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Phloroglucinol Derivatives in Plant-Beneficial Pseudomonas Spp

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Phloroglucinol Derivatives in Plant-Beneficial Pseudomonas Spp H OH metabolites OH Review Phloroglucinol Derivatives in Plant-Beneficial Pseudomonas spp.: Biosynthesis, Regulation, and Functions Adrien Biessy and Martin Filion * Agriculture and Agri-Food Canada, Saint-Jean-sur-Richelieu Research and Development Center, Saint-Jean-sur-Richelieu, QC J3B 7B5, Canada; [email protected] * Correspondence: martin.fi[email protected] Abstract: Plant-beneficial Pseudomonas spp. aggressively colonize the rhizosphere and produce nu- merous secondary metabolites, such as 2,4-diacetylphloroglucinol (DAPG). DAPG is a phloroglucinol derivative that contributes to disease suppression, thanks to its broad-spectrum antimicrobial activity. A famous example of this biocontrol activity has been previously described in the context of wheat monoculture where a decline in take-all disease (caused by the ascomycete Gaeumannomyces tritici) has been shown to be associated with rhizosphere colonization by DAPG-producing Pseudomonas spp. In this review, we discuss the biosynthesis and regulation of phloroglucinol derivatives in the genus Pseudomonas, as well as investigate the role played by DAPG-producing Pseudomonas spp. in natural soil suppressiveness. We also tackle the mode of action of phloroglucinol derivatives, which can act as antibiotics, signalling molecules and, in some cases, even as pathogenicity factors. Finally, we discuss the genetic and genomic diversity of DAPG-producing Pseudomonas spp. as well as its importance for improving the biocontrol of plant pathogens. Citation: Biessy, A.; Filion, M. Keywords: 2,4-diacetylphloroglucinol; DAPG; Pseudomonas; biocontrol; antibiotic Phloroglucinol Derivatives in Plant-Beneficial Pseudomonas spp.: Biosynthesis, Regulation, and Functions. Metabolites 2021, 11, 182. 1. Introduction https://doi.org/10.3390/ Phloroglucinol derivatives are a large class of secondary metabolites widely dis- metabo11030182 tributed in plants and brown algae. Over a thousand phloroglucinol derivatives have been characterized to date. As an example, 429 phloroglucinol derivatives have been Academic Editor: Shawn isolated from the genus Hypericum alone [1]. Phloroglucinol derivatives found in plants A. Christensen and brown algae have extremely diverse structures, ranging from the simple grandinol, an acylphloroglucinol produced by several Eucalyptus species, to the more complex phlorotan- Received: 12 February 2021 nins found in several families of brown algae [2,3]. These compounds often exhibit antiviral, Accepted: 17 March 2021 Published: 20 March 2021 antibacterial and antifungal activity [2]. Phloroglucinol derivatives are also produced by some microorganisms [2,4]. By contrast with the phloroglucinol derivatives found in plants Publisher’s Note: MDPI stays neutral and brown algae, phloroglucinol derivatives of microbial origin are rather simple. Some with regard to jurisdictional claims in Pseudomonas strains produce 2,4-diacetylphlorglucinol (DAPG) alongside its biosynthetic published maps and institutional affil- intermediates monoacetylphloroglucinol (MAPG) and phloroglucinol. iations. DAPG-producing Pseudomonas spp. have received particular attention due to their ability to control numerous soil-borne plant diseases, including take-all of wheat, tobacco black root rot and sugar beet damping-off [4,5]. These bacteria also play an important role in natural disease suppressiveness found in several soils across the world. Besides their presence in the rhizosphere, DAPG-producing Pseudomonas spp. are also known Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. to colonize various environment, including the phyllosphere [6], the skin surface of cer- This article is an open access article tain amphibians [7] and the surface of marine algae [8]. This review specifically covers distributed under the terms and rhizosphere-inhabiting DAPG-producing Pseudomonas spp. conditions of the Creative Commons Several reviews have been previously published on rhizosphere-inhabiting DAPG- Attribution (CC BY) license (https:// producing Pseudomonas spp. and their role in take-all decline [4,9]. In this review, we discuss creativecommons.org/licenses/by/ the biosynthesis and regulation of phloroglucinol derivatives in the genus Pseudomonas. 