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Deciphering the differential expression patterns of yield-related negative regulators in hexaploid wheat cultivars and hybrids at different growth stages

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Abstract

Background

Hexaploid bread wheat underwent a series of polyploidization events through interspecific hybridizations that conferred adaptive plasticity and resulted in duplication and neofunctionalization of major agronomic genes. The genetic architecture of polyploid wheat not only confers adaptive plasticity but also offers huge genetic diversity. However, the contribution of different gene copies (homeologs) encoded from different subgenomes (A, B, D) at different growth stages remained unexplored.

Methods

In this study, hybrid of elite cultivars of wheat were developed via reciprocal crosses (cytoplasm swap**) and phenotypically evaluated. We assessed differential expression profiles of yield-related negative regulators in these cultivars and their F1 hybrids and identified various cis-regulatory signatures by employing bioinformatics tools. Furthermore, the preferential expression patterns of the syntenic triads encoded from A, B, and D subgenomes were assessed to decipher their functional redundancy at six different growth stages.

Results

Hybrid progenies showed better heterosis such as up to 17% increase in the average number of grains and up to 50% increase in average thousand grains weight as compared to mid-parents. Based on the expression profiling, our results indicated significant dynamic transcriptional expression patterns, portraying the different homeolog-dominance at the same stage in the different cultivars and their hybrids. Albeit belonging to same syntenic triads, a dynamic trend was observed in the regulatory signatures of these genes that might be influencing their expression profiles.

Conclusion

These findings can substantially contribute and provide insights for the selective introduction of better cultivars into traditional and hybrid breeding programs which can be harnessed for the improvement of future wheat.

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Data availability

The authors have utilized public databases and tools for data retrieval and analysis. All the databases and tools or software utilized with their access web links have been properly given in the relevant material and methods section for clarity and use by other researchers.

Abbreviations

TGW:

Thousand-grain weight

CKX:

Cytokinin oxidase/dehydrogenase

SL:

Strigolactones

NJ:

Neighbor-joining

miRNAs:

Micro-RNAs

GO:

Gene ontology

TFBS:

Transcriptional factor binding sites

qPCR:

Real-time quantitative PCR

CC:

Cellular component

MF:

Molecular function

BP:

Biological process

CREs:

cis-acting elements

AP2/ERF:

APETALA2/ethylene-responsive element binding factors

SRS:

SHI-related sequence

TD1:

TD-1

Gap:

GA-2002

AUQ:

Auqaab-2000

PCA:

Principal component analysis

PH:

Plant height

SL:

Spike length

LL:

Leaf length

LA:

Flag leaf area

TGP:

Total grains per plant

TGW:

Thousand grains weight

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Acknowledgements

The authors acknowledge Mr. Atiq-ur-Rehman (NIBGE), Dr. Muhammad Asif (NIBGE, Faisalabad), Dr. Mudassir Ahmed (NIBGE), Dr. Asma Imran (NIBGE), Dr. Imtiaz (NIBGE), Dr. Fatiha (NIBGE), Dr. Javed Ahmad (AARI, Faisalabad) & Dr. Aziz-ur-Rehman (AARI, Faisalabad) for their technical support.

Funding

The authors declare that no funds, grants, or other support were received during the preparation of this manuscript.

Author information

Authors and Affiliations

  1. Agricultural Biotechnology Division, National Institute for Biotechnology and Genetic Engineering (NIBGE), Constituent College of Pakistan Institute of Engineering and Applied Sciences, Jhang Road, Faisalabad, Pakistan

    Muhammad Jawad Akbar Awan, Muhammad Awais Farooq, Rubab Zahra Naqvi, Muhammad Abu Bakar Waqas, Muhammad Arslan Mahmood, Muhammad Ismail Buzdar, Imran Amin, Nasir A. Saeed & Shahid Mansoor

  2. State Key Laboratory of North China Crop Improvement and Regulation, Key Laboratory of Vegetable Germplasm Innovation and Utilization of Hebei, Collaborative Innovation Center of Vegetable Industry in Hebei, College of Horticulture, Hebei Agricultural University, Baoding, China

    Muhammad Awais Farooq & Umer Karamat

  3. School of Natural Sciences, University of Tasmania, Hobart, TAS, Australia

    Sayyad Ali Raza Bukhari

  4. Department of Plant Sciences, Quaid-i-Azam University, Islamabad, 45320, Pakistan

    Awais Rasheed

  5. Institute of Crop Science, Chinese Academy of Agricultural Sciences (CAAS) & CIMMYT-China office, 12 Zhongguancun South Street, Bei**g, 100081, China

    Awais Rasheed

  6. International Center for Chemical and Biological Sciences, University of Karachi, Karachi, Pakistan

    Shahid Mansoor

  7. Department of Biotechnology, University of Sargodha, Sargodha, Pakistan

    Sayyad Ali Raza Bukhari

  8. Guangdong Key Laboratory for New Technology Research of Vegetables, Vegetable Research Institute, Guangdong Academy of Agricultural Sciences, Guangzhou, China

    Umer Karamat

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  1. Muhammad Jawad Akbar Awan
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Contributions

SM, IA, AR, and NAS provided the concept, guidance, resources, and supervised the whole project. MJAA, MAF, RZN, UK, and SARB performed the in-silico data analysis and validation. MJAA, MABW, MAM, and MIB conducted field experiments and collected data. MJAA and RZN conducted the RT-PCR experiments. MAF, UK, and SARB performed the statistical data analysis. MJAA, MAF, RZN, and UK prepared the manuscript. All authors have contributed to the article and approved the submitted version.

Corresponding author

Correspondence to Shahid Mansoor.

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Awan, M.J.A., Farooq, M.A., Naqvi, R.Z. et al. Deciphering the differential expression patterns of yield-related negative regulators in hexaploid wheat cultivars and hybrids at different growth stages. Mol Biol Rep 51, 537 (2024). https://doi.org/10.1007/s11033-024-09454-0

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