Proline-2′-deoxymugineic acid, a phytosiderophore analog, drives beneficial rhizobacterial community formation to promote peanut micronutrition

Highlights

	● Proline-2′-deoxymugineic (PDMA) significantly altered the bacterial community in the peanut rhizosphere.
	● PDMA resulting in a substantial increase of beneficial bacteria related with micronutrition in plant and soil, especially Actinobacteriota.
	● PDMA application led to the development of a tight, stable microbial network and fosters microbial communication in the rhizosphere.

Abstract

2′-Deoxymugineic (DMA), a phytosiderophore secreted by Poaceae species, can improve iron nutrition in plants. However, little is known about how DMA influences beneficial bacteria in rhizosphere microecosystem. To address this gap, the DMA analog proline-2′-deoxymugineic (PDMA) was used to evaluate its positive effect on peanut rhizobacterial communities and network structure. This study demonstrated that PDMA can promote the absorption of several mineral nutrients in plants and activate micronutrients in the rhizosphere. Specifically, PDMA led to significant impact on the bacterial community structure in the peanut rhizosphere, resulting in a substantial increase in the relative abundance of Actinobacteriota with six beneficial rhizobacterial genera in this phylum. The Cellulosimicrobium and Marmoricola of Actinobacteriota recruited by PDMA may enhance micronutrient availability both to peanut plants and in soil. PDMA application led to the development of a tight, stable microbial network, as indicated by higher topological parameters and a greater variety of keystone genera. Functional prediction revealed that PDMA fosters microbial communication in the rhizosphere. Overall, PDMA was shown to recruit beneficial bacteria and to modulate bacterial network structure in the peanut rhizosphere. It is concluded that these findings demonstrate that phytosiderophore might promote plant growth and nutrition absorption by regulating plant–soil microecosystem.

Graphical abstract

Keywords

Beneficial rhizobacteria recruitment / peanut / plant-soil micronutrition enhancement / proline-2′-deoxymugineic acid / stable microbial network

References

[1] Bastías D A, Balestrini R, Pollmann S, Gundel P E. Environmental interference of plant−microbe interactions. Plant, Cell & Environment, 2022, 45(12): 3387–3398

[2] Dong W, Song Y. The significance of flavonoids in the process of biological nitrogen fixation. International Journal of Molecular Sciences, 2020, 21(16): 5926

[3] Stassen M J J, Hsu S H, Pieterse C M J, Stringlis I A. Coumarin communication along the microbiome−root−shoot axis. Trends in Plant Science, 2021, 26(2): 169–183

[4] Marschner H, Römheld V, Kissel M. Different strategies in higher plants in mobilization and uptake of iron. Journal of Plant Nutrition, 1986, 9(3): 695–713

[5] Clemens S. Metal ligands in micronutrient acquisition and homeostasis. Plant, Cell & Environment, 2019, 42(10): 2902–2912

[6] Xiong H, Kakei Y, Kobayashi T, Guo X, Nakazono M, Takahashi H, Nakanishi H, Shen H, Zhang F, Nishizawa N K, Zuo Y. Molecular evidence for phytosiderophore-induced improvement of iron nutrition of peanut intercropped with maize in calcareous soil. Plant, Cell & Environment, 2013, 36(10): 1888–1902

[7] Mimmo T, Del Buono D, Terzano R, Tomasi N, Vigani G, Crecchio C, Pinton R, Zocchi G, Cesco S. Rhizospheric organic compounds in the soil–microorganism–plant system: their role in iron availability. European Journal of Soil Science, 2014, 65(5): 629–642

[8] Suzuki M, Urabe A, Sasaki S, Tsugawa R, Nishio S, Mukaiyama H, Murata Y, Masuda H, Aung M S, Mera A, Takeuchi M, Fukushima K, Kanaki M, Kobayashi K, Chiba Y, Shrestha B B, Nakanishi H, Watanabe T, Nakayama A, Fujino H, Kobayashi T, Tanino K, Nishizawa N K, Namba K. Development of a mugineic acid family phytosiderophore analog as an iron fertilizer. Nature Communications, 2021, 12(1): 1558

[9] Ueno D, Ito Y, Ohnishi M, Miyake C, Sohtome T, Suzuki M. A synthetic phytosiderophore analog, proline-2′-deoxymugineic acid, is efficiently utilized by dicots. Plant and Soil, 2021, 469(1–2): 123–134

[10] Wang T, Wang N, Lu Q, Lang S, Wang K, Niu L, Suzuki M, Zuo Y. The active Fe chelator proline-2′-deoxymugineic acid enhances peanut yield by improving soil Fe availability and plant Fe status. Plant, Cell & Environment, 2023, 46(1): 239–250

[11] Liu C, Zhao D, Ma W, Guo Y, Wang A, Wang Q, Lee D J. Denitrifying sulfide removal process on high-salinity wastewaters in the presence of Halomonas sp. Applied Microbiology and Biotechnology, 2016, 100(3): 1421–1426

[12] Chen S, Zhou Y, Chen Y, Gu J. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics, 2018, 34(17): i884–i890

[13] Magoč T, Salzberg S L. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics, 2011, 27(21): 2957–2963

[14] Edgar R C. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nature Methods, 2013, 10(10): 996–998

[15] Wang Q, Garrity G M, Tiedje J M, Cole J R. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology, 2007, 73(16): 5261–5267

[16] R core team. R: a language and environment for statistical computing. R Foundation for Statistical Computing, 2022

[17] Schloss P D, Westcott S L, Ryabin T, Hall J R, Hartmann M, Hollister E B, Lesniewski R A, Oakley B B, Parks D H, Robinson C J, Sahl J W, Stres B, Thallinger G G, Van Horn D J, Weber C F. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology, 2009, 75(23): 7537–7541

