Different hormonal regulation of cellular differentiation and function in nucellar projection and endosperm transfer cells: A microdissection-based transcriptome study of young barley grains

Johannes Thiel, Diana Weier, Nese Sreenivasulu, Marc Strickert, Nicola Weichert, Michael Melzer, Tobias Czauderna, Ulrich Wobus, Hans Weber, Winfriede Weschke

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78 Citations (Scopus)

Abstract

Nucellar projection (NP) and endosperm transfer cells (ETC) are essential tissues in growing barley (Hordeum vulgare) grains, responsible for nutrient transfer from maternal to filial tissues, endosperm/embryo nutrition, and grain development. A laser microdissection pressure catapulting-based transcriptome analysis was established to study NP and ETC separately using a barley 12K macroarray. A major challenge was to isolate high-quality mRNA from preembedded, fixed tissue while maintaining tissue integrity. We show that probes generated from fixed and embedded tissue sections represent largely the transcriptome (>70%) of nonchemically treated and nonamplified references. In NP, the top-down gradient of cellular differentiation is reflected by the expression of C3HC4-type ubiquitin ligases and different histone genes, cell wall biosynthesis and expansin/extensin genes, as well as genes involved in programmed cell death-related proteolysis coupled to nitrogen remobilization, indicating distinct areas simultaneously undergoing mitosis, cell elongation, and disintegration. Activated gene expression related to gibberellin synthesis and function suggests a regulatory role for gibberellins in establishment of the differentiation gradient. Upregulation of plasmalemma-intrinsic protein and tonoplast-intrinsic protein genes indicates involvement in nutrient transfer and/or unloading. In ETC, AP2/EREBP-like transcription factors and ethylene functions are transcriptionally activated, a response possibly coupled to activated defense mechanisms. Transcriptional activation of nucleotide sugar metabolism may be attributed to ascorbate synthesis and/or cell wall biosynthesis. These processes are potentially controlled by trehalose-6-P synthase/phosphatase, as suggested by expression of their respective genes. Up-regulation of amino acid permeases in ETC indicates important roles in active nutrient uptake from the apoplastic space into the endosperm.

Original languageEnglish
Pages (from-to)1436-1452
Number of pages17
JournalPlant Physiology
Volume148
Issue number3
DOIs
Publication statusPublished - 1 Nov 2008
Externally publishedYes

Cite this

Thiel, Johannes ; Weier, Diana ; Sreenivasulu, Nese ; Strickert, Marc ; Weichert, Nicola ; Melzer, Michael ; Czauderna, Tobias ; Wobus, Ulrich ; Weber, Hans ; Weschke, Winfriede. / Different hormonal regulation of cellular differentiation and function in nucellar projection and endosperm transfer cells : A microdissection-based transcriptome study of young barley grains. In: Plant Physiology. 2008 ; Vol. 148, No. 3. pp. 1436-1452.
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abstract = "Nucellar projection (NP) and endosperm transfer cells (ETC) are essential tissues in growing barley (Hordeum vulgare) grains, responsible for nutrient transfer from maternal to filial tissues, endosperm/embryo nutrition, and grain development. A laser microdissection pressure catapulting-based transcriptome analysis was established to study NP and ETC separately using a barley 12K macroarray. A major challenge was to isolate high-quality mRNA from preembedded, fixed tissue while maintaining tissue integrity. We show that probes generated from fixed and embedded tissue sections represent largely the transcriptome (>70{\%}) of nonchemically treated and nonamplified references. In NP, the top-down gradient of cellular differentiation is reflected by the expression of C3HC4-type ubiquitin ligases and different histone genes, cell wall biosynthesis and expansin/extensin genes, as well as genes involved in programmed cell death-related proteolysis coupled to nitrogen remobilization, indicating distinct areas simultaneously undergoing mitosis, cell elongation, and disintegration. Activated gene expression related to gibberellin synthesis and function suggests a regulatory role for gibberellins in establishment of the differentiation gradient. Upregulation of plasmalemma-intrinsic protein and tonoplast-intrinsic protein genes indicates involvement in nutrient transfer and/or unloading. In ETC, AP2/EREBP-like transcription factors and ethylene functions are transcriptionally activated, a response possibly coupled to activated defense mechanisms. Transcriptional activation of nucleotide sugar metabolism may be attributed to ascorbate synthesis and/or cell wall biosynthesis. These processes are potentially controlled by trehalose-6-P synthase/phosphatase, as suggested by expression of their respective genes. Up-regulation of amino acid permeases in ETC indicates important roles in active nutrient uptake from the apoplastic space into the endosperm.",
author = "Johannes Thiel and Diana Weier and Nese Sreenivasulu and Marc Strickert and Nicola Weichert and Michael Melzer and Tobias Czauderna and Ulrich Wobus and Hans Weber and Winfriede Weschke",
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Different hormonal regulation of cellular differentiation and function in nucellar projection and endosperm transfer cells : A microdissection-based transcriptome study of young barley grains. / Thiel, Johannes; Weier, Diana; Sreenivasulu, Nese; Strickert, Marc; Weichert, Nicola; Melzer, Michael; Czauderna, Tobias; Wobus, Ulrich; Weber, Hans; Weschke, Winfriede.

In: Plant Physiology, Vol. 148, No. 3, 01.11.2008, p. 1436-1452.

Research output: Contribution to journalArticleResearchpeer-review

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T2 - A microdissection-based transcriptome study of young barley grains

AU - Thiel, Johannes

AU - Weier, Diana

AU - Sreenivasulu, Nese

AU - Strickert, Marc

AU - Weichert, Nicola

AU - Melzer, Michael

AU - Czauderna, Tobias

AU - Wobus, Ulrich

AU - Weber, Hans

AU - Weschke, Winfriede

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