Possibility of Bacterial Recruitment of Plant Genes Associated with the Biosynthesis of Secondary Metabolites

Bode, Helge B.; Müller, Rolf

doi:10.1104/pp.102.019760

Cited by 46 publications

(39 citation statements)

References 56 publications

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“…A reciprocal horizontal exchange of genetic information between the plant material and microorganisms seems to have been occurring continuously and the possibility that the pathways of phytohormone biosynthesis in green plants are of prokaryotic origin cannot be ruled out. As pointed out by Bode and Müller (2003), in contrast to the generally accepted hypothesis, several plant-specific metabolic pathways have in recent years also been found in prokaryotes. For instance cellulase synthase in vascular plants has been suggested to been transferred from cyanobacteria to plants (Nobles et al, 2001).…”

Section: Conclusion and Future Perspectivesmentioning

confidence: 88%

“…Several observations indicate that a reciprocal horizontal exchange of genes has been occurring between the plant material and microorganisms and therefore microbial origin of phytohormone synthesis genes cannot be ruled out (Johri, 2004). First of all, many microorganisms grow in close association with plant material and this would enhance chances of DNA uptake (Bode and Müller, 2003). While discussing the origin of land plants, Pirozynski and Mallloch (1975) concluded "land plants never had an independence (from fungi); for if they had they could never have colonized land" (italics intentional by Johri for emphasis).…”

Section: Were the Pathways For The Biosynthesis Of Phytohormones In Gmentioning

confidence: 99%

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Hormonal regulation in green plant lineage families

Johri

2008

Physiol Mol Biol Plants

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The patterns of phytohormones distribution, their native function and possible origin of hormonal regulation across the green plant lineages (chlorophytes, charophytes, bryophytes and tracheophytes) are discussed. The five classical phytohormonesauxins, cytokinins, gibberellins (GA), abscisic acid (ABA) and ethylene occur ubiquitously in green plants. They are produced as secondary metabolites by microorganisms. Some of the bacterial species use phytohormones to interact with the plant as a part of their colonization strategy. Phytohormone biosynthetic pathways in plants seem to be of microbial origin and furthermore, the origin of high affinity perception mechanism could have preceded the recruitment of a metabolite as a hormone. The bryophytes represent the earliest land plants which respond to the phytohormones with the exception of gibberellins. The regulation by auxin and ABA may have evolved before the separation of green algal lineage. Auxin enhances rhizoid and caulonemal differentiation while cytokinins enhance shoot bud formation in mosses. Ethylene retards cell division but seems to promote cell elongation. The presence of responses specific to cytokinins and ethylene strongly suggest the origin of their regulation in bryophytes. The hormonal role of GAs could have evolved in some of the ferns where antheridiogens (compounds related to GAs) and GAs themselves regulate the formation of antheridia.During migration of life forms to land, the tolerance to desiccation may have evolved and is now observed in some of the microorganisms, animals and plants. Besides plants, sequences coding for late embryogenesis abundant-like proteins occur in the genomes of other anhydrobiotic species of microorganisms and nematodes. ABA acts as a stress signal and increases rapidly upon desiccation or in response to some of the abiotic stresses in green plants. As the salt stress also increases ABA release in the culture medium of cyanobacterium Trichormus variabilis, the recruitment of ABA in the regulation of stress responses could have been derived from prokaryotes and present at the level of common ancestor of green plants. The overall hormonal action mechanisms in mosses are remarkably similar to that of the higher plants. As plants are thought to be monophyletic in origin, the existence of remarkably similar hormonal mechanisms in the mosses and higher plants, suggests that some of the basic elements of regulation cascade could have also evolved at the level of common ancestor of plants. The networking of various steps in a cascade or the crosstalk between different cascades is variable and reflects the dynamic interaction between a species and its specific environment.

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Section: Conclusion and Future Perspectivesmentioning

confidence: 88%

Section: Were the Pathways For The Biosynthesis Of Phytohormones In Gmentioning

confidence: 99%

Hormonal regulation in green plant lineage families

Johri

2008

Physiol Mol Biol Plants

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“…The key biosynthetic gene is phlD, which displays interesting similarity to genes for plant chalcone synthases. This type III polyketide synthase is unusual in prokaryotes, and it was suggested that the gene may have been acquired by horizontal gene transfer (5,6,12). In contrast, phylogenetic analysis of phlD does not support this theory, so the provenance of 2,4-DAPG production remains uncertain (52,53).…”

mentioning

confidence: 89%

Evolutionary History of the phl Gene Cluster in the Plant-Associated Bacterium Pseudomonas fluorescens

