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Recently duplicated sesterterpene (C25) gene clusters in Arabidopsis thaliana modulate root microbiota

  • Qingwen Chen
  • Ting Jiang
  • Yong-Xin Liu
  • Haili Liu
  • Tao Zhao
  • Zhixi Liu
  • Xiangchao Gan
  • Asis Hallab
  • Xuemei Wang
  • Juan He
  • Yihua Ma
  • Fengxia Zhang
  • Tao Jin
  • M. Eric Schranz
  • Yong Wang
  • Yang BaiEmail author
  • Guodong WangEmail author
Research Paper

Abstract

Land plants co-speciate with a diversity of continually expanding plant specialized metabolites (PSMs) and root microbial communities (microbiota). Homeostatic interactions between plants and root microbiota are essential for plant survival in natural environments. A growing appreciation of microbiota for plant health is fuelling rapid advances in genetic mechanisms of controlling microbiota by host plants. PSMs have long been proposed to mediate plant and single microbe interactions. However, the effects of PSMs, especially those evolutionarily new PSMs, on root microbiota at community level remain to be elucidated. Here, we discovered sesterterpenes in Arabidopsis thaliana, produced by recently duplicated prenyltransferase-terpene synthase (PT-TPS) gene clusters, with neo-functionalization. A single-residue substitution played a critical role in the acquisition of sesterterpene synthase (sesterTPS) activity in Brassicaceae plants. Moreover, we found that the absence of two root-specific sesterterpenoids, with similar chemical structure, significantly affected root microbiota assembly in similar patterns. Our results not only demonstrate the sensitivity of plant microbiota to PSMs but also establish a complete framework of host plants to control root microbiota composition through evolutionarily dynamic PSMs.

En

plant specialized metabolites microbiota sesterterpene terpene synthase 

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Notes

Acknowledgements

This work was supported by the Priority Research Program of the Chinese Academy of Sciences (ZDRW-ZS-2019-2 and QYZDB-SSW-SMC021), the Strategic Priority Research Program of the Chinese Academy of Sciences (XDA08000000 and XDB11020700), the National Program on Key Basic Research Projects (2013CB127000), and the State Key Laboratory of Plant Genomics of China (2016A0219-11 and SKLPG2013A0125-5). We thank Dr. Jay D Keasling (University of California, Berkeley) for providing the pMBIS plasmid.

Supplementary material

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Supplementary material, approximately 2.44 MB

