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New aspect of plant-rhizobia interaction: alkaloid biosynthesis in Crotalaria depends on nodulation.

ABSTRACT: Infection of legume hosts by rhizobial bacteria results in the formation of a specialized organ, the nodule, in which atmospheric nitrogen is reduced to ammonia. Nodulation requires the reprogramming of the plant cell, allowing the microsymbiont to enter the plant tissue in a highly controlled manner. We have found that, in Crotalaria (Fabaceae), this reprogramming is associated with the biosynthesis of pyrrolizidine alkaloids (PAs). These compounds are part of the plant's chemical defense against herbivores and cannot be regarded as being functionally involved in the symbiosis. PAs in Crotalaria are detectable only when the plants form nodules after infection with their rhizobial partner. The identification of a plant-derived sequence encoding homospermidine synthase (HSS), the first pathway-specific enzyme of PA biosynthesis, suggests that the plant and not the microbiont is the producer of PAs. Transcripts of HSS are detectable exclusively in the nodules, the tissue with the highest concentration of PAs, indicating that PA biosynthesis is restricted to the nodules and that the nodules are the source from which the alkaloids are transported to the above ground parts of the plant. The link between nodulation and the biosynthesis of nitrogen-containing alkaloids in Crotalaria highlights a further facet of the effect of symbiosis with rhizobia on the ecologically important trait of the plant's chemical defense.

SUBMITTER: Irmer S

PROVIDER: S-EPMC4386363 | biostudies-literature | 2015 Mar

REPOSITORIES: biostudies-literature

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New aspect of plant-rhizobia interaction: alkaloid biosynthesis in Crotalaria depends on nodulation.

Irmer Simon S Podzun Nora N Langel Dorothee D Heidemann Franziska F Kaltenegger Elisabeth E Schemmerling Brigitte B Geilfus Christoph-Martin CM Zörb Christian C Ober Dietrich D

Proceedings of the National Academy of Sciences of the United States of America 20150316 13

Infection of legume hosts by rhizobial bacteria results in the formation of a specialized organ, the nodule, in which atmospheric nitrogen is reduced to ammonia. Nodulation requires the reprogramming of the plant cell, allowing the microsymbiont to enter the plant tissue in a highly controlled manner. We have found that, in Crotalaria (Fabaceae), this reprogramming is associated with the biosynthesis of pyrrolizidine alkaloids (PAs). These compounds are part of the plant's chemical defense again ...[more]

PMID: 25775562

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Project description:Ethylene plays an important role in regulating the rhizobial nodulation process. Consequently, numerous strains of rhizobia possess the ability to decrease plant ethylene levels by the expression of the enzyme 1-aminocyclopropane-1-carboxylate (ACC) deaminase or via the production of rhizobitoxine, thus, leading to an increased ability to nodulate leguminous plants. Nevertheless, not much is understood about the prevalence of these ethylene modulation genes in different rhizobial groups nor their role in the evolution of the symbiotic process. In this work, we analyze the prevalence and evolution of the enzymes ACC deaminase (AcdS) and dihydrorhizobitoxine desaturase (RtxC) in 395 NodC+ genomes from different rhizobial strains isolated from a wide range of locations and plant hosts, and discuss their importance in the evolution of the symbiotic process. The obtained results show that AcdS and RtxC are differentially prevalent in rhizobial groups, indicating the existence of several selection mechanisms governed by the rhizobial strain itself and its evolutionary origin, the environment, and, importantly, the leguminous plant host (co-evolution). Moreover, it was found that the prevalence of AcdS and RtxC is increased in Bradyrhizobium and Paraburkholderia, and lower in other groups. Data obtained from phylogenetic, evolutionary as well as gene localization analysis support the previous hypotheses regarding the ancient origin of the nodulation abilities in Bradyrhizobium and Paraburkholderia, and brings a new perspective for the importance of ethylene modulation genes in the development of the symbiotic process. The acquisition of AcdS by horizontal gene transfer and a positive selection in other rhizobial groups indicates that this enzyme plays an important role in the nodulation process of many rhizobia. On the other hand, RtxC is negatively selected in most symbioses. Understanding the evolution of ethylene modulation genes in rhizobia may be the key to the development of new strategies aiming for an increased nodulation and nitrogen fixation process.

Dataset Information

New aspect of plant-rhizobia interaction: alkaloid biosynthesis in Crotalaria depends on nodulation.

Publications

New aspect of plant-rhizobia interaction: alkaloid biosynthesis in Crotalaria depends on nodulation.

Similar Datasets

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