Transcriptomic analysis of transgressive segregants revealed the central role of photosynthetic capacity and efficiency in biomass accumulation in sugarcane
Abstract
Sugarcane is among the most efficient crops in converting solar energy into chemical energy. However, due to its complex genome structure and inheritance, the genetic and molecular basis of biomass yield in sugarcane is still largely unknown. We created an F2 segregating population by crossing S. officinarum and S. spontaneum and evaluated the biomass yield of the F2 individuals. The F2 individuals exhibited clear transgressive segregation in biomass yield. We sequenced transcriptomes of source and sink tissues from 12 selected extreme segregants to explore the molecular basis of high biomass yield for future breeding of high-yielding energy canes. Among the 103,664 assembled unigenes, 10,115 and 728 showed significant differential expression patterns between the two extreme segregating groups in the top visible dewlap leaf and the 9th culm internode, respectively. The most enriched functional categories were photosynthesis and fermentation in the high-biomass and the low-biomass groups, respectively. Our results revealed that high-biomass yield was mainly determined by assimilation of carbon in source tissues. The high-level expression of fermentative genes in the low-biomass group was likely induced by their low-energy status. Group-specific expression alleles which can be applied in the development of new high-yielding energy cane varieties via molecular breeding were identified.
- Authors:
-
[1];
[6]
- Texas A & M Univ., College Station, TX (United States)
- Hawaii Agriculture Research Center, Kunia, HI (United States)
- Univ. of Illinois, Urbana-Champaign, IL (United States)
- Texas A & M Univ., Weslaco, TX (United States) AgriLife Research Center
- Univ. of Illinois, Urbana-Champaign, IL (United States); Fujian Agriculture and Forestry Univ., Fuzhou (China)
- Texas A & M Univ., College Station, TX (United States); Fujian Agriculture and Forestry Univ., Fuzhou (China)
- Publication Date:
- Research Org.:
- Univ. of Illinois at Urbana-Champaign, IL (United States)
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1500033
- Grant/Contract Number:
- SC0010686
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Scientific Reports
- Additional Journal Information:
- Journal Volume: 8; Journal Issue: 1; Journal ID: ISSN 2045-2322
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Singh, Ratnesh, Jones, Tyler, Wai, Ching Man, Jifon, John, Nagai, Chifumi, Ming, Ray, and Yu, Qingyi. Transcriptomic analysis of transgressive segregants revealed the central role of photosynthetic capacity and efficiency in biomass accumulation in sugarcane. United States: N. p., 2018.
Web. doi:10.1038/s41598-018-22798-5.
Singh, Ratnesh, Jones, Tyler, Wai, Ching Man, Jifon, John, Nagai, Chifumi, Ming, Ray, & Yu, Qingyi. Transcriptomic analysis of transgressive segregants revealed the central role of photosynthetic capacity and efficiency in biomass accumulation in sugarcane. United States. https://doi.org/10.1038/s41598-018-22798-5
Singh, Ratnesh, Jones, Tyler, Wai, Ching Man, Jifon, John, Nagai, Chifumi, Ming, Ray, and Yu, Qingyi. Tue .
"Transcriptomic analysis of transgressive segregants revealed the central role of photosynthetic capacity and efficiency in biomass accumulation in sugarcane". United States. https://doi.org/10.1038/s41598-018-22798-5. https://www.osti.gov/servlets/purl/1500033.