References

  1. Aubourg, S., Lecharny, A., and Bohlmann, J. (2002). Genomic analysis of the terpenoid synthase (AtTPS) gene family of Arabidopsis thaliana. Mol Genets Genom 267, 730–745.CrossRefGoogle Scholar
  2. Benjamini, Y., and Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. J R Statist Soc-Ser B 57, 289–300.Google Scholar
  3. Berendsen, R.L., Pieterse, C.M.J., and Bakker, P.A.H.M. (2012). The rhizosphere microbiome and plant health. Trends Plant Sci 17, 478–486.CrossRefGoogle Scholar
  4. Bulgarelli, D., Rott, M., Schlaeppi, K., Ver Loren van Themaat, E., Ahmadinejad, N., Assenza, F., Rauf, P., Huettel, B., Reinhardt, R., Schmelzer, E., et al. (2012). Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488, 91–95.CrossRefGoogle Scholar
  5. Caporaso, J.G., Bittinger, K., Bushman, F.D., DeSantis, T.Z., Andersen, G. L., and Knight, R. (2010a). PyNAST: A flexible tool for aligning sequences to a template alignment. Bioinformatics 26, 266–267.CrossRefGoogle Scholar
  6. Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D., Costello, E.K., Fierer, N., Peña, A.G., Goodrich, J.K., Gordon, J.I., et al. (2010b). QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7, 335–336.CrossRefGoogle Scholar
  7. Castrillo, G., Teixeira, P.J.P.L., Paredes, S.H., Law, T.F., de Lorenzo, L., Feltcher, M.E., Finkel, O.M., Breakfield, N.W., Mieczkowski, P., Jones, C.D., et al. (2017). Root microbiota drive direct integration of phosphate stress and immunity. Nature 543, 513–518.CrossRefGoogle Scholar
  8. Chen, F., Tholl, D., Bohlmann, J., and Pichersky, E. (2011). The family of terpene synthases in plants: A mid-size family of genes for specialized metabolism that is highly diversified throughout the kingdom. Plant J 66, 212–229.CrossRefGoogle Scholar
  9. Chen, H., and Boutros, P.C. (2011). VennDiagram: A package for the generation of highly-customizable Venn and Euler diagrams in R. BMC Bioinf 12, 35.CrossRefGoogle Scholar
  10. Chen, Q., Fan, D., and Wang, G. (2015). Heteromeric geranyl (geranyl) diphosphate synthase is involved in monoterpene biosynthesis in Arabidopsis flowers. Mol Plant 8, 1434–1437.CrossRefGoogle Scholar
  11. Christianson, D.W. (2017). Structural and chemical biology of terpenoid cyclases. Chem Rev 117, 11570–11648.CrossRefGoogle Scholar
  12. DeSantis, T.Z., Hugenholtz, P., Larsen, N., Rojas, M., Brodie, E.L., Keller, K., Huber, T., Dalevi, D., Hu, P., and Andersen, G.L. (2006). Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72, 5069–5072.CrossRefGoogle Scholar
  13. Edgar, R.C. (2010). Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460–2461.CrossRefGoogle Scholar
  14. Edgar, R.C. (2013). UPARSE: Highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10, 996–998.CrossRefGoogle Scholar
  15. Edgar, R.C., Haas, B.J., Clemente, J.C., Quince, C., and Knight, R. (2011). UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27, 2194–2200.CrossRefGoogle Scholar
  16. Foster, K.R., Schluter, J., Coyte, K.Z., and Rakoff-Nahoum, S. (2017). The evolution of the host microbiome as an ecosystem on a leash. Nature 548, 43–51.CrossRefGoogle Scholar
  17. Gan, X., Hay, A., Kwantes, M., Haberer, G., Hallab, A., Ioio, R.D., Hofhuis, H., Pieper, B., Cartolano, M., Neumann, U., et al. (2016). The Cardamine hirsuta genome offers insight into the evolution of morphological diversity. Nat Plants 2, 16167.CrossRefGoogle Scholar
  18. Hartmann, T. (2007). From waste products to ecochemicals: Fifty years research of plant secondary metabolism. Phytochemistry 68, 2831–2846.CrossRefGoogle Scholar
  19. Huang, A.C., Kautsar, S.A., Hong, Y.J., Medema, M.H., Bond, A.D., Tantillo, D.J., and Osbourn, A. (2017). Unearthing a sesterterpene biosynthetic repertoire in the Brassicaceae through genome mining reveals convergent evolution. Proc Natl Acad Sci USA 114, E6005–E6014.CrossRefGoogle Scholar
  20. Kampranis, S.C., Ioannidis, D., Purvis, A., Mahrez, W., Ninga, E., Katerelos, N.A., Anssour, S., Dunwell, J.M., Degenhardt, J., Makris, A. M., et al. (2007). Rational conversion of substrate and product specificity in a Salvia monoterpene synthase: Structural insights into the evolution of terpene synthase function. Plant Cell 19, 1994–2005.CrossRefGoogle Scholar
  21. Katoh, K., Misawa, K., and Kuma, K.I. (2002). MAFFT: A novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucl Acids Res 30, 3059–3066.CrossRefGoogle Scholar
  22. Kliebenstein, D.J., and Osbourn, A. (2012). Making new molecules—Evolution of pathways for novel metabolites in plants. Curr Opin Plant Biol 15, 415–423.CrossRefGoogle Scholar
  23. Leach, J.E., Triplett, L.R., Argueso, C.T., and Trivedi, P. (2017). Communication in the phytobiome. Cell 169, 587–596.CrossRefGoogle Scholar
