Transcriptome and metabolome reveal distinct carbon allocation patterns during internode sugar accumulation in different sorghum genotypes

Yin Li, Wenqin Wang, Yaping Feng, Min Tu, Peter E. Wittich, Nicholas J. Bate, Joachim Messing

Research output: Contribution to journalArticle

Abstract

Sweet sorghum accumulates large amounts of soluble sugar in its stem. However, a system-based understanding of this carbohydrate allocation process is lacking. Here, we compared the dynamic transcriptome and metabolome between the conversion line R9188 and its two parents, sweet sorghum RIO and grain sorghum BTx406 that have contrasting sugar-accumulating phenotypes. We identified two features of sucrose metabolism, stable concentrations of sugar phosphates in RIO and opposite trend of trehalose-6-phosphate (T6P) between RIO vs R9188/BTx406. Integration of transcriptome and metabolome revealed R9188 is partially active in starch metabolism together with medium sucrose level, whereas sweet sorghum had the highest sucrose concentration and remained highly active in sucrose, starch, and cell wall metabolism post-anthesis. Similar expression pattern of genes involved in sucrose degradation decreased the pool of sugar phosphates for precursors of starch and cell wall synthesis in R9188 and BTx406. Differential T6P signal between RIO vs R9188/BTx406 is associated with introgression of T6P regulators from BTx406 into R9188, including C-group bZIP and trehalose 6-phosphate phosphatase (TPP). The inverted T6P signalling in R9188 appears to down-regulate sucrose and starch metabolism partly through transcriptome reprogramming, whereas introgressed metabolic genes could be related to reduced cell wall metabolism. Our results show that coordinated primary metabolic pathways lead to high sucrose demand and accumulation in sweet sorghum, providing us with targets for genetic improvements of carbohydrate allocation in bioenergy crops.

Original languageEnglish (US)
Pages (from-to)472-487
Number of pages16
JournalPlant biotechnology journal
Volume17
Issue number2
DOIs
StatePublished - Feb 1 2019

Fingerprint

metabolome
Sorghum
Metabolome
Transcriptome
transcriptome
internodes
Sucrose
Carbon
Genotype
sweet sorghum
sucrose
sugars
trehalose
carbon
genotype
Starch
metabolism
starch
phosphates
Cell Wall

All Science Journal Classification (ASJC) codes

  • Biotechnology
  • Agronomy and Crop Science
  • Plant Science

Keywords

  • RNA-seq
  • gene expression
  • internode
  • introgression
  • metabolomics
  • sorghum
  • sugar accumulation
  • trehalose-6-phosphate signalling

Cite this

Li, Yin ; Wang, Wenqin ; Feng, Yaping ; Tu, Min ; Wittich, Peter E. ; Bate, Nicholas J. ; Messing, Joachim. / Transcriptome and metabolome reveal distinct carbon allocation patterns during internode sugar accumulation in different sorghum genotypes. In: Plant biotechnology journal. 2019 ; Vol. 17, No. 2. pp. 472-487.
@article{afa93145874d4e55a89e54ae3eae0539,
title = "Transcriptome and metabolome reveal distinct carbon allocation patterns during internode sugar accumulation in different sorghum genotypes",
abstract = "Sweet sorghum accumulates large amounts of soluble sugar in its stem. However, a system-based understanding of this carbohydrate allocation process is lacking. Here, we compared the dynamic transcriptome and metabolome between the conversion line R9188 and its two parents, sweet sorghum RIO and grain sorghum BTx406 that have contrasting sugar-accumulating phenotypes. We identified two features of sucrose metabolism, stable concentrations of sugar phosphates in RIO and opposite trend of trehalose-6-phosphate (T6P) between RIO vs R9188/BTx406. Integration of transcriptome and metabolome revealed R9188 is partially active in starch metabolism together with medium sucrose level, whereas sweet sorghum had the highest sucrose concentration and remained highly active in sucrose, starch, and cell wall metabolism post-anthesis. Similar expression pattern of genes involved in sucrose degradation decreased the pool of sugar phosphates for precursors of starch and cell wall synthesis in R9188 and BTx406. Differential T6P signal between RIO vs R9188/BTx406 is associated with introgression of T6P regulators from BTx406 into R9188, including C-group bZIP and trehalose 6-phosphate phosphatase (TPP). The inverted T6P signalling in R9188 appears to down-regulate sucrose and starch metabolism partly through transcriptome reprogramming, whereas introgressed metabolic genes could be related to reduced cell wall metabolism. Our results show that coordinated primary metabolic pathways lead to high sucrose demand and accumulation in sweet sorghum, providing us with targets for genetic improvements of carbohydrate allocation in bioenergy crops.",
keywords = "RNA-seq, gene expression, internode, introgression, metabolomics, sorghum, sugar accumulation, trehalose-6-phosphate signalling",
author = "Yin Li and Wenqin Wang and Yaping Feng and Min Tu and Wittich, {Peter E.} and Bate, {Nicholas J.} and Joachim Messing",
year = "2019",
month = "2",
day = "1",
doi = "10.1111/pbi.12991",
language = "English (US)",
volume = "17",
pages = "472--487",
journal = "Plant Biotechnology Journal",
issn = "1467-7644",
publisher = "Wiley-Blackwell",
number = "2",

}

Transcriptome and metabolome reveal distinct carbon allocation patterns during internode sugar accumulation in different sorghum genotypes. / Li, Yin; Wang, Wenqin; Feng, Yaping; Tu, Min; Wittich, Peter E.; Bate, Nicholas J.; Messing, Joachim.

