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Mol. Cells 2022; 45(12): 883-885

Published online December 31, 2022

https://doi.org/10.14348/molcells.2022.0150

© The Korean Society for Molecular and Cellular Biology

How Does Global Warming Sabotage Plant Immunity?

Souvik Dhar1 and Ji-Young Lee1,2,3,*

1School of Biological Science, College of Natural Sciences, Seoul National University, Seoul 08826, Korea, 2Plant Genomics and Breeding Institute, Seoul National University, Seoul 08826, Korea, 3Plant Immunity Research Center, Seoul National University, Seoul 08826, Korea

Correspondence to : jl924@snu.ac.kr

Received: September 26, 2022; Revised: October 7, 2022; Accepted: October 18, 2022

This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial-ShareAlike 3.0 Unported License. To view a copy of this license, visit http://creativecommons.org/licenses/by-nc-sa/3.0/.


Temperature-induced vulnerability in the plant is regulated through the optimized CBP60g expression and salicylic acid (SA) biosynthesis: SA plays a vital role in plant defense. Under high temperatures, plant defense mechanism is compromised. A recent study by Kim et al. (2022) demonstrated that elevated temperature negatively affects GDAC (GBPL3 defense-activated biomolecular condensates) formation and its recruitment to the CBP60g promoter. This causes SA biosynthesis suppression. The findings of this work will serve as a benchmark in understanding the molecular mechanism underlying of plant-environment-disease triangle. PAMP, pathogen-associated molecular pattern; MAMP, microbe-associated molecular pattern; LRR, leucine-rich repeat; TF, transcription factor.

Plants often face a wide range of biotic and extreme environmental stresses as sessile organisms. These stresses cause physiological changes, resulting in plant growth and yield penalty. Since plants lack a circulatory immune system, they solely depend on the cell-autonomous local responses, for example, the transportation of signaling molecules through a membrane-separated vesicular system (Kwon et al., 2020; Won and Kim, 2020). Elevated temperature profoundly impacts plant defense responses and render plants vulnerable to pathogens. Research breakthroughs elucidating the underlying molecular mechanisms of this pathway were made in the last decade. Zhu et al. (2010) reported that a mutation in the resistance (R) gene sufficiently changes the temperature sensitivity of the plant immune response and confers resistance at high temperatures. Another study (Cheng et al., 2013) reported that high temperature decreased the secretion of pathogenic effectors but accelerated the proliferation of pathogenic organisms, inhibiting effector-triggered immunity (ETI) while enhancing PAMP-triggered immunity (PTI). Defense-related hormones, such as jasmonic acid, salicylic acid (SA), and ethylene, play an essential role in pathogen-induced hypersensitive responses (Huot et al., 2014). Previous studies have indicated that a higher temperature significantly suppresses pathogen-induced SA production while enhancing other hormone pathways (Gangappa et al., 2017; Huot et al., 2017; Malamy et al., 1992). However, the mechanism underlying the selective inhibition of SA signaling under high ambient temperatures in the presence of pathogens has remained elusive (Gangappa et al., 2017; Huot et al., 2017). Recently, Kim et al. (2022) found that the calmodulin-binding protein 60-like g (CBP60g) transcription factor impacts SA production, basal immunity, and ETI at an elevated temperature. CBP60g proteins are highly conserved in plants. Therefore, they might play an essential role in mediating the triangular interactions among crop plants, the pathogen, and the environment (Kim et al., 2022; Zhu et al., 2010).