  24. Lebeis, S.L., Paredes, S.H., Lundberg, D.S., Breakfield, N., Gehring, J., McDonald, M., Malfatti, S., Glavina del Rio, T., Jones, C.D., Tringe, S. G., et al. (2015). Salicylic acid modulates colonization of the root microbiome by specific bacterial taxa. Science 349, 860–864.CrossRefGoogle Scholar
  25. Li, W., Zhang, F., Chang, Y., Zhao, T., Schranz, M.E., and Wang, G. (2015). Nicotinate O-glucosylation is an evolutionarily metabolic trait important for seed germination under stress conditions in Arabidopsis thaliana. Plant Cell 21, 1907–1924.CrossRefGoogle Scholar
  26. Lundberg, D.S., Lebeis, S.L., Paredes, S.H., Yourstone, S., Gehring, J., Malfatti, S., Tremblay, J., Engelbrektson, A., Kunin, V., Del Rio, T.G., et al. (2012). Defining the core Arabidopsis thaliana root microbiome. Nature 488, 86–90.CrossRefGoogle Scholar
  27. Müller, D.B., Vogel, C., Bai, Y., and Vorholt, J.A. (2016). The plant microbiota: Systems-level insights and perspectives. Annu Rev Genet 50, 211–234.CrossRefGoogle Scholar
  28. Murrell, B., Wertheim, J.O., Moola, S., Weighill, T., Scheffler, K., and Kosakovsky Pond, S.L. (2012). Detecting individual sites subject to episodic diversifying selection. PLoS Genet 8, e1002764.CrossRefGoogle Scholar
  29. Robinson, M.D., McCarthy, D.J., and Smyth, G.K. (2010). edgeR: A bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139–140.CrossRefGoogle Scholar
  30. Schlaeppi, K., Dombrowski, N., Oter, R.G., Ver Loren van Themaat, E., and Schulze-Lefert, P. (2014). Quantitative divergence of the bacterial root microbiota in Arabidopsis thaliana relatives. Proc Natl Acad Sci USA 111, 585–592.CrossRefGoogle Scholar
  31. Shao, J., Chen, Q.W., Lv, H.J., He, J., Liu, Z.F., Lu, Y.N., Liu, H.L., Wang, G.D., and Wang, Y. (2011). (+)-Thalianatriene and (-)-retigeranin B catalyzed by sesterterpene synthases from Arabidopsis thaliana. Org Lett 19, 1816–1819.CrossRefGoogle Scholar
  32. Srividya, N., Davis, E.M., Croteau, R.B., and Markus Lange, B. (2015). Functional analysis of (4S)-limonene synthase mutants reveals determinants of catalytic outcome in a model monoterpene synthase. Proc Natl Acad Sci USA 112, 3332–3337.CrossRefGoogle Scholar
  33. Starks, C.M., Back, K., and Chappell, J. (1997). Structural basis for cyclic terpene biosynthesis by tobacco 5-epi-aristolochene synthase. Science 277, 1815–1820.CrossRefGoogle Scholar
  34. Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S. (2013). MEGA6: Molecular evolutionary genetics analysis Version 6.0. Mol Biol Evol 30, 2725–2729.CrossRefGoogle Scholar
  35. Tholl, D., and Lee, S. (2011). Terpene specialized metabolism in Arabidopsis thaliana. Arabidopsis Book 9, e0143.CrossRefGoogle Scholar
  36. van Dam, N.M., and Bouwmeester, H.J. (2016). Metabolomics in the rhizosphere: Tapping into belowground chemical communication. Trends Plant Sci 21, 256–265.CrossRefGoogle Scholar
  37. Verbon, E.H., and Liberman, L.M. (2016). Beneficial microbes affect endogenous mechanisms controlling root development. Trends Plant Sci 21, 218–229.CrossRefGoogle Scholar
  38. Vickers, C.E., Bongers, M., Liu, Q., Delatte, T., and Bouwmeester, H. (2014). Metabolic engineering of volatile isoprenoids in plants and microbes. Plant Cell Environ 37, 1753–1775.CrossRefGoogle Scholar
  39. Wang, C., Chen, Q., Fan, D., Li, J., Wang, G., and Zhang, P. (2016). Structural analyses of short-chain prenyltransferases identify an evolutionarily conserved GFPPS clade in Brassicaceae plants. Mol Plant 9, 195–204.CrossRefGoogle Scholar
  40. Wang, G., Tian, L., Aziz, N., Broun, P., Dai, X., He, J., King, A., Zhao, P. X., and Dixon, R.A. (2008). Terpene biosynthesis in glandular trichomes of hop. Plant Physiol 148, 1254–1266.CrossRefGoogle Scholar
  41. Wang, Q., Garrity, G.M., Tiedje, J.M., and Cole, J.R. (2007). Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ MicroBiol 73, 5261–5267.CrossRefGoogle Scholar
  42. Xu, H., Zhang, F., Liu, B., Huhman, D.V., Sumner, L.W., Dixon, R.A., and Wang, G. (2013). Characterization of the formation of branched short-chain fatty acid: CoAs for bitter acid biosynthesis in hop glandular trichomes. Mol Plant 6, 1301–1317.CrossRefGoogle Scholar
  43. Zhang, J., Zhang, N., Liu, Y.X., Zhang, X., Hu, B., Qin, Y., Xu, H., Wang, H., Guo, X., Qian, J., et al. (2018). Root microbiota shift in rice correlates with resident time in the field and developmental stage. Sci China Life Sci 61, 613–621.CrossRefGoogle Scholar
  44. Zhao, T., Holmer, R., de Bruijn, S., Angenent, G.C., van den Burg, H.A., and Schranz, M.E. (2011). Phylogenomic synteny network analysis of MADS-box transcription factor genes reveals lineage-specific transpositions, ancient tandem duplications, and deep positional conservation. Plant Cell 29, 1278–1292.Google Scholar

