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Comparison of the Nodule vs. Root Transcriptome of the Actinorhizal Plant Datisca glomerata: Actinorhizal Nodules Contain a Specific Class of Defensins
Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
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2013 (English)In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 8, no 8, e72442- p.Article in journal (Refereed) Published
Abstract [en]

Actinorhizal root nodule symbioses are very diverse, and the symbiosis of Datisca glomerata has previously been shown to have many unusual aspects. In order to gain molecular information on the infection mechanism, nodule development and nodule metabolism, we compared the transcriptomes of D. glomerata roots and nodules. Root and nodule libraries representing the 3'-ends of cDNAs were subjected to high-throughput parallel 454 sequencing. To identify the corresponding genes and to improve the assembly, Illumina sequencing of the nodule transcriptome was performed as well. The evaluation revealed 406 differentially regulated genes, 295 of which (72.7%) could be assigned a function based on homology. Analysis of the nodule transcriptome showed that genes encoding components of the common symbiosis signaling pathway were present in nodules of D. glomerata, which in combination with the previously established function of SymRK in D. glomerata nodulation suggests that this pathway is also active in actinorhizal Cucurbitales. Furthermore, comparison of the D. glomerata nodule transcriptome with nodule transcriptomes from actinorhizal Fagales revealed a new subgroup of nodule-specific defensins that might play a role specific to actinorhizal symbioses. The D. glomerata members of this defensin subgroup contain an acidic C-terminal domain that was never found in plant defensins before.

Place, publisher, year, edition, pages
2013. Vol. 8, no 8, e72442- p.
National Category
Natural Sciences
Identifiers
URN: urn:nbn:se:su:diva-94186DOI: 10.1371/journal.pone.0072442ISI: 000323734600020OAI: oai:DiVA.org:su-94186DiVA: diva2:652567
Note

AuthorCount:5;

Fundin Agency:

Forskningsradet Formas (Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning)  2005-2773-3234-80;  Vetenskapsradet (Swedish Research Council)  2007-17840-52674-16;  Fundacao para a Ciencia e Tecnologia (FCT)  SFRH/BPD/43228/2008

Available from: 2013-10-01 Created: 2013-09-30 Last updated: 2017-12-06Bibliographically approved
In thesis
1. The actinorhizal symbiosis of Datisca glomerata: Search for nodule-specific marker genes
Open this publication in new window or tab >>The actinorhizal symbiosis of Datisca glomerata: Search for nodule-specific marker genes
2013 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

The actinorhizal symbiosis is entered by nitrogen-fixing actinobacteria of the genus Frankia and a large group of woody plant species distributed among eight dicot families. The actinorhizal symbiosis, as well as the legume-rhizobia symbiosis, involves the stable intracellular accommodation of the microsymbionts in special organs called root nodules. Within the nodules, the nitrogen-fixing bacteria are provided with carbon sources by the host plant while supplying the plant with fixed nitrogen, which is often a limiting factor in plant growth and development.

Datisca glomerata (C. Presl.) Baill. (Datiscaceae, Cucurbitales) is a suffruticose plant with a relatively short generation time of six months, and therefore represents the actinorhizal species most suited as a genetic model system. In order to obtain an overview of nodule development and metabolism, the nodule transcriptome was analyzed. Comparison of nodule vs. root transcriptomes allowed identification of potential marker genes for nodule development. The activity of the promoters of two of these genes was studied in planta. Furthermore, auxins and cytokinins were quantified in roots and nodules, and the auxin responses in roots were compared in D. glomerata and the model legume Medicago truncatula.

Our results indicate that in actinorhizal plants signaling in the root epidermis leading to nodule organogenesis follows the common symbiosis pathway described for the legume-rhizobia symbiosis and arbuscular mycorrhiza. Moreover, we discovered a group of nodule-specific genes encoding defensin-like peptides with an unusual C-terminal domain that had not been found in other plant species. A possible role in the symbiosis-specific differentiation of the microsymbiont and in nodule development was suggested for these cysteine-rich peptides. Finally, we showed that D. glomerata and M. truncatula differ in their auxin and cytokinin requirements for the development of both nodules and lateral roots.

Place, publisher, year, edition, pages
Stockholm: Department of Ecology, Environment and Plant Sciences, Stockholm University, 2013. 46 p.
Keyword
actinorhizal symbiosis, Datisca glomerata, nodule transcriptome, nodule-specific marker genes, cysteine-rich peptides, auxins and cytokinins
National Category
Botany
Research subject
Plant Physiology
Identifiers
urn:nbn:se:su:diva-92857 (URN)978-91-7447-691-0 (ISBN)
Public defence
2013-09-25, föreläsningssalen, Institutionen för ekologi, miljö och botanik, Lilla Frescativägen 5, Stockholm, 13:00 (English)
Opponent
Supervisors
Note

At the time of the doctoral defense, the following papers were unpublished and had a status as follows: Paper 1: In press. Paper 2: Manuscript. Paper 3: Manuscript. Paper 4: Manuscript.

Available from: 2013-09-03 Created: 2013-08-22 Last updated: 2013-10-01Bibliographically approved
2. Molecular mechanisms in actinorhizal symbioses
Open this publication in new window or tab >>Molecular mechanisms in actinorhizal symbioses
2011 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

The symbiosis between the nitrogen fixing acinobacterium Frankia and its actinorhizal host plant is very old and their co-evolution has shaped their niche in the environment. Nitrogen is most often the limiting element in soil, and symbiotic plants can, with the help of their micrsymbionts, compete in an efficient way. Actinorhizal plants are found all over the world and the nitrogen fixing capability of Frankia contributes greatly to the global nitrogen cycle as well as to the microclimate around these particular plants. The symbiosis between the two is carried out in a modified lateral root known as a nodule, where the bacteria are hosted by the plant. The nodule is a specialized organ in which Frankia is provided with energy in exchange for fixed nitrogen. In this thesis the focus has been to examine the two actinorhizal plants Alnus glutinosa and Datisca glomerata and their two different Frankia symbionts, Frankia alni ACN14a and F. datiscae Dg1.

In order to compare the symbiosis of D. glomerata to other actinorhizal symbioses, the transcriptomes of roots and nodules were compared. F. datiscae Dg1, an unculturable bacterium, was isolated from D. glomerata nodules, and its genome was sequenced and analyzed. In this genome genes were found that are novel in the actinorhizal symbiosis and potentially involved in signaling to the plant host. These genes, known as common nod genes, have previously been described in the microsymbionts of legumes, rhizobia, where their products are involved in initiating nodulation and determining host specificity. Moreover we were able to show that the nod genes in actinobacteria could be the evolutionary origin of the nod genes in rhizobial species. To get a more comprehensive understanding of the comparative nitrogen and carbon metabolism in roots and nodules of D. glomerata and A. glutinosa, the nodule transcriptomes from both symbiotic bacteria were compared.

Place, publisher, year, edition, pages
Stockholm: Department of Botany, Stockholm University, 2011. 32 p.
National Category
Biological Sciences
Research subject
Plant Physiology
Identifiers
urn:nbn:se:su:diva-63411 (URN)978-91-7447-370-4 (ISBN)
Public defence
2011-11-25, föreläsningssalen, Botanicum, Lilla Frescativägen 5, Stockholm, 13:00 (English)
Opponent
Supervisors
Note

At the time of the doctoral defense, the following papers were unpublished and had a status as follows: Paper 1: Manuscript. Paper 2: In press. Paper 3: Manuscript. Paper 4: Manuscript.

Available from: 2011-11-03 Created: 2011-10-18 Last updated: 2013-10-02Bibliographically approved

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