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Comparative transcriptome analysis reveals the mechanism of exogenous substances inhibiting fertility alteration induced by low temperature in TGMS rice line

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Abstract

During two-line hybrid rice seed production, thermo-sensitive genic male sterile (TGMS) rice lines are susceptible to low temperature, leading to fertility alteration (from sterile to fertile) and production of false hybrids (self-pollination). To explore appropriate solutions to reduce the chance of seed production failure, two exogenous substances, d-Arg and ethephon, were applied to restrain the fertility alteration induced by low temperature (22.0 °C), respectively. The fertile pollen grains and bagged seed setting rate of TGMS rice line Jing 4155S (with the critical fertility/sterility alteration temperature of 23.5 °C) under low temperature could be reduced to 0% by spraying exogenous substances. Transcriptome analysis of young panicles of TGMS rice line Jing 4155S demonstrated that the expressions of multiple transcription factors (MYB, FAR1, and ERF, etc.) changed, and hence affecting various downstream related genes and metabolic processes, including hormonal signal transduction, plant pathogen interactions, circadian rhythm pathway, carbohydrate metabolism, cell wall synthesis, and lipid metabolism, etc. The enhanced ethylene biosynthesis and the prevented redox equilibrium from unbalance to balance in young panicles were one of the major reasons that fertility alteration was inhibited by exogenous substances. Our results made a contribution to the solution for inhibiting fertility alteration induced by low temperature in two-line TGMS rice lines during hybrid seed production.

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Abbreviations

ACO:

1-Aminocyclopropane-1-carboxylate oxidase

ACS:

1-Aminocyclopropane-1-carboxylic acid synthase

ADC:

Arginine decarboxylase

APX:

Ascorbate peroxidase

ARF:

Auxin response factor

AsA:

Ascorbate

CAT:

Catalase

CHA:

Chemical hybridization agents

CMS:

Cytoplasmic male sterile

DEG:

Differentially expression gene

DHAR:

Dehydroascorbate reductase

EGMS:

Environment sensitive genic male-sterility

ERE:

Ethylene response elements

FPKM:

Fragments per kilobase of transcript per million mapped reads

GO:

Gene ontology

GR:

Glutathione reductase

GPX:

Glutathione peroxidase

GSH:

Glutathione

KEGG:

Kyoto encyclopedia of genes and genomes

LT-inducement:

Long-time low temperature inducement

MDA:

Malondialdehyde

MDHAR:

Monodehydroascorbate reductase

MES:

Monosulfuron ester sodium

MGBG:

Methylglyoxal-bis (guanylhydrazone)

N-ac-PPT:

N-acetyl-phosphinothricin

PA:

Polyamines

PFK-1:

Phosphofructokinase-1

PGMS:

Photo-sensitive genic male sterile

PMS:

Physiology male sterility

POD:

Peroxidase

PVP:

Polyvinylpolypyrrolidone

qRT-PCR:

Quantitative real-time PCR

ROS:

Reactive oxygen species

SAM:

S-adenosyl methionine

SOD:

Superoxide dismutase

ST-inducement:

Short-time low temperature inducement

TF:

Transcription factor

TGMS:

Thermo-sensitive genic male sterile

TM:

Tribenuron-methyl

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Acknowledgements

The authors gratefully acknowledge the partial financial support from the project supported by the Ministry of Science and Technology of China (2018YFD0100905), the Open Research Fund of State Key Laboratory of Hybrid Rice (Hunan Hybrid Rice Research Center), and the Cyrus Tang Innovation Center for Seed Industry for this research.

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Authors and Affiliations

  1. State Key Laboratory of Crop Genetics and Germplasm Enhancement, Nanjing Agricultural University, Nanjing, 210095, China

    Xiaolin Liu, Lingkai Guo, Jiaping Wei & Hao Ma

  2. College of Agronomy, Hunan Agricultural University, Changsha, 410128, China

    Jiwai He & Haiqing Zhang

  3. State Key Laboratory of Hybrid Rice, Hunan Hybrid Rice Research Center, Changsha, 410128, China

    Jiwai He, Haiqing Zhang & Aimin Liu

  4. Southern Regional Collaborative Innovation Center for Grain and Oil Crops in China, Hunan Agricultural University, Changsha, 410128, China

    Haiqing Zhang, Aimin Liu, Langtao Xiao & Hao Ma

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  1. Xiaolin Liu
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Contributions

This study was performed in collaboration by all authors. X.L. and L.G. carried out most of the experiments and data analysis; J.W. carried out part of data analysis; J.H., H.Z. and A.L. carried out part of experimental treatment; L.X. carried out part of physiological experiment; H.M. designed the experiments and wrote the manuscript. All authors have read and approved the final manuscript.

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Correspondence to Hao Ma.

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Supplementary material 1 (JPEG 628 kb) Fig. S1. ROS levels in spikelet.

Supplementary material 2 (JPEG 865 kb) Fig. S2. Pearson correlation between samples.

10725_2019_560_MOESM3_ESM.jpg

Supplementary material 3 (JPEG 1425 kb) Fig. S3. Top 10 GO analysis of differentially expressed genes (DEGs). (A), (B), (C), (D), (E), (F) were the most enriched GO (biological process, cellular component, molecular function) between the water-treated group and the D-Arg-treated group in ST-inducement (C_S vs. D_S) and in LT-inducement (C_L vs. D_L), between the water-treated group and the ethephon-treated group in ST-inducement (C_S vs. Eth_S) and LT-inducement (C_L vs. Eth_L), and between the D-Arg-treated group and the ethephon-treated group in ST-inducement (D_S vs. Eth_S) and in LT-inducement (D_L vs. Eth_L), respectively.

10725_2019_560_MOESM4_ESM.jpg

Supplementary material 4 (JPEG 1328 kb) Fig. S4. Top 20 KEGG pathway analysis of differentially expressed genes (DEGs). (A), (B), (C), (D), (E), (F) were the most enriched Kyoto encyclopedia of genes and genomes (KEGG) pathway between the water-treated group and the D-Arg-treated group in ST-inducement (C_S vs. D_S) and in LT-inducement (C_L vs. D_L), between the water-treated group and the ethephon-treated group in ST-inducement (C_S vs. Eth_S) and LT-inducement (C_L vs. Eth_L), and between the D-Arg-treated group and the ethephon-treated group in ST-inducement (D_S vs. Eth_S) and in LT-inducement (D_L vs. Eth_L), respectively.

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Supplementary material 13 (XLSX 10 kb)

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Supplementary material 14 (XLSX 9 kb) The raw sequence data reported in this paper have been deposited in the Genome Sequence Archive (Genomics, Proteomics & Bioinformatics 2017) in BIG Data Center (Nucleic Acids Res 2019), Beijing Institute of Genomics (BIG), Chinese Academy of Sciences, under accession numbers CRA001549, Shared URL: http://bigd.big.ac.cn/gsa/s/dqaAhDEc.

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Liu, X., Guo, L., Wei, J. et al. Comparative transcriptome analysis reveals the mechanism of exogenous substances inhibiting fertility alteration induced by low temperature in TGMS rice line. Plant Growth Regul 90, 489–503 (2020). https://doi.org/10.1007/s10725-019-00560-9

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