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Title: A Dual-Promoter Gene Orchestrates the Sucrose-Coordinated Synthesis of Starch and Fructan in Barley

Abstract

Sequential carbohydrate synthesis is important for plant survival because it guarantees energy supplies for growth and development during plant ontogeny and reproduction. Starch and fructan are two important carbohydrates in many flowering plants and in human diets. Understanding this coordinated starch and fructan synthesis and unraveling how plants allocate photosynthates and prioritize different carbohydrate synthesis for survival could lead to improvements to cereals in agriculture for the purposes of greater food security and production quality. Here, we report a system from a single gene in barley employing two alternative promoters, one intronic/exonic, to generate two sequence-overlapping but functionally opposing transcription factors, in sensing sucrose, potentially via sucrose/glucose/fructose/trehalose 6-phosphate signaling. The system employs an autoregulatory mechanism in perceiving a sucrose-controlled trans activity on one promoter and orchestrating the coordinated starch and fructan synthesis by competitive transcription factor binding on the other promoter. As a case in point for the physiological roles of the system, we have demonstrated that this multitasking system can be exploited in breeding barley with tailored amounts of fructan to produce healthy food ingredients. The identification of an intron/exon-spanning promoter in a hosting gene, resulting in proteins with distinct functions, adds to the complexity of plant genomes.

Authors:
 [1];  [2];  [3];  [1];  [4];  [4];  [3];  [5];  [3];  [6];  [7];  [6];  [8];  [9];  [6];  [3]
  1. Hunan Agricultural University (China). Hunan Provincial Key Laboratory of Crop Germplasm Innovation and Utilization; Swedish University of Agricultural Sciences, Uppsala (Sweden). Department of Plant Biology, Uppsala BioCenter, Linnean Centre for Plant Biology
  2. Hunan Agricultural University (China). Hunan Provincial Key Laboratory of Crop Germplasm Innovation and Utilization and Key Laboratory of Education, Department of Hunan Province on Plant Genetics and Molecular Biology, College of Bioscience and Biotechnology; Swedish University of Agricultural Sciences, Uppsala (Sweden). Department of Plant Biology, Uppsala BioCenter, Linnean Centre for Plant Biology
  3. Swedish University of Agricultural Sciences, Uppsala (Sweden). Department of Plant Biology, Uppsala BioCenter, Linnean Centre for Plant Biology
  4. Swedish University of Agricultural Sciences, Uppsala (Sweden). Department of Chemistry and Biotechnology, Uppsala BioCenter
  5. The Swedish NMR Centre at University of Gothenburg (Sweden)
  6. Swedish University of Agricultural Sciences, Uppsala (Sweden). Department of Molecular Sciences, Uppsala BioCenter
  7. Hunan Agricultural University (China). Hunan Provincial Key Laboratory of Crop Germplasm Innovation and Utilization and Key Laboratory of Education, Department of Hunan Province on Plant Genetics and Molecular Biology, College of Bioscience and Biotechnology
  8. Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab. (EMSL)
  9. Hunan Agricultural University (China). Hunan Provincial Key Laboratory of Crop Germplasm Innovation and Utilization
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1413506
Report Number(s):
PNNL-SA-130518
Journal ID: ISSN 1674-2052; PII: S1674205217303325
Grant/Contract Number:  
AC05-76RL01830
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Molecular Plant
Additional Journal Information:
Journal Volume: 10; Journal Issue: 12; Journal ID: ISSN 1674-2052
Publisher:
Elsevier
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Jin, Yunkai, Fei, Mingliang, Rosenquist, Sara, Jin, Lu, Gohil, Suresh, Sandström, Corine, Olsson, Helena, Persson, Cecilia, Höglund, Anna-Stina, Fransson, Gunnel, Ruan, Ying, Åman, Per, Jansson, Christer, Liu, Chunlin, Andersson, Roger, and Sun, Chuanxin. A Dual-Promoter Gene Orchestrates the Sucrose-Coordinated Synthesis of Starch and Fructan in Barley. United States: N. p., 2017. Web. doi:10.1016/J.MOLP.2017.10.013.
Jin, Yunkai, Fei, Mingliang, Rosenquist, Sara, Jin, Lu, Gohil, Suresh, Sandström, Corine, Olsson, Helena, Persson, Cecilia, Höglund, Anna-Stina, Fransson, Gunnel, Ruan, Ying, Åman, Per, Jansson, Christer, Liu, Chunlin, Andersson, Roger, & Sun, Chuanxin. A Dual-Promoter Gene Orchestrates the Sucrose-Coordinated Synthesis of Starch and Fructan in Barley. United States. doi:10.1016/J.MOLP.2017.10.013.
Jin, Yunkai, Fei, Mingliang, Rosenquist, Sara, Jin, Lu, Gohil, Suresh, Sandström, Corine, Olsson, Helena, Persson, Cecilia, Höglund, Anna-Stina, Fransson, Gunnel, Ruan, Ying, Åman, Per, Jansson, Christer, Liu, Chunlin, Andersson, Roger, and Sun, Chuanxin. Tue . "A Dual-Promoter Gene Orchestrates the Sucrose-Coordinated Synthesis of Starch and Fructan in Barley". United States. doi:10.1016/J.MOLP.2017.10.013. https://www.osti.gov/servlets/purl/1413506.
@article{osti_1413506,
title = {A Dual-Promoter Gene Orchestrates the Sucrose-Coordinated Synthesis of Starch and Fructan in Barley},
author = {Jin, Yunkai and Fei, Mingliang and Rosenquist, Sara and Jin, Lu and Gohil, Suresh and Sandström, Corine and Olsson, Helena and Persson, Cecilia and Höglund, Anna-Stina and Fransson, Gunnel and Ruan, Ying and Åman, Per and Jansson, Christer and Liu, Chunlin and Andersson, Roger and Sun, Chuanxin},
abstractNote = {Sequential carbohydrate synthesis is important for plant survival because it guarantees energy supplies for growth and development during plant ontogeny and reproduction. Starch and fructan are two important carbohydrates in many flowering plants and in human diets. Understanding this coordinated starch and fructan synthesis and unraveling how plants allocate photosynthates and prioritize different carbohydrate synthesis for survival could lead to improvements to cereals in agriculture for the purposes of greater food security and production quality. Here, we report a system from a single gene in barley employing two alternative promoters, one intronic/exonic, to generate two sequence-overlapping but functionally opposing transcription factors, in sensing sucrose, potentially via sucrose/glucose/fructose/trehalose 6-phosphate signaling. The system employs an autoregulatory mechanism in perceiving a sucrose-controlled trans activity on one promoter and orchestrating the coordinated starch and fructan synthesis by competitive transcription factor binding on the other promoter. As a case in point for the physiological roles of the system, we have demonstrated that this multitasking system can be exploited in breeding barley with tailored amounts of fructan to produce healthy food ingredients. The identification of an intron/exon-spanning promoter in a hosting gene, resulting in proteins with distinct functions, adds to the complexity of plant genomes.},
doi = {10.1016/J.MOLP.2017.10.013},
journal = {Molecular Plant},
number = 12,
volume = 10,
place = {United States},
year = {Tue Nov 07 00:00:00 EST 2017},
month = {Tue Nov 07 00:00:00 EST 2017}
}

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