A Lotus japonicus β-type carbonic anhydrase gene expression pattern suggests distinct physiological roles during nodule development

Flemetakis, Emmanouil; Dimou, Maria; Cotzur, Daniela; Aivalakis, Georgios; Efrose, Rodica; Kenoutis, Christos A.; Udvardi, Michael K.; Katinakis, Panagiotis

doi:10.1016/s0167-4781(03)00142-8

Cited by 30 publications

(20 citation statements)

References 34 publications

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“…Previous work had demonstrated that genes encoding nodule-specific CA isoforms are present in various legume species, including Medicago sativa (10), Glycine max (19), and L. japonicus (14). In contrast, to our knowledge, nothing is known about the presence and the physiological roles of CA isoforms in the microsymbiont.…”

Section: Resultsmentioning

confidence: 99%

Characterization of a Mesorhizobium loti α-Type Carbonic Anhydrase and Its Role in Symbiotic Nitrogen Fixation

et al. 2009

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.1) is a widespread enzyme catalyzing the reversible hydration of CO 2 to bicarbonate, a reaction that participates in many biochemical and physiological processes. Mesorhizobium loti, the microsymbiont of the model legume Lotus japonicus, possesses on the symbiosis island a gene (msi040) encoding an ␣-type CA homologue, annotated as CAA1. In the present work, the CAA1 open reading frame from M. loti strain R7A was cloned, expressed, and biochemically characterized, and it was proven to be an active ␣-CA. The biochemical and physiological roles of the CAA1 gene in free-living and symbiotic rhizobia were examined by using an M. loti R7A disruption mutant strain. Our analysis revealed that CAA1 is expressed in both nitrogen-fixing bacteroids and free-living bacteria during growth in batch cultures, where gene expression was induced by increased medium pH. L. japonicus plants inoculated with the CAA1 mutant strain showed no differences in top-plant traits and nutritional status but consistently formed a higher number of nodules exhibiting higher fresh weight, N content, nitrogenase activity, and ␦ 13C abundance. Based on these results, we propose that although CAA1 is not essential for nodule development and symbiotic nitrogen fixation, it may participate in an auxiliary mechanism that buffers the bacteroid periplasm, creating an environment favorable for NH 3 protonation, thus facilitating its diffusion and transport to the plant. In addition, changes in the nodule ␦ 13C abundance suggest the recycling of at least part of the HCO 3 ؊ produced by CAA1.

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Section: Resultsmentioning

confidence: 99%

Characterization of a Mesorhizobium loti α-Type Carbonic Anhydrase and Its Role in Symbiotic Nitrogen Fixation

et al. 2009

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“…In Situ Hybridization-In situ hybridization experiments were performed as previously described (39,40). L. japonicus nodules harvested at 21 days post-infection with M. loti (strain E1R.pMP2112) were fixed in 4% paraformaldehyde supplemented with 0.25% glutaraldehyde in 10 mM sodium phosphate buffer, pH 7.4, for 4 h in a vacuum aspirator.…”

Section: Lipid Extraction and Quantification Of Polar Lipids Fatty Amentioning

confidence: 99%

The Galactolipid Digalactosyldiacylglycerol Accumulates in the Peribacteroid Membrane of Nitrogen-fixing Nodules of Soybean and Lotus

Gaude

Tippmann

Flemetakis

et al. 2004

Journal of Biological Chemistry

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The peribacteroid membrane (PBM) surrounding nitrogen fixing rhizobia in the nodules of legumes is crucial for the exchange of ammonium and nutrients between the bacteria and the host cell. Digalactosyldiacylglycerol (DGDG), a galactolipid abundant in chloroplasts, was detected in the PBM of soybean (Glycine max) and Lotus japonicus. Analyses of membrane marker proteins and of fatty acid composition confirmed that DGDG represents an authentic PBM lipid of plant origin and is not derived from the bacteria or from plastid contamination. In Arabidopsis, DGDG is known to accumulate in extraplastidic membranes during phosphate deprivation. However, the presence of DGDG in soybean PBM was not restricted to phosphate limiting conditions. Complementary DNA sequences corresponding to the two DGDG synthases, DGD1 and DGD2 from Arabidopsis, were isolated from soybean and Lotus. The two genes were expressed during later stages of nodule development in infected cells and in cortical tissue. Because nodule development depends on the presence of high amounts of phosphate in the growth medium, the accumulation of the non-phosphorus galactolipid DGDG in the PBM might be important to save phosphate for other essential processes, i.e. nucleic acid synthesis in bacteroids and host cells.

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“…Transgenic Flaveria with mesophyll cell CA activities below 10% of wild-type levels had low rates of CO 2 assimilation and grew poorly at ambient levels of CO 2 . In an analogous but nonphotosynthetic role, bCA isoforms have been localized to nodules of legumes where they are presumed to catalyze the synthesis of HCO 3 2 for use by PEPCase in its anaplerotic role as the source of C-4 acids for amination reactions or bacteroid carbon catabolism (Flemetakis et al, 2003). In addition, the synthesis of nodule localized C-4 acids (with the coordinated expression of CA and PEPCase) has also been postulated as part of the mechanism to control gas diffusion within this tissue (Atkins et al, 2001).…”

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Reduction of Plastid-Localized Carbonic Anhydrase Activity Results in Reduced Arabidopsis Seedling Survivorship

2008

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Carbonic anhydrase (CA; EC 4.2.1.1) catalyzes the interconversion of CO2 and HCO3 − and is a major protein constituent of the C3 higher plant chloroplast where it is presumed to play a role in photosynthetic carbon assimilation. In this study, we have used both RNA antisense and gene knockout lines to specifically reduce the activity of the chloroplast βCA1 polypeptide (At3g01500) in the model plant Arabidopsis (Arabidopsis thaliana). Although able to germinate, seedling establishment of transgenic plants is significantly reduced relative to wild-type plants when grown at ambient levels of CO2. Growth at elevated (1,500 μL L−1) CO2 or on plates supplemented with sucrose restores seedling establishment rates to wild-type levels. Seed from wild-type and transgenic plants exhibited no significant differences in seed protein, lipid content, or reserve mobilization during seedling growth. βCA1-deficient seedlings do, however, exhibit reduced capacity for light-dependent 14CO2 assimilation prior to the development of true leaves. The small number of surviving seedlings able to grow and develop are phenotypically similar to wild-type plants, even when subsequently grown at subambient levels of CO2. Microarray analysis of mature leaves of βCA1-deficient plants shows some differences in transcript abundance, particularly with genes involved in ethylene signaling and response. The data suggest that reduced levels of seedling establishment by βCA1-deficient plants could be the result of poor cotyledon photosynthetic performance at the onset of phototrophic growth and prior to the development of true leaves.

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A Lotus japonicus β-type carbonic anhydrase gene expression pattern suggests distinct physiological roles during nodule development

Cited by 30 publications

References 34 publications

Characterization of a Mesorhizobium loti α-Type Carbonic Anhydrase and Its Role in Symbiotic Nitrogen Fixation

Characterization of a Mesorhizobium loti α-Type Carbonic Anhydrase and Its Role in Symbiotic Nitrogen Fixation

The Galactolipid Digalactosyldiacylglycerol Accumulates in the Peribacteroid Membrane of Nitrogen-fixing Nodules of Soybean and Lotus

Reduction of Plastid-Localized Carbonic Anhydrase Activity Results in Reduced Arabidopsis Seedling Survivorship

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