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Columnar apple primary roots share some features of the columnar-specific gene expression profile of aerial plant parts as evidenced by RNA-Seq analysis.

Petersen R, Djozgic H, Rieger B, Rapp S, Schmidt ER - BMC Plant Biol. (2015)

Bottom Line: Radicles mainly express genes associated with primary metabolism, growth and development.Homozygous columnar embryos are viable and form normal radicles under natural conditions, and selection towards heterozygous plants most likely occurs due to breeders' preferences.Cell wall and phytohormone biosynthesis and metabolism experience differential regulation in columnar radicles.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular Genetics, Johannes Gutenberg-University, Mainz, D-55128, Germany. peterser@uni-mainz.de.

ABSTRACT

Background: Primary roots (radicles) represent the first visible developmental stages of the plant and are crucial for nutrient supply and the integration of environmental signals. Few studies have analyzed primary roots at a molecular level, and were mostly limited to Arabidopsis. Here we study the primary root transcriptomes of standard type, heterozygous columnar and homozygous columnar apple (Malus x domestica) by RNA-Seq and quantitative real-time PCR. The columnar growth habit is characterized by a stunted main axis and the development of short fruit spurs instead of long lateral branches. This compact growth possesses economic potential because it allows high density planting and mechanical harvesting of the trees. Its molecular basis has been identified as a nested Gypsy-44 retrotransposon insertion; however the link between the insertion and the phenotype as well as the timing of the phenotype emergence are as yet unclear. We extend the transcriptomic studies of columnar tissues to the radicles, which are the earliest developmental stage and investigate whether homozygous columnar seedlings are viable.

Results: Radicles mainly express genes associated with primary metabolism, growth and development. About 200 genes show differential regulation in a comparison of heterozygous columnar radicles with non-columnar radicles, whereas the comparison of homozygous columnar radicles with non-columnar radicles yields about 300 differentially regulated genes. Genes involved in cellulose and phenylpropanoid biosynthesis, cell wall modification, transcription and translation, ethylene and jasmonate biosynthesis are upregulated in columnar radicles. Genes in the vicinity of the columnar-specific Gypsy-44 insertion experience an especially strong differential regulation: the direct downstream neighbor, dmr6-like, is downregulated in heterozygous columnar radicles, but strongly upregulated in columnar shoot apical meristems.

Conclusions: The transcriptomic profile of primary roots reflects their pivotal role in growth and development. Homozygous columnar embryos are viable and form normal radicles under natural conditions, and selection towards heterozygous plants most likely occurs due to breeders' preferences. Cell wall and phytohormone biosynthesis and metabolism experience differential regulation in columnar radicles. Presumably the first step of the differential regulation most likely happens within the region of the retrotransposon insertion and its tissue-specificity suggests involvement of one (or several) tissue-specific regulator(s).

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Differential gene expression in heterozygous compared with non-columnar primary roots. LOG2 fold changes of significantly differentially expressed genes (normalized to the non-columnar sample) as listed in Additional file 3 were imported and visualized in MapMan for the heterozygous columnar sample with regard to a metabolism overview (A), pathogen/pest attack (B) and transcription and translation (C). Genes upregulated in heterozygous columnar radicles are shown as red boxes, downregulated genes are shown as blue boxes.
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Fig2: Differential gene expression in heterozygous compared with non-columnar primary roots. LOG2 fold changes of significantly differentially expressed genes (normalized to the non-columnar sample) as listed in Additional file 3 were imported and visualized in MapMan for the heterozygous columnar sample with regard to a metabolism overview (A), pathogen/pest attack (B) and transcription and translation (C). Genes upregulated in heterozygous columnar radicles are shown as red boxes, downregulated genes are shown as blue boxes.

Mentions: The comparison of non-columnar versus heterozygous columnar primary roots identified 194 significantly differentially expressed genes (see Additional file 3). Visualization in MapMan (Figure 2) showed that many genes were upregulated in heterozygous columnar roots when compared with non-columnar roots. This applied to genes involved in cellulose synthesis, cell wall modification and degradation, glycolysis, the oxidative pentose phosphate pathway, the biosynthesis of phenylpropanoids, starch and fatty acids and the mitochondrial electron transport. On the other hand, single genes involved in lipid and starch degradation and photorespiration were downregulated in the heterozygous columnar radicles (Figure 2A). Some genes associated with stress reactions such as ethylene biosynthesis and signaling (Figure 2B) were also more highly expressed in heterozygous columnar than in non-columnar primary roots. This also holds true for genes encoding the plastidic ribosomal proteins (Figure 2C).Figure 2


Columnar apple primary roots share some features of the columnar-specific gene expression profile of aerial plant parts as evidenced by RNA-Seq analysis.

