A barley pan-transcriptome reveals layers of genotype-dependent transcriptional complexity

Wenbin Guo; Miriam Schreiber; Vanda  Marosi; Paolo Bagnaresi; Morten E. Jørgensen; Kenneth J. Chalmers; Brett Chapman; Viet  Dang; Christoph Dockter; Anne Fiebig; Geoffrey B. Fincher; Agostino Fricano; John Fuller; Allison M. Haaning; Georg Haberer; Axel Himmelbach; Murukarthick Jayakodi; Yong  Jia; Nadia Kamal; Peter Langridge; Chengdao Li; Qiongxian Lu; Thomas Lux; Martin Mascher; Klaus F. X. Mayer; Nicola McCallum; Linda  Milne; Gary J. Muehlbauer; Sudharsan Padmarasu; Klaus Pillen; Pai Rosager Pedas; Curtis Pozniak; Kazuhiro Sato; Thomas Schmutzer; Uwe Scholz; Danuta Schüler; Hana Šimková; Birgitte Skadhauge; Nils Stein; Penghao Wang; Ronja Wonneberger; Xiao-Qi Zhang; Guoping Zhang; Katarzyna Birch Braune; Luigi Cattivelli; Manuel Spannagl; Micha Bayer; Craig Simpson; Runxuan Zhang; Robbie Waugh

doi:10.1038/s41588-024-02069-y

A barley pan-transcriptome reveals layers of genotype-dependent transcriptional complexity

Wenbin Guo
, Miriam Schreiber
, Vanda Marosi
, Paolo Bagnaresi
, Morten E. Jørgensen
, Kenneth J. Chalmers
, Brett Chapman
, Viet Dang
, Christoph Dockter
, Anne Fiebig
, Geoffrey B. Fincher
, Agostino Fricano
, John Fuller
, Allison M. Haaning
, Georg Haberer
, Axel Himmelbach
, Murukarthick Jayakodi
, Yong Jia
, Nadia Kamal
, Peter Langridge

Chengdao Li, Qiongxian Lu, Thomas Lux, Martin Mascher, Klaus F. X. Mayer, Nicola McCallum, Linda Milne, Gary J. Muehlbauer, Sudharsan Padmarasu, Klaus Pillen, Pai Rosager Pedas, Curtis Pozniak, Kazuhiro Sato, Thomas Schmutzer, Uwe Scholz, Danuta Schüler, Hana Šimková, Birgitte Skadhauge, Nils Stein, Penghao Wang, Ronja Wonneberger, Xiao-Qi Zhang, Guoping Zhang, Katarzyna Birch Braune, Luigi Cattivelli, Manuel Spannagl, Micha Bayer (Lead / Corresponding author), Craig Simpson (Lead / Corresponding author), Runxuan Zhang (Lead / Corresponding author), Robbie Waugh (Lead / Corresponding author)

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Abstract

A pan-transcriptome describes the transcriptional and post-transcriptional consequences of genome diversity from multiple individuals within a species. We developed a barley pan-transcriptome using 20 inbred genotypes representing domesticated barley diversity by generating and analyzing short- and long-read RNA-sequencing datasets from multiple tissues. To overcome single reference bias in transcript quantification, we constructed genotype-specific reference transcript datasets (RTDs) and integrated these into a linear pan-genome framework to create a pan-RTD, allowing transcript categorization as core, shell or cloud. Focusing on the core (expressed in all genotypes), we observed significant transcript abundance variation among tissues and between genotypes driven partly by RNA processing, gene copy number, structural rearrangements and conservation of promotor motifs. Network analyses revealed conserved co-expression module::tissue correlations and frequent functional diversification. To complement the pan-transcriptome, we constructed a comprehensive cultivar (cv.) Morex gene-expression atlas and illustrate how these combined datasets can be used to guide biological inquiry.

