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Conservation of transcription factors in infected cells of nitrogen-fixing root nodules
Stockholm University, Faculty of Science, Department of Botany. (Pawlowski)
2010 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Infected cells of nitrogen-fixing root nodules are the only plant cells that can stably internally accommodate a eubacterial symbiont. In the context of studying the differentiation of infected cells, we set about to analyse the conservation of infected cell-specific transcription factors using altogether four different promoters from genes showing infected cell-specific expression, or nodule-specific expression. The activity of promoter-reporter gene constructs was compared in transgenic hairy root systems of three different root nodule-forming plant species. The model species were two actinorhizal plants; the tree Casuarina glauca and the riparian weed Datisca glomerata, and the model legume Lotus japonicus. C. glauca and D. glomerata belong to different phylogenetic subgroups (Fagales vs. Cucurbitales) of actinorhizal plants showing strong differences with regard to nodule morphology, -metabolism and infection mechanism.

The results indicate one type of infected cell-specific transcription factors previously shown to be conserved between legumes and C. glauca is also conserved in D. glomerata. However, another type of transcription factor specific to infection thread-containing cells of C. glauca and the model legume Medicago truncatula is not conserved in D. glomerata. These results indicate that in this group of actinorhizal plants, infection thread growth occurs via a different mechanism, a conclusion supported by cytological analysis.

Furthermore, the results indicate that gene expression in infected cells of root nodules can be achieved by control mechanisms other than cell type-specific transcription factors, and that in this context, phytohormone regulation deserves further study.

Place, publisher, year, edition, pages
Stockholm: Department of Botany, Stockholm University , 2010. , 69 p.
Keyword [en]
root nodules, actinorhiza, legumes, infection thread, Frankia, subtilase, leghemoglobin, chitinase
National Category
Botany
Research subject
Plant Physiology
Identifiers
URN: urn:nbn:se:su:diva-42389ISBN: 978-91-7447-140-3 (print)OAI: oai:DiVA.org:su-42389DiVA: diva2:345905
Public defence
2010-10-08, Föresläsningssalen Botanicum, Lilla Frescativägen 5, Stockholm, 10:00 (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: Manuscript. Paper 3: Manuscript. Paper 4: Manuscript.Available from: 2010-09-16 Created: 2010-08-27 Last updated: 2010-08-30Bibliographically approved
List of papers
1. Infection thread growth mechanism is conserved between legumes and actinorhizal Casuarina glauca, but seems different in actinorhizal Datisca glomerata
Open this publication in new window or tab >>Infection thread growth mechanism is conserved between legumes and actinorhizal Casuarina glauca, but seems different in actinorhizal Datisca glomerata
(English)Manuscript (preprint) (Other academic)
Abstract [en]

In this study, two previously analysed infection-related promoters were examined for their expression pattern in nodules formed on transgenic hairy roots of the actinorhizal species Datisca glomerata. The infected cell-specific expression pattern of a leghemoglobin promoter from the indeterminate nodule-forming legume Vicia faba was conserved in the determinate nodule-forming legume Lotus japonicus, the actinorhizal species Casuarina glauca (Fagales) and also in D. glomerata (Cucurbitales). Hence, the conservation of the infected cell-specific transcription factors responsible for the activation of leghemoglobin genes in legumes, and the symbiotic haemoglobin gene in C. glauca, extends to actinorhizal Cucurbitales. However, the infection thread containing cell-specific expression pattern of the C. glauca Cg12 promoter which had been found to be conserved in legumes (Svistoonoff et al. 2004), was not conserved in D. glomerata. In order to find out whether this result, in combination with the long-known fact that infection thread growth in D. glomerata does not involve the formation of pre-infection thread structures like in legumes and actinorhizal Fagales, points at an alternative infection thread growth mechanism in actinorhizal Cucurbitales, a cytological analysis of infection thread growth in D. glomerata vs. Alnus rubra (Fagales) was performed. In D. glomerata, infection threads crossed the cell wall through the center of pit fields, while in A. rubra no correlation between infection thread crossing points and thin cell wall regions could be found.  Moreover, extensive ramification of infection threads in the cell periphery of D. glomerata infected cells leads to multiple pit field penetrations in a given host cell and a large degree of inter-host cell communication by the microsymbiont, in contrast to only a few wall penetration sites, aligned axially, in A. rubra

Identifiers
urn:nbn:se:su:diva-42403 (URN)
Available from: 2010-08-30 Created: 2010-08-30 Last updated: 2010-08-30Bibliographically approved
2. The promoter of a nodule-specific chitinase from Casuarina glauca, CgChi3, is down-regulated by wounding in a jasmonic acid-independent manner
Open this publication in new window or tab >>The promoter of a nodule-specific chitinase from Casuarina glauca, CgChi3, is down-regulated by wounding in a jasmonic acid-independent manner
(English)Manuscript (preprint) (Other academic)
Abstract [en]

The promoter of the nodule-specific class III chitinase CgChi3 from the Australian actinorhizal tree Casuarina glauca (Fortunato et al., 2007) was amplified by genome walking. A CgChi3::GUS fusion was used to examine whether the organ- and cell type-specific expression pattern of CgChi3 could be transferred to other root nodule-forming plants, and whether the repression of promoter activity by wounding that had been found in C. glauca nodules, was conserved and whether it was due to jasmonic acid (JA) signalling.