@article{osti_1500033,
title = {Transcriptomic analysis of transgressive segregants revealed the central role of photosynthetic capacity and efficiency in biomass accumulation in sugarcane},
author = {Singh, Ratnesh and Jones, Tyler and Wai, Ching Man and Jifon, John and Nagai, Chifumi and Ming, Ray and Yu, Qingyi},
abstractNote = {Sugarcane is among the most efficient crops in converting solar energy into chemical energy. However, due to its complex genome structure and inheritance, the genetic and molecular basis of biomass yield in sugarcane is still largely unknown. We created an F2 segregating population by crossing S. officinarum and S. spontaneum and evaluated the biomass yield of the F2 individuals. The F2 individuals exhibited clear transgressive segregation in biomass yield. We sequenced transcriptomes of source and sink tissues from 12 selected extreme segregants to explore the molecular basis of high biomass yield for future breeding of high-yielding energy canes. Among the 103,664 assembled unigenes, 10,115 and 728 showed significant differential expression patterns between the two extreme segregating groups in the top visible dewlap leaf and the 9th culm internode, respectively. The most enriched functional categories were photosynthesis and fermentation in the high-biomass and the low-biomass groups, respectively. Our results revealed that high-biomass yield was mainly determined by assimilation of carbon in source tissues. The high-level expression of fermentative genes in the low-biomass group was likely induced by their low-energy status. Group-specific expression alleles which can be applied in the development of new high-yielding energy cane varieties via molecular breeding were identified.},
doi = {10.1038/s41598-018-22798-5},
journal = {Scientific Reports},
number = 1,
volume = 8,
place = {United States},
year = {Tue Mar 13 00:00:00 EDT 2018},
month = {Tue Mar 13 00:00:00 EDT 2018}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 8 works
Citation information provided by
Web of Science
Web of Science
Figures / Tables:
Figure 1: Distribution of the stalk volumes of the S. officinarum × S. spontaneum F2 clones.
All figures and tables
(6 total)
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
RFLP Mapping in Cultivated Sugarcane ( Saccharum spp.): Genome Organization in a Highly Polyploid and Aneuploid Interspecific Hybrid
journal, March 1996
- Grivet, Laurent; D'Hont, Angelique; Roques, Daniele
- Genetics, Vol. 142, Issue 3
Characterisation of the double genome structure of modern sugarcane cultivars (Saccharum spp.) by molecular cytogenetics
journal, March 1996
- D'Hont, A.; Grivet, L.; Feldmann, P.
- MGG Molecular & General Genetics, Vol. 250, Issue 4
Multi-scale comparative transcriptome analysis reveals key genes and metabolic reprogramming processes associated with oil palm fruit abscission
journal, February 2021
- Fooyontphanich, Kim; Morcillo, Fabienne; Joët, Thierry
- BMC Plant Biology, Vol. 21, Issue 1
RNAmmer: consistent and rapid annotation of ribosomal RNA genes
journal, April 2007
- Lagesen, Karin; Hallin, Peter; Rødland, Einar Andreas
- Nucleic Acids Research, Vol. 35, Issue 9
De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis
journal, July 2013
- Haas, Brian J.; Papanicolaou, Alexie; Yassour, Moran
- Nature Protocols, Vol. 8, Issue 8
The Brazilian biofuels industry
journal, January 2008
- Goldemberg, José
- Biotechnology for Biofuels, Vol. 1, Issue 1
Genetic dissection of a modern sugarcane cultivar (Saccharum spp.). I. Genome mapping with AFLP markers
journal, July 2001
- Hoarau, J. -Y.; Offmann, B.; D’Hont, A.
- Theoretical and Applied Genetics, Vol. 103, Issue 1
SignalP 4.0: discriminating signal peptides from transmembrane regions
journal, September 2011
- Petersen, Thomas Nordahl; Brunak, Søren; von Heijne, Gunnar
- Nature Methods, Vol. 8, Issue 10
Transcriptional profiling of two contrasting genotypes uncovers molecular mechanisms underlying salt tolerance in alfalfa
journal, March 2021
- Kaundal, Rakesh; Duhan, Naveen; Acharya, Biswa R.
- Scientific Reports, Vol. 11, Issue 1
Identification and characterisation of sugarcane intergeneric hybrids, Saccharum officinarum x Erianthus arundinaceus, with molecular markers and DNA in situ hybridisation
journal, July 1995
- D'Hont, A.; Rao, P. S.; Feldmann, P.
