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A jasmonate ZIM-domain protein NaJAZd regulates floral jasmonic acid levels and counteracts flower abscission in Nicotiana attenuata plants.

Oh Y, Baldwin IT, Galis I - PLoS ONE (2013)

Bottom Line: Although NaJAZd transcripts were strongly and transiently up-regulated in the rosette leaves by simulated herbivory treatment, we did not observe strong defense-related phenotypes, such as altered herbivore performance or the constitutive accumulation of defense-related secondary metabolites in irJAZd plants compared to wild type plants, both in the glasshouse and the native habitat of Nicotiana attenuata in the Great Basin Desert, Utah, USA.The early- and mid-developmental stages of irJAZd flowers had reduced levels of jasmonic acid and jasmonoyl-L-isoleucine, while fully open flowers had normal levels, but these were impaired in NaMYB305 transcript accumulations.This novel insight into the function of JAZ proteins in flower and seed development highlights the diversity of functions played by jasmonates and JAZ proteins.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Jena, Germany.

ABSTRACT
Jasmonic acid is an important regulator of plant growth, development and defense. The jasmonate-ZIM domain (JAZ) proteins are key regulators in jasmonate signaling ubiquitously present in flowering plants but their functional annotation remains largely incomplete. Recently, we identified 12 putative JAZ proteins in native tobacco, Nicotiana attenuata, and initiated systematic functional characterization of these proteins by reverse genetic approaches. In this report, Nicotiana attenuata plants silenced in the expression of NaJAZd (irJAZd) by RNA interference were used to characterize NaJAZd function. Although NaJAZd transcripts were strongly and transiently up-regulated in the rosette leaves by simulated herbivory treatment, we did not observe strong defense-related phenotypes, such as altered herbivore performance or the constitutive accumulation of defense-related secondary metabolites in irJAZd plants compared to wild type plants, both in the glasshouse and the native habitat of Nicotiana attenuata in the Great Basin Desert, Utah, USA. Interestingly, irJAZd plants produced fewer seed capsules than did wild type plants as a result of increased flower abscission in later stages of flower development. The early- and mid-developmental stages of irJAZd flowers had reduced levels of jasmonic acid and jasmonoyl-L-isoleucine, while fully open flowers had normal levels, but these were impaired in NaMYB305 transcript accumulations. Previously, NaMYB305-silenced plants were shown to have strong flower abscission phenotypes and contained lower NECTARIN 1 transcript levels, phenotypes which are copied in irJAZd plants. We propose that the NaJAZd protein is required to counteract flower abscission, possibly by regulating jasmonic acid and jasmonoyl-L-isoleucine levels and/or expression of NaMYB305 gene in Nicotiana attenuata flowers. This novel insight into the function of JAZ proteins in flower and seed development highlights the diversity of functions played by jasmonates and JAZ proteins.

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NaJAZd-silencing negatively affects seed capsule production.WT and two independent irJAZd lines (irJAZd-4 and -8) were grown in the glasshouse and their capsules were counted at specified time points. irJAZd plants produced significantly fewer seed capsules at 51, 54, 57, 60 and 63 d after germination compared to WT plants; significant differences between genotypes were determined at each time point by one-way-ANOVA (**P≤0.01, ***P≤0.001). There were no significant differences in number of seed capsules between two independent irJAZd lines (irJAZd-4 and -8). The exact numbers of capsules are displayed in table under the graph and different letters in the table indicate significant differences among the different genotypes (WT vs. independent NaJAZd silenced lines, irJAZd-4, -8) at the same time points. Differences at 42–48 d were not significant.
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pone-0057868-g004: NaJAZd-silencing negatively affects seed capsule production.WT and two independent irJAZd lines (irJAZd-4 and -8) were grown in the glasshouse and their capsules were counted at specified time points. irJAZd plants produced significantly fewer seed capsules at 51, 54, 57, 60 and 63 d after germination compared to WT plants; significant differences between genotypes were determined at each time point by one-way-ANOVA (**P≤0.01, ***P≤0.001). There were no significant differences in number of seed capsules between two independent irJAZd lines (irJAZd-4 and -8). The exact numbers of capsules are displayed in table under the graph and different letters in the table indicate significant differences among the different genotypes (WT vs. independent NaJAZd silenced lines, irJAZd-4, -8) at the same time points. Differences at 42–48 d were not significant.

Mentions: NaJAZd-silencing only slightly affected defense responses. Considering the extensively described role of JA in growth and development (reviewed in [9]), we decided to carefully examine the growth and development of irJAZd plants. The irJAZd plants showed no obvious vegetative growth deficiencies: they had similar size of rosettes, leaf shape, and stalk length (data not shown). However, in contrast to vegetative growth, their reproductive fitness was significantly compromised. During the harvesting of seeds, we noticed that irJAZd plants produced significantly less seed mass compared to WT plants. When we carefully counted the number of mature seed capsules during entire reproduction of WT and irJAZd-4 and -8 plants, both irJAZd lines had about 11∼35% fewer capsules compared to WT between 51–63 d after germination (Figure 4).