4.0/). Then, we tackle the role that DAPG-producing Pseudomonas spp. play in several soils Metabolites 2021, 11, 182. https://doi.org/10.3390/metabo11030182 https://www.mdpi.com/journal/metabolites Metabolites 2021, 11, x FOR PEER REVIEW 2 of 20 cuss the biosynthesis and regulation of phloroglucinol derivatives in the genus Pseudomo- nas. Then, we tackle the role that DAPG-producing Pseudomonas spp. play in several soils naturally suppressive to soil-borne plant diseases. We also discuss the mode of action of Metabolitesphloroglucinol2021, 11, 182 derivatives, which can act as antibiotics, signalling molecules and, in some2 of 19 cases, even as pathogenicity factors. Finally, we discuss the genetic and genomic diversity of DAPG-producing Pseudomonas spp. as well as its importance for improving the biocon- trol of plant pathogens.naturally suppressive to soil-borne plant diseases. We also discuss the mode of action of phloroglucinol derivatives, which can act as antibiotics, signalling molecules and, in 2. Genetics, Biochemistrysome cases,, and even Evolution as pathogenicity of DAPG factors. Biosynthesis Finally, we discuss the genetic and genomic diversity of DAPG-producing Pseudomonas spp. as well as its importance for improving 2.1. The Phl Biosyntheticthe biocontrol Gene Cluster of plant pathogens. Genes involved in DAPG biosynthesis were cloned several times from three different 2. Genetics, Biochemistry, and Evolution of DAPG Biosynthesis DAPG-producing Pseudomonas strains: Pseudomonas sp. Q2-87 [10,11], P. kilonensis F113 2.1. The Phl Biosynthetic Gene Cluster [12] and P. protegens CHA0 [13]. Further characterization of the genomic fragment isolated Genes involved in DAPG biosynthesis were cloned several times from three different from Pseudomonas DAPG-producingsp. Q2-87 led toPseudomonas the descriptionstrains: Pseudomonas of the so-sp.called Q2-87 phl [10 b,11iosynthetic], P. kilonensis geneF113 [12] cluster (BCG) [14].and SixP .genesprotegens wereCHA0 originally [13]. Further described: characterization four were of the found genomic to fragmentbe directly isolated involved in DAPGfrom biosynthesisPseudomonas (phlABCDsp. Q2-87) led and to thethe description two others of thewere so-called shownphl tobiosynthetic encode a gene putative permeasecluster (phlE) (BCG) and [a14 TetR]. Six genesregulatory were originally protein described:(phlF). Three four wereother found genes to bewere directly involved in DAPG biosynthesis (phlABCD) and the two others were shown to encode a later discovered andputative associated permease with (phlE the) andBCG: a TetR phlG regulatory, which encodes protein (phlF a hydrolase). Three other involved genes were in DAPG degradationlater [15] discovered, phlH, and which associated encodes with another the BCG: TetRphlG, regulatory which encodes protein a hydrolase [15] involvedand phlI, which encodesin an DAPG uncharacterized degradation [15 protein], phlH, which[16,17] encodes. The organization another TetR regulatory of the phl protein BCG [15] is conserved in all DAPGand phlI-,producing which encodes Pseudomonas an uncharacterized spp. sequence protein [d16 to,17 date]. The [18] organization. The biosyn- of the phl BCG is conserved in all DAPG-producing Pseudomonas spp. sequenced to date [18]. The thetic cluster and the current understanding of the DAPG biosynthesis pathway are pre- biosynthetic cluster and the current understanding of the DAPG biosynthesis pathway are sented in Figure 1.presented in Figure1. FigureFigure 1. Organization 1. Organization of the 2,4-DAPG of the 2,4 biosynthetic-DAPG biosynthetic cluster and current cluster understanding and current of the understanding biosynthesis scheme. of the (A ) Or- phl Pseudomonas ganizationbiosynthesis of the scheme.biosynthetic (A) gene Organization cluster found of in the DAPG-producing phl biosynthetic gene clusterspp. (B) found Current in understanding DAPG-produc- of the biosynthesis and degradation of DAPG in the genus Pseudomonas. MAPG ATase is an enzyme multiplex composed of PhlA, ing Pseudomonas spp. (B) Current understanding of the biosynthesis and degradation of DAPG in PhlB and PhlC units. Abbreviations are as follows: MAPG, monoacetylphloroglucinol; DAPG, 2,4-diacetylphloroglucinol. the genus Pseudomonas. MAPG ATase is an enzyme multiplex composed of PhlA, PhlB and PhlC units. Abbreviations 2.2.are Biosynthesisas follows: andMAPG, Degradation monoacetylphloroglucinol; of DAPG DAPG, 2,4-diace- tylphloroglucinol. The first step in the biosynthesis of DAPG is catalysed by the type III polyketide synthase (PKS) PhlD [14,19]. Type III PKSs are homodimeric enzymes that catalyse the 2.2. Biosynthesis anditerative Degradation condensation of DAPG of a starter substrate (usually an acyl-CoA) with several extender sub- The first step in the biosynthesis of DAPG is catalysed by the type III polyketide syn- thase (PKS) PhlD [14,19]. Type III PKSs are homodimeric enzymes that catalyse the itera- Metabolites 2021, 11, 182 3 of 19 strate units (usually malonyl-CoA) to generate a linear polyketide, which is subsequently cyclized [20]. Bangera and Thomashow [14] proposed that PhlD uses acetoacetyl-CoA as the starter substrate to produce monoacetylphloroglucinol (MAPG), but it was later showed that PhlD produces phloroglucinol from malonyl-CoA instead
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