- Theoretical and Applied Genetics, Vol. 91, Issue 2
Regulation of glycolysis in heterotrophic cell suspension cultures of Chenopodium rubrum in response to proton fluxes at the plasmalemma
journal, January 1991
- Hatzfeld, Wolf-Dieter; Stitt, Mark
- Physiologia Plantarum, Vol. 81, Issue 1
Characterisation of the double genome structure of modern sugarcane cultivars (
journal, January 1996
- D’Hont, Angélique; Grivet, Laurent; Feldmann, Philippe
- MGG Molecular & General Genetics, Vol. 250, Issue 4
Determination of basic chromosome numbers in the genus Saccharum by physical mapping of ribosomal RNA genes
journal, April 1998
- D'Hont, Angélique; Ison, David; Alix, Karine
- Genome, Vol. 41, Issue 2
Determination of basic chromosome numbers in the genus Saccharum by physical mapping of ribosomal RNA genes
journal, April 1998
- D'Hont, Angélique; Ison, David; Alix, Karine
- Genome, Vol. 41, Issue 2
Carbon Partitioning during Sucrose Accumulation in Sugarcane Internodal Tissue
journal, December 1997
- Whittaker, A.; Botha, F. C.
- Plant Physiology, Vol. 115, Issue 4
Orthologous comparison in a gene-rich region among grasses reveals stability in the sugarcane polyploid genome: Genomic stability in the highly polyploid sugarcane
journal, April 2007
- Jannoo, Nazeema; Grivet, Laurent; Chantret, Nathalie
- The Plant Journal, Vol. 50, Issue 4
Extensive Allelic Variation in Gene Expression in Populus F 1 Hybrids
journal, December 2007
- Zhuang, Yan; Adams, Keith L.
- Genetics, Vol. 177, Issue 4
Full-length transcriptome assembly from RNA-Seq data without a reference genome
journal, May 2011
- Grabherr, Manfred G.; Haas, Brian J.; Yassour, Moran
- Nature Biotechnology, Vol. 29, Issue 7
Pfam: the protein families database
journal, November 2013
- Finn, Robert D.; Bateman, Alex; Clements, Jody
- Nucleic Acids Research, Vol. 42, Issue D1
What is the maximum efficiency with which photosynthesis can convert solar energy into biomass?
journal, April 2008
- Zhu, Xin-Guang; Long, Stephen P.; Ort, Donald R.
- Current Opinion in Biotechnology, Vol. 19, Issue 2
Mercator: a fast and simple web server for genome scale functional annotation of plant sequence data: Mercator: sequence functional annotation server
journal, December 2013
- Lohse, Marc; Nagel, Axel; Herter, Thomas
- Plant, Cell & Environment, Vol. 37, Issue 5
Genetic dissection of a modern sugarcane cultivar (Saccharum spp.). I. Genome mapping with AFLP markers
journal, July 2001
- Hoarau, J. -Y.; Offmann, B.; D’Hont, A.
- Theoretical and Applied Genetics, Vol. 103, Issue 1
Coordination of carbon supply and plant growth
journal, September 2007
- Smith, Alison M.; Stitt, Mark
- Plant, Cell & Environment, Vol. 30, Issue 9
SignalP 4.0: discriminating signal peptides from transmembrane regions
journal, September 2011
- Petersen, Thomas Nordahl; Brunak, Søren; von Heijne, Gunnar
- Nature Methods, Vol. 8, Issue 10
The Brazilian biofuels industry
journal, January 2008
- Goldemberg, José
- Biotechnology for Biofuels, Vol. 1, Issue 1
Plants to power: bioenergy to fuel the future
journal, August 2008
- Yuan, Joshua S.; Tiller, Kelly H.; Al-Ahmad, Hani
- Trends in Plant Science, Vol. 13, Issue 8
BCFtools/csq: haplotype-aware variant consequences
journal, February 2017
- Danecek, Petr; McCarthy, Shane A.
- Bioinformatics, Vol. 33, Issue 13
Genome remodelling in three modern S. officinarumxS. spontaneum sugarcane cultivars
journal, March 2004
- Cuadrado, A.
- Journal of Experimental Botany, Vol. 55, Issue 398
Supply and demand: sink regulation of sugar accumulation in sugarcane
journal, January 2009
- McCormick, A. J.; Watt, D. A.; Cramer, M. D.
- Journal of Experimental Botany, Vol. 60, Issue 2
Diurnal Changes in Maize Leaf Photosynthesis: I. Carbon Exchange Rate, Assimilate Export Rate, and Enzyme Activities
journal, February 1987
- Kalt-Torres, Willy; Kerr, Phillip S.; Usuda, Hideaki
- Plant Physiology, Vol. 83, Issue 2
Challenges in homology search: HMMER3 and convergent evolution of coiled-coil regions
journal, April 2013
- Mistry, Jaina; Finn, Robert D.; Eddy, Sean R.
