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Metabolomic profiling of SQ-1-induced changes in starch metabolism in sterile anthers of wheat

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Abstract

The metabolome and starch contents are closely related with the normal pollen development in plants. Thus, in this study, metabolome profiling, including principal component analysis, hierarchical cluster analysis, and metabolite–metabolite correlations were performed, and the changes induced by SQ-1 in the expression of starch synthetase genes in a male sterility line (PHYMS-1376) and male fertility line (MF-1376) were analysed to elucidate the relationship between the metabolite contents (metabolomes and starches) and pollen abortion and, consequently, explore the mechanisms underlying male-sterility induced by SQ-1. Results from this study showed that PHYMS-1376 displayed a high male-sterility rate (up to 99.07%), accompanied by low starch content in pollen. Metabolomic profiling revealed 93 metabolites present at significantly different levels using two-tailed unpaired Student's t-test (p-value ≤ 0.05) between the anthers of PHYMS-1376 and MF-1376, which were classified into five clusters. These 93 differential metabolites were analysed using principal component analysis and partial least squares-discriminant analysis found that all 60 samples were separated into four classes based on their developmental stage: (1) tetrad, (2) early uninucleate, (3) late uninucleate, and (4) binucleate and trinucleate stages in MF-1376 and PHYMS-1376 anthers. A total of 4278 correlations were identified among these 93 differential metabolites; thus, 107 significantly correlated pairs were found. The pathway analysis of the 93 differential metabolites showed that 67 metabolites play roles in the aminoacyl-transfer ribonucleic acid biosynthesis, tricarboxylic acid cycle, glycolysis, starch and sucrose metabolism, and other metabolic pathways. Meanwhile, an integrated metabolic map revealed relationships in terms of metabolic pathways among 84 metabolites from the 93 differential metabolites. Furthermore, the expression of key starch synthetase genes was dysregulated during the anther development from the tetrad to trinucleate stage in PHYMS-1376. In conclusion, we hypothesised that the expression patterns of most analysed metabolites (e.g. amino acids, fatty acids, and sugars) affected the numerous metabolic pathways, thereby probably harbouring insufficient nutrients for the abnormal regulation of starch synthetase genes for pollen development, leading to an abnormal or lack of starch formation and ultimately resulting in pollen abortion in the male sterility line induced by SQ-1.

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Abbreviations

T:

Tetrad

EU:

Early uninucleate

LU:

Late uninucleate

B:

Binucleate

TR:

Trinucleate

TMF:

Tetrad in MF-1376

EUMF:

Early uninucleate stage in MF-1376

LUMF:

Late uninucleate stage in MF-1376

BMF:

Binucleate stage in MF-1376

TRMF:

Trinucleate stage in MF-1376

TPS:

Tetrad in PHYMS-1376

EUPS:

Early uninucleate stage in PHYMS-1376

LUPS:

Late uninucleate stage in PHYMS-1376

BPS:

Binucleate stage in PHYMS-1376

TRPS:

Trinucleate stage in PHYMS-1376

TCA:

The Tricarboxylic Acid Cycle

SSS I:

Soluble starch synthase I

SSS II:

Soluble starch synthase II

SSS III:

Soluble starch synthase III

GBSS I:

Granule-bound starch synthase I

GBSS II:

Granule-bound starch synthase II

SBE I:

Starch branching enzyme I

SBE IIa:

Starch branching enzyme IIa

SBE IIb:

Starch branching enzyme IIb

DBE:

Debranching enzyme

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Acknowledgements

Wheat materials used in this study were provided by Key Laboratory of Crop Heterosis of Shaanxi province. We would like to appreciate the State Key Laboratory of Crop Stress Biology for Arid Areas staff for technical assistance. We are thankful to Wei Zhang and Rui Ma for their support during the anther collecting.

Funding

The design of the study, sample collection, cytological observation, metabolites identification and analysis, gene quantification, interpretation of data and the writing of the manuscript was financially supported by National Natural Science Foundation of China (No. 31701500); China Postdoctoral Science Foundation (No. 2017M613222); Fundamental Research Funds of Northwest A&F University (No. 2452017056); Ph.D. Start-up Fund of Northwest A&F University (No. 2452015263);National Support Program of China (No.2015BAD27B01), and The Technological Innovation and Over Planning Projects of Shaanxi Province (No. 2014KTZB02-01–02).

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Authors and Affiliations

  1. College of Agronomy, Northwest A&F University, Yangling, 712100, Shaanxi, People’s Republic of China

    Huali Tang, Yuxin Zhou, Jialin Guo, Ying Li, Junwei Wang, Na Niu, Shoucai Ma, Yulong Song & Gaisheng Zhang

  2. Institute of Crop Science, Chinese Academy of Agriculture Sciences, Beijing, 100081, People’s Republic of China

    Huali Tang, Yulong Song & Gaisheng Zhang

  3. National Yangling Agricultural Biotechnology & Breeding Center, Yangling, 712100, Shaanxi, People’s Republic of China

    Huali Tang, Jialin Guo, Junwei Wang, Na Niu, Shoucai Ma, Yulong Song & Gaisheng Zhang

  4. Yangling Branch of State Wheat Improvement Center, Yangling, 712100, Shaanxi, People’s Republic of China

    Huali Tang, Jialin Guo, Junwei Wang, Na Niu, Shoucai Ma, Yulong Song & Gaisheng Zhang

  5. Wheat Breeding Engineering Research Center, Ministry of Education, Yangling, 712100, Shaanxi, People’s Republic of China

    Huali Tang, Jialin Guo, Junwei Wang, Na Niu, Shoucai Ma, Yulong Song & Gaisheng Zhang

  6. Key Laboratory of Crop Heterosis of Shaanxi Province, Yangling, 712100, Shaanxi, People’s Republic of China

    Huali Tang, Jialin Guo, Junwei Wang, Na Niu, Shoucai Ma, Yulong Song & Gaisheng Zhang

  7. Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, 100101, People’s Republic of China

    Yuxin Zhou

  8. College of Agronomy, Henan University of Science and Technology, No.263 Kaiyuan Road, Luolong District, Luoyang city, 471023, Henan Province, People’s Republic of China

    Chunping Wang

  9. Suzhou SmartNuclide, Co., Ltd, Suzhou, 215125, Jiangsu, People’s Republic of China

    Jiufeng Wang

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  1. Huali Tang
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Contributions

YL and GS conceived and designed the experiments. YL and HL carried out the experiments and analyzed datum. HL wrote this manuscript. YL revised the manuscript. SC, JW and NN planted and treated the experimental materials. YX, JF, LY, JL and CP analyzed datum. All authors have read and approved the manuscript.

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Correspondence to Yulong Song or Gaisheng Zhang.

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Communicated by wenying zhang.

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Tang, H., Zhou, Y., Guo, J. et al. Metabolomic profiling of SQ-1-induced changes in starch metabolism in sterile anthers of wheat. Plant Growth Regul 95, 381–398 (2021). https://doi.org/10.1007/s10725-021-00748-y

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