Arabidopsis inositol polyphosphate kinase activities regulate COP9 deneddylation functions in phosphate homeostasis

doi:10.1111/jipb.70268

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Arabidopsis inositol polyphosphate kinase activities regulate COP9 deneddylation functions in phosphate homeostasis

Yashika Walia^1†, Medha Noopur^1†, Ishana Bhattacharya¹, Bhaskar Chandra Sahoo¹, Mritunjay Kasera¹, Naga Jyothi Pullagurla², Smritikana Dutta³, Guizhen Liu⁴, Gabriel Schaaf⁵, Henning Jessen⁴, Debabrata Laha², Souvik Bhattacharjee³ and Saikat Bhattacharjee^1*

1. Laboratory of Signal Transduction and Plant Resistance, UNESCO‐Regional Centre for Biotechnology (RCB), NCR Biotech Science Cluster, Faridabad 121001, India
2. Department of Biochemistry, Indian Institute of Science, Bengaluru 560012, India
3. Special Centre for Molecular Medicine, Jawaharlal Nehru University, New Delhi 110067, India
4. Faculty of Chemistry and Pharmacy & CIBSS‐The Center for Biological Signalling Studies, University of Freiburg, Freiburg 79104, Germany
5. Department of Plant Nutrition, Institute of Crop Science and Resource Conservation, Rheinische Friedrich‐Wilhelms‐Universitat Bonn, Bonn 53115, Germany
^†These authors contributed equally to this work.
^*Correspondence: Saikat Bhattacharjee (saikat@rcb.res.in)

Received:2025-08-22 Accepted:2026-03-26 Online:2026-05-05
Supported by:
This work was supported by financial support from the Regional Centre for Biotechnology (RCB) core funds and Grants (No. BT/PR45561/AGIII/103/103/2023 and EMR/2016/001899) to S.B. and S.B.; Young Investigator award and DBT‐RA fellowship (DBT‐RA/2021/January/N/218) to Y.W.; SERB N‐PDF award (No. PDF/2023/001938) to B.C.S.; and DBT‐RA fellowship (DBTRA/2023 24/N/JNU/118) to S.D. M.N. and I.B. thank CSIR [09/0937 (13803) 2022‐EMR‐I] and UGC, respectively, for funding support. D.L. acknowledges the Indian Institute of Science for start‐up funds and the Infosys Young Investigator award (IISc). G.S. acknowledges funding from the Deutsche Forschungsgemeinschaft under Germany's Excellence Strategy‐EXC 2070‐390732324 (PhenoRob) and grant SCHA 1274/5‐1.

Abstract

Abstract: Plant Cullin RING Ubiquitin E3 ligases (CRLs) play a critical role in targeted protein degradation, essential for physiological development and stress adaptation. The deneddylase activity of the COP9 signalosome (CSN) tightly regulates the cellular balance of neddylated cullins, which is crucial for maintaining the full spectrum of CRL functions. Although selective inositol polyphosphates (InsPs) act as cofactors in plant responses that involve ubiquitylation of negative regulators, their connection to CSN–CRL activities has remained unclear. In this study, we reveal that the two Arabidopsis thaliana InsP-kinases, IPK1 and ITPK1, physically interact and orchestrate the metabolic regulation of the CSN holo-complex activity. Notably, ITPK1 deficiency lowers Nedd8 processing rates, elevates the cellular ratios of neddylated cullins, and disturbs the dissociation equilibrium of CSN5 and CUL1 from the holo-complex. These findings uncover a novel autoregulatory switch in CSN functions, governed by deneddylation activity. Furthermore, we demonstrate that the phosphate starvation response (PSR), induced in phosphate-limited wild-type plants and constitutively active in the InsP-kinase mutants, is partly regulated by reduced deneddylation rates, which affect the stability of SPX4, a key negative regulator of PSR. Pharmacological inhibition of cullin neddylation stabilizes SPX4 and impairs PSR, thereby linking CSN–CRL dynamics to phosphate sensing. Conversely, pharmacologically inhibiting CSN5 deneddylase activity causes wild-type plants to exhibit PSR phenotypes similar to those of the InsP-kinase mutants. Collectively, these results reveal that specific InsP-kinases are partly involved in modulating plant PSR by fine-tuning the coordination between CRL and CSN activities.

Key words: COP9 signalosome, cullin RING ubiquitin ligase, inositol 1,3,4‐trisphosphate 5/6‐kinase 1, inositol hexakisphosphate (InsP₆) kinase 1, inositol polyphosphates, InsP7, deneddylation, phosphate homeostasis, phosphate‐starvation response, SPX4, ubiquitination

Yashika Walia, Medha Noopur, Ishana Bhattacharya, Bhaskar Chandra Sahoo, Mritunjay Kasera, Naga Jyothi Pullagurla, Smritikana Dutta, Guizhen Liu, Gabriel Schaaf, Henning Jessen, Debabrata Laha, Souvik Bhattacharjee, Saikat Bhattacharjee. Arabidopsis inositol polyphosphate kinase activities regulate COP9 deneddylation functions in phosphate homeostasis[J]. J Integr Plant Biol., DOI: 10.1111/jipb.70268.

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Arabidopsis inositol polyphosphate kinase activities regulate COP9 deneddylation functions in phosphate homeostasis

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