Plant Immunity
Plant immunity research has potential benefits in agriculture by reducing losses and increasing food security, as well as mitigating environmental impacts. Insights into host-pathogen interactions can also be relevant to human and animal health. Understanding plant immunity can lead to strategies to improve plant productivity and the yield of various compounds.
Plant immunity is a complex system that involves various molecular mechanisms to detect and respond to pathogens. Plants have evolved two major types of immune systems: Pattern-Triggered Immunity (PTI) and Effector-Triggered Immunity (ETI).
PTI is the first line of defense against pathogens, where plant cells detect common pathogen-associated molecular patterns (PAMPs) using Pattern Recognition Receptors (PRRs) on the cell surface. The binding of PAMPs to PRRs initiates a cascade of molecular events, leading to the activation of defense responses such as the production of reactive oxygen species (ROS), callose deposition, and expression of defense-related genes. However, some pathogens can overcome PTI by secreting effector molecules that manipulate plant cellular processes to promote their growth and colonization. In response, plants have evolved intracellular receptors called Nucleotide-binding leucine-rich repeat receptors (NLRs) to recognize and respond to pathogen effectors. Upon effector recognition, NLRs undergo oligomerization to form a complex called the resistosome, which activates defense responses including programmed cell death (PCD) to restrict pathogen growth. The molecular events leading to NLR activation are complex and involve various signaling pathways. One such pathway is mediated by Calcium (Ca2+), which plays a critical role in activating plant immune responses. Upon effector recognition, NLRs trigger a Ca2+ influx, which leads to the activation of various kinases and downstream transcription factors that activate the expression of defense-related genes. In addition to these pathways, recent studies have shown that translational regulation plays a crucial role in plant immune responses. Upon pathogen recognition, plants undergo dramatic transcriptional and translational reprogramming to produce defense-related proteins. The assembly of the eIF2 initiation complex is enhanced during ETI induction, leading to an increase in global translational activity required for NLR-mediated defense.
In summary, plant immunity is a complex molecular process involving various signaling pathways, receptors, and transcriptional and translational regulation. Understanding these mechanisms is essential for developing strategies to enhance plant resistance against pathogens and improve crop yields.
Below are a series of three papers which discuss the use of various translatomics tool in determining the role translation plays in plant immunity. Chen et al. (2023a) used polysome profiling to examine the global translational activity in response to pathogen challenge. Chen et al. (2023b) examine redox regulation of cytosolic translation using TMT-based quantitative proteomics to identify changes in protein oxidation, and ribosome profiling to measure translational efficiency.
Global translational induction during NLR-mediated immunity in plants is dynamically regulated by CDC123, an ATP-sensitive protein.
Cell Host & Microbe, 2023
Chen, T., Xu, G., Mou, R., Greene, G.H., Liu, L. et al.
Plants have evolved receptors called nucleotide-binding leucine-rich repeats (NLRs) that can recognise pathogen effectors and initiate an immune response called effector-triggered immunity (ETI). When activated, NLRs undergo oligomerisation to form a resistosome that triggers programmed cell death (PCD) to restrict pathogen proliferation. This immune response involves dramatic transcriptional and translational reprogramming, which is not passively driven by transcript abundance.
It is unclear whether translation regulation during ETI in plants is through the well-studied integrated stress response pathway, involving eIF2a phosphorylation. While this pathway is known to inhibit recycling of the eIF2 complex and slow ribosome assembly, it’s unknown if it plays a role in ETI, as it hasn’t been genetically tested in the GCN2 knockout mutant, the only known kinase to phosphorylate eIF2a.
In this particular study, In this study, the authors introduced a translational reporter 35S:5′LSTBF1-FLUC into both wild-type (WT) Arabidopsis and the rps2 mutant defective in the coiled-coil (CC)-NLR receptor (CNL), Resistance to P. syringae 2 (RPS2), for the bacterial effector AvrRpt2. They used polysome profiling to examine the global translational activity in response to pathogen challenge. The authors also performed a surface sensing of translation (SUnSET) assay to evaluate the rate of protein synthesis during ETI. The authors examined the translational changes during ETI mediated by other NLRs, such as RPM1 and RPS4.
