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Whole transcriptome profiling of maize during early somatic embryogenesis reveals altered expression of stress factors and embryogenesis-related genes.

Salvo SA, Hirsch CN, Buell CR, Kaeppler SM, Kaeppler HF - PLoS ONE (2014)

Bottom Line: We utilized RNA based sequencing (RNA-seq) to characterize the transcriptome of immature embryo explants of the highly embryogenic and regenerable maize genotype A188 at 0, 24, 36, 48, and 72 hours after placement of explants on tissue culture initiation medium.Genes annotated as functioning in stress response, such as glutathione-S-transferases and germin-like proteins, and genes involved with hormone transport, such as PINFORMED, increased in expression over 8-fold in the study.Maize genes with high sequence similarity to genes previously described in the initiation of embryogenic cultures, such as transcription factors BABY BOOM, LEAFY COTYLEDON, and AGAMOUS, and important receptor-like kinases such as SOMATIC EMBRYOGENESIS RECEPTOR LIKE KINASES and CLAVATA, were also expressed in this time course study.

View Article: PubMed Central - PubMed

Affiliation: Department of Agronomy, University of Wisconsin, Madison, Wisconsin, United States of America.

ABSTRACT
Embryogenic tissue culture systems are utilized in propagation and genetic engineering of crop plants, but applications are limited by genotype-dependent culture response. To date, few genes necessary for embryogenic callus formation have been identified or characterized. The goal of this research was to enhance our understanding of gene expression during maize embryogenic tissue culture initiation. In this study, we highlight the expression of candidate genes that have been previously regarded in the literature as having important roles in somatic embryogenesis. We utilized RNA based sequencing (RNA-seq) to characterize the transcriptome of immature embryo explants of the highly embryogenic and regenerable maize genotype A188 at 0, 24, 36, 48, and 72 hours after placement of explants on tissue culture initiation medium. Genes annotated as functioning in stress response, such as glutathione-S-transferases and germin-like proteins, and genes involved with hormone transport, such as PINFORMED, increased in expression over 8-fold in the study. Maize genes with high sequence similarity to genes previously described in the initiation of embryogenic cultures, such as transcription factors BABY BOOM, LEAFY COTYLEDON, and AGAMOUS, and important receptor-like kinases such as SOMATIC EMBRYOGENESIS RECEPTOR LIKE KINASES and CLAVATA, were also expressed in this time course study. By combining results from whole genome transcriptome analysis with an in depth review of key genes that play a role in the onset of embryogenesis, we propose a model of coordinated expression of somatic embryogenesis-related genes, providing an improved understanding of genomic factors involved in the early steps of embryogenic culture initiation in maize and other plant species.

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Relative expression of coexpressed somatic embryogenesis-related genes.A proposed model of somatic embryogenesis-related gene expression networks as determined by coexpression (solid lines) with a correlation coefficient greater or equal to 0.9 between genes expressed during the early stages of somatic embryogenesis. Relative expression of transcripts detected in immature zygotic embryo explant tissues in tissue culture were detected in the inbred line A188 and reported as the average log2 expression displayed by color coded values as depicted by the figure legend for each gene. The first left most box under each gene name is the average log2 transformation of fragments per kilobase of exon model per million fragments mapped (FPKM) at 0 h, the second box at 24 h, the third at 36 h, the fourth at 48 h, and the fifth right most box is the average FPKM 72 h. Glutathione-S-transferases (GSTs) and germin-like proteins (GLPs) are stress response genes that are triggered in early somatic embryogenesis. BABY BOOM (BBM), an APETALA-like ethylene-responsive element transcription factor, and LEAFY COTYLEDON2 (LEC2), a B3 domain transcription factor, promote somatic embryogenesis. PINFORMED (PIN) genes mediate auxin transport and establish essential endogenous auxin concentrations in the cell. SOMATIC EMBRYOGENESIS RECEPTOR LIKE KINASES (SERK) genes are also involved in somatic embryogenesis and hormone metabolism. WUSCHEL (WUS), a homeodomain transcription factor, regulates stem cell fate during embryo formation and development. AGAMOUS like-15 (AGL15), a MADS box transcription factor, also promotes somatic embryo formation and is also involved in meristem development. WUSCHEL-related homeobox domain (WOX) genes have also been detected during somatic embryogenesis in embryogenic genotypes but not in non-embryogenic genotypes.
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pone-0111407-g005: Relative expression of coexpressed somatic embryogenesis-related genes.A proposed model of somatic embryogenesis-related gene expression networks as determined by coexpression (solid lines) with a correlation coefficient greater or equal to 0.9 between genes expressed during the early stages of somatic embryogenesis. Relative expression of transcripts detected in immature zygotic embryo explant tissues in tissue culture were detected in the inbred line A188 and reported as the average log2 expression displayed by color coded values as depicted by the figure legend for each gene. The first left most box under each gene name is the average log2 transformation of fragments per kilobase of exon model per million fragments mapped (FPKM) at 0 h, the second box at 24 h, the third at 36 h, the fourth at 48 h, and the fifth right most box is the average FPKM 72 h. Glutathione-S-transferases (GSTs) and germin-like proteins (GLPs) are stress response genes that are triggered in early somatic embryogenesis. BABY BOOM (BBM), an APETALA-like ethylene-responsive element transcription factor, and LEAFY COTYLEDON2 (LEC2), a B3 domain transcription factor, promote somatic embryogenesis. PINFORMED (PIN) genes mediate auxin transport and establish essential endogenous auxin concentrations in the cell. SOMATIC EMBRYOGENESIS RECEPTOR LIKE KINASES (SERK) genes are also involved in somatic embryogenesis and hormone metabolism. WUSCHEL (WUS), a homeodomain transcription factor, regulates stem cell fate during embryo formation and development. AGAMOUS like-15 (AGL15), a MADS box transcription factor, also promotes somatic embryo formation and is also involved in meristem development. WUSCHEL-related homeobox domain (WOX) genes have also been detected during somatic embryogenesis in embryogenic genotypes but not in non-embryogenic genotypes.