Calcium signaling is essential in plant defense responses associated with PTI and ETI (Wang et al., 2009). Within the cell, calcium signals are transduced by binding calcium ions to calmodulins (CaMs), which subsequently bind to CaM binding proteins (Bouché et al., 2005). In Arabidopsis thaliana, Arabidopsis hereafter, the CBP60 family comprised seven members (CBP60a-CBP60g). A previous report (Wang et al., 2009) suggested that CBP60g is induced by infection with Pseudomonas and plays a critical role in disease resistance through the activation of SA signaling. In a recently published study, Kim et al. (2022) discovered that the temperature-induced inhibition of SA biosynthesis in response to pathogens is because of the transcriptional suppression of CBP60g. Through bulk RNA-sequencing analysis between Col-0 seedlings, which were challenged with Pseudomonas syringae pv. tomato (Pst) DC3000 at ambient (23°C) and high temperatures (28°C), the authors discovered that the transcription of CBP60g and SARD1, a closely related gene of CBP60g (Wang et al., 2011), were down-regulated at the high temperature. Kim et al. (2022) further examined the upstream regulators that transcriptionally repressed CBP60g and SARD1 expression.

GUANYLATE BINDING PROTEIN-LIKE 3 (GBPL3) forms GBPL defense-activated biomolecular condensates called GDACs, which bind to the promoters of CBP60g and other defense-related genes by recruiting mediator complex and RNA polymerase II (Huang et al., 2021). Kim et al. (2022) discovered the disassembly of the GDACs at a higher growth temperature (28°C) and concomitant inhibition in the expression of CBP60g and SARD1. This observation unveils a previously unknown pathway behind the inhibition of SA production at elevated temperatures when plants are challenged with a pathogenic elicitor.

To survive in an unfavorable environment, plants must manage limited resources to relocate to the designated organ for growth and accelerate their defense mechanisms. During this process, plants often activate defense signaling at the expense of growth. However, recent studies (Figueroa-Macías et al., 2021; Neuser et al., 2019) suggested that there could be an alternative instead of this ‘trade-off’ signaling between growth and defense regulatory mechanism that reprogram developmental pathways based on the hostile environment. When Kim et al. (2022) over-expressed CBP60g under the 35S promoter using the uORFsTBF1 strategy, which contains the upstream open reading frame (uORF) region of the TBF1 gene, they found that transgenic Arabidopsis plants could maintain a defense system and SA production even at high temperatures. Notably, the uORFsTBF1 region allows controlled protein translation in response to pathogenic infection (Xu et al., 2017). This observation, with the other conclusion led by Kim et al. (2022), strongly proposed that CBP60g is the missing link that inversely regulates plant vulnerability toward the pathogen under high temperatures.

Recent studies (Jing et al., 2019; Okada et al., 2021; Poncini et al., 2017) reported that root growth was impaired by perceiving biotic or abiotic stress signals. Consistent with this finding, we also identified that plant elicitor peptide 1 (PEP1), a general sensor of biotic and abiotic stresses, affects the reprograming of Arabidopsis root apical meristem and vascular development (Dhar et al., 2021). In addition, PEP1 strongly impacts the cell-to-cell symplastic connection, which is responsible for transporting developmental signals over a long distance. A molecular link between PEP1 perception and reprograming of the developmental signal is yet to be uncovered, which could also be employed in engineering plants with intact danger sensing without root growth penalty.

In summary, the study led by Kim et al. (2022) provided comprehensive evidence of how environmental factors control the SA-induced defense signaling pathway in connection to plant immunity. The author’s results will serve as a benchmark for understanding the concept of the plant-environment-disease triangle and prompt future researchers to identify the mechanistic approach toward the underlying defense response pathways.

We thank all members of the Lee lab for their discussions and comments at various stages. This work was supported by the grants NRF-2018R1A5A1023599 and NRF-2021R1A2C3006061 to J.-Y.L. from the National Research Foundation of Korea. S.D. was supported by the Brain Korea 21 Four Program.

