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Seed after-ripening is a discrete developmental pathway associated with specific gene networks in Arabidopsis.

Carrera E, Holman T, Medhurst A, Dietrich D, Footitt S, Theodoulou FL, Holdsworth MJ - Plant J. (2007)

Bottom Line: Both metabolism and perception of the phytohormone abscisic acid (ABA) are important in the initiation and maintenance of dormancy.However, molecular mechanisms that regulate the capacity for dormancy or germination through AR are unknown.It was shown that secondary dormancy states reinstate AR status-specific gene expression patterns.

View Article: PubMed Central - PubMed

Affiliation: Crop Performance and Improvement Division, Rothamsted Research, Harpenden, Hertfordshire AL5 2JQ, UK.

ABSTRACT
After-ripening (AR) is a time and environment regulated process occurring in the dry seed, which determines the germination potential of seeds. Both metabolism and perception of the phytohormone abscisic acid (ABA) are important in the initiation and maintenance of dormancy. However, molecular mechanisms that regulate the capacity for dormancy or germination through AR are unknown. To understand the relationship between ABA and AR, we analysed genome expression in Arabidopsis thaliana mutants defective in seed ABA synthesis (aba1-1) or perception (abi1-1). Even though imbibed mutant seeds showed no dormancy, they exhibited changes in global gene expression resulting from dry AR that were comparable with changes occurring in wild-type (WT) seeds. Core gene sets were identified that were positively or negatively regulated by dry seed storage. Each set included a gene encoding repression or activation of ABA function (LPP2 and ABA1, respectively), thereby suggesting a mechanism through which dry AR may modulate subsequent germination potential in WT seeds. Application of exogenous ABA to after-ripened WT seeds did not reimpose characteristics of freshly harvested seeds on imbibed seed gene expression patterns. It was shown that secondary dormancy states reinstate AR status-specific gene expression patterns. A model is presented that separates the action of ABA in seed dormancy from AR and dry storage regulated gene expression. These results have major implications for the study of genetic mechanisms altered in seeds as a result of crop domestication into agriculture, and for seed behaviour during dormancy cycling in natural ecosystems.

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Influence of primary and secondary dormancy status on expression characteristics of after-ripening (AR)-regulated gene sets at 24 h of imbibition. Average ratio of expression of the ‘AR-upregulated’ and ‘AR-downregulated’ gene sets in Cvi are shown (Cadman et al., 2006). In each case ratio components are indicated. Normalized expression values and ratio averages for gene sets derived from microarray datasets (Table S3). Ratio values for ABA1 and LPP2 are plotted. A more complete box-plot analysis showing statistical data associated with means is given in Figure S4. For each gene set, data are presented for ratios for the following datasets: primary dormant 24-h imbibed (PD24), primary dormant 30 days imbibed (PD30), AR seeds imbibed in the dark (non-germinating, DL), AR seeds imbibed in the dark given a flash of red light to induce germination (LIG), secondary dormancy state 1 (SD1), secondary dormancy state 2 (SD2). AR, after-ripened; D, dormant; F, freshly harvested; S, stored seeds.
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fig05: Influence of primary and secondary dormancy status on expression characteristics of after-ripening (AR)-regulated gene sets at 24 h of imbibition. Average ratio of expression of the ‘AR-upregulated’ and ‘AR-downregulated’ gene sets in Cvi are shown (Cadman et al., 2006). In each case ratio components are indicated. Normalized expression values and ratio averages for gene sets derived from microarray datasets (Table S3). Ratio values for ABA1 and LPP2 are plotted. A more complete box-plot analysis showing statistical data associated with means is given in Figure S4. For each gene set, data are presented for ratios for the following datasets: primary dormant 24-h imbibed (PD24), primary dormant 30 days imbibed (PD30), AR seeds imbibed in the dark (non-germinating, DL), AR seeds imbibed in the dark given a flash of red light to induce germination (LIG), secondary dormancy state 1 (SD1), secondary dormancy state 2 (SD2). AR, after-ripened; D, dormant; F, freshly harvested; S, stored seeds.

Mentions: In addition to effects of exogenous application of hormones, environmental conditions of the imbibed seed, in particular light, can radically influence germination potential, but would not be expected to influence AR-associated gene expression, as this is a post-imbibition associated phenomenon. Treatment with red light is a common mechanism for breaking some types of dormancy (Bewley and Black, 1994). Cadman et al. (2006) showed that imbibed AR Arabidopsis Cvi accession seeds would not germinate in the dark (DL, light requiring), but would do so following a 4-h red light treatment (LIG, light induced to germinate). Therefore, DL and LIG seeds have completed AR, but have opposite germination potential. We used the transcriptome datasets of Cadman et al. (2006)to analyse the behaviour of the gene sets identified here. As both studies assayed transcriptomes of unchilled seeds imbibed on water–agarose at 24 h (mid phase II), direct comparison of datasets was possible. Analysis of developmental signatures showed that the LIG > PD24 (PD24, 24-h imbibed primary D seeds) and DL > PD24 differentially regulated gene sets were highly similar (Figure 2d), and virtually indistinguishable from the CviAR > D set (Figure 2a), despite exhibiting opposite germination potential. In addition, average ratios of expression of ‘AR-upregulated’ and ‘AR-downregulated’ gene sets were similar in both PD24/DL and PD24/LIG comparisons (Figure 5).


