Abstract

Abiotic and biotic stress can have a detrimental impact on plant growth and productivity. Hence, there is a substantial demand for key factors of stress responses to improve yield stability of crops. Members of the poly(ADP-ribose)polymerase (PARP) protein family, which post-translationally modify (PARylate) nuclear proteins, have been suggested as such universal determinants of plant stress responses. A role under abiotic stress has been inferred from studies in which a genetic or, more commonly, pharmacological inhibition of PARP activity improved the performance of stressed plants. To further elucidate the role of PARP proteins under stress, T-DNA knockout mutants for the three Arabidopsis thaliana PARP genes were subjected to drought, osmotic, salt, and oxidative stress. To exclude a functional redundancy, which was indicated by a transcriptional upregulation of the remaining parp genes, a parp triple mutant was generated. Surprisingly, parp mutant plants did not differ from wild type plants in any of these stress experiments, independent from the number of PARP genes mutated. The parp triple mutant was also analyzed for callose formation in response to the pathogenassociated molecular pattern flg22. Unexpectedly, callose formation was unaltered in the mutant, albeit pharmacological PARP inhibition robustly blocked this immune response, confirming previous reports. Evidently, pharmacological inhibition appears to be more robust than the abolition of all PARP genes, indicating the presence of so-far undescribed proteins with PARP activity. This was supported by the finding that protein PARylation was not absent, but even increased in the parp triple mutant. Candidates for novel PARP-inhibitor targets may be found in the SRO protein family. These proteins harbor a catalytic PARP-like domain and are centrally involved in stress responses. Molecular modeling analyses, employing animal PARPs as templates, indeed indicated a capability of the SRO proteins RCD1 and SRO1 to bind nicotinamide-derived inhibitors. Collectively, the results of our study suggest that the stress-related phenotypes of parp mutants are highly conditional, and they call for a reconsideration of PARP inhibitor studies. In the context of this study, we also propose a unifying nomenclature of PARP genes and parp mutants, which is currently highly inconsistent and redundant.

Highlights

  • The frequency and severity of abiotic stress conditions, such as drought or heat waves, are prospected to increase markedly in the near future due to the prevalent climate change

  • PARP1 stands for the protein with the highest similarity to HsPARP1, encoded by At2g31320, while PARP2 is the protein encoded by At4g02390

  • PARP3 gave a similar picture in most cases, albeit the upregulation was more pronounced in few instances, reaching up to 80-fold in one drought stress study

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Summary

Introduction

The frequency and severity of abiotic stress conditions, such as drought or heat waves, are prospected to increase markedly in the near future due to the prevalent climate change. To safeguard crop productivity and food security, it is necessary to find ways to improve the plants’ performance under such conditions in the field For this reason, there has been an intense search for key regulators in the plant’s genetic set-up that have robust and consistent effects on stress tolerance. Activated upon DNA strand breaks, HsPARP1 forms poly(ADP-ribose) chains by attaching ADP-ribose molecules to nuclear proteins, including itself, using NAD+ as substrate. This fast and transient protein modification activates the DNA repair machinery (Pines et al, 2013). We propose a unified mutant nomenclature, as described in the “Results” section

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