  1. Bouché N., Yellin A., Snedden W.A., and Fromm H. (2005). Plant-specific calmodulin-binding proteins. Annu. Rev. Plant Biol. 56, 435-466.
    Pubmed CrossRef
  2. Cheng C., Gao X., Feng B., Sheen J., Shan L., and He P. (2013). Plant immune response to pathogens differs with changing temperatures. Nat. Commun. 4, 2530.
    Pubmed KoreaMed CrossRef
  3. Dhar S., Kim H., Segonzac C., and Lee J.Y. (2021). The danger-associated peptide PEP1 directs cellular reprogramming in the Arabidopsis root vascular system. Mol. Cells 44, 830-842.
    Pubmed KoreaMed CrossRef
  4. Figueroa-Macías J.P., García Y.C., Núñez M., Díaz K., Olea A.F., and Espinoza L. (2021). Plant growth-defense trade-offs: molecular processes leading to physiological changes. Int. J. Mol. Sci. 22, 693.
    Pubmed KoreaMed CrossRef
  5. Gangappa S.N., Berriri S., and Kumar S.V. (2017). PIF4 coordinates thermosensory growth and immunity in Arabidopsis. Curr. Biol. 27, 243-249.
    Pubmed KoreaMed CrossRef
  6. Huang S., Zhu S., Kumar P., and MacMicking J.D. (2021). A phase-separatednuclear GBPL circuit controls immunity in plants. Nature 594, 424-429.
    Pubmed KoreaMed CrossRef
  7. Huot B., Castroverde C.D.M., Velásquez A.C., Hubbard E., Pulman J.A., Yao J., Childs K.L., Tsuda K., Montgomery B.L., and He S.Y. (2017). Dual impact of elevated temperature on plant defence and bacterial virulence in Arabidopsis. Nat. Commun. 8, 1808.
    Pubmed KoreaMed CrossRef
  8. Huot B., Yao J., Montgomery B.L., and He S.Y. (2014). Growth-defense tradeoffs in plants: a balancing act to optimize fitness. Mol. Plant 7, 1267-1287.
    Pubmed KoreaMed CrossRef
  9. Jing Y., Zheng X., Zhang D., Shen N., Wang Y., Yang L., Fu A., Shi J., Zhao F., and Lan W., et al. (2019). Danger-associated peptides interact with PIN-dependent local auxin distribution to inhibit root growth in Arabidopsis. Plant Cell 31, 1767-1787.
    Pubmed KoreaMed CrossRef
  10. Kim J.H., Castroverde C.D.M., Huang S., Li C., Hilleary R., Seroka A., Sohrabi R., Medina-Yerena D., Huot B., and Wang J., et al. (2022). Increasing the resilience of plant immunity to a warming climate. Nature 607, 339-344.
    Pubmed KoreaMed CrossRef
  11. Kwon C., Lee J.H., and Yun H.S. (2020). SNAREs in plant biotic and abiotic stress responses. Mol. Cells 43, 501-508.
    Pubmed KoreaMed CrossRef
  12. Malamy J., Hennig J., and Klessig D.F. (1992). Temperature-dependent induction of salicylic acid and its conjugates during the resistance response to tobacco mosaic virus infection. Plant Cell 4, 359-366.
    Pubmed KoreaMed CrossRef
  13. Neuser J., Metzen C.C., Dreyer B.H., Feulner C., van Dongen J.T., Schmidt R.R., and Schippers J.H. (2019). HBI1 mediates the trade-off between growth and immunity through its impact on apoplastic ROS homeostasis. Cell Rep. 28, 1670-1678.e3.
    Pubmed CrossRef
  14. Okada K., Kubota Y., Hirase T., Otani K., Goh T., Hiruma K., and Saijo Y. (2021). Uncoupling root hair formation and defence activation from growth inhibition in response to damage‐associated Pep peptides in Arabidopsis thaliana. New Phytol. 229, 2844-2858.
    Pubmed CrossRef
  15. Poncini L., Wyrsch I., Dénervaud Tendon V., Vorley T., Boller T., Geldner N., Métraux J.P., and Lehmann S. (2017). In roots of Arabidopsis thaliana, the damage-associated molecular pattern AtPep1 is a stronger elicitor of immune signalling than flg22 or the chitin heptamer. PLoS One 12, e0185808.
    Pubmed KoreaMed CrossRef
  16. Wang L., Tsuda K., Sato M., Cohen J.D., Katagiri F., and Glazebrook J. (2009). Arabidopsis CaM binding protein CBP60g contributes to MAMP-induced SA accumulation and is involved in disease resistance against Pseudomonas syringae. PLoS Pathog. 5, e1000301.
    Pubmed KoreaMed CrossRef
  17. Wang L., Tsuda K., Truman W., Sato M., Nguyen L.V., Katagiri F., and Glazebrook J. (2011). CBP60g and SARD1 play partially redundant critical roles in salicylic acid signaling. Plant J. 67, 1029-1041.
    Pubmed CrossRef
  18. Won K.H. and Kim H. (2020). Functions of the plant Qbc SNARE SNAP25 in cytokinesis and biotic and abiotic stress responses. Mol. Cells 43, 313-322.
    Pubmed KoreaMed CrossRef
  19. Xu G., Yuan M., Ai C., Liu L., Zhuang E., Karapetyan S., Wang S., and Dong X. (2017). uORF-mediated translation allows engineered plant disease resistance without fitness costs. Nature 545, 491-494.
    Pubmed KoreaMed CrossRef
  20. Zhu Y., Qian W., and Hua J. (2010). Temperature modulates plant defense responses through NB-LRR proteins. PLoS Pathog. 6, e1000844.
    Pubmed KoreaMed CrossRef