In: Plant biotechnology journal, Vol. 17, No. 2, 01.02.2019, p. 472-487.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Transcriptome and metabolome reveal distinct carbon allocation patterns during internode sugar accumulation in different sorghum genotypes

AU - Li, Yin

AU - Wang, Wenqin

AU - Feng, Yaping

AU - Tu, Min

AU - Wittich, Peter E.

AU - Bate, Nicholas J.

AU - Messing, Joachim

PY - 2019/2/1

Y1 - 2019/2/1

N2 - Sweet sorghum accumulates large amounts of soluble sugar in its stem. However, a system-based understanding of this carbohydrate allocation process is lacking. Here, we compared the dynamic transcriptome and metabolome between the conversion line R9188 and its two parents, sweet sorghum RIO and grain sorghum BTx406 that have contrasting sugar-accumulating phenotypes. We identified two features of sucrose metabolism, stable concentrations of sugar phosphates in RIO and opposite trend of trehalose-6-phosphate (T6P) between RIO vs R9188/BTx406. Integration of transcriptome and metabolome revealed R9188 is partially active in starch metabolism together with medium sucrose level, whereas sweet sorghum had the highest sucrose concentration and remained highly active in sucrose, starch, and cell wall metabolism post-anthesis. Similar expression pattern of genes involved in sucrose degradation decreased the pool of sugar phosphates for precursors of starch and cell wall synthesis in R9188 and BTx406. Differential T6P signal between RIO vs R9188/BTx406 is associated with introgression of T6P regulators from BTx406 into R9188, including C-group bZIP and trehalose 6-phosphate phosphatase (TPP). The inverted T6P signalling in R9188 appears to down-regulate sucrose and starch metabolism partly through transcriptome reprogramming, whereas introgressed metabolic genes could be related to reduced cell wall metabolism. Our results show that coordinated primary metabolic pathways lead to high sucrose demand and accumulation in sweet sorghum, providing us with targets for genetic improvements of carbohydrate allocation in bioenergy crops.

AB - Sweet sorghum accumulates large amounts of soluble sugar in its stem. However, a system-based understanding of this carbohydrate allocation process is lacking. Here, we compared the dynamic transcriptome and metabolome between the conversion line R9188 and its two parents, sweet sorghum RIO and grain sorghum BTx406 that have contrasting sugar-accumulating phenotypes. We identified two features of sucrose metabolism, stable concentrations of sugar phosphates in RIO and opposite trend of trehalose-6-phosphate (T6P) between RIO vs R9188/BTx406. Integration of transcriptome and metabolome revealed R9188 is partially active in starch metabolism together with medium sucrose level, whereas sweet sorghum had the highest sucrose concentration and remained highly active in sucrose, starch, and cell wall metabolism post-anthesis. Similar expression pattern of genes involved in sucrose degradation decreased the pool of sugar phosphates for precursors of starch and cell wall synthesis in R9188 and BTx406. Differential T6P signal between RIO vs R9188/BTx406 is associated with introgression of T6P regulators from BTx406 into R9188, including C-group bZIP and trehalose 6-phosphate phosphatase (TPP). The inverted T6P signalling in R9188 appears to down-regulate sucrose and starch metabolism partly through transcriptome reprogramming, whereas introgressed metabolic genes could be related to reduced cell wall metabolism. Our results show that coordinated primary metabolic pathways lead to high sucrose demand and accumulation in sweet sorghum, providing us with targets for genetic improvements of carbohydrate allocation in bioenergy crops.

KW - RNA-seq

KW - gene expression

KW - internode

KW - introgression

KW - metabolomics

KW - sorghum

KW - sugar accumulation

KW - trehalose-6-phosphate signalling

UR - http://www.scopus.com/inward/record.url?scp=85053447335&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85053447335&partnerID=8YFLogxK

U2 - 10.1111/pbi.12991

DO - 10.1111/pbi.12991

M3 - Article

C2 - 30051585

AN - SCOPUS:85053447335

VL - 17

SP - 472

EP - 487

JO - Plant Biotechnology Journal

JF - Plant Biotechnology Journal

SN - 1467-7644

IS - 2

ER -