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

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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.

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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.

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  1. Contributed equally to this work

Authors and Affiliations

  1. State Key Laboratory of Plant Genomics and National Center for Plant Gene Research, Institute of Genetics and Developmental Biology, The Innovative Academy of Seed Design, Chinese Academy of Sciences, Beijing, 100101, China

    Qingwen Chen, Ting Jiang, Yong-Xin Liu, Zhixi Liu, Xuemei Wang, Juan He, Yihua Ma, Fengxia Zhang, Yang Bai & Guodong Wang

  2. Key Laboratory of Synthetic Biology, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, 200032, China

    Haili Liu & Yong Wang

  3. Biosystematics Group, Wageningen University, 6708 PB, Arnhem, Wageningen, The Netherlands

    Tao Zhao & M. Eric Schranz

  4. CAS-JIC Centre of Excellence for Plant and Microbial Sciences (CEPAMS), Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, 100101, China

    Ting Jiang, Yong-Xin Liu & Yang Bai

  5. Max Planck Institute for Plant Breeding Research, Carl-von-Linné-Weg 10, 50829, Köln, Germany

    Xiangchao Gan

  6. Forschungszentrum Jülich, Plant Sciences (IBG-2) Wilhelm-Johnen-Straße, 52428, Jülich, Germany

    Asis Hallab

  7. China National Genebank-Shenzhen, the Beijing Genomics Institute (BGI-Shenzhen), Shenzhen, 518083, China

    Tao Jin

  8. College of Advanced Agricultural Sciences, University of Chinese Academy of Sciences, Beijing, 100039, China

    Qingwen Chen, Ting Jiang, Zhixi Liu, Xuemei Wang, Juan He, Yihua Ma, Yang Bai & Guodong Wang

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  1. Qingwen Chen
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Corresponding authors

Correspondence to Yang Bai or Guodong Wang.

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Supporting Information

Figure S1 Functional characterization of 16 plant sesterTPSs in E.coli system.

Figure S2 Terpene synthase assays of TPS18 and TPS18G328W analyzed by GC-MS.

Figure S3 Terpene synthase assays of TPS19 and TPS19G325W analyzed by GC-MS.

Figure S4 Terpene synthase assays of TPS25 and TPS25G328W analyzed by GC-MS.

Figure S5 Terpene synthase assays of TPS30 and TPS30P328W analyzed by GC-MS.

Figure S6 Characterization of TPS25 T-DNA insertion mutants.

Figure S7 Characterization of TPS30 T-DNA insertion mutant (tps30-1|CS805958).

Figure S8tps30-2 and tps30/tps25-1 double mutants generated via CRISPR/Cas9.

Figure S9tps30-3 and tps30/tps25-2 double mutants generated via CRISPR/Cas9.

Figure S10 Sesterterpene profiling in various tissues of Arabidopsis and different transgenic plants by GC-QQQ-MS.

Figure S11 Phenotypes of sesterTPS mutants and Col-0 when grown in natural soil (Changping farm in Beijing) under climate control conditions.

Figure S12 Sample diversity (α/β-diversity) measurements among each genotype.

Figure S13 Stack plot showing relative abundance distribution of the OTUs in phylum.

Figure S14 Taxonomic difference and overlap of specific differential OTUs between TPS mutants and Col-0.

Table S1 The MRM settings for four sesterterpene (C25) backbones analyzed by GC-QQQ-MS in this study

Table S2 The primers used in this study

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Chen, Q., Jiang, T., Liu, YX. et al. Recently duplicated sesterterpene (C25) gene clusters in Arabidopsis thaliana modulate root microbiota. Sci. China Life Sci. 62, 947–958 (2019). https://doi.org/10.1007/s11427-019-9521-2

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