Coordinated regulation of photosynthesis and translation via NIK1/RPL10/LIMYB signaling module in response to biotic and abiotic stresses

Background

Energy management is an essential task to ensure living organisms’ survival. Maintaining a balance between production and consumption is essential for autotrophic and unmovable creatures like plants. During photosynthesis, plants incorporate carbon into the Calvin-Benson-Bassham cycle, providing a substrate for ATP-generating mitochondrial reactions. On the other hand, protein translation consumes considerable energy. These are major physiological events that cause energy fluctuation and are prone to be affected by various external stimuli.

To coordinate multiple inputs from changing environments, plants have evolved a signal hub like NUCLEAR SHUTTLE PROTEIN (NSP) – INTERACTING KINASE 1 (NIK1), which is known as a virulence target of begomoviral NSP to mediate antiviral signaling. NIK1 is a leucine-rich repeat receptor-like kinase (LRR-RLK) and undergoes dimerization and trans-phosphorylation at 474 Threonine residues. Activated NIK1 then mediates RIBOSOMAL PROTEIN L10 (RPL10) phosphorylation and redirects it to the nucleus. In the nucleus, the phosphorylated RPL10 interacts with the transcription repressor L10-Interacting Myb domain-contain protein (LIMYB), which thoroughly represses translational machinery-related genes, including RP genes, translational initiation, and elongation factors.

In this preprint, the authors expected NIK1 to act as an information spreader by coordinating environmental stresses through the RPL10/LIMYB signaling cascade, thereby adjusting photosynthesis and translation. They performed ChIP-seq on LIMYB-GFP seedlings to uncover the transcriptional landscape mediated by NIK1 activation and also monitored how NIK1 was activated under various biotic and abiotic stresses.

Aim

To elucidate the role of NIK1 activation in the modulation and synchronization of diverse signaling pathways under different stimuli in Arabidopsis thaliana.

 

Key findings

 

1. LIMYB was found to be phosphorylated, repressed the expression of photosynthetic apparatus-related genes, and inhibited photosynthesis, which depends on NIK1 activation under biotic stress. In the presence of viral PAMPs, NIK1/NIK2 – but not FLS2 or BAK1 – were required to mediate RPL10 phosphorylation.
2. Abiotic stimuli, like heat and osmotic stress, triggered NIK1 and RPL10 phosphorylation, activating antiviral signaling and LIMYB-mediated inhibition of translation and photosynthesis.

 

Why I chose this preprint

 

I selected this preprint because I am interested in translational control in plants responding to changing environments. The preprint nicely demonstrates how multiple stress stimuli were transferred through the NIK1-RPL10 phosphorylation cascade and the translation repressor LIMYB to suppress the expression of photosynthate- and translation machinery-related genes. This study shows how plants collect various external sources of information via numerous receptor combinations to regulate photosynthesis and translation.

Questions for the Authors

1. Under drought stress, have you examined the immunity gene expression in the constitutively activated NIK1-T474D transgenic lines? Another recent preprint mentioned that drought recovery induces immunity and confers pathogen resistance (Illouz-Eliaz et al., 2023). If the ectopic expression of NIK1-T474D confers drought tolerance, you could consider checking the expression of immunity genes and/or drought-responsive genes by qPCR analyses.

2. de novo protein biosynthesis was examined in previous studies about NIK1 (Brustolini et al., 2015; Zorzatto et al., 2015), and here you’ve performed RT-qPCR analysis of the translation machinery-related genes. Can the gene expression correlate quantitatively to the corresponding peptide translation?

3. Why do you think PHSIIOEC and FD1 expression are regulated in both 35S:NIK1-T474D and nik2-1 mutants but not in nik1-1 or nik1-1 nik2-1 mutants? This means that photosynthetic gene expression was negatively correlated with the presence of NIK1 – or is there another potential molecular scenario?

References

 

Brustolini OJB, Machado JPB, Condori-Apfata JA, Coco D, Deguchi M, Loriato VAP, Pereira WA, Alfenas-Zerbini P, Zerbini FM, Inoue-Nagata AK, Santos AA, Chory J, Silva FF, Fontes EPB (2015) Sustained NIK-mediated antiviral signalling confers broad-spectrum tolerance to begomoviruses in cultivated plants. Plant Biotechnol J 13: 1300-1311

Illouz-Eliaz N, Lande K, Yu J, Jow B, Swift J, Lee T, Nobori T, Castanon RG, Nery JR, Ecker JR (2023) Drought Recovery Induced Immunity Confers Pathogen Resistance. bioRxiv: 2023.2002.2027.530256

Zorzatto C, Machado JP, Lopes KV, Nascimento KJ, Pereira WA, Brustolini OJ, Reis PA, Calil IP, Deguchi M, Sachetto-Martins G, Gouveia BC, Loriato VA, Silva MA, Silva FF, Santos AA, Chory J, Fontes EP (2015) NIK1-mediated translation suppression functions as a plant antiviral immunity mechanism. Nature 520: 679-682

 

 

doi: https://doi.org/10.1242/prelights.35061

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