Copyright information

© Science China Press and Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Qingwen Chen
    • 1
    • 8
  • Ting Jiang
    • 1
    • 4
    • 8
  • Yong-Xin Liu
    • 1
    • 4
  • Haili Liu
    • 2
  • Tao Zhao
    • 3
  • Zhixi Liu
    • 1
    • 8
  • Xiangchao Gan
    • 5
  • Asis Hallab
    • 6
  • Xuemei Wang
    • 1
    • 8
  • Juan He
    • 1
    • 8
  • Yihua Ma
    • 1
    • 8
  • Fengxia Zhang
    • 1
  • Tao Jin
    • 7
  • M. Eric Schranz
    • 3
  • Yong Wang
    • 2
  • Yang Bai
    • 1
    • 4
    • 8
    Email author
  • Guodong Wang
    • 1
    • 8
    Email author
  1. 1.State Key Laboratory of Plant Genomics and National Center for Plant Gene Research, Institute of Genetics and Developmental BiologyThe Innovative Academy of Seed Design, Chinese Academy of SciencesBeijingChina
  2. 2.Key Laboratory of Synthetic Biology, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological SciencesChinese Academy of SciencesShanghaiChina
  3. 3.Biosystematics GroupWageningen UniversityArnhem, WageningenThe Netherlands
  4. 4.CAS-JIC Centre of Excellence for Plant and Microbial Sciences (CEPAMS), Institute of Genetics and Developmental BiologyChinese Academy of SciencesBeijingChina
  5. 5.Max Planck Institute for Plant Breeding ResearchKölnGermany
  6. 6.Forschungszentrum Jülich, Plant Sciences (IBG-2) Wilhelm-Johnen-StraßeJülichGermany
  7. 7.China National Genebank-Shenzhenthe Beijing Genomics Institute (BGI-Shenzhen)ShenzhenChina
  8. 8.College of Advanced Agricultural SciencesUniversity of Chinese Academy of SciencesBeijingChina

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