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In BriefIN BRIEF
Open Access

Plant Systemic Immunity Comes Full Circle: A Positive Regulatory Loop for Defense Amplification

Christian Danve M. Castroverde
Christian Danve M. Castroverde
MSU-DOE Plant Research Laboratory and MSU Plant Resilience Institute, Michigan State University, East Lansing, Michigan
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  • ORCID record for Christian Danve M. Castroverde
  • For correspondence: castrov3@msu.edu

Published October 2018. DOI: https://doi.org/10.1105/tpc.18.00712

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  • © 2018 American Society of Plant Biologists. All rights reserved.

The plant immune system is effective in conferring resistance to various invading pathogens and pests. Membrane-localized pattern recognition receptors (PRRs) and intracellular nucleotide binding domain, leucine-rich repeat proteins (NLRs) recognize pathogen-associated molecular patterns and pathogen virulence effectors, respectively, to initiate robust downstream responses that effectively contain or eliminate the invader. Infection at a local site with either virulent or avirulent pathogens can then activate a primed state in the whole plant termed systemic acquired resistance (SAR; Fu and Dong, 2013). The pathogen-inducible AGD2-LIKE DEFENSE RESPONSE PROTEIN1 (ALD1)-mediated biosynthesis of the l-lysine-derived amino acid pipecolic acid (Pip) and a subsequent FLAVIN-DEPENDENT MONOOXYGENASE1 (FMO1)-catalyzed hydroxylation leading to N-hydroxypipecolic acid (NHP) are integral metabolic events for SAR establishment (Hartmann and Zeier, 2018).

Although it is well-established that the signaling cascade downstream of PRRs and NLRs leads to MAP kinase (MPK) transphosphorylation, how MPK signaling relates to systemic plant immunity is only starting to be unraveled. In a previous study by Beckers et al. (2009), MPK3 and MPK6 were found to play a role in SAR establishment. These authors showed that MPK3 is more important than MPK6 to defense priming and SAR in Arabidopsis, but both enzymes are needed for full priming and SAR (Beckers et al., 2009). Now, Wang et al. (2018) provide additional convincing evidence for the SAR-MPK connection through a novel combination of genetic, biochemical, and physiological approaches.

The first line of evidence came from characterizing the MKK4DD mutant, which leads to constitutive activation of MPK3 and 6 (Ren et al., 2002). Localized MPK activation led to induced expression of the SAR-associated gene ALD1 and accumulation of the SAR metabolites Pip and NHP. These physiological changes consequently enhanced bacterial resistance in systemic leaves. Significantly, this enhanced systemic resistance persisted in the salicylic acid (SA)-deficient sid2 background, suggesting that sustained MPK activation acts redundantly with SA during SAR by increasing levels of NHP. Consistent with this, mutations in ALD1 and FMO1 abolished the MPK-induced SAR phenotype.

One of the target proteins of activated MPK3/6 is the WRKY33 transcription factor, which is a central regulator of plant immune responses (Mao et al., 2011). Mutation of WRKY33 compromised MKK4DD induction of SAR, concomitant with reduced SAR gene expression and Pip levels. Because these observations were shown not just for Pto but for another pathogen as well (Pseudomonas syringae pv maculicola), this suggested that MPK-activated SAR converges at WRKY33. Consistent with this hypothesis, this study and a previous study (Birkenbihl et al., 2017) demonstrated that the WRKY33 transcription factor binds to the promoter of the ALD1.

To come full circle, Wang et al. (2018) showed that Pip could induce MPK3/6 phosphorylation (see figure). They first noticed that the retarded growth phenotype after Pip treatment is dependent on BRI1-ASSOCIATED RECEPTOR KINASE1 (BAK1) and BAK1-LIKE 1 (BKK1), which are coreceptors during PRR signaling. This observation suggested that Pip might be perceived by a PRR, which would be expected to activate MAP kinase signaling. The authors confirmed this prediction, demonstrating a positive feedback loop consisting of Pip/NHP activating MPK3/6, which activates WRKY33, which induces ALD1, thus leading to elevated levels of Pip and NHP.

