2015) Leaf N:P stoichiometry across plant functional groups in the karst region of southwestern China. Trees, 29, 883–892.
Parra‐Sánchez, Á., Antequera‐Zambrano, L., Martínez‐Navarrete, G., Zorrilla‐Muñoz, V., Paz, J.L., Alvarado, Y.J. et al. (2023) Comparative analysis of CRISPR‐Cas systems in Pseudomonas genomes. Genes, 14, 1337.
Peleg, Z. & Blumwald, E. (2011) Hormone balance and abiotic stress tolerance in crop plants. Current Opinion in Plant Biology, 14, 290–295.
Purwaningsih, Radian, Dewi, W.S. & Pujiasmanto, B. (2019) Indigenous phosphate‐solubilizing bacteria enhance germination in deteriorated rice seed. Bulgarian Journal of Agricultural Science, 25, 486–493.
Roberts, E. & Lindow, S. (2014) Loline alkaloid production by fungal endophytes of Fescue species select for particular epiphytic bacterial microflora. ISME Journal, 8, 359–368.
Rozpadek, P., Wezowicz, K., Nosek, M., Ważny, R., Tokarz, K., Lembicz, M. et al. (2015) The fungal endophyte Epichloë typhina improves photosynthesis efficiency of itshost orchard grass (Dactylis glomerata). Planta, 242, 1025–1035.
Soucy, S.M., Huang, J.L. & Gogarten, J.P. (2015) Horizontal gene transfer: building the web of life. Nature Reviews Genetics, 16, 472–482.
Sreenivasulu, N., Harshavardhan, V.T., Govind, G., Seiler, C. & Kohli, A. (2012) Contrapuntal role of ABA: does it mediate stress tolerance or plant growth retardation under long‐term drought stress? Gene, 506, 265–273.
Tan, T.S., Syed, H.S. & Yap, W.B. (2017) Expression of surfacebound non‐structural 1 (NS1) protein of infuenza virus A H5N1 on Lactobacillus casei strain C1. Letters in Applied Microbiology, 64, 446–451.
Thomas, C.M. & Nielsen, K.M. (2005) Mechanisms of, and barriers to, horizontal gene transfer between bacteria. Nature Reviews Microbiology, 3, 711–721.
Trivedi, P., Leach, J.E., Tringe, S.G., Sa, T. & Singh, B.K. (2020) Plant‐microbiome interactions: from community assembly to plant health. Nature Reviews Microbiology, 18, 607–621.
van der Voort, M., Meijer, H.J.G., Schmidt, Y., Watrous, J., Dekkers, E., Mendes, R. et al. (2015) Genome mining and metabolic profiling of the rhizosphere bacterium Pseudomonas sp. SH‐C52 for antimicrobial compounds. Frontiers in Microbiology, 6, 693.
Vernikos, G.S. & Parkhill, J. (2006) Interpolated variable order motifs for identification of horizontally acquired DNA: revisiting the Salmonella pathogenicity islands. Bioinformatics, 22, 2196–2203.
Wang, J.F., Tian, P., Christensen, M.J., Zhang, X., Li, C. & Nan, Z. (2018) Effect of Epichloë gansuensis endophyte on the activity of enzymes of nitrogen metabolism, nitrogen use efficiency and photosynthetic ability of Achnatherum inebrians under various NaCl concentrations. Plant and Soil, 66, 4022–4031.
Xia, C., Christensen, M.J., Zhang, X.X. & Nan, Z.B. (2018) Effect of Epichloë gansuensis endophyte and transgenerational effects on the water use efficiency, nutrient and biomass accumulation of Achnatherum inebrians under soil water deficit. Plant and Soil, 424, 1–17.
Xu, W.B., Li, M.M., Lin, W.H., Nan, Z. & Tian, P. (2021) Effects of Epichloë sinensis endophyte and host ecotype on physiology of Festuca sinensis under different soil moisture conditions. Plants, 10, 1649.
Yang, R., Li, S., Li, Y., Yan, Y., Fang, Y., Zou, L. et al. (2021) Bactericidal effect of Pseudomonas oryziphila sp. nov., a novel Pseudomonas species against Xanthomonas oryzae reduces disease severity of bacterial leaf streak of rice. Frontiers in Microbiology, 12, 759536.
Yang, R.H., Shi, Q., Huang, T.T., Yan, Y., Li, S., Fang, Y. et al. (2023) The natural pyrazolotriazine pseudoiodinine from Peudomonas mosselii 923 inhibits plant bacterial and fungal pathogens. Nature Communitions, 14, 734.
Ye, W., Hu, S., Wu, L., Ge, C., Cui, Y., Chen, P. et al. (2017) Fine mapping a major QTL qFCC7L for chlorophyll content in rice (Oryza sativa L) cv. PA64s. Plant Growth Regulation, 81, 81–90.
Zhang, X.X., Li, C.J., Nan, Z.B. & Matthew, C. (2012) Neotyphodium endophyte increases Achnatherum inebrians (drunken horse grass) resistance to herbivores and seed predators. Weed Research, 52, 70–78.
Zhang, X.X., Nan, Z.B., Li, C.J. & Gao, K. (2014) Cytotoxic effect of ergot alkaloids in Achnatherum inebrians infected by the Neotyphodium gansuense endophyte. Journal of Agricultural and Food Chemistry, 62, 7419–7422.
Zhao, Z.R., Kou, M.Z., Zhong, R., Xia, C., Christensen, M.J. & Zhang, X. (2021) Transcriptome analysis revealed plant hormone biosynthesis and response pathway modification by Epichloë gansuensis in Achnatherum inebrians under different soil moisture availability. Journal of Fungi, 7, 640.
Zhong, R., Bastías, D.A., Zhang, X.C., Li, C. & Nan, Z. (2022) Vertically transmitted Epichloë systemic endophyte enhances drought tolerance of Achnatherum inebrians host plants through promoting photosynthesis and biomass accumulation. Journal of Fungi, 8, 512.
Zou, Z.W., Guo, B.J., Guo, Y., Ma, X., Luo, S., Feng, L. et al. (2024) A comprehensive “quality‐quantity‐activity” approach based on portable near‐infrared spectrometer and membership function analysis to systematically evaluate spice quality: Cinnamomum cassia as an example. Food Chemistry, 439, 138142.

Auteurs

Jinjin Liang (J)

State Key Laboratory of Herbage Improvement and Grassland Agroecosystems, Center for Grassland Microbiome, Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Affairs, College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou, China.

Bowen Liu (B)

State Key Laboratory of Herbage Improvement and Grassland Agroecosystems, Center for Grassland Microbiome, Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Affairs, College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou, China.

Michael J Christensen (MJ)

Grasslands Research Centre, AgResearch, Palmerston North, New Zealand.

Chunjie Li (C)

State Key Laboratory of Herbage Improvement and Grassland Agroecosystems, Center for Grassland Microbiome, Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Affairs, College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou, China.

Xingxu Zhang (X)

State Key Laboratory of Herbage Improvement and Grassland Agroecosystems, Center for Grassland Microbiome, Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Affairs, College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou, China.

Zhibiao Nan (Z)

State Key Laboratory of Herbage Improvement and Grassland Agroecosystems, Center for Grassland Microbiome, Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Affairs, College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou, China.

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