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G-protein α-subunit (GPA1) regulates stress, nitrate and phosphate response, flavonoid biosynthesis, fruit/seed development and substantially shares GCR1 regulation in A. thaliana

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Abstract

Heterotrimeric G-proteins are implicated in several plant processes, but the mechanisms of signal-response coupling and the roles of G-protein coupled receptors in general and GCR1 in particular, remain poorly understood. We isolated a knock-out mutant of the Arabidopsis G-protein α subunit (gpa1-5) and analysed its transcriptome to understand the genomewide role of GPA1 and compared it with that of our similar analysis of a GCR1 mutant (Chakraborty et al. 2015, PLoS ONE 10(2):e0117819). We found 394 GPA1-regulated genes spanning 79 biological processes, including biotic and abiotic stresses, development, flavonoid biosynthesis, transcription factors, transporters and nitrate/phosphate responses. Many of them are either unknown or unclaimed explicitly in other published gpa1 mutant transcriptome analyses. A comparison of all known GPA1-regulated genes (including the above 394) with 350 GCR1-regulated genes revealed 114 common genes. This can be best explained by GCR1–GPA1 coupling, or by convergence of their independent signaling pathways. Though the common genes in our GPA1 and GCR1 mutant datasets constitute only 26 % of the GPA1-regulated and 30 % of the GCR1-responsive genes, they belong to nearly half of all the processes affected in both the mutants. Thus, GCR1 and GPA1 regulate not only some common genes, but also different genes belonging to the same processes to achieve similar outcomes. Overall, we validate some known and report many hitherto unknown roles of GPA1 in plants, including agronomically important ones such as biotic stress and nutrient response, and also provide compelling genetic evidence to revisit the role of GCR1 in G-protein signalling.

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Abbreviations

GPA1:

G-protein α subunit

GCR1:

G-protein coupled receptor

GEO:

Gene expression omnibus

GO:

Gene ontology

SEA:

Singular enrichment analysis

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Acknowledgments

This work was supported in part by research grant to NR [60(0056)/02/EMRII and 38(1246)/10/EMRII] and research fellowships to NC (09/806(015)/2008-EMR1) and PS (60(0056)/02/EMRII) from the Council of Scientific and Industrial Research (CSIR), Government of India. This paper is dedicated to the co-author Priyanka Sharma who is no more.

Author contributions

NC performed the phenotypic analysis of the mutant, microarray and RT-qPCR experiments, analyzed the data and wrote the initial draft of the manuscript; RRP, PS and NR conceptualized the project; KK generated the mutants; DC provided initial training for data analysis to RRP and PS; NR assisted NC in finalizing the manuscript; NR and RH supervised the project.

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Authors and Affiliations

  1. University School of Biotechnology, G.G.S. Indraprastha University, Sector 16 C, Dwarka, New Delhi, 110078, India

    Navjyoti Chakraborty, Priyanka Sharma, Ravi Ramesh Pathak & Nandula Raghuram

  2. Department of Plant Biology and Crop Science, Rothamsted Research, Harpenden, Hertfordshire, AL5 2JQ, UK

    Kostya Kanyuka

  3. School of Biotechnology, Jawaharlal Nehru University, New Delhi, India

    Devapriya Choudhury

  4. Department of Biology and Biochemistry, University of Bath, Claverton Down, Bath, BA2 7AY, UK

    Richard Hooley

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  1. Navjyoti Chakraborty
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  2. Priyanka Sharma
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  3. Kostya Kanyuka
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  4. Ravi Ramesh Pathak
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  5. Devapriya Choudhury
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  6. Richard Hooley
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  7. Nandula Raghuram
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Correspondence to Nandula Raghuram.

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Data Access: GEO accession number GSE 40217 (GSM 988507, GSM 988508, GSM988505 and GSM988506).

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Chakraborty, N., Sharma, P., Kanyuka, K. et al. G-protein α-subunit (GPA1) regulates stress, nitrate and phosphate response, flavonoid biosynthesis, fruit/seed development and substantially shares GCR1 regulation in A. thaliana . Plant Mol Biol 89, 559–576 (2015). https://doi.org/10.1007/s11103-015-0374-2

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