Petersen R, Djozgic H, Rieger B, Rapp S, Schmidt ER - BMC Plant Biol. (2015)

Differential gene expression in heterozygous compared with non-columnar primary roots. LOG2 fold changes of significantly differentially expressed genes (normalized to the non-columnar sample) as listed in Additional file 3 were imported and visualized in MapMan for the heterozygous columnar sample with regard to a metabolism overview (A), pathogen/pest attack (B) and transcription and translation (C). Genes upregulated in heterozygous columnar radicles are shown as red boxes, downregulated genes are shown as blue boxes.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4352258&req=5

Fig2: Differential gene expression in heterozygous compared with non-columnar primary roots. LOG2 fold changes of significantly differentially expressed genes (normalized to the non-columnar sample) as listed in Additional file 3 were imported and visualized in MapMan for the heterozygous columnar sample with regard to a metabolism overview (A), pathogen/pest attack (B) and transcription and translation (C). Genes upregulated in heterozygous columnar radicles are shown as red boxes, downregulated genes are shown as blue boxes.
Mentions: The comparison of non-columnar versus heterozygous columnar primary roots identified 194 significantly differentially expressed genes (see Additional file 3). Visualization in MapMan (Figure 2) showed that many genes were upregulated in heterozygous columnar roots when compared with non-columnar roots. This applied to genes involved in cellulose synthesis, cell wall modification and degradation, glycolysis, the oxidative pentose phosphate pathway, the biosynthesis of phenylpropanoids, starch and fatty acids and the mitochondrial electron transport. On the other hand, single genes involved in lipid and starch degradation and photorespiration were downregulated in the heterozygous columnar radicles (Figure 2A). Some genes associated with stress reactions such as ethylene biosynthesis and signaling (Figure 2B) were also more highly expressed in heterozygous columnar than in non-columnar primary roots. This also holds true for genes encoding the plastidic ribosomal proteins (Figure 2C).Figure 2

Bottom Line: Radicles mainly express genes associated with primary metabolism, growth and development.Homozygous columnar embryos are viable and form normal radicles under natural conditions, and selection towards heterozygous plants most likely occurs due to breeders' preferences.Cell wall and phytohormone biosynthesis and metabolism experience differential regulation in columnar radicles.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular Genetics, Johannes Gutenberg-University, Mainz, D-55128, Germany. peterser@uni-mainz.de.

ABSTRACT

Background: Primary roots (radicles) represent the first visible developmental stages of the plant and are crucial for nutrient supply and the integration of environmental signals. Few studies have analyzed primary roots at a molecular level, and were mostly limited to Arabidopsis. Here we study the primary root transcriptomes of standard type, heterozygous columnar and homozygous columnar apple (Malus x domestica) by RNA-Seq and quantitative real-time PCR. The columnar growth habit is characterized by a stunted main axis and the development of short fruit spurs instead of long lateral branches. This compact growth possesses economic potential because it allows high density planting and mechanical harvesting of the trees. Its molecular basis has been identified as a nested Gypsy-44 retrotransposon insertion; however the link between the insertion and the phenotype as well as the timing of the phenotype emergence are as yet unclear. We extend the transcriptomic studies of columnar tissues to the radicles, which are the earliest developmental stage and investigate whether homozygous columnar seedlings are viable.

Results: Radicles mainly express genes associated with primary metabolism, growth and development. About 200 genes show differential regulation in a comparison of heterozygous columnar radicles with non-columnar radicles, whereas the comparison of homozygous columnar radicles with non-columnar radicles yields about 300 differentially regulated genes. Genes involved in cellulose and phenylpropanoid biosynthesis, cell wall modification, transcription and translation, ethylene and jasmonate biosynthesis are upregulated in columnar radicles. Genes in the vicinity of the columnar-specific Gypsy-44 insertion experience an especially strong differential regulation: the direct downstream neighbor, dmr6-like, is downregulated in heterozygous columnar radicles, but strongly upregulated in columnar shoot apical meristems.

Conclusions: The transcriptomic profile of primary roots reflects their pivotal role in growth and development. Homozygous columnar embryos are viable and form normal radicles under natural conditions, and selection towards heterozygous plants most likely occurs due to breeders' preferences. Cell wall and phytohormone biosynthesis and metabolism experience differential regulation in columnar radicles. Presumably the first step of the differential regulation most likely happens within the region of the retrotransposon insertion and its tissue-specificity suggests involvement of one (or several) tissue-specific regulator(s).

Show MeSH
Related in: MedlinePlus