Original language	English
Pages (from-to)	441-450
Number of pages	10
Journal	Nature Genetics
Volume	57
Issue number	2
DOIs	https://doi.org/10.1038/s41588-024-02069-y
Publication status	Published - 3 Feb 2025

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Guo, W., Schreiber, M., Marosi, V., Bagnaresi, P., Jørgensen, M. E., Chalmers, K. J., Chapman, B., Dang, V., Dockter, C., Fiebig, A., Fincher, G. B., Fricano, A., Fuller, J., Haaning, A. M., Haberer, G., Himmelbach, A., Jayakodi, M., Jia, Y., Kamal, N., ... Waugh, R. (2025). A barley pan-transcriptome reveals layers of genotype-dependent transcriptional complexity. Nature Genetics, 57(2), 441-450. https://doi.org/10.1038/s41588-024-02069-y

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title = "A barley pan-transcriptome reveals layers of genotype-dependent transcriptional complexity",

abstract = "A pan-transcriptome describes the transcriptional and post-transcriptional consequences of genome diversity from multiple individuals within a species. We developed a barley pan-transcriptome using 20 inbred genotypes representing domesticated barley diversity by generating and analyzing short- and long-read RNA-sequencing datasets from multiple tissues. To overcome single reference bias in transcript quantification, we constructed genotype-specific reference transcript datasets (RTDs) and integrated these into a linear pan-genome framework to create a pan-RTD, allowing transcript categorization as core, shell or cloud. Focusing on the core (expressed in all genotypes), we observed significant transcript abundance variation among tissues and between genotypes driven partly by RNA processing, gene copy number, structural rearrangements and conservation of promotor motifs. Network analyses revealed conserved co-expression module::tissue correlations and frequent functional diversification. To complement the pan-transcriptome, we constructed a comprehensive cultivar (cv.) Morex gene-expression atlas and illustrate how these combined datasets can be used to guide biological inquiry.",

author = "Wenbin Guo and Miriam Schreiber and Vanda Marosi and Paolo Bagnaresi and J{\o}rgensen, \{Morten E.\} and Chalmers, \{Kenneth J.\} and Brett Chapman and Viet Dang and Christoph Dockter and Anne Fiebig and Fincher, \{Geoffrey B.\} and Agostino Fricano and John Fuller and Haaning, \{Allison M.\} and Georg Haberer and Axel Himmelbach and Murukarthick Jayakodi and Yong Jia and Nadia Kamal and Peter Langridge and Chengdao Li and Qiongxian Lu and Thomas Lux and Martin Mascher and Mayer, \{Klaus F. X.\} and Nicola McCallum and Linda Milne and Muehlbauer, \{Gary J.\} and Sudharsan Padmarasu and Klaus Pillen and Pedas, \{Pai Rosager\} and Curtis Pozniak and Kazuhiro Sato and Thomas Schmutzer and Uwe Scholz and Danuta Sch{\"u}ler and Hana {\v S}imkov{\'a} and Birgitte Skadhauge and Nils Stein and Penghao Wang and Ronja Wonneberger and Xiao-Qi Zhang and Guoping Zhang and Braune, \{Katarzyna Birch\} and Luigi Cattivelli and Manuel Spannagl and Micha Bayer and Craig Simpson and Runxuan Zhang and Robbie Waugh",

year = "2025",

month = feb,

day = "3",

doi = "10.1038/s41588-024-02069-y",

language = "English",

volume = "57",

pages = "441--450",

journal = "Nature Genetics",

issn = "1061-4036",

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}

Guo, W, Schreiber, M, Marosi, V, Bagnaresi, P, Jørgensen, ME, Chalmers, KJ, Chapman, B, Dang, V, Dockter, C, Fiebig, A, Fincher, GB, Fricano, A, Fuller, J, Haaning, AM, Haberer, G, Himmelbach, A, Jayakodi, M, Jia, Y, Kamal, N, Langridge, P, Li, C, Lu, Q, Lux, T, Mascher, M, Mayer, KFX, McCallum, N, Milne, L, Muehlbauer, GJ, Padmarasu, S, Pillen, K, Pedas, PR, Pozniak, C, Sato, K, Schmutzer, T, Scholz, U, Schüler, D, Šimková, H, Skadhauge, B, Stein, N, Wang, P, Wonneberger, R, Zhang, X-Q, Zhang, G, Braune, KB, Cattivelli, L, Spannagl, M, Bayer, M, Simpson, C, Zhang, R & Waugh, R 2025, 'A barley pan-transcriptome reveals layers of genotype-dependent transcriptional complexity', Nature Genetics, vol. 57, no. 2, pp. 441-450. https://doi.org/10.1038/s41588-024-02069-y

TY - JOUR

T1 - A barley pan-transcriptome reveals layers of genotype-dependent transcriptional complexity

AU - Guo, Wenbin

AU - Schreiber, Miriam

AU - Marosi, Vanda

AU - Bagnaresi, Paolo

AU - Jørgensen, Morten E.

