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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 regulates phytohormone levels and flower development-related genes.WT and irJAZd plants (irJAZd-8) were grown in the glasshouse and four different developmental stages of flowers (F1, F2, F3, and F4) were collected 57 d after germination. (A) Transcript abundances of NaJAZd determined by qPCR in irJAZd-8 flowers were significantly lower compared to WT. (B) Mean JA and JA-Ile levels ± SE determined by LC-ESI-MS/MS using individual stage flowers and mean ethylene levels ± SE measured by photoacoustic spectrometer using a mixture of five flowers of each stage. (C) Transcripts abundances ± SE of flower development-related genes, NaMYB305, NaNEC1, and NaCHAL determined by qPCR: irJAZd-8 plants were impaired in expression of NaMYB305 and NaNEC1genes in last stage of flower development (F4) while NaCHAL transcripts remained unaltered in irJAZd-8 compared to WT flowers. Bars ± SE in (C) show EF1α-normalized relative transcript abundances. Statistical differences in phytohormones, JA, JA-Ile, ethylene (n = 4) and transcript abundances (n = 4) were determined by Student t-test. Asterisks represent significant differences between WT and irJAZd in same stage of flowers (*P≤0.05, **P≤0.01, ***P≤0.001); n.s, not significantly different; FM, fresh mass.
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pone-0057868-g006: NaJAZd regulates phytohormone levels and flower development-related genes.WT and irJAZd plants (irJAZd-8) were grown in the glasshouse and four different developmental stages of flowers (F1, F2, F3, and F4) were collected 57 d after germination. (A) Transcript abundances of NaJAZd determined by qPCR in irJAZd-8 flowers were significantly lower compared to WT. (B) Mean JA and JA-Ile levels ± SE determined by LC-ESI-MS/MS using individual stage flowers and mean ethylene levels ± SE measured by photoacoustic spectrometer using a mixture of five flowers of each stage. (C) Transcripts abundances ± SE of flower development-related genes, NaMYB305, NaNEC1, and NaCHAL determined by qPCR: irJAZd-8 plants were impaired in expression of NaMYB305 and NaNEC1genes in last stage of flower development (F4) while NaCHAL transcripts remained unaltered in irJAZd-8 compared to WT flowers. Bars ± SE in (C) show EF1α-normalized relative transcript abundances. Statistical differences in phytohormones, JA, JA-Ile, ethylene (n = 4) and transcript abundances (n = 4) were determined by Student t-test. Asterisks represent significant differences between WT and irJAZd in same stage of flowers (*P≤0.05, **P≤0.01, ***P≤0.001); n.s, not significantly different; FM, fresh mass.

Mentions: To elucidate the molecular mechanisms involved in NaJAZd-regulated flower abscission, we analyzed the levels of phytohormones and flower-related gene expression at four different developmental stages of flowers in WT and irJAZd-8 plants: buds (F1), early elongated flowers (∼10 mm length, F2), fully elongated flowers (still green and completely closed corollas, F3) and open flowers (completely opened white corollas, F4). First, we determined the expression of NaJAZd in WT and irJAZd-8 flowers to examine if (1) NaJAZd is expressed in stage-specific manner, and (2) to evaluate the efficiency of gene silencing in irJAZd flowers by RNAi. In WT plants, the gene showed comparably high transcript levels during F1–F3 stages but its expression declined in the F4 stage. NaJAZd transcript levels were strongly reduced in irJAZd-8 flowers compared to WT levels (Figure 6A).


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 regulates phytohormone levels and flower development-related genes.WT and irJAZd plants (irJAZd-8) were grown in the glasshouse and four different developmental stages of flowers (F1, F2, F3, and F4) were collected 57 d after germination. (A) Transcript abundances of NaJAZd determined by qPCR in irJAZd-8 flowers were significantly lower compared to WT. (B) Mean JA and JA-Ile levels ± SE determined by LC-ESI-MS/MS using individual stage flowers and mean ethylene levels ± SE measured by photoacoustic spectrometer using a mixture of five flowers of each stage. (C) Transcripts abundances ± SE of flower development-related genes, NaMYB305, NaNEC1, and NaCHAL determined by qPCR: irJAZd-8 plants were impaired in expression of NaMYB305 and NaNEC1genes in last stage of flower development (F4) while NaCHAL transcripts remained unaltered in irJAZd-8 compared to WT flowers. Bars ± SE in (C) show EF1α-normalized relative transcript abundances. Statistical differences in phytohormones, JA, JA-Ile, ethylene (n = 4) and transcript abundances (n = 4) were determined by Student t-test. Asterisks represent significant differences between WT and irJAZd in same stage of flowers (*P≤0.05, **P≤0.01, ***P≤0.001); n.s, not significantly different; FM, fresh mass.
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Related In: Results  -  Collection

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pone-0057868-g006: NaJAZd regulates phytohormone levels and flower development-related genes.WT and irJAZd plants (irJAZd-8) were grown in the glasshouse and four different developmental stages of flowers (F1, F2, F3, and F4) were collected 57 d after germination. (A) Transcript abundances of NaJAZd determined by qPCR in irJAZd-8 flowers were significantly lower compared to WT. (B) Mean JA and JA-Ile levels ± SE determined by LC-ESI-MS/MS using individual stage flowers and mean ethylene levels ± SE measured by photoacoustic spectrometer using a mixture of five flowers of each stage. (C) Transcripts abundances ± SE of flower development-related genes, NaMYB305, NaNEC1, and NaCHAL determined by qPCR: irJAZd-8 plants were impaired in expression of NaMYB305 and NaNEC1genes in last stage of flower development (F4) while NaCHAL transcripts remained unaltered in irJAZd-8 compared to WT flowers. Bars ± SE in (C) show EF1α-normalized relative transcript abundances. Statistical differences in phytohormones, JA, JA-Ile, ethylene (n = 4) and transcript abundances (n = 4) were determined by Student t-test. Asterisks represent significant differences between WT and irJAZd in same stage of flowers (*P≤0.05, **P≤0.01, ***P≤0.001); n.s, not significantly different; FM, fresh mass.
Mentions: To elucidate the molecular mechanisms involved in NaJAZd-regulated flower abscission, we analyzed the levels of phytohormones and flower-related gene expression at four different developmental stages of flowers in WT and irJAZd-8 plants: buds (F1), early elongated flowers (∼10 mm length, F2), fully elongated flowers (still green and completely closed corollas, F3) and open flowers (completely opened white corollas, F4). First, we determined the expression of NaJAZd in WT and irJAZd-8 flowers to examine if (1) NaJAZd is expressed in stage-specific manner, and (2) to evaluate the efficiency of gene silencing in irJAZd flowers by RNAi. In WT plants, the gene showed comparably high transcript levels during F1–F3 stages but its expression declined in the F4 stage. NaJAZd transcript levels were strongly reduced in irJAZd-8 flowers compared to WT levels (Figure 6A).

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