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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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Plant damage caused by herbivores in N. attenuata’s native habitat.EV and irJAZd-8 plants were planted in a size-matched paired-design in their native habitat, Great Basin Desert, Utah, USA and damage by native herbivores was scored throughout the 2010 field season. Herbivore damage was determined as the % of leaf canopy damaged by (1) cell-damaging feeding of Tupiocoris notatus mirid bugs (mirids), (2) the small feeding holes that characterize flea beetle feeding, and (3) leaf chewing Lepidopteran larvae (Noctuidae). No significant differences (n.s) between the two genotypes determined by Student t-test were observed.
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pone-0057868-g003: Plant damage caused by herbivores in N. attenuata’s native habitat.EV and irJAZd-8 plants were planted in a size-matched paired-design in their native habitat, Great Basin Desert, Utah, USA and damage by native herbivores was scored throughout the 2010 field season. Herbivore damage was determined as the % of leaf canopy damaged by (1) cell-damaging feeding of Tupiocoris notatus mirid bugs (mirids), (2) the small feeding holes that characterize flea beetle feeding, and (3) leaf chewing Lepidopteran larvae (Noctuidae). No significant differences (n.s) between the two genotypes determined by Student t-test were observed.

Mentions: In natural environments, plants are exposed to substantially more stresses compared to their relatively safe containment in the glasshouse. We therefore examined if NaJAZd-silenced plants could perform differently in high stress conditions characterized by high UV irradiance, high and variable temperatures, low humidity and communities of voracious native herbivores. In the 2010 field season, we planted empty vector-transformed (EV) and irJAZd-8 plants in a pairwise design in the native habitat of N. attenuata (Great Basin Desert, Utah, USA) and compared herbivore damage to these plants (Figure 3). Field-grown irJAZd plants showed similar levels of damage from native herbivores, mirids (Tupiocoris notatus), flea beetles (Epitrix spp.), and noctuidae larvae (Spodoptera spp.) compared to WT plants, providing additional evidence that NaJAZd has only a minor role in defense against biotic and abiotic stresses. This prompted our intensive search for alternative functions of this protein.


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)

Plant damage caused by herbivores in N. attenuata’s native habitat.EV and irJAZd-8 plants were planted in a size-matched paired-design in their native habitat, Great Basin Desert, Utah, USA and damage by native herbivores was scored throughout the 2010 field season. Herbivore damage was determined as the % of leaf canopy damaged by (1) cell-damaging feeding of Tupiocoris notatus mirid bugs (mirids), (2) the small feeding holes that characterize flea beetle feeding, and (3) leaf chewing Lepidopteran larvae (Noctuidae). No significant differences (n.s) between the two genotypes determined by Student t-test were observed.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0057868-g003: Plant damage caused by herbivores in N. attenuata’s native habitat.EV and irJAZd-8 plants were planted in a size-matched paired-design in their native habitat, Great Basin Desert, Utah, USA and damage by native herbivores was scored throughout the 2010 field season. Herbivore damage was determined as the % of leaf canopy damaged by (1) cell-damaging feeding of Tupiocoris notatus mirid bugs (mirids), (2) the small feeding holes that characterize flea beetle feeding, and (3) leaf chewing Lepidopteran larvae (Noctuidae). No significant differences (n.s) between the two genotypes determined by Student t-test were observed.
Mentions: In natural environments, plants are exposed to substantially more stresses compared to their relatively safe containment in the glasshouse. We therefore examined if NaJAZd-silenced plants could perform differently in high stress conditions characterized by high UV irradiance, high and variable temperatures, low humidity and communities of voracious native herbivores. In the 2010 field season, we planted empty vector-transformed (EV) and irJAZd-8 plants in a pairwise design in the native habitat of N. attenuata (Great Basin Desert, Utah, USA) and compared herbivore damage to these plants (Figure 3). Field-grown irJAZd plants showed similar levels of damage from native herbivores, mirids (Tupiocoris notatus), flea beetles (Epitrix spp.), and noctuidae larvae (Spodoptera spp.) compared to WT plants, providing additional evidence that NaJAZd has only a minor role in defense against biotic and abiotic stresses. This prompted our intensive search for alternative functions of this protein.

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
Related in: MedlinePlus