Mentions: Somatic embryogenesis-related genes have been extensively characterized in Arabidopsis; however, relatively few have been evaluated in maize. Using transcriptome data of maize in embryogenic tissue culture initiation, this study provides an in-depth look at the major candidate genes discussed in previous reviews and research studies on somatic embryogenesis. Moreover, we propose a model (Figure 5) based on coordinated expression (Table S8) of somatic embryogenesis-related genes highlighted in this study and their relative expression in early embryogenic tissue culture response.


Whole transcriptome profiling of maize during early somatic embryogenesis reveals altered expression of stress factors and embryogenesis-related genes.

Salvo SA, Hirsch CN, Buell CR, Kaeppler SM, Kaeppler HF - PLoS ONE (2014)

Relative expression of coexpressed somatic embryogenesis-related genes.A proposed model of somatic embryogenesis-related gene expression networks as determined by coexpression (solid lines) with a correlation coefficient greater or equal to 0.9 between genes expressed during the early stages of somatic embryogenesis. Relative expression of transcripts detected in immature zygotic embryo explant tissues in tissue culture were detected in the inbred line A188 and reported as the average log2 expression displayed by color coded values as depicted by the figure legend for each gene. The first left most box under each gene name is the average log2 transformation of fragments per kilobase of exon model per million fragments mapped (FPKM) at 0 h, the second box at 24 h, the third at 36 h, the fourth at 48 h, and the fifth right most box is the average FPKM 72 h. Glutathione-S-transferases (GSTs) and germin-like proteins (GLPs) are stress response genes that are triggered in early somatic embryogenesis. BABY BOOM (BBM), an APETALA-like ethylene-responsive element transcription factor, and LEAFY COTYLEDON2 (LEC2), a B3 domain transcription factor, promote somatic embryogenesis. PINFORMED (PIN) genes mediate auxin transport and establish essential endogenous auxin concentrations in the cell. SOMATIC EMBRYOGENESIS RECEPTOR LIKE KINASES (SERK) genes are also involved in somatic embryogenesis and hormone metabolism. WUSCHEL (WUS), a homeodomain transcription factor, regulates stem cell fate during embryo formation and development. AGAMOUS like-15 (AGL15), a MADS box transcription factor, also promotes somatic embryo formation and is also involved in meristem development. WUSCHEL-related homeobox domain (WOX) genes have also been detected during somatic embryogenesis in embryogenic genotypes but not in non-embryogenic genotypes.
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Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4214754&req=5

