ATG6 interacting with NPR1 increases Arabidopsis thaliana resistance to Pst DC3000/avrRps4 by increasing its nuclear accumulation and stability
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Curated by eLife
eLife assessment
The study reports on a previously unrecognized function of ATG6 in plant immunity. The work is valuable because it proposes a direct interaction between ATG6 and a well-studied salicylic acid receptor protein, NPR1, which may interest researchers investigating plant immunity regulation. While the data presented are compelling, more information regarding the specificity of ATG6's role would improve the overall impact of the study, especially with an eye towards consistency with prior work.
This article has been Reviewed by the following groups
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- Evaluated articles (eLife)
- Plant Biology (eLife)
Abstract
Autophagy-related gene 6 (ATG6) plays a crucial role in plant immunity. Nonexpressor of pathogenesis-related genes1 (NPR1) acts as a signaling hub of plant immunity. However, the relationship between ATG6 and NPR1 is unclear. Here, we find that ATG6 directly interacts with NPR1. ATG6 overexpression significantly increased nuclear accumulation of NPR1. Furthermore, we demonstrate that ATG6 increases NPR1 protein levels and improves its stability. Interestingly, ATG6 promotes the formation of SINCs (SA-induced NPR1 condensates)-like condensates. Additionally, ATG6 and NPR1 synergistically promote the expression of pathogenesis-related genes. Further results showed that silencing ATG6 in NPR1-GFP exacerbates Pst DC3000/ avrRps4 invasion, while double overexpression of ATG6 and NPR1 synergistically inhibits Pst DC3000/ avrRps4 invasion. In summary, our findings unveil an interplay of NPR1 with ATG6 and elucidate important molecular mechanisms for enhancing plant immunity.We unveil a novel relationship in which ATG6 positively regulates NPR1 in plant immunity.
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eLife assessment
The study reports on a previously unrecognized function of ATG6 in plant immunity. The work is valuable because it proposes a direct interaction between ATG6 and a well-studied salicylic acid receptor protein, NPR1, which may interest researchers investigating plant immunity regulation. While the data presented are compelling, more information regarding the specificity of ATG6's role would improve the overall impact of the study, especially with an eye towards consistency with prior work.
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Reviewer #1 (Public Review):
Summary:
The authors showed that autophagy-related genes are involved in plant immunity by regulating the protein level of the salicylic acid receptor, NPR1.
Strengths:
The experiments are carefully designed and the data is convincing. The authors did a good job of understanding the relationship between ATG6 and NRP1.
Weaknesses:
- The authors can do a few additional experiments to test the role of ATG6 in plant immunity.
I recommend the authors to test the interaction between ATGs and other NPR1 homologs (such as NPR2).-The concentration of SA used in the experiment (0.5-1 mM) seems pretty high. Does a lower concentration of SA induce ATG6 accumulation in the nucleus?
-Does the silencing of ATG6 affect the cell death (or HR) triggered by AvrRPS4?
-SA and NPR1 are also required for immunity and are …
Reviewer #1 (Public Review):
Summary:
The authors showed that autophagy-related genes are involved in plant immunity by regulating the protein level of the salicylic acid receptor, NPR1.
Strengths:
The experiments are carefully designed and the data is convincing. The authors did a good job of understanding the relationship between ATG6 and NRP1.
Weaknesses:
- The authors can do a few additional experiments to test the role of ATG6 in plant immunity.
I recommend the authors to test the interaction between ATGs and other NPR1 homologs (such as NPR2).-The concentration of SA used in the experiment (0.5-1 mM) seems pretty high. Does a lower concentration of SA induce ATG6 accumulation in the nucleus?
-Does the silencing of ATG6 affect the cell death (or HR) triggered by AvrRPS4?
-SA and NPR1 are also required for immunity and are activated by other NLRs (such as RPS2 and RPM1). Is ATG6 also involved in immunity activated by these NLRs?
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Reviewer #2 (Public Review):
Summary:
The manuscript by Zhang et al. explores the effect of autophagy regulator ATG6 on NPR1-mediated immunity. The authors propose that ATG6 directly interacts with NPR1 in the nucleus to increase its stability and promote NPR1-dependent immune gene expression and pathogen resistance. This novel role of ATG6 is proposed to be independent of its role in autophagy in the cytoplasm. The authors demonstrate through biochemical analysis that ATG6 interacts with NPR1 in yeast and very weakly in vitro. They further demonstrate using overexpression transgenic plants that in the presence of ATG6-mcherry the stability of NPR1-GFP and its nuclear pool is increased.
However, the overall conclusions of the study are not well supported experimentally. The significance of the findings is low because of their mostly …
Reviewer #2 (Public Review):
Summary:
The manuscript by Zhang et al. explores the effect of autophagy regulator ATG6 on NPR1-mediated immunity. The authors propose that ATG6 directly interacts with NPR1 in the nucleus to increase its stability and promote NPR1-dependent immune gene expression and pathogen resistance. This novel role of ATG6 is proposed to be independent of its role in autophagy in the cytoplasm. The authors demonstrate through biochemical analysis that ATG6 interacts with NPR1 in yeast and very weakly in vitro. They further demonstrate using overexpression transgenic plants that in the presence of ATG6-mcherry the stability of NPR1-GFP and its nuclear pool is increased.
However, the overall conclusions of the study are not well supported experimentally. The significance of the findings is low because of their mostly correlational nature, and lack of consistency with earlier reports on the same protein.
Based on the integrity and quality of the data as well as the depth of analysis, it is not yet clear if ATG6 is a specific regulator of NPR1 or if it is affecting NPR1's stability indirectly, through inducing an elevation of SA levels in plants. As such, the current study demonstrates a correlation between overexpression of ATG6, SA accumulation, and NPR1 stability, however, whether and how these components work together is not yet demonstrated.
Based on the provided biochemical data, it is not yet clear if the ATG6 functions specifically through NPR1 or through its paralogs NPR3 and NPR4, which are negative regulators of immunity. It is quite possible that interaction with NPR1 (or any NPR) is not the major regulatory step in the activity of ATG6 in plant immunity. The effect of ATG6 on NPR1 could well be indirect, through a change in the SA level and redox environment of the cell during the immune response. Both SA level and redox state of the cell were reported to induce accumulation of NPR1 in the nucleus and increase in stability.
Another major issue is the poor quality of the subcellular analyses. In contradiction to previous studies, ATG6 in this study is not localized to autophagosome puncta, which suggests that the soluble localization pattern presented here does not reflect the true localization of ATG6. Even if the authors propose a novel, non-canonical nuclear localization for ATG6, they still should have detected the canonical autophagy-like localization of this protein.
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