Article

Journal Club

Mol. Cells 2022; 45(12): 883-885

Published online December 31, 2022 https://doi.org/10.14348/molcells.2022.0150

Copyright © The Korean Society for Molecular and Cellular Biology.

How Does Global Warming Sabotage Plant Immunity?

Souvik Dhar1 and Ji-Young Lee1,2,3,*

1School of Biological Science, College of Natural Sciences, Seoul National University, Seoul 08826, Korea, 2Plant Genomics and Breeding Institute, Seoul National University, Seoul 08826, Korea, 3Plant Immunity Research Center, Seoul National University, Seoul 08826, Korea

Correspondence to:jl924@snu.ac.kr

Received: September 26, 2022; Revised: October 7, 2022; Accepted: October 18, 2022

This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial-ShareAlike 3.0 Unported License. To view a copy of this license, visit http://creativecommons.org/licenses/by-nc-sa/3.0/.

PLANT DEFENSE IS COMPROMISED IN HIGH-TEMPERATURE STRESSES

Plants often face a wide range of biotic and extreme environmental stresses as sessile organisms. These stresses cause physiological changes, resulting in plant growth and yield penalty. Since plants lack a circulatory immune system, they solely depend on the cell-autonomous local responses, for example, the transportation of signaling molecules through a membrane-separated vesicular system (Kwon et al., 2020; Won and Kim, 2020). Elevated temperature profoundly impacts plant defense responses and render plants vulnerable to pathogens. Research breakthroughs elucidating the underlying molecular mechanisms of this pathway were made in the last decade. Zhu et al. (2010) reported that a mutation in the resistance (R) gene sufficiently changes the temperature sensitivity of the plant immune response and confers resistance at high temperatures. Another study (Cheng et al., 2013) reported that high temperature decreased the secretion of pathogenic effectors but accelerated the proliferation of pathogenic organisms, inhibiting effector-triggered immunity (ETI) while enhancing PAMP-triggered immunity (PTI). Defense-related hormones, such as jasmonic acid, salicylic acid (SA), and ethylene, play an essential role in pathogen-induced hypersensitive responses (Huot et al., 2014). Previous studies have indicated that a higher temperature significantly suppresses pathogen-induced SA production while enhancing other hormone pathways (Gangappa et al., 2017; Huot et al., 2017; Malamy et al., 1992). However, the mechanism underlying the selective inhibition of SA signaling under high ambient temperatures in the presence of pathogens has remained elusive (Gangappa et al., 2017; Huot et al., 2017). Recently, Kim et al. (2022) found that the calmodulin-binding protein 60-like g (CBP60g) transcription factor impacts SA production, basal immunity, and ETI at an elevated temperature. CBP60g proteins are highly conserved in plants. Therefore, they might play an essential role in mediating the triangular interactions among crop plants, the pathogen, and the environment (Kim et al., 2022; Zhu et al., 2010).

