Host-mediated microbiome engineering (HMME) of drought tolerance in the wheat rhizosphere

Autoři: Michael D. Jochum aff001;  Kelsey L. McWilliams aff001;  Elizabeth A. Pierson aff002;  Young-Ki Jo aff001
Působiště autorů: Department of Plant Pathology & Microbiology, Texas A&M University, College Station, Texas, United States of America aff001;  Department of Horticultural Sciences, Texas A&M University, College Station, Texas, United States of America aff002
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article


Host-mediated microbiome engineering (HMME) is a strategy that utilizes the host phenotype to indirectly select microbiomes though cyclic differentiation and propagation. In this experiment, the host phenotype of delayed onset of seedling water deficit stress symptoms was used to infer beneficial microbiome-host interactions over multiple generations. By utilizing a host-centric selection approach, microbiota are selected at a community level, therein using artificial selection to alter microbiomes through both ecological and evolutionary processes. After six rounds of artificial selection using host-mediated microbiome engineering (HMME), a microbial community was selected that mediated a 5-day delay in the onset of drought symptoms in wheat seedlings. Seedlings grown in potting medium inoculated with the engineered rhizosphere from the 6th round of HMME produced significantly more biomass and root system length, dry weight, and surface area than plants grown in medium similarly mixed with autoclaved inoculum (negative control). The effect on plant water stress tolerance conferred by the inoculum was transferable at subsequent 10-fold and 100-fold dilutions in fresh non-autoclaved medium but was lost at 1000-fold dilution and was completely abolished by autoclaving, indicating the plant phenotype is mediated by microbial population dynamics. The results from 16S rRNA amplicon sequencing of the rhizosphere microbiomes at rounds 0, 3, and 6 revealed taxonomic increases in proteobacteria at the phylum level and betaproteobacteria at the class level. There were significant decreases in alpha diversity in round 6, divergence in speciation with beta diversity between round 0 and 6, and changes in overall community composition. This study demonstrates the potential of using the host as a selective marker to engineer microbiomes that mediate changes in the rhizosphere environment that improve plant adaptation to drought stress.

Klíčová slova:

Drought adaptation – Engineering and technology – Microbiome – Plant resistance to abiotic stress – Rhizosphere – Seedlings – Water resources – Wheat


1. Swenson W, Wilson DS, Elias R. Artificial ecosystem selection. Proc Natl Acad Sci U S A. 2000;97(16):9110–4. Epub 2000/07/13. doi: 10.1073/pnas.150237597 10890915; PubMed Central PMCID: PMC16830.

2. Mueller UG, Sachs JL. Engineering microbiomes to improve plant and animal health. Trends Microbiol. 2015;23(10):606–17. Epub 2015/10/01. doi: 10.1016/j.tim.2015.07.009 26422463.

3. Panke-Buisse K, Lee S, Kao-Kniffin J. Cultivated sub-populations of soil microbiomes retain early flowering plant trait. Microb Ecol. 2017;73(2):394–403. Epub 2016/09/23. doi: 10.1007/s00248-016-0846-1 27655524; PubMed Central PMCID: PMC5272889.

4. Panke-Buisse K, Poole AC, Goodrich JK, Ley RE, Kao-Kniffin J. Selection on soil microbiomes reveals reproducible impacts on plant function. ISME J. 2014;9:980. doi: 10.1038/ismej.2014.196 25350154

5. Mueller UG, Juenger T, Kardish M, Carlson A, Burns K, Smith C, et al. Artificial microbiome-selection to engineer microbiomes that confer salt-tolerance to plants. bioRxiv. 2016:081521. doi: 10.1101/081521

6. Pessarakli M. Handbook of plant and crop stress. 2nd ed. New York: M. Dekker; 1999. xviii, 1254 p. p.

7. Himmelbauer ML, Loiskandl W, Kastanek F. Estimating length, average diameter and surface area of roots using two different Image analyses systems. Plant Soil. 2004;260(1–2):111–20. doi: 10.1023/B:Plso.0000030171.28821.55 WOS:000221763000011.

8. Arsenault J-L, Poulcur S, Messier C, Guay R. WinRHlZO™, a root-measuring system with a unique overlap correction method. HortScience. 1995;30(4):906.

9. Garnier E. Growth analysis of congeneric annual and perennial grass species. J Ecol. 1992;80(4):665–75. doi: 10.2307/2260858 WOS:A1992KF83700007.

10. Thompson LR, Sanders JG, McDonald D, Amir A, Ladau J, Locey KJ, et al. A communal catalogue reveals Earth’s multiscale microbial diversity. Nature. 2017;551:457. doi: 10.1038/nature24621 29088705

11. Cock PJ, Fields CJ, Goto N, Heuer ML, Rice PM. The Sanger FASTQ file format for sequences with quality scores, and the Solexa/Illumina FASTQ variants. Nucleic Acids Res. 2010;38(6):1767–71. Epub 2009/12/18. doi: 10.1093/nar/gkp1137 20015970; PubMed Central PMCID: PMC2847217.

12. Hansen KD, Brenner SE, Dudoit S. Biases in Illumina transcriptome sequencing caused by random hexamer priming. Nucleic Acids Res. 2010;38(12):e131. Epub 2010/04/17. doi: 10.1093/nar/gkq224 20395217; PubMed Central PMCID: PMC2896536.

13. Erlich Y, Mitra PP, delaBastide M, McCombie WR, Hannon GJ. Alta-Cyclic: a self-optimizing base caller for next-generation sequencing. Nat Methods. 2008;5(8):679–82. Epub 2008/07/08. doi: 10.1038/nmeth.1230 18604217; PubMed Central PMCID: PMC2978646.

14. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30(15):2114–20. Epub 2014/04/04. doi: 10.1093/bioinformatics/btu170 24695404; PubMed Central PMCID: PMC4103590.

15. Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJ, Holmes SP. DADA2: High-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13(7):581–3. Epub 2016/05/24. doi: 10.1038/nmeth.3869 27214047; PubMed Central PMCID: PMC4927377.

16. Santhanam R, Luu VT, Weinhold A, Goldberg J, Oh Y, Baldwin IT. Native root-associated bacteria rescue a plant from a sudden-wilt disease that emerged during continuous cropping. Proc Natl Acad Sci U S A. 2015;112(36):E5013–E20. doi: 10.1073/pnas.1505765112 26305938

17. Comas LH, Becker SR, Cruz VM, Byrne PF, Dierig DA. Root traits contributing to plant productivity under drought. Front Plant Sci. 2013;4(442):442. Epub 2013/11/10. doi: 10.3389/fpls.2013.00442 24204374; PubMed Central PMCID: PMC3817922.

18. Ngumbi E, Kloepper J. Bacterial-mediated drought tolerance: Current and future prospects. Appl Soil Ecol. 2016;105:109–25. doi: 10.1016/j.apsoil.2016.04.009 WOS:000377358300014.

19. Barnawal D, Bharti N, Pandey SS, Pandey A, Chanotiya CS, Kalra A. Plant growth-promoting rhizobacteria enhance wheat salt and drought stress tolerance by altering endogenous phytohormone levels and TaCTR1/TaDREB2 expression. Physiol Plant. 2017;161(4):502–14. Epub 2017/08/09. doi: 10.1111/ppl.12614 28786221.

20. Vardharajula S, Ali SZ, Grover M, Reddy G, Bandi V. Drought-tolerant plant growth promoting Bacillus spp.: effect on growth, osmolytes, and antioxidant status of maize under drought stress. J Plant Interact. 2011;6(1):1–14. doi: 10.1080/17429145.2010.535178 WOS:000286491900001.

21. Naseem H, Bano A. Role of plant growth-promoting rhizobacteria and their exopolysaccharide in drought tolerance of maize. J Plant Interact. 2014;9(1):689–701. doi: 10.1080/17429145.2014.902125 WOS:000345150700050.

22. Mendes R, Kruijt M, de Bruijn I, Dekkers E, van der Voort M, Schneider JH, et al. Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science. 2011;332(6033):1097–100. Epub 2011/05/10. doi: 10.1126/science.1203980 21551032.

23. Dimkpa C, Weinand T, Asch F. Plant-rhizobacteria interactions alleviate abiotic stress conditions. Plant Cell Environ. 2009;32(12):1682–94. Epub 2009/08/13. doi: 10.1111/j.1365-3040.2009.02028.x 19671096.

24. Dodd IC, Zinovkina NY, Safronova VI, Belimov AA. Rhizobacterial mediation of plant hormone status. Ann Appl Biol. 2010;157(3):361–79. doi: 10.1111/j.1744-7348.2010.00439.x WOS:000283157700004.

25. Timmusk S, Abd El-Daim IA, Copolovici L, Tanilas T, Kannaste A, Behers L, et al. Drought-tolerance of wheat improved by rhizosphere bacteria from harsh environments: enhanced biomass production and reduced emissions of stress volatiles. PLoS One. 2014;9(5):e96086. Epub 2014/05/09. doi: 10.1371/journal.pone.0096086 24811199; PubMed Central PMCID: PMC4014485.

26. Yang J, Kloepper JW, Ryu CM. Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci. 2009;14(1):1–4. Epub 2008/12/06. doi: 10.1016/j.tplants.2008.10.004 19056309.

27. Chang WS, van de Mortel M, Nielsen L, Nino de Guzman G, Li X, Halverson LJ. Alginate production by Pseudomonas putida creates a hydrated microenvironment and contributes to biofilm architecture and stress tolerance under water-limiting conditions. J Bacteriol. 2007;189(22):8290–9. Epub 2007/07/03. doi: 10.1128/JB.00727-07 17601783; PubMed Central PMCID: PMC2168710.

28. Yan Y, Kuramae EE, de Hollander M, Klinkhamer PGL, van Veen JA. Functional traits dominate the diversity-related selection of bacterial communities in the rhizosphere. ISME J. 2017;11(1):56–66. doi: 10.1038/ismej.2016.108 27482928

29. Ngumbi E, Kloepper J. Bacterial-mediated drought tolerance: Current and future prospects. Appl Soil Ecol. 2016;105:109–25. doi: 10.1016/j.apsoil.2016.04.009 WOS:000377358300014.

30. Fitzpatrick CR, Copeland J, Wang PW, Guttman DS, Kotanen PM, Johnson MTJ. Assembly and ecological function of the root microbiome across angiosperm plant species. Proc Natl Acad Sci U S A. 2018;115(6):E1157–E65. doi: 10.1073/pnas.1717617115 29358405; PubMed Central PMCID: PMC5819437.

31. Xu L, Naylor D, Dong Z, Simmons T, Pierroz G, Hixson KK, et al. Drought delays development of the sorghum root microbiome and enriches for monoderm bacteria. Proc Natl Acad Sci U S A. 2018;115(18):E4284–E93. doi: 10.1073/pnas.1717308115 29666229; PubMed Central PMCID: PMC5939072.

32. Langille MG, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, et al. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol. 2013;31(9):814–21. Epub 2013/08/27. doi: 10.1038/nbt.2676 23975157; PubMed Central PMCID: PMC3819121.

33. Jochum MD. Enhanced Drought Tolerance through Plant Growth Promoting Rhizobacteria and Microbiome Engineering Applications. Texas A & M University. 2019:107.

Článek vyšel v časopise


2019 Číslo 12
Nejčtenější tento týden