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Influence of Sugarcane Variety on Rhizosphere Microbiota Under Irrigated and Water-Limiting Conditions

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Abstract

Drought is one of the main problems linked to climate change that is faced by agriculture, affecting various globally important crops, including sugarcane. Environmentally sustainable strategies have been sought to mitigate the effects of climate change on crops. Among them, the use of beneficial microorganisms offers a promising approach. However, it is still necessary to understand the mechanisms that regulate plant-microorganism interactions, in normal situations and under stress. In this work, the rhizosphere metagenomes of two sugarcane varieties, one resistant and the other susceptible to drought, were compared under normal conditions and under water-limiting conditions. The results showed that for the drought-resistant sugarcane variety, bacteria belonging to the order Sphingomonadales and the family Xanthomonadaceae presented increased activities in terms of mobility, colonization, and cell growth. In contrast, the rhizosphere associated with the drought-sensitive variety exhibited increases of bacteria belonging to the family Polyangiaceae, and the genus Streptomyces, with modifications in DNA metabolism and ribosome binding proteins. The results pointed to variation in the rhizosphere microbiota that was modulated by the host plant genotype, revealing potential bacterial candidates that could be recruited to assist plants during water-limiting conditions.

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Data Availability

The datasets generated during the current study are available in the NCBI Sequence Read Archive (SRA), under accession numbers SRX10956439 to SRX10956441. The rhizosphere microbiome associated with the drought-resistant sugarcane has been previously deposited by Pereira et al. [12], under accession numbers SRR10617562 to SRR10617570.

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References

  1. Naylor D, Coleman-Derr D (2018) Drought stress and root-associated bacterial communities. Front Plant Sci 8:2223

    Article  PubMed  PubMed Central  Google Scholar 

  2. De La Fuente GN, Frei UK, Lübberstedt T (2013) Accelerating plant breeding. Trends Plant Sci 18:667–672

    Article  CAS  Google Scholar 

  3. Scudeletti D, Crusciol CAC, Bossolani JW et al (2021) Trichoderma asperellum inoculation as a tool for attenuating drought stress in sugarcane. Front Plant Sci 12:645542

    Article  PubMed  PubMed Central  Google Scholar 

  4. Vargas L, Santa Brígida AB, Mota Filho JP et al (2014) Drought tolerance conferred to sugarcane by association with Gluconacetobacter diazotrophicus: a transcriptomic view of hormone pathways. PLoS ONE 9:e114744

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  5. Armanhi JSL, de Souza RSC, Biazotti BB et al (2021) Modulating drought stress response of maize by a synthetic bacterial community. Front Microbiol 12:747541

    Article  PubMed  PubMed Central  Google Scholar 

  6. van Dam NM, Bouwmeester HJ (2016) Metabolomics in the rhizosphere: tapping into belowground chemical communication. Trends Plant Sci 21:256–265

    Article  PubMed  CAS  Google Scholar 

  7. Berendsen RL, Pieterse CMJ, Bakker PAHM (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486

    Article  CAS  PubMed  Google Scholar 

  8. Da Costa DP, Dias ACF, Durrer A et al (2014) Differential composition of bacterial communities in the rhizosphere of sugarcane varieties. Rev Bras Ciênc Solo 38:1694–1702

    Article  Google Scholar 

  9. Mahoney AK, Yin C, Hulbert SH (2017) Community structure, species variation, and potential functions of rhizosphere-associated bacteria of different winter wheat (Triticum aestivum) cultivars. Front Plant Sci. https://doi.org/10.3389/fpls.2017.00132

    Article  PubMed  PubMed Central  Google Scholar 

  10. Walters WA, Jin Z, Youngblut N et al (2018) Large-scale replicated field study of maize rhizosphere identifies heritable microbes. Proc Natl Acad Sci 115:7368–7373

    Article  PubMed  PubMed Central  Google Scholar 

  11. Mehnaz S (2013) Microbes—friends and foes of sugarcane. J Basic Microbiol 53:954–971

    Article  PubMed  Google Scholar 

  12. Pereira LB, de Oliveira Gambarini VM, de Menezes AB et al (2021) Responses of the sugarcane rhizosphere microbiota to different levels of water stress. Appl Soil Ecol 159:103817

    Article  Google Scholar 

  13. Abrahão A, Lambers H, Sawaya ACHF et al (2014) Convergence of a specialized root trait in plants from nutrient-impoverished soils: phosphorus-acquisition strategy in a nonmycorrhizal cactus. Oecologia 176:345–355