TEMPERATURE-SENSITIVE PHASE TRANSITION OF GBPL3 COORDINATES CBP60g MEDIATED DEFENSE SIGNALING

Calcium signaling is essential in plant defense responses associated with PTI and ETI (Wang et al., 2009). Within the cell, calcium signals are transduced by binding calcium ions to calmodulins (CaMs), which subsequently bind to CaM binding proteins (Bouché et al., 2005). In Arabidopsis thaliana, Arabidopsis hereafter, the CBP60 family comprised seven members (CBP60a-CBP60g). A previous report (Wang et al., 2009) suggested that CBP60g is induced by infection with Pseudomonas and plays a critical role in disease resistance through the activation of SA signaling. In a recently published study, Kim et al. (2022) discovered that the temperature-induced inhibition of SA biosynthesis in response to pathogens is because of the transcriptional suppression of CBP60g. Through bulk RNA-sequencing analysis between Col-0 seedlings, which were challenged with Pseudomonas syringae pv. tomato (Pst) DC3000 at ambient (23°C) and high temperatures (28°C), the authors discovered that the transcription of CBP60g and SARD1, a closely related gene of CBP60g (Wang et al., 2011), were down-regulated at the high temperature. Kim et al. (2022) further examined the upstream regulators that transcriptionally repressed CBP60g and SARD1 expression.

GUANYLATE BINDING PROTEIN-LIKE 3 (GBPL3) forms GBPL defense-activated biomolecular condensates called GDACs, which bind to the promoters of CBP60g and other defense-related genes by recruiting mediator complex and RNA polymerase II (Huang et al., 2021). Kim et al. (2022) discovered the disassembly of the GDACs at a higher growth temperature (28°C) and concomitant inhibition in the expression of CBP60g and SARD1. This observation unveils a previously unknown pathway behind the inhibition of SA production at elevated temperatures when plants are challenged with a pathogenic elicitor.

SECURING PLANT DEFENSE UNDER HIGH TEMPERATURES WITHOUT GROWTH PENALTY

To survive in an unfavorable environment, plants must manage limited resources to relocate to the designated organ for growth and accelerate their defense mechanisms. During this process, plants often activate defense signaling at the expense of growth. However, recent studies (Figueroa-Macías et al., 2021; Neuser et al., 2019) suggested that there could be an alternative instead of this ‘trade-off’ signaling between growth and defense regulatory mechanism that reprogram developmental pathways based on the hostile environment. When Kim et al. (2022) over-expressed CBP60g under the 35S promoter using the uORFsTBF1 strategy, which contains the upstream open reading frame (uORF) region of the TBF1 gene, they found that transgenic Arabidopsis plants could maintain a defense system and SA production even at high temperatures. Notably, the uORFsTBF1 region allows controlled protein translation in response to pathogenic infection (Xu et al., 2017). This observation, with the other conclusion led by Kim et al. (2022), strongly proposed that CBP60g is the missing link that inversely regulates plant vulnerability toward the pathogen under high temperatures.

Recent studies (Jing et al., 2019; Okada et al., 2021; Poncini et al., 2017) reported that root growth was impaired by perceiving biotic or abiotic stress signals. Consistent with this finding, we also identified that plant elicitor peptide 1 (PEP1), a general sensor of biotic and abiotic stresses, affects the reprograming of Arabidopsis root apical meristem and vascular development (Dhar et al., 2021). In addition, PEP1 strongly impacts the cell-to-cell symplastic connection, which is responsible for transporting developmental signals over a long distance. A molecular link between PEP1 perception and reprograming of the developmental signal is yet to be uncovered, which could also be employed in engineering plants with intact danger sensing without root growth penalty.

In summary, the study led by Kim et al. (2022) provided comprehensive evidence of how environmental factors control the SA-induced defense signaling pathway in connection to plant immunity. The author’s results will serve as a benchmark for understanding the concept of the plant-environment-disease triangle and prompt future researchers to identify the mechanistic approach toward the underlying defense response pathways.