- Nucleic Acids Research, Vol. 41, Issue 12
Regulation of Respiration and Fermentation to Control the Plant Internal Oxygen Concentration
journal, December 2008
- Zabalza, Ana; van Dongen, Joost T.; Froehlich, Anja
- Plant Physiology, Vol. 149, Issue 2
mapman: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes
journal, March 2004
- Thimm, Oliver; Bläsing, Oliver; Gibon, Yves
- The Plant Journal, Vol. 37, Issue 6, p. 914-939
edgeR: a Bioconductor package for differential expression analysis of digital gene expression data
journal, November 2009
- Robinson, M. D.; McCarthy, D. J.; Smyth, G. K.
- Bioinformatics, Vol. 26, Issue 1
Opposing T cell responses in experimental autoimmune encephalomyelitis
journal, August 2019
- Saligrama, Naresha; Zhao, Fan; Sikora, Michael J.
- Nature, Vol. 572, Issue 7770
Targeting redox metabolism: the perfect storm induced by acrylamide poisoning in the brain
journal, January 2020
- Raldúa, Demetrio; Casado, Marta; Prats, Eva
- Scientific Reports, Vol. 10, Issue 1
Genome remodelling in three modern S. officinarumxS. spontaneum sugarcane cultivars
journal, March 2004
- Cuadrado, A.
- Journal of Experimental Botany, Vol. 55, Issue 398
Supply and demand: sink regulation of sugar accumulation in sugarcane
journal, January 2009
- McCormick, A. J.; Watt, D. A.; Cramer, M. D.
- Journal of Experimental Botany, Vol. 60, Issue 2
Diurnal Changes in Maize Leaf Photosynthesis: I. Carbon Exchange Rate, Assimilate Export Rate, and Enzyme Activities
journal, February 1987
- Kalt-Torres, Willy; Kerr, Phillip S.; Usuda, Hideaki
- Plant Physiology, Vol. 83, Issue 2
Coordination of carbon supply and plant growth
journal, September 2007
- Smith, Alison M.; Stitt, Mark
- Plant, Cell & Environment, Vol. 30, Issue 9
Diurnal Changes in Maize Leaf Photosynthesis: II. Levels of Metabolic Intermediates of Sucrose Synthesis and the Regulatory Metabolite Fructose 2,6-Bisphosphate
journal, February 1987
- Usuda, Hideaki; Kalt-Torres, Willy; Kerr, Phillip S.
- Plant Physiology, Vol. 83, Issue 2
Sink strength regulates photosynthesis in sugarcane
journal, September 2006
- McCormick, A. J.; Cramer, M. D.; Watt, D. A.
- New Phytologist, Vol. 171, Issue 4
Fast gapped-read alignment with Bowtie 2
journal, March 2012
- Langmead, Ben; Salzberg, Steven L.
- Nature Methods, Vol. 9, Issue 4
Regulation of Respiration and Fermentation to Control the Plant Internal Oxygen Concentration
journal, December 2008
- Zabalza, Ana; van Dongen, Joost T.; Froehlich, Anja
- Plant Physiology, Vol. 149, Issue 2
Characterizing the molecular regulation of inhibitory immune checkpoints with multimodal single-cell screens
journal, March 2021
- Papalexi, Efthymia; Mimitou, Eleni P.; Butler, Andrew W.
- Nature Genetics, Vol. 53, Issue 3
Enrichment of Triticum aestivum gene annotations using ortholog cliques and gene ontologies in other plants
journal, April 2015
- Tulpan, Dan; Leger, Serge; Tchagang, Alain
- BMC Genomics, Vol. 16, Issue 1
Predicting transmembrane protein topology with a hidden markov model: application to complete genomes11Edited by F. Cohen
journal, January 2001
- Krogh, Anders; Larsson, Björn; von Heijne, Gunnar
- Journal of Molecular Biology, Vol. 305, Issue 3
Basic local alignment search tool
journal, October 1990
- Altschul, Stephen F.; Gish, Warren; Miller, Webb
- Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410
Predicting transmembrane protein topology with a hidden markov model: application to complete genomes11Edited by F. Cohen
journal, January 2001
- Krogh, Anders; Larsson, Björn; von Heijne, Gunnar
- Journal of Molecular Biology, Vol. 305, Issue 3
Plants to power: bioenergy to fuel the future
journal, August 2008
- Yuan, Joshua S.; Tiller, Kelly H.; Al-Ahmad, Hani
- Trends in Plant Science, Vol. 13, Issue 8
QTL Analysis in a Complex Autopolyploid: Genetic Control of Sugar Content in Sugarcane
journal, November 2001
- Ming, R.