Seed after-ripening is a discrete developmental pathway associated with specific gene networks in Arabidopsis.

Carrera E, Holman T, Medhurst A, Dietrich D, Footitt S, Theodoulou FL, Holdsworth MJ - Plant J. (2007)

Influence of primary and secondary dormancy status on expression characteristics of after-ripening (AR)-regulated gene sets at 24 h of imbibition. Average ratio of expression of the ‘AR-upregulated’ and ‘AR-downregulated’ gene sets in Cvi are shown (Cadman et al., 2006). In each case ratio components are indicated. Normalized expression values and ratio averages for gene sets derived from microarray datasets (Table S3). Ratio values for ABA1 and LPP2 are plotted. A more complete box-plot analysis showing statistical data associated with means is given in Figure S4. For each gene set, data are presented for ratios for the following datasets: primary dormant 24-h imbibed (PD24), primary dormant 30 days imbibed (PD30), AR seeds imbibed in the dark (non-germinating, DL), AR seeds imbibed in the dark given a flash of red light to induce germination (LIG), secondary dormancy state 1 (SD1), secondary dormancy state 2 (SD2). AR, after-ripened; D, dormant; F, freshly harvested; S, stored seeds.
© Copyright Policy
Related In: Results  -  Collection

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fig05: Influence of primary and secondary dormancy status on expression characteristics of after-ripening (AR)-regulated gene sets at 24 h of imbibition. Average ratio of expression of the ‘AR-upregulated’ and ‘AR-downregulated’ gene sets in Cvi are shown (Cadman et al., 2006). In each case ratio components are indicated. Normalized expression values and ratio averages for gene sets derived from microarray datasets (Table S3). Ratio values for ABA1 and LPP2 are plotted. A more complete box-plot analysis showing statistical data associated with means is given in Figure S4. For each gene set, data are presented for ratios for the following datasets: primary dormant 24-h imbibed (PD24), primary dormant 30 days imbibed (PD30), AR seeds imbibed in the dark (non-germinating, DL), AR seeds imbibed in the dark given a flash of red light to induce germination (LIG), secondary dormancy state 1 (SD1), secondary dormancy state 2 (SD2). AR, after-ripened; D, dormant; F, freshly harvested; S, stored seeds.
Mentions: In addition to effects of exogenous application of hormones, environmental conditions of the imbibed seed, in particular light, can radically influence germination potential, but would not be expected to influence AR-associated gene expression, as this is a post-imbibition associated phenomenon. Treatment with red light is a common mechanism for breaking some types of dormancy (Bewley and Black, 1994). Cadman et al. (2006) showed that imbibed AR Arabidopsis Cvi accession seeds would not germinate in the dark (DL, light requiring), but would do so following a 4-h red light treatment (LIG, light induced to germinate). Therefore, DL and LIG seeds have completed AR, but have opposite germination potential. We used the transcriptome datasets of Cadman et al. (2006)to analyse the behaviour of the gene sets identified here. As both studies assayed transcriptomes of unchilled seeds imbibed on water–agarose at 24 h (mid phase II), direct comparison of datasets was possible. Analysis of developmental signatures showed that the LIG > PD24 (PD24, 24-h imbibed primary D seeds) and DL > PD24 differentially regulated gene sets were highly similar (Figure 2d), and virtually indistinguishable from the CviAR > D set (Figure 2a), despite exhibiting opposite germination potential. In addition, average ratios of expression of ‘AR-upregulated’ and ‘AR-downregulated’ gene sets were similar in both PD24/DL and PD24/LIG comparisons (Figure 5).

Bottom Line: Both metabolism and perception of the phytohormone abscisic acid (ABA) are important in the initiation and maintenance of dormancy.However, molecular mechanisms that regulate the capacity for dormancy or germination through AR are unknown.It was shown that secondary dormancy states reinstate AR status-specific gene expression patterns.

View Article: PubMed Central - PubMed

Affiliation: Crop Performance and Improvement Division, Rothamsted Research, Harpenden, Hertfordshire AL5 2JQ, UK.

ABSTRACT
After-ripening (AR) is a time and environment regulated process occurring in the dry seed, which determines the germination potential of seeds. Both metabolism and perception of the phytohormone abscisic acid (ABA) are important in the initiation and maintenance of dormancy. However, molecular mechanisms that regulate the capacity for dormancy or germination through AR are unknown. To understand the relationship between ABA and AR, we analysed genome expression in Arabidopsis thaliana mutants defective in seed ABA synthesis (aba1-1) or perception (abi1-1). Even though imbibed mutant seeds showed no dormancy, they exhibited changes in global gene expression resulting from dry AR that were comparable with changes occurring in wild-type (WT) seeds. Core gene sets were identified that were positively or negatively regulated by dry seed storage. Each set included a gene encoding repression or activation of ABA function (LPP2 and ABA1, respectively), thereby suggesting a mechanism through which dry AR may modulate subsequent germination potential in WT seeds. Application of exogenous ABA to after-ripened WT seeds did not reimpose characteristics of freshly harvested seeds on imbibed seed gene expression patterns. It was shown that secondary dormancy states reinstate AR status-specific gene expression patterns. A model is presented that separates the action of ABA in seed dormancy from AR and dry storage regulated gene expression. These results have major implications for the study of genetic mechanisms altered in seeds as a result of crop domestication into agriculture, and for seed behaviour during dormancy cycling in natural ecosystems.

Show MeSH