An operon for production of bioactive gibberellin A4 phytohormone with wide distribution in the bacterial rice leaf streak pathogen Xanthomonas oryzae pv. oryzicola

Nagel, Raimund; Turrini, Paula Cristina Gasperazzo; Nett, Ryan S.; Leach, Jan E.; Verdier, Valérie; Sluys, Marie‐Anne Van; Peters, Reuben J.

doi:10.1111/nph.14441

Cited by 29 publications

(37 citation statements)

References 41 publications

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“…Further support for HGT of the GA operon has been suggested by the presence of insertional sequence (IS) elements flanking the operon (e.g. transposases and integrases) in many species [5, 22]. Overall, these collective observations strongly support HGT of the GA operon, consistent with its widely-scattered distribution throughout the proteobacteria.…”

Section: Resultsmentioning

confidence: 69%

“…The ability for bacteria to produce gibberellin (GA), a ubiquitous plant hormone, is imparted by a GA biosynthetic operon (GA operon; Figure 1 ), which is found in both nitrogen-fixing rhizobia and phytopathogenic bacteria [3–5]. While the diterpenoid GA phytohormones act as endogenous signaling molecules for growth and development in vascular plants [6], plant-associated fungi and bacteria have convergently evolved the ability to produce GA as a mechanism for host manipulation [4, 7–9].…”

Section: Introductionmentioning

confidence: 99%

“…Analogous GA operons can be found in certain gammaproteobacterial plant pathogens as well (e.g. Xanthomonas and Erwinia species), and characterization of the GA operon from several distant gammaproteobacterial lineages has demonstrated that the biosynthetic functionality of this operon is conserved [5, 9, 20].…”

Section: Introductionmentioning

confidence: 99%

“…The abundance of sequenced bacterial genomes indicates that the GA operon structure is more complex and variable than that initially described for the α-rhizobia B. diazoefficiens in which this operon was initially identified [14, 15]. Specifically, certain bacteria with the GA operon were found to contain a full length cyp115 gene at the 5’ end of the gene cluster, as opposed to a pseudo-gene/fragment, and this enzyme has been shown to catalyze the final step in bioactive GA biosynthesis, converting GA 9 into bioactive GA 4 [5, 20, 22]. Additionally, many bacterial strains possess a putative isopentenyl diphosphate δ-isomerase ( idi ) gene located at the 3’ end of the operon, which presumably functions in balancing the concentrations of the (di)terpenoid building blocks, isopentenyl diphosphate (IPP) and dimethylallyl diphosphate (DMAPP) [23].…”

Section: Introductionmentioning

confidence: 99%

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Unraveling a tangled skein: Evolutionary analysis of the bacterial gibberellin biosynthetic operon

Nett

Nguyen

Nagel

et al. 2019

Preprint

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Running title: Evolution of the bacterial gibberellin operon 12 13ABSTRACT 14Gibberellin (GA) phytohormones are ubiquitous regulators of growth and developmental processes 15 in vascular plants. The convergent evolution of GA production by plant-associated bacteria, including both 16 symbiotic, nitrogen-fixing rhizobia and phytopathogens, suggests that manipulation of GA signaling is a 17 powerful mechanism for microbes to gain an advantage in these interactions. Although homologous 18 operons encode GA biosynthetic enzymes in both rhizobia and phytopathogens, notable genetic 19 heterogeneity and scattered operon distribution in these lineages suggests distinct functions for GA in varied 20 plant-microbe interactions. Therefore, deciphering GA operon evolutionary history could provide crucial 21 evidence for understanding the distinct biological roles for bacterial GA production. To further establish 22The clustering of bacterial biosynthetic genes within operons allows for the controlled co-33 expression of functionally-related genes under a single promoter, and the opportunity for these genes to be 34 mobilized and co-inherited as a complete metabolic unit via horizontal gene transfer (HGT) [1, 2]. Because 35 operons are responsible for many fundamental biosynthetic pathways in bacteria, analysis of the genetic 36 structure of complex operons can provide important clues regarding the selective pressures driving the 37 evolution of bacterial metabolism, and can also give insight into the occurrences and mechanisms of HGT. 38The ability for bacteria to produce gibberellin (GA), a ubiquitous plant hormone, is imparted by a 39 GA biosynthetic operon (GA operon; Figure 1), which is found in both nitrogen-fixing rhizobia and 40 phytopathogenic bacteria [3][4][5]. While the diterpenoid GA phytohormones act as endogenous signaling 41 molecules for growth and development in vascular plants [6], plant-associated fungi and bacteria have 42 convergently evolved the ability to produce GA as a mechanism for host manipulation [4,[7][8][9]. The 43 phenomenon of GA production by plant-associated microbes has important biological implications, as 44 perturbation in GA signaling can lead to extreme phenotypic changes in plants. For example, production of 45 GA by the rice pathogen Gibberella fujikuroi leads to dramatic elongation and eventual lodging of rice 46 crops [10], and impaired GA metabolism is responsible for the semi-dwarf crop phenotypes associated with 47 aforementioned genes other than cyp115, is widely distributed in symbiotic nitrogen-fixing rhizobia from 59 the alphaproteobacteria class (α-rhizobia) [15], and biochemical characterization of GA operon genes in 60 several α-rhizobia, including B. diazoefficiens, Sinorhizobium fredii, and Mesorhizobium loti, has 61 demonstrated that this core operon is responsible for biosynthesis of GA9, the penultimate intermediate to 62the bioactive phytohormone GA4 [3, 4,[16][17][18]. While exclusively found in plant-associated bacteria [19], 63 the GA operon exhibits scattered d...