A jasmonate ZIM-domain protein NaJAZd regulates floral jasmonic acid levels and counteracts flower abscission in Nicotiana attenuata plants.

Oh Y, Baldwin IT, Galis I - PLoS ONE (2013)

NaJAZd-silencing negatively affects seed capsule production.WT and two independent irJAZd lines (irJAZd-4 and -8) were grown in the glasshouse and their capsules were counted at specified time points. irJAZd plants produced significantly fewer seed capsules at 51, 54, 57, 60 and 63 d after germination compared to WT plants; significant differences between genotypes were determined at each time point by one-way-ANOVA (**P≤0.01, ***P≤0.001). There were no significant differences in number of seed capsules between two independent irJAZd lines (irJAZd-4 and -8). The exact numbers of capsules are displayed in table under the graph and different letters in the table indicate significant differences among the different genotypes (WT vs. independent NaJAZd silenced lines, irJAZd-4, -8) at the same time points. Differences at 42–48 d were not significant.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3585257&req=5

pone-0057868-g004: NaJAZd-silencing negatively affects seed capsule production.WT and two independent irJAZd lines (irJAZd-4 and -8) were grown in the glasshouse and their capsules were counted at specified time points. irJAZd plants produced significantly fewer seed capsules at 51, 54, 57, 60 and 63 d after germination compared to WT plants; significant differences between genotypes were determined at each time point by one-way-ANOVA (**P≤0.01, ***P≤0.001). There were no significant differences in number of seed capsules between two independent irJAZd lines (irJAZd-4 and -8). The exact numbers of capsules are displayed in table under the graph and different letters in the table indicate significant differences among the different genotypes (WT vs. independent NaJAZd silenced lines, irJAZd-4, -8) at the same time points. Differences at 42–48 d were not significant.
Mentions: NaJAZd-silencing only slightly affected defense responses. Considering the extensively described role of JA in growth and development (reviewed in [9]), we decided to carefully examine the growth and development of irJAZd plants. The irJAZd plants showed no obvious vegetative growth deficiencies: they had similar size of rosettes, leaf shape, and stalk length (data not shown). However, in contrast to vegetative growth, their reproductive fitness was significantly compromised. During the harvesting of seeds, we noticed that irJAZd plants produced significantly less seed mass compared to WT plants. When we carefully counted the number of mature seed capsules during entire reproduction of WT and irJAZd-4 and -8 plants, both irJAZd lines had about 11∼35% fewer capsules compared to WT between 51–63 d after germination (Figure 4).

Bottom Line: Although NaJAZd transcripts were strongly and transiently up-regulated in the rosette leaves by simulated herbivory treatment, we did not observe strong defense-related phenotypes, such as altered herbivore performance or the constitutive accumulation of defense-related secondary metabolites in irJAZd plants compared to wild type plants, both in the glasshouse and the native habitat of Nicotiana attenuata in the Great Basin Desert, Utah, USA.The early- and mid-developmental stages of irJAZd flowers had reduced levels of jasmonic acid and jasmonoyl-L-isoleucine, while fully open flowers had normal levels, but these were impaired in NaMYB305 transcript accumulations.This novel insight into the function of JAZ proteins in flower and seed development highlights the diversity of functions played by jasmonates and JAZ proteins.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Jena, Germany.

ABSTRACT
Jasmonic acid is an important regulator of plant growth, development and defense. The jasmonate-ZIM domain (JAZ) proteins are key regulators in jasmonate signaling ubiquitously present in flowering plants but their functional annotation remains largely incomplete. Recently, we identified 12 putative JAZ proteins in native tobacco, Nicotiana attenuata, and initiated systematic functional characterization of these proteins by reverse genetic approaches. In this report, Nicotiana attenuata plants silenced in the expression of NaJAZd (irJAZd) by RNA interference were used to characterize NaJAZd function. Although NaJAZd transcripts were strongly and transiently up-regulated in the rosette leaves by simulated herbivory treatment, we did not observe strong defense-related phenotypes, such as altered herbivore performance or the constitutive accumulation of defense-related secondary metabolites in irJAZd plants compared to wild type plants, both in the glasshouse and the native habitat of Nicotiana attenuata in the Great Basin Desert, Utah, USA. Interestingly, irJAZd plants produced fewer seed capsules than did wild type plants as a result of increased flower abscission in later stages of flower development. The early- and mid-developmental stages of irJAZd flowers had reduced levels of jasmonic acid and jasmonoyl-L-isoleucine, while fully open flowers had normal levels, but these were impaired in NaMYB305 transcript accumulations. Previously, NaMYB305-silenced plants were shown to have strong flower abscission phenotypes and contained lower NECTARIN 1 transcript levels, phenotypes which are copied in irJAZd plants. We propose that the NaJAZd protein is required to counteract flower abscission, possibly by regulating jasmonic acid and jasmonoyl-L-isoleucine levels and/or expression of NaMYB305 gene in Nicotiana attenuata flowers. This novel insight into the function of JAZ proteins in flower and seed development highlights the diversity of functions played by jasmonates and JAZ proteins.

Show MeSH