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Localization of RNS2 ribonuclease to the vacuole is required for its role in cellular homeostasis

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Abstract

Main conclusion

Localization of the RNase RNS2 to the vacuole via a C-terminal targeting signal is essential for its function in rRNA degradation and homeostasis.

RNase T2 ribonucleases are highly conserved enzymes present in the genomes of nearly all eukaryotes and many microorganisms. Their constitutive expression in different tissues and cell types of many organisms suggests a housekeeping role in RNA homeostasis. The Arabidopsis thaliana class II RNase T2, RNS2, is encoded by a single gene and functions in rRNA degradation. Loss of RNS2 results in RNA accumulation and constitutive activation of autophagy, possibly as a compensatory mechanism. While the majority of RNase T2 enzymes is secreted, RNS2 is located within the vacuole and in the endoplasmic reticulum (ER), possibly within ER bodies. As RNS2 has a neutral pH optimum, and the endomembrane organelles are connected by vesicle transport, the site within the endomembrane system at which RNS2 functions is unclear. Here we demonstrate that localization to the vacuole is essential for the physiological function of RNS2. A mutant allele of RNS2, rns2-1, results in production of an active RNS2 RNase but with a mutation that removes a putative C-terminal vacuolar targeting signal. The mutant protein is, therefore, secreted from the cell. This results in a constitutive autophagy phenotype similar to that observed in rns2 null mutants. These findings illustrate that the intracellular retention of RNS2 and localization within the vacuole are critical for its cellular function.

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Abbreviations

ConcA:

Concanamycin A

ER:

Endoplasmic reticulum

MDC:

Monodansylcadaverine

WT:

Wild-type

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Acknowledgements

This work was supported by Grant No. MCB-1051818 from the United States National Science Foundation to GCM and DCB and Grant No. DE-SC0014038 from the United States Department of Energy to DCB. We thank Danielle Ebany for isolation of an rns2-1 homozygote and Junmarie Soto-Burgos for assistance with confocal microscopy.

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    Authors and Affiliations

    1. Department of Genetics, Development and Cell Biology, Iowa State University, Ames, IA, 50011, USA

      Brice E. Floyd, Yosia Mugume & Diane C. Bassham

    2. Roy J. Carver Department of Biochemistry, Biophysics and Molecular Biology, Iowa State University, Ames, IA, 50011, USA

      Stephanie C. Morriss & Gustavo C. MacIntosh

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    1. Brice E. Floyd
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    2. Yosia Mugume
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    3. Stephanie C. Morriss
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    4. Gustavo C. MacIntosh
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    5. Diane C. Bassham
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    Correspondence to Gustavo C. MacIntosh or Diane C. Bassham.

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    B. E. Floyd and Y. Mugume contributed equally to this work.

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    Floyd, B.E., Mugume, Y., Morriss, S.C. et al. Localization of RNS2 ribonuclease to the vacuole is required for its role in cellular homeostasis. Planta 245, 779–792 (2017). https://doi.org/10.1007/s00425-016-2644-x

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