    Article  PubMed  Google Scholar 

  14. Kruskal WH, Wallis WA (1952) Use of ranks in one-criterion variance analysis. J Am Stat Assoc 47:583–621

    Article  Google Scholar 

  15. Fagerland MW, Sandvik L (2009) The Wilcoxon-Mann-Whitney test under scrutiny. Stat Med 28:1487–1497

    Article  PubMed  Google Scholar 

  16. Hammer O, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4:1–9

    Google Scholar 

  17. Patel RK, Jain M (2012) NGS QC Toolkit: a toolkit for quality control of next generation sequencing data. PLoS ONE 7:e30619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Schimel J, Balser TC, Wallenstein M (2007) Microbial stress-response physiology and its implications for ecosystem function. Ecology 88:1386–1394

    Article  PubMed  Google Scholar 

  19. Li H (2013) Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. ArXiv13033997 Q-Bio

  20. Liao Y, Smyth GK, Shi W (2014) featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30:923–930

    Article  CAS  PubMed  Google Scholar 

  21. Allen HK, Bayles DO, Looft T et al (2016) Pipeline for amplifying and analyzing amplicons of the V1–V3 region of the 16S rRNA gene. BMC Res Notes 9:380

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  22. Huson DH, Auch AF, Qi J, Schuster SC (2007) MEGAN analysis of metagenomic data. Genome Res 17:377–386

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Parks DH, Beiko RG (2010) Identifying biologically relevant differences between metagenomic communities. Bioinformatics 26:715–721

    Article  CAS  PubMed  Google Scholar 

  24. Alexa A, Rahnenfuhrer J (2021) topGO: enrichment analysis for gene ontology. R Package Version 2.46.0

  25. R Core Team R: A language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria. URL https://www.R-project.org/. Accessed 25 Sep 2021

  26. Supek F, Bošnjak M, Škunca N, Šmuc T (2011) REVIGO summarizes and visualizes long lists of gene ontology terms. PLoS ONE 6:e21800

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Simões Neto DE, de Oliveira AC, da Rocha AT et al (2012) Industrial characteristics of sugarcane under phosphate fertilization in soils of Pernambuco Brazil. Rev Bras Eng Agríc E Ambient 16:347–354

    Article  Google Scholar 

  28. Chaparro JM, Sheflin AM, Manter DK, Vivanco JM (2012) Manipulating the soil microbiome to increase soil health and plant fertility. Biol Fertil Soils 48:489–499

    Article  Google Scholar 

  29. Sasse J, Martinoia E, Northen T (2018) Feed your friends: do plant exudates shape the root microbiome? Trends Plant Sci 23:25–41

    Article  CAS  PubMed  Google Scholar 

  30. Song F, Han X, Zhu X, Herbert SJ (2012) Response to water stress of soil enzymes and root exudates from drought and non-drought tolerant corn hybrids at different growth stages. Can J Soil Sci 92:501–507

    Article  CAS  Google Scholar 

  31. Gargallo-Garriga A, Preece C, Sardans J et al (2018) Root exudate metabolomes change under drought and show limited capacity for recovery. Sci Rep 8:12696

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  32. Rabbi SMF, Tighe MK, Warren CR et al (2021) High water availability in drought tolerant crops is driven by root engineering of the soil micro-habitat. Geoderma 383:114738

    Article  CAS  Google Scholar 

  33. Mendes R, Garbeva P, Raaijmakers JM (2013) The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. FEMS Microbiol Rev 37:634–663

    Article  CAS  PubMed  Google Scholar 

  34. Uroz S, Buée M, Murat C et al (2010) Pyrosequencing reveals a contrasted bacterial diversity between oak rhizosphere and surrounding soil. Environ Microbiol Rep 2:281–288

    Article  CAS  PubMed  Google Scholar 

  35. Pathan SI, Ceccherini MT, Hansen MA et al (2015) Maize lines with different nitrogen use efficiency select bacterial communities with different β-glucosidase-encoding genes and glucosidase activity in the rhizosphere. Biol Fertil Soils 51:995–1004

    Article  CAS  Google Scholar 

  36. Lacerda Júnior GV, Noronha MF, de Sousa STP et al (2017) Potential of semiarid soil from Caatinga biome as a novel source for mining lignocellulose-degrading enzymes. FEMS Microbiol Ecol 93:fiw248

    Article  PubMed  CAS  Google Scholar 

  37. Thompson C, Beys-da-Silva W, Santi L et al (2013) A potential source for cellulolytic enzyme discovery and environmental aspects revealed through metagenomics of Brazilian mangroves. AMB Express 3:65