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Section: Resultsmentioning

confidence: 69%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Unraveling a tangled skein: Evolutionary analysis of the bacterial gibberellin biosynthetic operon

Nett

Nguyen

Nagel

et al. 2019

Preprint

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“…An answer is suggested by the function of GA 4 for gram‐negative pathogenic Proteobacteria belonging to the Class Gammaproteobacteria (Table ). They are able to carry out all of the steps necessary for making bioactive GA 4 (Zi et al , ; Nagel & Peters, ; Nagel et al , , ) and use their GA 4 for a different purpose – to suppress jasmonic acid‐induced plant defense (Robert‐Seilaniantz et al , ; De Bruyne et al , ). Given the dual actions of GA 4 – one good for the plant and one bad – it makes sense that plants might want to control when and where deployment of GA 4 increases the risk of invasion.…”

Section: Galls As Mutualismmentioning

confidence: 99%

Plants make galls to accommodate foreigners: some are friends, most are foes

Harris

Pitzschke

2020

New Phytologist

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At the colonization site of a foreign entity, plant cells alter their trajectory of growth and development. The resulting structurea plant gallaccommodates various needs of the foreigner, which are phylogenetically diverse: viruses, bacteria, protozoa, oomycetes, true fungi, parasitic plants, and many types of animals, including rotifers, nematodes, insects, and mites. The plant species that make galls also are diverse. We assume gall production costs the plant. All is well if the foreigner provides a gift that makes up for the cost. Nitrogen-fixing nodule-inducing bacteria provide nutritional services. Gall wasps pollinate fig trees. Unfortunately for plants, most galls are made for foes, some of which are deeply studied pathogens and pests: Agrobacterium tumefaciens, Rhodococcus fascians, Xanthomonas citri, Pseudomonas savastanoi, Pantoea agglomerans, 'Candidatus' phytoplasma, rust fungi, Ustilago smuts, root knot and cyst nematodes, and gall midges. Galls are an understudied phenomenon in plant developmental biology. We propose gall inception for discovering unifying features of the galls that plants make for friends and foes, talk about molecules that plants and gall-inducers use to get what they want from each other, raise the question of whether plants colonized by arbuscular mycorrhizal fungi respond in a gall-like manner, and present a research agenda.'Only connect!' E. M. Forster, Howard's End

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Diverging Mechanisms: Cytochrome‐P450‐Catalyzed Demethylation and γ‐Lactone Formation in Bacterial Gibberellin Biosynthesis

Nagel

Peters

2018

Angewandte Chemie

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Biosynthesis of the gibberellin (GA) plant hormones evolved independently in plants and microbes,b ut the pathways proceed by similar transformations.T he combined demethylation and g-lactone ring forming transformation is of significant mechanistic interest, yet remains unclear.T he relevant CYP112 from bacteria was probed by activity assays and 18 O 2 -labeling experiments.Notably,the ability of tert-butyl hydroperoxide to drive this transformation indicates use of the ferryl-oxo(Compound I) from the CYP catalytic cycle for this reaction. Together with the confirmed loss of C20 as CO 2 ,this necessitates two catalytic cycles for carbon-carbon bond scission and g-lactone formation. The ability of CYP112 to hydroxylate the d-lactone form of GA 15 ,shown by the labeling studies,i sc onsistent with the implied use of af urther oxygenated heterocycle in the final conversion of GA 24 into GA 9 , with the partial labeling of GA 9 ,t hus demonstrating that CYP112 partitions its reactants between two diverging mechanisms.

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An operon for production of bioactive gibberellin A₄ phytohormone with wide distribution in the bacterial rice leaf streak pathogen Xanthomonas oryzae pv. oryzicola

Cited by 29 publications

References 41 publications

Unraveling a tangled skein: Evolutionary analysis of the bacterial gibberellin biosynthetic operon

Unraveling a tangled skein: Evolutionary analysis of the bacterial gibberellin biosynthetic operon

Plants make galls to accommodate foreigners: some are friends, most are foes

Diverging Mechanisms: Cytochrome‐P450‐Catalyzed Demethylation and γ‐Lactone Formation in Bacterial Gibberellin Biosynthesis

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