pone-0111407-g005: Relative expression of coexpressed somatic embryogenesis-related genes.A proposed model of somatic embryogenesis-related gene expression networks as determined by coexpression (solid lines) with a correlation coefficient greater or equal to 0.9 between genes expressed during the early stages of somatic embryogenesis. Relative expression of transcripts detected in immature zygotic embryo explant tissues in tissue culture were detected in the inbred line A188 and reported as the average log2 expression displayed by color coded values as depicted by the figure legend for each gene. The first left most box under each gene name is the average log2 transformation of fragments per kilobase of exon model per million fragments mapped (FPKM) at 0 h, the second box at 24 h, the third at 36 h, the fourth at 48 h, and the fifth right most box is the average FPKM 72 h. Glutathione-S-transferases (GSTs) and germin-like proteins (GLPs) are stress response genes that are triggered in early somatic embryogenesis. BABY BOOM (BBM), an APETALA-like ethylene-responsive element transcription factor, and LEAFY COTYLEDON2 (LEC2), a B3 domain transcription factor, promote somatic embryogenesis. PINFORMED (PIN) genes mediate auxin transport and establish essential endogenous auxin concentrations in the cell. SOMATIC EMBRYOGENESIS RECEPTOR LIKE KINASES (SERK) genes are also involved in somatic embryogenesis and hormone metabolism. WUSCHEL (WUS), a homeodomain transcription factor, regulates stem cell fate during embryo formation and development. AGAMOUS like-15 (AGL15), a MADS box transcription factor, also promotes somatic embryo formation and is also involved in meristem development. WUSCHEL-related homeobox domain (WOX) genes have also been detected during somatic embryogenesis in embryogenic genotypes but not in non-embryogenic genotypes.
Mentions: Somatic embryogenesis-related genes have been extensively characterized in Arabidopsis; however, relatively few have been evaluated in maize. Using transcriptome data of maize in embryogenic tissue culture initiation, this study provides an in-depth look at the major candidate genes discussed in previous reviews and research studies on somatic embryogenesis. Moreover, we propose a model (Figure 5) based on coordinated expression (Table S8) of somatic embryogenesis-related genes highlighted in this study and their relative expression in early embryogenic tissue culture response.

Bottom Line: We utilized RNA based sequencing (RNA-seq) to characterize the transcriptome of immature embryo explants of the highly embryogenic and regenerable maize genotype A188 at 0, 24, 36, 48, and 72 hours after placement of explants on tissue culture initiation medium.Genes annotated as functioning in stress response, such as glutathione-S-transferases and germin-like proteins, and genes involved with hormone transport, such as PINFORMED, increased in expression over 8-fold in the study.Maize genes with high sequence similarity to genes previously described in the initiation of embryogenic cultures, such as transcription factors BABY BOOM, LEAFY COTYLEDON, and AGAMOUS, and important receptor-like kinases such as SOMATIC EMBRYOGENESIS RECEPTOR LIKE KINASES and CLAVATA, were also expressed in this time course study.

View Article: PubMed Central - PubMed

Affiliation: Department of Agronomy, University of Wisconsin, Madison, Wisconsin, United States of America.

ABSTRACT
Embryogenic tissue culture systems are utilized in propagation and genetic engineering of crop plants, but applications are limited by genotype-dependent culture response. To date, few genes necessary for embryogenic callus formation have been identified or characterized. The goal of this research was to enhance our understanding of gene expression during maize embryogenic tissue culture initiation. In this study, we highlight the expression of candidate genes that have been previously regarded in the literature as having important roles in somatic embryogenesis. We utilized RNA based sequencing (RNA-seq) to characterize the transcriptome of immature embryo explants of the highly embryogenic and regenerable maize genotype A188 at 0, 24, 36, 48, and 72 hours after placement of explants on tissue culture initiation medium. Genes annotated as functioning in stress response, such as glutathione-S-transferases and germin-like proteins, and genes involved with hormone transport, such as PINFORMED, increased in expression over 8-fold in the study. Maize genes with high sequence similarity to genes previously described in the initiation of embryogenic cultures, such as transcription factors BABY BOOM, LEAFY COTYLEDON, and AGAMOUS, and important receptor-like kinases such as SOMATIC EMBRYOGENESIS RECEPTOR LIKE KINASES and CLAVATA, were also expressed in this time course study. By combining results from whole genome transcriptome analysis with an in depth review of key genes that play a role in the onset of embryogenesis, we propose a model of coordinated expression of somatic embryogenesis-related genes, providing an improved understanding of genomic factors involved in the early steps of embryogenic culture initiation in maize and other plant species.

Show MeSH
Related in: MedlinePlus