[18] Oksanen J, Simpson G, Blanchet F G, Kindt R, Legendre P, Minchin P R, O'Hara R B, Solymos P, Stevens M H H, Szoecs E, Wagner H, Barbour M, Bedward M, Bolker B, Borcard D, Carvalho G, Chirico M, De Caceres M, Durand S, Evangelista H B A, FitzJohn R, Friendly M, Furneaux B, Hannigan G, Hill M O, Lahti L, McGlinn D, Ouellette M H, Ribeiro Cunha E, Smith T, Stier A, Ter Braak C J F, Weedon J. Vegan: Community Ecology Package. R Package Version 2.6-4, 2022

[19] Bray J R, Curtis J T. An ordination of the upland forest communities of southern Wisconsin. Ecological Monographs, 1957, 27(4): 326–349

[20] Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett W S, Huttenhower C. Metagenomic biomarker discovery and explanation. Genome Biology, 2011, 12(6): R60

[21] Revelle W. Psych: Procedures for Psychological, Psychometric, and Personality Research. R Package Version 2.3.3, 2023

[22] Kolde R. Pheatmap: Pretty Heatmaps. R Package Version 1.0.12, 2019

[23] Barberán A, Bates S T, Casamayor E O, Fierer N. Using network analysis to explore co-occurrence patterns in soil microbial communities. ISME Journal, 2012, 6(2): 343–351

[24] Douglas G M, Maffei V J, Zaneveld J R, Yurgel S N, Brown J R, Taylor C M, Huttenhower C, Langille M G I. PICRUSt2 for prediction of metagenome functions. Nature Biotechnology, 2020, 38(6): 685–688

[25] Xu L, Dong Z, Chiniquy D, Pierroz G, Deng S, Gao C, Diamond S, Simmons T, Wipf H M L, Caddell D, Varoquaux N, Madera M A, Hutmacher R, Deutschbauer A, Dahlberg J A, Guerinot M L, Purdom E, Banfield J F, Taylor J W, Lemaux P G, Coleman-Derr D. Genome-resolved metagenomics reveals role of iron metabolism in drought-induced rhizosphere microbiome dynamics. Nature Communications, 2021, 12(1): 3209

[26] Dahal B, NandaKafle G, Perkins L, Brözel V S. Diversity of free-living nitrogen fixing Streptomyces in soils of the badlands of South Dakota. Microbiological Research, 2017, 195: 31–39

[27] Anwar S, Ali B, Sajid I. Screening of rhizospheric Actinomycetes for various in-vitro and in-vivo plant growth promoting (PGP) traits and for agroactive compounds. Frontiers in Microbiology, 2016, 7: 1334

[28] El-Tarabily K A, AlKhajeh A S, Ayyash M M, Alnuaimi L H, Sham A, ElBaghdady K Z, Tariq S, AbuQamar S F. Growth promotion of Salicornia bigelovii by Micromonospora chalcea UAE1, an endophytic 1-aminocyclopropane-1-carboxylic acid deaminase-producing actinobacterial isolate. Frontiers in Microbiology, 2019, 10: 1694

[29] Franke-Whittle I H, Manici L M, Insam H, Stres B. Rhizosphere bacteria and fungi associated with plant growth in soils of three replanted apple orchards. Plant and Soil, 2015, 395(1–2): 317–333

[30] Chatterjee S, Sau G B, Sinha S, Mukherjee S K. Effect of co-inoculation of plant growth-promoting rhizobacteria on the growth of amaranth plants. Archives of Agronomy and Soil Science, 2012, 58(12): 1387–1397

[31] Pan X, Zhang S, Zhong Q, Gong G, Wang G, Guo X, Xu X. Effects of soil chemical properties and fractions of Pb, Cd, and Zn on bacterial and fungal communities. Science of the Total Environment, 2020, 715: 136904

[32] Trivedi P, Leach J E, Tringe S G, Sa T, Singh B K. Plant-microbiome interactions: from community assembly to plant health. Nature Reviews. Microbiology, 2020, 18(11): 607–621

[33] Chaney L, Baucom R S. The soil microbial community alters patterns of selection on flowering time and fitness-related traits in Ipomoea purpurea. American Journal of Botany, 2020, 107(2): 186–194

[34] Shakir S, Zaidi S S, de Vries F T, Mansoor S. Plant genetic networks shaping phyllosphere microbial community. Trends in Genetics, 2021, 37(4): 306–316

[35] Boiteau R M, Markillie L M, Hoyt D W, Hu D, Chu R K, Mitchell H D, Pasa-Tolic L, Jansson J K, Jansson C. Metabolic interactions between Brachypodium and Pseudomonas fluorescens under controlled iron-limited conditions. mSystems, 2021, 6(1): e00580–e20

Supplementary materials

The online version of this article at https://doi.org/10.15302/J-FASE-2023531 contains supplementary materials (Tables S1–S18).

Acknowledgements

The authors thank Prof. Kosuke Namba in Tokushima University for the development of PDMA, and express our profound gratefulness to researchers from our laboratory for the support given. This work was supported by the National Key Research and Development Program of China (2022YFD1901500/2022YFD1901501) and National Natural Science Foundation of China (32372810, 31872183).

Compliance with ethics guidelines

Tianqi Wang, Nanqi Wang, Kunguang Wang, Qiaofang Lu, Zhechao Dou, Zhiguang Chi, Dongming Cui, Motofumi Suzuki, and Yuanmei Zuo declare that they have no conflicts of interest or financial conflicts to disclose. This article does not contain any studies with human or animal subjects performed by any of the authors.

RIGHTS & PERMISSIONS

The Author(s) 2023. Published by Higher Education Press. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0)