Moynihan

Morrissey

Coppoolse

et al. 2009

Appl Environ Microbiol

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Pseudomonas fluorescens is of agricultural and economic importance as a biological control agent largely because of its plant association and production of secondary metabolites, in particular 2,4-diacetylphloroglucinol (2,4-DAPG). This polyketide, which is encoded by the eight-gene phl cluster, has antimicrobial effects on phytopathogens, promotes amino acid exudation from plant roots, and induces systemic resistance in plants. Despite its importance, 2,4-DAPG production is limited to a subset of P. fluorescens strains. Determination of the evolution of the phl cluster and understanding the selective pressures promoting its retention or loss in lineages of P. fluorescens will help in the development of P. fluorescens as a viable and effective inoculant for application in agriculture. In this study, genomic and sequence-based approaches were integrated to reconstruct the phylogeny of P. fluorescens and the phl cluster. It was determined that 2,4-DAPG production is an ancestral trait in the species P. fluorescens but that most lineages have lost this capacity through evolution. Furthermore, intragenomic recombination has relocated the phl cluster within the P. fluorescens genome at least three times, but the integrity of the cluster has always been maintained. The possible evolutionary and functional implications for retention of the phl cluster and 2,4-DAPG production in some lineages of P. fluorescens are discussed.

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“…Gene sce1440, encoding a terpene cyclase, has substantial similarity to genes in other bacteria that are involved in biosynthesis of geosmin 29,30 , a sesquiterpene-derived natural product that gives soil its characteristic smell. The genome also encodes an unusual L-dopa decarboxylase 31 and two type III PKSs; a gene encoding one of the PKSs, sce2133, shows similarity to bacterial RppA-encoding genes (61% identity) 32 . Although the compound has not yet been isolated from S. cellulosum So ce56, expression of sce2133 in Pseudomonas putida resulted in biosynthesis of flaviolin 33 , supporting the utility of heterologous hosts for identifying the products of cryptic myxobacterial clusters and dissecting gene function.…”

Section: Secondary Metabolism and Biotechnological Potentialmentioning

confidence: 99%

Complete genome sequence of the myxobacterium Sorangium cellulosum

et al. 2007

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The genus Sorangium synthesizes approximately half of the secondary metabolites isolated from myxobacteria, including the anti-cancer metabolite epothilone. We report the complete genome sequence of the model Sorangium strain S. cellulosum So ce56, which produces several natural products and has morphological and physiological properties typical of the genus. The circular genome, comprising 13,033,779 base pairs, is the largest bacterial genome sequenced to date. No global synteny with the genome of Myxococcus xanthus is apparent, revealing an unanticipated level of divergence between these myxobacteria. A large percentage of the genome is devoted to regulation, particularly post-translational phosphorylation, which probably supports the strain's complex, social lifestyle. This regulatory network includes the highest number of eukaryotic protein kinase-like kinases discovered in any organism. Seventeen secondary metabolite loci are encoded in the genome, as well as many enzymes with potential utility in industry.Natural products and their derivatives provide the basis for medicines targeting a wide range of human diseases. The Gram-negative myxobacteria, members of the d-subgroup of proteobacteria, are an important source of novel classes of secondary metabolites 1 . Of these, the genus Sorangium is particularly valuable, as 46% of metabolites isolated from myxobacteria 1 , including the potent antitumor compound epothilone 2 , derive from this group. The majority of myxobacterial metabolites are polyketides, nonribosomal polypeptides or hybrids of the two structures, many of which are synthesized on gigantic molecular assembly lines composed of polyketide synthase (PKS) and nonribosomal polypeptide synthetase (NRPS) multienzymes 3 . Sorangium strains exhibit additional characteristic features, including 'social behavior' , cell movement by gliding, biofilm formation and morphological differentiation culminating in complex multicellular structures called fruiting bodies 4 . Three myxobacterial suborders are known 5 and the availability of the genome sequence of Myxococcus xanthus (Cystobacterineae) 6 enables comparative analysis with the Sorangium cellulosum (Sorangiineae) genome to illuminate the basis for several important behavioral and metabolic differences. These include the ability of Sorangium strains to degrade complex plant materials (Fig. 1). S. cellulosum So ce56, an obligate aerobe, was established previously as a model Sorangium strain 7 by virtue of its favorable growth characteristics and ability to differentiate reproducibly under laboratory conditions. It synthesizes the cytotoxic chivosazoles 7 and the catecholate-type siderophores myxochelins 8 . Comparison of the complete genome sequence of strain S. cellulosum

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Possibility of Bacterial Recruitment of Plant Genes Associated with the Biosynthesis of Secondary Metabolites

Cited by 46 publications

References 56 publications

Hormonal regulation in green plant lineage families

Hormonal regulation in green plant lineage families

Evolutionary History of the phl Gene Cluster in the Plant-Associated Bacterium Pseudomonas fluorescens

Complete genome sequence of the myxobacterium Sorangium cellulosum

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