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Nitrate-responsive transcriptome analysis of rice RGA1 mutant reveals the role of G-protein alpha subunit in negative regulation of nitrogen-sensitivity and use efficiency

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Abstract

Key message

Nitrate-responsive transcriptomic, phenotypic and physiological analyses of rice RGA1 mutant revealed many novel RGA1-regulated genes/processes/traits related to nitrogen use efficiency, and provided robust genetic evidence of RGA1-regulation of NUE.

Abstract

Nitrogen (N) use efficiency (NUE) is important for sustainable agriculture. G-protein signalling was implicated in N-response/NUE in rice, but needed firm genetic characterization of the role of alpha subunit (RGA1). The knock-out mutant of RGA1 in japonica rice exhibited lesser nitrate-dose sensitivity than the wild type (WT), in yield and NUE. We, therefore, investigated its genomewide nitrate-response relative to WT. It revealed 3416 differentially expressed genes (DEGs), including 719 associated with development, grain yield and phenotypic traits for NUE. The upregulated DEGs were related to photosynthesis, chlorophyll, tetrapyrrole and porphyrin biosynthesis, while the downregulated DEGs belonged to cellular protein metabolism and transport, small GTPase signalling, cell redox homeostasis, etc. We validated 26 nitrate-responsive DEGs across functional categories by RT-qPCR. Physiological validation of nitrate-response in the mutant and the WT at 1.5 and 15 mM doses revealed higher chlorophyll and stomatal length but decreased stomatal density, conductance and transpiration. The consequent increase in photosynthesis and water use efficiency may have contributed to better yield and NUE in the mutant, whereas the WT was N-dose sensitive. The mutant was not as N-dose-responsive as the WT in shoot/root growth, productive tillers and heading date, but equally responsive as WT in total N and protein content. The RGA1 mutant was less impacted by higher N-dose or salt stress in terms of yield, protein content, photosynthetic performance, relative water content, water use efficiency and catalase activity. PPI network analyses revealed known NUE-related proteins as RGA1 interactors. Therefore, RGA1 negatively regulates N-dose sensitivity and NUE in rice.

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Data availability/accession numbers

Our raw microarray data that support the findings of this study have been deposited in NCBI–GEO database (https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE62164) with the accession number GSE62164 (GSM1520728, GSM1520729, GSM1520733, GSM1520732, GSM1520736 and GSM1520737). Additional transcriptome datasets were obtained from either the published supplementary materials and/or their authors cited in the article. All other datasets pertaining to the analyses are included in the supplementary information files.

Abbreviations

NUE:

Nitrogen use efficiency

N:

Nitrogen or nitrate

WUE:

Water use efficiency

PPI:

Protein–protein interaction

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Acknowledgements

We thank Prof. T. Kumamaru from Kyushu University for providing the rice seeds and Regional Centre for Biotechnology (RCB), Faridabad for their help with the scanning electron microscopy.

Funding

This work was supported by research grants to NR from DST-SERB (F. No. CRG/2021/007467), ICAR (F. No. 2-2(60)/10-11/NICRA), Department of Biotechnology (DBT) [BT/IN/UK-VNC/44/NR/2015-16], UKRI GCRF South Asian Nitrogen Hub (SANH) [NE/S009019/1], GGSIPU[GGSIPU/DRC/Ph.D/Adm/2016/1549], [GGSIPU/DRC/FRGS/2018/22] and [GGSIPU/DRC/FRGS/2019/1553/24]. Fellowships were paid to VKM from DBT (DBT/JRF/14/AL/445) and GGSIPU (STRF: GGSIPU/DRC/2020/2049), APJ from CSIR (09/806(013)2008-EMR-I) and NC from UKRI GCRF-SANH [NE/S009019/1].

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Author notes

  1. Jangam Annie Prasanna and Vikas Kumar Mandal have contributed equally to this work.

Authors and Affiliations

  1. Centre for Sustainable Nitrogen and Nutrient Management, School of Biotechnology, Guru Gobind Singh Indraprastha University, Sector 16C, Dwarka, New Delhi, 110078, India

    Jangam Annie Prasanna, Vikas Kumar Mandal, Navjyoti Chakraborty & Nandula Raghuram

  2. Prof. H.S. Srivastava Foundation for Science and Society, 10B/7, Madan Mohan Malviya Marg, Lucknow, India

    Vikas Kumar Mandal

  3. Division of Agronomy, ICAR-Indian Agricultural Research Institute, Pusa Campus, New Delhi, India

    Dinesh Kumar

Authors
  1. Jangam Annie Prasanna
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  2. Vikas Kumar Mandal
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  3. Dinesh Kumar
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  4. Navjyoti Chakraborty
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  5. Nandula Raghuram
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Contributions

JAP: planned the experiment, performed the microarray. VKM: performed the phenotypic, physiological, biochemical and qPCR validation. Performed part of in-silico analysis of microarray data. Assisted in writing and finalizing the draft of the manuscript. NC: performed most of the in-silico analysis of the microarray data, assisted in performing the phenotypic, physiological and qPCR validation. Wrote the initial draft of the manuscript. DK: Planned and supervised the experiments for total nitrogen and protein contents. NR: conceived, planned and supervised the transcriptome analyses, data interpretation, edited and finalized the manuscript. All authors have reviewed the manuscript.

Corresponding authors

Correspondence to Navjyoti Chakraborty or Nandula Raghuram.

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Prasanna, J.A., Mandal, V.K., Kumar, D. et al. Nitrate-responsive transcriptome analysis of rice RGA1 mutant reveals the role of G-protein alpha subunit in negative regulation of nitrogen-sensitivity and use efficiency. Plant Cell Rep 42, 1987–2010 (2023). https://doi.org/10.1007/s00299-023-03078-7

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