Organellar genome divergence and environmental stress induce transcriptional cytonuclear responses in wheat alloplasmic hybrids

Y Yue Zhao K Keren Zhang (Key Laboratory of Molecular Epigenetics of the Ministry of Education, Northeast Normal University) G Guo Li (Key Laboratory of Molecular Epigenetics of the Ministry of Education, Northeast Normal University) Y Yuming Wang X Xiaoyang Ding (Soybean Research Institute, Jilin Academy of Agricultural Sciences) S Shuo Wang X Xi Pang (Key Laboratory of Molecular Epigenetics of the Ministry of Education, Northeast Normal University) X Xueru Zhao (Chemistry Department) Y Yue Yu J Jiaqi Liu T Tingting Yu (Key Laboratory of Molecular Epigenetics of the Ministry of Education, Northeast Normal University) G Guixian Bao (Key Laboratory of Molecular Epigenetics of the Ministry of Education, Northeast Normal University) T Tianya Wang (Key Laboratory of Molecular Epigenetics of the Ministry of Education, Northeast Normal University) Z Zhongfu Ni (Frontiers Science Center for Molecular Design Breeding, Key Laboratory of crop Heterosis and Utilization, and Beijing Key Laboratory of Crop Genetic Improvement, China Agricultural University) M Mingming Xin (Frontiers Science Center for Molecular Design Breeding, Key Laboratory of crop Heterosis and Utilization, and Beijing Key Laboratory of Crop Genetic Improvement, China Agricultural University) B Bao Liu (Automotive Engineering Research Institute) J Jonathan F. Wendel (Department of Ecology, Evolution and Organismal Biology, Iowa State University) Z Zhibin Zhang (State Key Laboratory for Mesoscopic Physics, Frontiers Science Centre for Nano-optoelectronics, School of Physics, Peking University, Beijing, China.) L Lei Gong (College of Chemistry and Chemical Engineering)

Abstract

The union of two or more different nuclear genomes with maternally inherited organellar genomes may lead to cytonuclear incompatibilities in plant allopolyploids. These incompatibilities may be reconciled by coevolutionary responses at the genomic and transcriptional levels. To date, the relationship between extent of divergence among parental organellar genomes and cytonuclear coevolutionary responses remains largely unexplored. Here, we studied transcriptional cytonuclear expression in synthetic alloplasmic allohexaploid wheat lines having the same nuclear subgenomic composition (the nuclear genome of Chinese Spring) but with varying cytoplasmic organelles (plasmon donors from B- and D- lineage Triticum/Aegilops species). A positive association between the extent of plastid organellar divergence from naturally occurring organelles in euplasmic Chinese Spring and transcriptional cytonuclear responses was observed. This response was enhanced under stress (highlight) treatment and was determined to be related to differential subgenomic methylation levels. These data comprise a transcriptional dimension of cytonuclear responses to polyploidy and point to a potentially responsible epigenomic regulatory mechanism.

Article Details

Volume / Issue Vol. 122, Issue 24
Published June 17, 2025
ISSN 0027-8424
Publisher National Academy of Sciences

Authors (19)

Y

Yue Zhao

K

Keren Zhang

Key Laboratory of Molecular Epigenetics of the Ministry of Education, Northeast Normal University

G

Guo Li

Key Laboratory of Molecular Epigenetics of the Ministry of Education, Northeast Normal University

Y

Yuming Wang

X

Xiaoyang Ding

Soybean Research Institute, Jilin Academy of Agricultural Sciences

S

Shuo Wang

X

Xi Pang

Key Laboratory of Molecular Epigenetics of the Ministry of Education, Northeast Normal University

X

Xueru Zhao

Chemistry Department

Y

Yue Yu

J

Jiaqi Liu

T

Tingting Yu

Key Laboratory of Molecular Epigenetics of the Ministry of Education, Northeast Normal University

G

Guixian Bao

Key Laboratory of Molecular Epigenetics of the Ministry of Education, Northeast Normal University

T

Tianya Wang

Key Laboratory of Molecular Epigenetics of the Ministry of Education, Northeast Normal University

Z

Zhongfu Ni

Frontiers Science Center for Molecular Design Breeding, Key Laboratory of crop Heterosis and Utilization, and Beijing Key Laboratory of Crop Genetic Improvement, China Agricultural University

M

Mingming Xin

Frontiers Science Center for Molecular Design Breeding, Key Laboratory of crop Heterosis and Utilization, and Beijing Key Laboratory of Crop Genetic Improvement, China Agricultural University

B

Bao Liu

Automotive Engineering Research Institute

J

Jonathan F. Wendel

Department of Ecology, Evolution and Organismal Biology, Iowa State University

Z

Zhibin Zhang

State Key Laboratory for Mesoscopic Physics, Frontiers Science Centre for Nano-optoelectronics, School of Physics, Peking University, Beijing, China.

L

Lei Gong

College of Chemistry and Chemical Engineering