- Genome Research, Vol. 11, Issue 12
Carbon Partitioning during Sucrose Accumulation in Sugarcane Internodal Tissue
journal, December 1997
- Whittaker, A.; Botha, F. C.
- Plant Physiology, Vol. 115, Issue 4
QTL Analysis in a Complex Autopolyploid: Genetic Control of Sugar Content in Sugarcane
journal, November 2001
- Ming, R.
- Genome Research, Vol. 11, Issue 12
What is the maximum efficiency with which photosynthesis can convert solar energy into biomass?
journal, April 2008
- Zhu, Xin-Guang; Long, Stephen P.; Ort, Donald R.
- Current Opinion in Biotechnology, Vol. 19, Issue 2
Pfam: the protein families database
journal, November 2013
- Finn, Robert D.; Bateman, Alex; Clements, Jody
- Nucleic Acids Research, Vol. 42, Issue D1
RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome
journal, August 2011
- Li, Bo; Dewey, Colin N.
- BMC Bioinformatics, Vol. 12, Issue 1
Nonsyntenic genes drive tissue-specific dynamics of differential, nonadditive and allelic expression patterns in maize hybrids
journal, April 2016
- Baldauf, Jutta; Marcon, Caroline; Paschold, Anja
- Plant Physiology
Challenges in homology search: HMMER3 and convergent evolution of coiled-coil regions
journal, April 2013
- Mistry, Jaina; Finn, Robert D.; Eddy, Sean R.
- Nucleic Acids Research, Vol. 41, Issue 12
Full-length transcriptome assembly from RNA-Seq data without a reference genome
journal, May 2011
- Grabherr, Manfred G.; Haas, Brian J.; Yassour, Moran
- Nature Biotechnology, Vol. 29, Issue 7
Extensive Allelic Variation in Gene Expression in Populus F 1 Hybrids
journal, December 2007
- Zhuang, Yan; Adams, Keith L.
- Genetics, Vol. 177, Issue 4
Accumulation of DNA damage alters microRNA gene transcription in Arabidopsis thaliana
journal, December 2022
- Du, Juan; Liu, Yang; Lu, Lu
- BMC Plant Biology, Vol. 22, Issue 1
Microcollinearity between autopolyploid sugarcane and diploid sorghum genomes
journal, January 2010
- Wang, Jianping; Roe, Bruce; Macmil, Simone
- BMC Genomics, Vol. 11, Issue 1
Enrichment of Triticum aestivum gene annotations using ortholog cliques and gene ontologies in other plants
journal, April 2015
- Tulpan, Dan; Leger, Serge; Tchagang, Alain
- BMC Genomics, Vol. 16, Issue 1
A combination of AFLP and SSR markers provides extensive map coverage and identification of homo(eo)logous linkage groups in a sugarcane cultivar
journal, February 2005
- Aitken, K. S.; Jackson, P. A.; McIntyre, C. L.
- Theoretical and Applied Genetics, Vol. 110, Issue 5
RFLP Mapping in Cultivated Sugarcane ( Saccharum spp.): Genome Organization in a Highly Polyploid and Aneuploid Interspecific Hybrid
journal, March 1996
- Grivet, Laurent; D'Hont, Angelique; Roques, Daniele
- Genetics, Vol. 142, Issue 3
Works referencing / citing this record:
Suberin and hemicellulose in sugarcane cell wall architecture and crop digestibility: A biotechnological perspective
journal, February 2019
- Figueiredo, Raquel; Araújo, Pedro; Llerena, Juan Pablo P.
- Food and Energy Security, Vol. 8, Issue 3
Figures / Tables found in this record:
Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.