AU - Chalmers, Kenneth J.

AU - Chapman, Brett

AU - Dang, Viet

AU - Dockter, Christoph

AU - Fiebig, Anne

AU - Fincher, Geoffrey B.

AU - Fricano, Agostino

AU - Fuller, John

AU - Haaning, Allison M.

AU - Haberer, Georg

AU - Himmelbach, Axel

AU - Jayakodi, Murukarthick

AU - Jia, Yong

AU - Kamal, Nadia

AU - Langridge, Peter

AU - Li, Chengdao

AU - Lu, Qiongxian

AU - Lux, Thomas

AU - Mascher, Martin

AU - Mayer, Klaus F. X.

AU - McCallum, Nicola

AU - Milne, Linda

AU - Muehlbauer, Gary J.

AU - Padmarasu, Sudharsan

AU - Pillen, Klaus

AU - Pedas, Pai Rosager

AU - Pozniak, Curtis

AU - Sato, Kazuhiro

AU - Schmutzer, Thomas

AU - Scholz, Uwe

AU - Schüler, Danuta

AU - Šimková, Hana

AU - Skadhauge, Birgitte

AU - Stein, Nils

AU - Wang, Penghao

AU - Wonneberger, Ronja

AU - Zhang, Xiao-Qi

AU - Zhang, Guoping

AU - Braune, Katarzyna Birch

AU - Cattivelli, Luigi

AU - Spannagl, Manuel

AU - Bayer, Micha

AU - Simpson, Craig

AU - Zhang, Runxuan

AU - Waugh, Robbie

PY - 2025/2/3

Y1 - 2025/2/3

N2 - A pan-transcriptome describes the transcriptional and post-transcriptional consequences of genome diversity from multiple individuals within a species. We developed a barley pan-transcriptome using 20 inbred genotypes representing domesticated barley diversity by generating and analyzing short- and long-read RNA-sequencing datasets from multiple tissues. To overcome single reference bias in transcript quantification, we constructed genotype-specific reference transcript datasets (RTDs) and integrated these into a linear pan-genome framework to create a pan-RTD, allowing transcript categorization as core, shell or cloud. Focusing on the core (expressed in all genotypes), we observed significant transcript abundance variation among tissues and between genotypes driven partly by RNA processing, gene copy number, structural rearrangements and conservation of promotor motifs. Network analyses revealed conserved co-expression module::tissue correlations and frequent functional diversification. To complement the pan-transcriptome, we constructed a comprehensive cultivar (cv.) Morex gene-expression atlas and illustrate how these combined datasets can be used to guide biological inquiry.

AB - A pan-transcriptome describes the transcriptional and post-transcriptional consequences of genome diversity from multiple individuals within a species. We developed a barley pan-transcriptome using 20 inbred genotypes representing domesticated barley diversity by generating and analyzing short- and long-read RNA-sequencing datasets from multiple tissues. To overcome single reference bias in transcript quantification, we constructed genotype-specific reference transcript datasets (RTDs) and integrated these into a linear pan-genome framework to create a pan-RTD, allowing transcript categorization as core, shell or cloud. Focusing on the core (expressed in all genotypes), we observed significant transcript abundance variation among tissues and between genotypes driven partly by RNA processing, gene copy number, structural rearrangements and conservation of promotor motifs. Network analyses revealed conserved co-expression module::tissue correlations and frequent functional diversification. To complement the pan-transcriptome, we constructed a comprehensive cultivar (cv.) Morex gene-expression atlas and illustrate how these combined datasets can be used to guide biological inquiry.

U2 - 10.1038/s41588-024-02069-y

DO - 10.1038/s41588-024-02069-y

M3 - Article

C2 - 39901014

SN - 1061-4036

VL - 57

SP - 441

EP - 450

JO - Nature Genetics

JF - Nature Genetics

IS - 2

ER -

A barley pan-transcriptome reveals layers of genotype-dependent transcriptional complexity

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