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MYB72-Dependent Coumarin Exudation Shapes Root Microbiome Assembly to Promote Plant Health

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MYB72-Dependent Coumarin Exudation Shapes Root Microbiome Assembly to Promote Plant Health MYB72-dependent coumarin exudation shapes root microbiome assembly to promote plant health Ioannis A. Stringlisa,1,KeYua,1, Kirstin Feussnerb,1, Ronnie de Jongea,c,d, Sietske Van Bentuma, Marcel C. Van Verka, Roeland L. Berendsena, Peter A. H. M. Bakkera, Ivo Feussnerb,e, and Corné M. J. Pietersea,2 aPlant–Microbe Interactions, Department of Biology, Science4Life, Utrecht University, 3508 TB Utrecht, The Netherlands; bDepartment of Plant Biochemistry, Albrecht-von-Haller-Institute for Plant Sciences, University of Göttingen, 37077 Göttingen, Germany; cDepartment of Plant Systems Biology, Vlaams Instituut voor Biotechnologie, 9052 Ghent, Belgium; dDepartment of Plant Biotechnology and Bioinformatics, Ghent University, 9052 Ghent, Belgium; and eDepartment of Plant Biochemistry, Göttingen Center for Molecular Biosciences, University of Göttingen, 37077 Göttingen, Germany Edited by Jeffery L. Dangl, University of North Carolina at Chapel Hill, Chapel Hill, NC, and approved April 3, 2018 (received for review December 22, 2017) Plant roots nurture a tremendous diversity of microbes via exudation of leaves do not display abundant transcriptional changes (9). photosynthetically fixed carbon sources. In turn, probiotic members of However, upon pathogen or insect attack, ISR-expressing leaves the root microbiome promote plant growth and protect the host plant develop an accelerated, primed defense response that is associated against pathogens and pests. In the Arabidopsis thaliana–Pseudomonas with enhanced resistance (9–11). In contrast to foliar tissues, simiae WCS417 model system the root-specific transcription factor WCS417-colonized roots show abundant transcriptional changes MYB72 and the MYB72-controlled β-glucosidase BGLU42 emerged as (9, 11–13). Among the WCS417-induced genes, the root-specific important regulators of beneficial rhizobacteria-induced systemic resis- R2R3-type MYB transcription factor gene MYB72 emerged as a tance (ISR) and iron-uptake responses. MYB72 regulates the biosynthe- central regulator of the onset of ISR (9, 14). MYB72 is also in- sis of iron-mobilizing fluorescent phenolic compounds, after which duced in Arabidopsis roots in response to colonization by the ISR- BGLU42 activity is required for their excretion into the rhizosphere. inducing fungi Trichoderma asperellum T-34 and Trichoderma Metabolite fingerprinting revealed the antimicrobial coumarin scopole- harzianum T-78 (15). myb72-knockout mutants are unable to mount tin as a dominant metabolite that is produced in the roots and excreted ISR upon colonization of the roots by WCS417 or T. asperellum T-34 into the rhizosphere in a MYB72- and BGLU42-dependent manner. (14, 16), suggesting that MYB72 plays a central role in the regulation Shotgun-metagenome sequencing of root-associated microbiota of ISR triggered by different root-associated beneficial microbes. PLANT BIOLOGY of Col-0, myb72, and the scopoletin biosynthesis mutant f6′h1 Downstream of MYB72 action, the β-glucosidase BGLU42 was showed that scopoletin selectively impacts the assembly of the identified as an important player in the onset of ISR (12). Consti- microbial community in the rhizosphere. We show that scopoletin tutive overexpression of BGLU42 resulted in enhanced systemic Fusarium selectively inhibits the soil-borne fungal pathogens disease resistance against Botrytis cinerea, Pseudomonas syringae,and oxysporum Verticillium dahliae and , while the growth-promoting Hyaloperonospora arabidopsidis, while the ability of mutant bglu42 P. simiae Pseudomonas and ISR-inducing rhizobacteria WCS417 and to mount WCS417-ISR was blocked. capeferrum WCS358 are highly tolerant of the antimicrobial effect of scopoletin. Collectively, our results demonstrate a role for couma- Significance rins in microbiome assembly and point to a scenario in which plants and probiotic rhizobacteria join forces to trigger MYB72/BGLU42- dependent scopolin production and scopoletin excretion, resulting Plant roots nurture a large diversity of soil microbes via exudation in improved niche establishment for the microbial partner and growth of chemical compounds into the rhizosphere. In turn, beneficial and immunity benefits for the host plant. root microbiota promote plant growth and immunity. The root- specific transcription factor MYB72 has emerged as a central root metabolome | coumarin | induced systemic resistance | regulator in this process. Here, we show that MYB72 regulates the iron-deficiency response | microbiome assembly excretion of the coumarin scopoletin, an iron-mobilizing phenolic compound with selective antimicrobial activity that shapes the root-associated