ACKNOWLEDGMENTS

We thank all members of the Lee lab for their discussions and comments at various stages. This work was supported by the grants NRF-2018R1A5A1023599 and NRF-2021R1A2C3006061 to J.-Y.L. from the National Research Foundation of Korea. S.D. was supported by the Brain Korea 21 Four Program.

AUTHOR CONTRIBUTIONS

S.D. and J.-Y.L. wrote the paper.

CONFLICT OF INTEREST

The authors have no potential conflicts of interest to disclose.

Fig. 1.Temperature-induced vulnerability in the plant is regulated through the optimized CBP60g expression and salicylic acid (SA) biosynthesis: SA plays a vital role in plant defense. Under high temperatures, plant defense mechanism is compromised. A recent study by Kim et al. (2022) demonstrated that elevated temperature negatively affects GDAC (GBPL3 defense-activated biomolecular condensates) formation and its recruitment to the CBP60g promoter. This causes SA biosynthesis suppression. The findings of this work will serve as a benchmark in understanding the molecular mechanism underlying of plant-environment-disease triangle. PAMP, pathogen-associated molecular pattern; MAMP, microbe-associated molecular pattern; LRR, leucine-rich repeat; TF, transcription factor.

Fig 1.

Figure 1.Temperature-induced vulnerability in the plant is regulated through the optimized CBP60g expression and salicylic acid (SA) biosynthesis: SA plays a vital role in plant defense. Under high temperatures, plant defense mechanism is compromised. A recent study by Kim et al. (2022) demonstrated that elevated temperature negatively affects GDAC (GBPL3 defense-activated biomolecular condensates) formation and its recruitment to the CBP60g promoter. This causes SA biosynthesis suppression. The findings of this work will serve as a benchmark in understanding the molecular mechanism underlying of plant-environment-disease triangle. PAMP, pathogen-associated molecular pattern; MAMP, microbe-associated molecular pattern; LRR, leucine-rich repeat; TF, transcription factor.
Molecules and Cells 2022; 45: 883-885https://doi.org/10.14348/molcells.2022.0150