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Defense amplification through the Pip-NHP-MAPK-WRKY33-ALD1 regulatory loop during SAR. Recognition of pathogen effectors and the SAR metabolite Pip leads to MPK3/6 phosphorylation and eventual activation of the WRKY33 transcription factor. WRKY33 regulates transcription of the ALD1, a key gene for Pip biosynthesis. (Adapted from Wang et al. [2018], Figure 7F.)

This comprehensive mechanistic investigation of SAR answers long-standing mysteries in plant immunity. However, several interesting observations in this study raise important questions. Why is SA necessary for Pto-mediated SAR but not for Pto AvrRpt2-mediated SAR? What is the receptor for Pip and its derivatives that is dependent on BAK1/BKK1? Is Pip behaving like a host-derived damage-associated molecular pattern? Is SAR a manifestation of long-distance pattern-triggered immunity? These and other questions provide exciting opportunities for more breakthroughs in the future.

Footnotes

  • www.plantcell.org/cgi/doi/10.1105/tpc.18.00712

  • ↵[OPEN] Articles can be viewed without a subscription.

References

  1. ↵
    1. Beckers, G.J.M.,
    2. Jaskiewicz, M.,
    3. Liu, Y.,
    4. Underwood, W.R.,
    5. He, S.Y.,
    6. Zhang, S., and
    7. Conrath, U.
    (2009). Mitogen-activated protein kinases 3 and 6 are required for full priming of stress responses in Arabidopsis thaliana. Plant Cell 21: 944–953.
    OpenUrlAbstract/FREE Full Text
  2. ↵
    1. Birkenbihl, R.P.,
    2. Kracher, B.,
    3. Somssich, I.E.
    (2017). Induced genome-wide binding of three Arabidopsis WRKY transcription factors during early MAMP-triggered immunity. Plant Cell 29: 20–38.
    OpenUrlCrossRefPubMed
  3. ↵
    1. Fu, Z.Q.,
    2. Dong, X.
    (2013). Systemic acquired resistance: turning local infection into global defense. Annu. Rev. Plant Biol. 64: 839–863.
    OpenUrl
  4. ↵
    1. Hartmann, M.,
    2. Zeier, J.
    (2018). L-lysine metabolism to N-hydroxypipecolic acid: an integral immune-activating pathway in plants. Plant J. 96: 5–21.
    OpenUrlAbstract/FREE Full Text
  5. ↵
    1. Mao, G.,
    2. Meng, X.,
    3. Liu, Y.,
    4. Zheng, Z.,
    5. Chen, Z.,
    6. Zhang, S.
    (2011). Phosphorylation of a WRKY transcription factor by two pathogen-responsive MAPKs drives phytoalexin biosynthesis in Arabidopsis. Plant Cell 23: 1639–1653.
    OpenUrlAbstract/FREE Full Text
  6. ↵
    1. Ren, D.,
    2. Yang, H.,
    3. Zhang, S.
    (2002). Cell death mediated by MAPK is associated with hydrogen peroxide production in Arabidopsis. J. Biol. Chem. 277: 559–565.
    OpenUrlAbstract/FREE Full Text
  7. ↵
    1. Wang, Y.,
    2. Schuck, S.,
    3. Wua, J.,
    4. Yang, P.,
    5. Döring, A.C.,
    6. Zeier, J.,
    7. Tsuda, K.
    (2018). A MPK3/6-WRKY33-ALD1-pipecolic acid regulatory loop contributes to systemic acquired resistance. Plant Cell 30: 2480–2494.
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Plant Systemic Immunity Comes Full Circle: A Positive Regulatory Loop for Defense Amplification
Christian Danve M. Castroverde
The Plant Cell Oct 2018, 30 (10) 2238-2239; DOI: 10.1105/tpc.18.00712

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Plant Systemic Immunity Comes Full Circle: A Positive Regulatory Loop for Defense Amplification
Christian Danve M. Castroverde
The Plant Cell Oct 2018, 30 (10) 2238-2239; DOI: 10.1105/tpc.18.00712
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The Plant Cell: 30 (10)
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Vol. 30, Issue 10
Oct 2018
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