microbial community. Selected soil-borne fungal lant roots exude a significant proportion of their photosyn- pathogens appeared to be highly sensitive to the antimicrobial Pthetically fixed carbon into the rhizosphere (1). As a result, activity of scopoletin, while two MYB72-inducing beneficial rhi- the rhizosphere nurtures one of the richest microbial ecosystems zobacteria were tolerant. Our results suggest that probiotic root- on Earth. The microbial community that inhabits the root–soil 11 associated microbes that activate the iron-deficiency response interface contains up to 10 microbial cells per gram of root and during colonization stimulate MYB72-dependent excretion of collectively represents the root microbiome (2, 3). Root exudates scopoletin, thereby potentially improving their niche establish- greatly influence the composition of the root microbiome, a ment and enhancing plant growth and protection. phenomenon called the “rhizosphere effect” (2, 4). Besides det- rimental pathogens, the root microbiome also harbors beneficial Author contributions: I.A.S., K.Y., K.F., M.C.V.V., R.L.B., P.A.H.M.B., I.F., and C.M.J.P. de- members that promote plant growth or stimulate plant health signed research; I.A.S., K.Y., K.F., and S.V.B. performed research; I.A.S., K.Y., K.F., and (2, 5). Such mutualistic microbes serve plants in acquiring water R.d.J. analyzed data; and I.A.S. and C.M.J.P. wrote the paper. and nutrients, fixing nitrogen, suppressing soil-borne pathogens, The authors declare no conflict of interest. or stimulating plant immunity (2, 4). This article is a PNAS Direct Submission. Selected plant growth-promoting rhizobacteria (PGPR) can This open access article is distributed under Creative Commons Attribution-NonCommercial- NoDerivatives License 4.0 (CC BY-NC-ND). trigger an induced systemic resistance (ISR) that is effective Data deposition: The data reported in this article have been deposited in the National against a broad range of foliar pathogens and even insect herbi- Center for Biotechnology Information Short Read Archive BioProject database (BioProject vores (6). ISR is well studied in the interaction between Arabi- ID: PRJNA435676). dopsis thaliana and the PGPR Pseudomonas simiae WCS417 (7). 1I.A.S., K.Y., and K.F. contributed equally to this work. WCS417-ISR in Arabidopsis functions independently of the de- 2To whom correspondence should be addressed. Email: [email protected]. fense hormone salicylic acid (SA) but instead requires a functional This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. response to the plant hormones ethylene and jasmonic acid (JA) 1073/pnas.1722335115/-/DCSupplemental. (6, 8). In the absence of a pathogen, WCS417-ISR–expressing www.pnas.org/cgi/doi/10.1073/pnas.1722335115 PNAS Latest Articles | 1of10 Downloaded by guest on September 24, 2021 Besides being essential for the onset of ISR, MYB72 emerged selectively inhibits the growth of two soil-borne fungal pathogens as an integral part of the plant’s adaptive strategy to iron de- in vitro but has little or no effect on the growth of two beneficial ficiency. Together with its closest paralog, MYB10, MYB72 is ISR-inducing rhizobacteria. Collectively, our results suggest that essential for plant survival in alkaline soils where iron availability the MYB72–BGLU42–mediated production and excretion of is largely restricted (17). Under iron-limiting conditions, MYB72 scopoletin favors the interaction between plant roots and pro- is strongly induced in the roots of Arabidopsis as part of a set of biotic members of the root microbiome. coordinated responses that boost iron mobilization and uptake from the soil environment (collectively referred to as the Results “strategy I iron-deficiency response”) (18, 19). The core of this Metabolite Fingerprinting of Root Exudates. In Arabidopsis roots response consists of rhizosphere acidification by the activity of MYB72 and BGLU42 are both required for the onset of + the H -ATPase AHA2 (20), which increases the concentration rhizobacteria-mediated ISR. Moreover, MYB72 is required for + + of soluble ferric iron (Fe3 ). Fe3 is subsequently reduced to the biosynthesis of iron-mobilizing fluorescent phenolic com- + ferrous iron (Fe2 ) by FERRIC REDUCTION OXIDASE2 pounds, while BGLU42 has a role in their subsequent excretion (FRO2), after which it is transported from the soil environment into the rhizosphere (12). Under iron-starvation conditions, Col- into root cells via IRON-REGULATED TRANSPORTER1 0 roots exuded high quantities of fluorescent phenolic com- (IRT1) (21, 22). The basic helix–loop–helix (bHLH) transcription pounds (Fig. 1A) and activated the iron-deficiency marker genes factor FIT (FER-LIKE IRON DEFICIENCY TRANSCRIPTION FRO2, IRT1, MYB72, and F6′H1 (Fig. 1B). The mutant myb72 FACTOR) is a central regulator of the iron-uptake response (19) did not exude detectable
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