References

  1. Bouché N., Yellin A., Snedden W.A., and Fromm H. (2005). Plant-specific calmodulin-binding proteins. Annu. Rev. Plant Biol. 56, 435-466.
    Pubmed CrossRef
  2. Cheng C., Gao X., Feng B., Sheen J., Shan L., and He P. (2013). Plant immune response to pathogens differs with changing temperatures. Nat. Commun. 4, 2530.
    Pubmed KoreaMed CrossRef
  3. Dhar S., Kim H., Segonzac C., and Lee J.Y. (2021). The danger-associated peptide PEP1 directs cellular reprogramming in the Arabidopsis root vascular system. Mol. Cells 44, 830-842.
    Pubmed KoreaMed CrossRef
  4. Figueroa-Macías J.P., García Y.C., Núñez M., Díaz K., Olea A.F., and Espinoza L. (2021). Plant growth-defense trade-offs: molecular processes leading to physiological changes. Int. J. Mol. Sci. 22, 693.
    Pubmed KoreaMed CrossRef
  5. Gangappa S.N., Berriri S., and Kumar S.V. (2017). PIF4 coordinates thermosensory growth and immunity in Arabidopsis. Curr. Biol. 27, 243-249.
    Pubmed KoreaMed CrossRef
  6. Huang S., Zhu S., Kumar P., and MacMicking J.D. (2021). A phase-separatednuclear GBPL circuit controls immunity in plants. Nature 594, 424-429.
    Pubmed KoreaMed CrossRef
  7. Huot B., Castroverde C.D.M., Velásquez A.C., Hubbard E., Pulman J.A., Yao J., Childs K.L., Tsuda K., Montgomery B.L., and He S.Y. (2017). Dual impact of elevated temperature on plant defence and bacterial virulence in Arabidopsis. Nat. Commun. 8, 1808.
    Pubmed KoreaMed CrossRef
  8. Huot B., Yao J., Montgomery B.L., and He S.Y. (2014). Growth-defense tradeoffs in plants: a balancing act to optimize fitness. Mol. Plant 7, 1267-1287.
    Pubmed KoreaMed CrossRef
  9. Jing Y., Zheng X., Zhang D., Shen N., Wang Y., Yang L., Fu A., Shi J., Zhao F., and Lan W., et al. (2019). Danger-associated peptides interact with PIN-dependent local auxin distribution to inhibit root growth in Arabidopsis. Plant Cell 31, 1767-1787.
    Pubmed KoreaMed CrossRef
  10. Kim J.H., Castroverde C.D.M., Huang S., Li C., Hilleary R., Seroka A., Sohrabi R., Medina-Yerena D., Huot B., and Wang J., et al. (2022). Increasing the resilience of plant immunity to a warming climate. Nature 607, 339-344.
    Pubmed KoreaMed CrossRef
  11. Kwon C., Lee J.H., and Yun H.S. (2020). SNAREs in plant biotic and abiotic stress responses. Mol. Cells 43, 501-508.
    Pubmed KoreaMed CrossRef
  12. Malamy J., Hennig J., and Klessig D.F. (1992). Temperature-dependent induction of salicylic acid and its conjugates during the resistance response to tobacco mosaic virus infection. Plant Cell 4, 359-366.
    Pubmed KoreaMed CrossRef
  13. Neuser J., Metzen C.C., Dreyer B.H., Feulner C., van Dongen J.T., Schmidt R.R., and Schippers J.H. (2019). HBI1 mediates the trade-off between growth and immunity through its impact on apoplastic ROS homeostasis. Cell Rep. 28, 1670-1678.e3.
    Pubmed CrossRef
  14. Okada K., Kubota Y., Hirase T., Otani K., Goh T., Hiruma K., and Saijo Y. (2021). Uncoupling root hair formation and defence activation from growth inhibition in response to damage‐associated Pep peptides in Arabidopsis thaliana. New Phytol. 229, 2844-2858.
    Pubmed CrossRef
  15. Poncini L., Wyrsch I., Dénervaud Tendon V., Vorley T., Boller T., Geldner N., Métraux J.P., and Lehmann S. (2017). In roots of Arabidopsis thaliana, the damage-associated molecular pattern AtPep1 is a stronger elicitor of immune signalling than flg22 or the chitin heptamer. PLoS One 12, e0185808.
    Pubmed KoreaMed CrossRef
  16. Wang L., Tsuda K., Sato M., Cohen J.D., Katagiri F., and Glazebrook J. (2009). Arabidopsis CaM binding protein CBP60g contributes to MAMP-induced SA accumulation and is involved in disease resistance against Pseudomonas syringae. PLoS Pathog. 5, e1000301.
    Pubmed KoreaMed CrossRef
  17. Wang L., Tsuda K., Truman W., Sato M., Nguyen L.V., Katagiri F., and Glazebrook J. (2011). CBP60g and SARD1 play partially redundant critical roles in salicylic acid signaling. Plant J. 67, 1029-1041.
    Pubmed CrossRef
  18. Won K.H. and Kim H. (2020). Functions of the plant Qbc SNARE SNAP25 in cytokinesis and biotic and abiotic stress responses. Mol. Cells 43, 313-322.
    Pubmed KoreaMed CrossRef
  19. Xu G., Yuan M., Ai C., Liu L., Zhuang E., Karapetyan S., Wang S., and Dong X. (2017). uORF-mediated translation allows engineered plant disease resistance without fitness costs. Nature 545, 491-494.
    Pubmed KoreaMed CrossRef
  20. Zhu Y., Qian W., and Hua J. (2010). Temperature modulates plant defense responses through NB-LRR proteins. PLoS Pathog. 6, e1000844.
    Pubmed KoreaMed CrossRef
Mol. Cells
Jan 31, 2023 Vol.46 No.1, pp. 1~67
COVER PICTURE
RNAs form diverse shapes and play multiple functions as central molecules of gene expression. In this special issue on RNA, seven minireviews illustrate how basic concepts and recent RNA biology findings are transformed into new and exciting RNA therapeutics.

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