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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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Defense responses against specialized herbivore M. sexta are mostly unaltered in irJAZd plants.(A) Herbivory performance of M. sexta on rosette leaves of WT and two independent irJAZd lines (irJAZd-4 and -8) was determined by measuring larval mass at 4, 6, 8, 10 and 12 d after placement of freshly hatched neonates on the plants. Mean fresh masses ± SE of irJAZd-4 and -8-fed caterpillars (n = 20) were not significantly different from WT-fed caterpillars. (B) Mean ± SE levels of JA-Ile (n = 3) determined by LC- ESI-MS/MS showed no significant differences in irJAZd compared to WT leaves. (C) Mean ± SE levels of nicotine (n = 3) determined by HPLC coupled to PDA (Photo Diode Array) detector were significantly higher at 48 and 72 h after W+OS treatment of irJAZd plants compared to WT. Statistical differences in (A)–(C) were determined by one-way-ANOVA (P≤0.05). Different letters indicate significant differences among the different genotypes (WT vs. independent NaJAZd silenced lines, irJAZd-4, -8, 10) at the same time points; n.s, not significantly different; FM, fresh mass.
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pone-0057868-g002: Defense responses against specialized herbivore M. sexta are mostly unaltered in irJAZd plants.(A) Herbivory performance of M. sexta on rosette leaves of WT and two independent irJAZd lines (irJAZd-4 and -8) was determined by measuring larval mass at 4, 6, 8, 10 and 12 d after placement of freshly hatched neonates on the plants. Mean fresh masses ± SE of irJAZd-4 and -8-fed caterpillars (n = 20) were not significantly different from WT-fed caterpillars. (B) Mean ± SE levels of JA-Ile (n = 3) determined by LC- ESI-MS/MS showed no significant differences in irJAZd compared to WT leaves. (C) Mean ± SE levels of nicotine (n = 3) determined by HPLC coupled to PDA (Photo Diode Array) detector were significantly higher at 48 and 72 h after W+OS treatment of irJAZd plants compared to WT. Statistical differences in (A)–(C) were determined by one-way-ANOVA (P≤0.05). Different letters indicate significant differences among the different genotypes (WT vs. independent NaJAZd silenced lines, irJAZd-4, -8, 10) at the same time points; n.s, not significantly different; FM, fresh mass.

Mentions: To determine the role of NaJAZd in defense, we carried out performance assays with the specialist herbivore, M. sexta, with rosette stage WT and irJAZd plants. We placed a freshly hatched M. sexta neonate on the leaves of each 20 replicates of WT and irJAZd-4 and -8 plants and determined the mass of caterpillars after 4, 6, 8, 10, and 12 d of feeding on the plants (Figure 2A). NaJAZd-silencing did not affect the performance of M. sexta caterpillars as on both irJAZd genotypes and WT plants the larvae had similar growth rates.


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)

Defense responses against specialized herbivore M. sexta are mostly unaltered in irJAZd plants.(A) Herbivory performance of M. sexta on rosette leaves of WT and two independent irJAZd lines (irJAZd-4 and -8) was determined by measuring larval mass at 4, 6, 8, 10 and 12 d after placement of freshly hatched neonates on the plants. Mean fresh masses ± SE of irJAZd-4 and -8-fed caterpillars (n = 20) were not significantly different from WT-fed caterpillars. (B) Mean ± SE levels of JA-Ile (n = 3) determined by LC- ESI-MS/MS showed no significant differences in irJAZd compared to WT leaves. (C) Mean ± SE levels of nicotine (n = 3) determined by HPLC coupled to PDA (Photo Diode Array) detector were significantly higher at 48 and 72 h after W+OS treatment of irJAZd plants compared to WT. Statistical differences in (A)–(C) were determined by one-way-ANOVA (P≤0.05). Different letters indicate significant differences among the different genotypes (WT vs. independent NaJAZd silenced lines, irJAZd-4, -8, 10) at the same time points; n.s, not significantly different; FM, fresh mass.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3585257&req=5

pone-0057868-g002: Defense responses against specialized herbivore M. sexta are mostly unaltered in irJAZd plants.(A) Herbivory performance of M. sexta on rosette leaves of WT and two independent irJAZd lines (irJAZd-4 and -8) was determined by measuring larval mass at 4, 6, 8, 10 and 12 d after placement of freshly hatched neonates on the plants. Mean fresh masses ± SE of irJAZd-4 and -8-fed caterpillars (n = 20) were not significantly different from WT-fed caterpillars. (B) Mean ± SE levels of JA-Ile (n = 3) determined by LC- ESI-MS/MS showed no significant differences in irJAZd compared to WT leaves. (C) Mean ± SE levels of nicotine (n = 3) determined by HPLC coupled to PDA (Photo Diode Array) detector were significantly higher at 48 and 72 h after W+OS treatment of irJAZd plants compared to WT. Statistical differences in (A)–(C) were determined by one-way-ANOVA (P≤0.05). Different letters indicate significant differences among the different genotypes (WT vs. independent NaJAZd silenced lines, irJAZd-4, -8, 10) at the same time points; n.s, not significantly different; FM, fresh mass.
Mentions: To determine the role of NaJAZd in defense, we carried out performance assays with the specialist herbivore, M. sexta, with rosette stage WT and irJAZd plants. We placed a freshly hatched M. sexta neonate on the leaves of each 20 replicates of WT and irJAZd-4 and -8 plants and determined the mass of caterpillars after 4, 6, 8, 10, and 12 d of feeding on the plants (Figure 2A). NaJAZd-silencing did not affect the performance of M. sexta caterpillars as on both irJAZd genotypes and WT plants the larvae had similar growth rates.

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