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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 counteracts flower abscission in N. attenuata.Each individual plant was placed in an individual plastic tray (30×52 cm) in the glasshouse to avoid mixing of abscised flowers, and number of buds (A), elongated flowers (B), open flowers (C), and abscised flowers (D) in each plant from 42 d to 63 d after germination was determined in 3 d intervals. Both irJAZd-4 and -8 plants had similar number of buds and elongated flowers as WT plants but displayed significantly reduced numbers of open flowers (significant at 48, 51, 63 d) and higher numbers of abscised flowers (significant at most time points) compared to WT plants. Significant differences between genotypes were determined separately for each time point by one-way-ANOVA (*P≤0.05, **P≤0.01, ***P≤0.001).
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pone-0057868-g005: NaJAZd counteracts flower abscission in N. attenuata.Each individual plant was placed in an individual plastic tray (30×52 cm) in the glasshouse to avoid mixing of abscised flowers, and number of buds (A), elongated flowers (B), open flowers (C), and abscised flowers (D) in each plant from 42 d to 63 d after germination was determined in 3 d intervals. Both irJAZd-4 and -8 plants had similar number of buds and elongated flowers as WT plants but displayed significantly reduced numbers of open flowers (significant at 48, 51, 63 d) and higher numbers of abscised flowers (significant at most time points) compared to WT plants. Significant differences between genotypes were determined separately for each time point by one-way-ANOVA (*P≤0.05, **P≤0.01, ***P≤0.001).

Mentions: We hypothesized that NaJAZd was involved in flower initiation, which would ultimately affect the lifetime seed capsule production in irJAZd plants. However, the numbers of flower buds in irJAZd plants seemed comparable in WT and irJAZd plants and flower parameters such as degree of flower opening, pollen maturation or length of pistils were not visibly altered in irJAZd plants. In addition, we examined if self-pollination ability was impaired in irJAZd flowers by hand pollination experiments using ripe pollen from the same flowers and spreading it on stigma with fine brush (Figure S5). The hand pollination, assuring that each stigma received sufficient amount of pollen in a timely coordinated fashion, failed to recover the formation of seed capsules in irJAZd plants to WT levels. These results suggested that irJAZd flowers have normal anthesis and otherwise completely normal morphology (Figure S6) but experience another problem in flower development. We therefore conducted another more detailed experiment in which we quantified flower production distinguishing 4 categories: buds, elongated flowers, fully opened flowers and abscised flowers, which were counted every 3 d starting 42 d after germination when the first buds and a few elongated flowers but no open flowers were present on the plants (Figure 5). To prevent mixing of abscised flowers from different plants, we placed each single plant in individual 30×52 cm plastic tray which captured all abscised flowers from a single plant. While irJAZd plants had similar or even higher number of buds and elongated flowers, they produced significantly fewer open flowers on 48, 51, and 63 d-old plants and correspondingly higher numbers of abscised flowers at these and additional time points. Notably, the abscised flowers were all fully open flowers; abscission of younger stages or flower buds was not occurring. These data suggested that the function of NaJAZd is to prevent flower abscission in the later stages of flower development that directly affects lifetime production of seed capsules and fitness of N. attenuata. Whether this was mediated by direct function of NaJAZd in flowers was examined next.


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 counteracts flower abscission in N. attenuata.Each individual plant was placed in an individual plastic tray (30×52 cm) in the glasshouse to avoid mixing of abscised flowers, and number of buds (A), elongated flowers (B), open flowers (C), and abscised flowers (D) in each plant from 42 d to 63 d after germination was determined in 3 d intervals. Both irJAZd-4 and -8 plants had similar number of buds and elongated flowers as WT plants but displayed significantly reduced numbers of open flowers (significant at 48, 51, 63 d) and higher numbers of abscised flowers (significant at most time points) compared to WT plants. Significant differences between genotypes were determined separately for each time point by one-way-ANOVA (*P≤0.05, **P≤0.01, ***P≤0.001).
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3585257&req=5

pone-0057868-g005: NaJAZd counteracts flower abscission in N. attenuata.Each individual plant was placed in an individual plastic tray (30×52 cm) in the glasshouse to avoid mixing of abscised flowers, and number of buds (A), elongated flowers (B), open flowers (C), and abscised flowers (D) in each plant from 42 d to 63 d after germination was determined in 3 d intervals. Both irJAZd-4 and -8 plants had similar number of buds and elongated flowers as WT plants but displayed significantly reduced numbers of open flowers (significant at 48, 51, 63 d) and higher numbers of abscised flowers (significant at most time points) compared to WT plants. Significant differences between genotypes were determined separately for each time point by one-way-ANOVA (*P≤0.05, **P≤0.01, ***P≤0.001).
Mentions: We hypothesized that NaJAZd was involved in flower initiation, which would ultimately affect the lifetime seed capsule production in irJAZd plants. However, the numbers of flower buds in irJAZd plants seemed comparable in WT and irJAZd plants and flower parameters such as degree of flower opening, pollen maturation or length of pistils were not visibly altered in irJAZd plants. In addition, we examined if self-pollination ability was impaired in irJAZd flowers by hand pollination experiments using ripe pollen from the same flowers and spreading it on stigma with fine brush (Figure S5). The hand pollination, assuring that each stigma received sufficient amount of pollen in a timely coordinated fashion, failed to recover the formation of seed capsules in irJAZd plants to WT levels. These results suggested that irJAZd flowers have normal anthesis and otherwise completely normal morphology (Figure S6) but experience another problem in flower development. We therefore conducted another more detailed experiment in which we quantified flower production distinguishing 4 categories: buds, elongated flowers, fully opened flowers and abscised flowers, which were counted every 3 d starting 42 d after germination when the first buds and a few elongated flowers but no open flowers were present on the plants (Figure 5). To prevent mixing of abscised flowers from different plants, we placed each single plant in individual 30×52 cm plastic tray which captured all abscised flowers from a single plant. While irJAZd plants had similar or even higher number of buds and elongated flowers, they produced significantly fewer open flowers on 48, 51, and 63 d-old plants and correspondingly higher numbers of abscised flowers at these and additional time points. Notably, the abscised flowers were all fully open flowers; abscission of younger stages or flower buds was not occurring. These data suggested that the function of NaJAZd is to prevent flower abscission in the later stages of flower development that directly affects lifetime production of seed capsules and fitness of N. attenuata. Whether this was mediated by direct function of NaJAZd in flowers was examined next.

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