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  38. de Souza RSC, Okura VK, Armanhi JSL et al (2016) Unlocking the bacterial and fungal communities assemblages of sugarcane microbiome. Sci Rep 6:28774

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  39. Labeda DP (2011) Multilocus sequence analysis of phytopathogenic species of the genus Streptomyces. Int J Syst Evol Microbiol 61:2525–2531

    Article  PubMed  Google Scholar 

  40. Erlacher A, Cernava T, Cardinale M et al (2015) Rhizobiales as functional and endosymbiontic members in the lichen symbiosis of Lobaria pulmonaria L. Front Microbiol. https://doi.org/10.3389/fmicb.2015.00053

    Article  PubMed  PubMed Central  Google Scholar 

  41. Widhalm JR, Dudareva N (2015) A familiar ring to it: biosynthesis of plant benzoic acids. Mol Plant 8:83–97

    Article  CAS  PubMed  Google Scholar 

  42. Carlos C, Fan H, Currie CR (2018) Substrate shift reveals roles for members of bacterial consortia in degradation of plant cell wall polymers. Front Microbiol 9:364

    Article  PubMed  PubMed Central  Google Scholar 

  43. Wu L, Wang J, Huang W et al (2015) Plant-microbe rhizosphere interactions mediated by Rehmannia glutinosa root exudates under consecutive monoculture. Sci Rep 5:15871

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Galán JE, Collmer A (1999) Type III secretion machines: bacterial devices for protein delivery into host cells. Science 284:1322–1328

    Article  PubMed  Google Scholar 

  45. Marchi M, Boutin M, Gazengel K et al (2013) Genomic analysis of the biocontrol strain Pseudomonas fluorescens Pf29Arp with evidence of T3SS and T6SS gene expression on plant roots. Environ Microbiol Rep 5:393–403

    Article  CAS  PubMed  Google Scholar 

  46. Placella SA, Brodie EL, Firestone MK (2012) Rainfall-induced carbon dioxide pulses result from sequential resuscitation of phylogenetically clustered microbial groups. Proc Natl Acad Sci 109:10931–10936

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Scott MD, Meshnick SR, Eaton JW (1987) Superoxide dismutase-rich bacteria: paradoxical increase in oxidant toxicity. J Biol Chem 262:3640–3645

    Article  CAS  PubMed  Google Scholar 

  48. Santos R, Herouart D, Puppo A, Touati D (2000) Critical protective role of bacterial superoxide dismutase in Rhizobium-legume symbiosis. Mol Microbiol 38:750–759

    Article  CAS  PubMed  Google Scholar 

  49. Kim YC, Miller CD, Anderson AJ (2000) Superoxide dismutase activity in Pseudomonas putida affects utilization of sugars and growth on root surfaces. Appl Environ Microbiol 66:1460–1467

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Wang Y, Wang H, Yang C-H et al (2007) Two distinct manganese-containing superoxide dismutase genes in Bacillus cereus : their physiological characterizations and roles in surviving in wheat rhizosphere. FEMS Microbiol Lett 272:206–213

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors thank the Centre for Sugar Technology for supplying the plant material, Dr Alexandra Sawaya for assistance in the chromatographic analyses, and the Irish Centre for High-End Computing (ICHEC) for supporting the bioinformatic analyses. We are also grateful to the São Paulo State Research Foundation (FAPESP), Coordination for the Improvement of Higher Education Personnel (CAPES), and the National Council for Scientific and Technological Development (CNPq).

Funding

This work was supported by the São Paulo State Research Foundation (FAPESP, Grant Numbers 2015/00408–5 and 2016/08994–3), FAPESP/CAPES (Grant Number 2014/05929–0), and the National Council for Scientific and Technological Development (CNPq, Grant Number 140547/2014–2).

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LBP: carried out the experiments. LBP, VMOG, ABM, and RV: analyzed the data. LBP: wrote the manuscript, with support from VMOG, ABM, RV, and LMMO. LMMO and RV: supervised the project.

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Correspondence to Leticia B. Pereira.

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Pereira, L.B., Gambarini, V.M.d., de Menezes, A.B. et al. Influence of Sugarcane Variety on Rhizosphere Microbiota Under Irrigated and Water-Limiting Conditions. Curr Microbiol 79, 246 (2022). https://doi.org/10.1007/s00284-022-02946-x

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  • DOI: https://doi.org/10.1007/s00284-022-02946-x

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