Key Findings
ETI induction involves a major increase in protein synthesis
- There is a switch in translation from uORF to mORF in response to pathogen challenge, and enhanced global translational activity during ETI, mediated by various NLRs (e.g. (RPM1) and RPS4).
CDC123 positively regulates ETI-mediated translation and resistance
- The authors identified CDC123, an ATP-grasp protein, as a key regulator of ETI-associated translational increase, using the mutant dst7, which has a recessive mutation in the CDC123 gene.
eIF2ƴ, a CDC123 interactor, is involved in ETI
- CDC123 interacts with translation initiation factors, particularly eIF2ƴ, and facilitates eIF2 assembly, which confers ETI-induced translational activity and resistance.
ETI-elevated ATP concentration enhances the assembly of the eIF2 complex through CDC123
- The assembly of the eIF2 complex is increased by CDC123 during ETI, and this is dependent on the increase in ATP concentration during ETI.
Implications
This paper shows that CDC123 plays a crucial role in the regulation of protein synthesis during effector-triggered immunity (ETI) in plants. This provides new insights into the molecular mechanisms underlying plant immune responses and highlights the importance of translational regulation in mounting effective immune responses.
Comparative oxidation proteomics analyses suggest redox regulation of cytosolic translation in rice leaves upon Magnaporthe oryzae infection.
Plant Communications, 2023
Chen, X., Xu, Q., Yue, Y., Duan, Y., Liu, H., Chen, X., Huang, J. and Zheng, L.,
Pathogens can trigger an increase in reactive oxygen species (ROS) levels in plants, which are essential for activating the plant’s defense mechanisms. To gain insights into this defense mechanism, researchers used iodo-tandem mass tag (TMT)-based quantitative proteomics and ribosome profiling (Ribo-seq) to investigate the role of redox regulation in cytosolic translation during an infection by the fungus Magnaporthe oryzae, which causes rice blast disease.
(TMT)-based quantitative proteomics – a technique that labels peptides from multiple samples with a unique isobaric tag, and uses liquid chromatography and tandem mass spectrometry – allowed them to identify changes in protein oxidation, while ribosome profiling was used to measure translational efficiency. This comprehensive approach allowed the researchers to study how the plant’s defense mechanisms respond to pathogen infection at both the protein synthesis and regulation levels.
Key Findings
Identification of oxidation sites and proteins in rice leaves
- Using the TMT-based approach, the study identified 4292 unique cysteine-containing peptides in 2808 proteins and quantified 3362 sites from 2275 proteins in at least two of three biological replicates, with AUXIN TRANSPORT PROTEIN was identified as the most oxidised.
Functional annotation of oxidized proteins
- Pathway enrichment analysis showed that protein oxidation might have important regulatory roles in gene expression, translation, stress-response, metabolism, and more under normal conditions.
M. oryzae infection leads to hyperoxidation of proteins
- Increased ROS caused the hyperoxidation of proteins. Of the 438 proteins that showed increased oxidation levels, most were localized to the chloroplasts and cytoplasm.
M. oryzae infection leads to increased oxidation of ribosomal proteins
- The authors confirmed that M. oryzae infection leads to increased oxidation levels in RPL38 and other ribosomal proteins.
M. oryzae infection promotes cytosolic ribosome translation
- Oxidation of ribosomal proteins may promote cytosolic translation by increasing mRNA levels of highly expressed genes that contain CCT-rich sequences in their 5′ untranslated regions.
Implications
This paper reveals how redox regulation of cytosolic translation affects plant immunity against fungal pathogens, during both PTI and ETI. The findings offer new insights into the role of redox regulation in stress response and have potential implications for enhancing crop resistance. The study also identifies important oxidation-sensitive proteins that can inform future research on protein redox regulation.
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