Organ- and cell type-specific expression of the CgChi3 promoter was conserved in the distantly related actinorhizal species Datisca glomerata, but not in the legume Lotus japonicus where CgChi3 was active in roots, not in nodules. The repression of promoter activity in response to wounding was conserved in L. japonicus and independent of JA signalling.

Identifiers
urn:nbn:se:su:diva-42404 (URN)
Available from: 2010-08-30 Created: 2010-08-30 Last updated: 2010-08-30Bibliographically approved
3. Activity of the promoter of a nodule infected cell-specific gene, Cg164, from Casuarina glauca, in transgenic Lotus japonicus: is infected cell-specific transcription conserved between different root nodule symbioses?
Open this publication in new window or tab >>Activity of the promoter of a nodule infected cell-specific gene, Cg164, from Casuarina glauca, in transgenic Lotus japonicus: is infected cell-specific transcription conserved between different root nodule symbioses?
(English)Manuscript (preprint) (Other academic)
Abstract [en]

In order to examine the conservation of transcription factors in infected cells of nitrogen-fixing root nodules, the activity of promoter::reporter gene constructs was compared in transgenic hairy root systems of different root nodule forming plant species. The promoter under examination, Cg164, was taken from the Australian tree Casuarina glauca. Cg164 encodes a homologue of a nodule infected cell-specific gene family from the closely related actinorhizal tree Alnus glutinosa. After infection of Agrobacterium rhizogenes-induced transgenic hairy root systems of the model legume Lotus japonicus with Mesorhizobium loti strain TONO, the Cg164::GUS construct led to GUS activity in the roots, in the nodule outer cortex and in the nodule vascular system, but not in the infected cells of the nodules. Hence, the cell type-specificity of expression of Cg164 was not conserved. In order to find out which factors determined infected cell-specific expression, the effects of ROS and ethylene signaling on Cg164 promoter activity were examined. Ethylene signaling was required for the expression of Cg164::GUS, while salt stress, leading to ROS production, repressed Cg164 promoter activity.

Identifiers
urn:nbn:se:su:diva-42405 (URN)
Available from: 2010-08-30 Created: 2010-08-30 Last updated: 2010-08-30Bibliographically approved
4. The Casuarina glauca metallothionein I promoter in transgenic nodulated hairy roots of the actinorhizal plant Datisca glomerata and the legume Lotus japonicus: auxin and cytokinin affect promoter activity
Open this publication in new window or tab >>The Casuarina glauca metallothionein I promoter in transgenic nodulated hairy roots of the actinorhizal plant Datisca glomerata and the legume Lotus japonicus: auxin and cytokinin affect promoter activity
(English)Manuscript (preprint) (Other academic)
Abstract [en]

In the past, the activity of the promoter of a metallothionein gene expressed in actinorhizal nodules of Casuarina glauca, CgMT1, has been analysed in Casaurinaceae and in tobacco, Arabidopsis and rice. In all these plants, the promoter showed high activity in the root cortex and –epidermis, making it a useful tool for the expression of transgenes. Therefore, its activity was now analysed in transgenic root systems of Datisca glomerata, an actinorhizal plant from a different phylogenetic group than C. glauca, using the same CgMT1::GUS fusion as in previous studies. However, in contrast with all other plant species examined previously, the CgMT1::GUS construct showed no activity at all in D. glomerata hairy roots, while the expression pattern in nodules resembled that found in C. glauca nodules. This is probably due to the changed hormone balance in hairy roots since experiments on the CgMT1::GUS construct in transgenic Arabidopsis showed that CgMT1 promoter activity was repressed by auxin or cytokinin, respectively. Yet, in hairy roots of the model legume Lotus japonicus induced by the same Agrobacterium rhizogenes strain, the CgMT1 promoter was active in roots and not in nodules, indicating that while pRi T-DNA genes lead to a changed hormone balance, the changes do not abolish the differences in phytorhomone levels/-sensitivity between plant species.

 

Identifiers
urn:nbn:se:su:diva-42406 (URN)
Available from: 2010-08-30 Created: 2010-08-30 Last updated: 2010-08-30Bibliographically approved

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