Chloroplast is the site for photosynthesis through which light energy is converted into chemical energy. Besides photosynthesis, chloroplast has a role in plant immunity through synthesis of secondary metabolites, amino acid and phytohormone such as jasmonic acid and salicylic acid (Trotta et al., 2014; Kretschmer et al., 2020). Chloroplasts play a key role in orchestrating cellular responses to stress, including pathogen infection. These autonomous organelles can regulate plant immune response by transmitting signals to the nucleus and other cell compartments through retrograde signaling pathways and they alter their stromule frequency in reaction to internal signal transduction pathway.  Upon pathogen infection, chloroplasts either congregate around the nucleus or send out dynamic tubular extensions called stromules to establish a physical contact with the nucleus (Caplan et al., 2015; Kumar et al., 2018; Ding et al., 2019). Stromules are stroma filled tubules extending from surface of all type of plastids such as proplastids, chloroplast, etioplasts, leucoplast, amyloplast and chromoplast (Natesan et al., 2005). Microtubules and actin filaments facilitates perinuclear clustering of chloroplast during an innate immune response (Kumar et al., 2018). Stromules aid in the amplification and/or transport of pro-defense signals into the nucleus and other subcellular compartments during immunity (Caplan et al., 2015).  A decline in photosynthesis is often accompanied by plant immunity. Stromules facilitates the direct transfer of chloroplast sourced hydrogen per oxide (H2O2) to the nucleus. Stromule formation increases with enhanced ROS generation in chloroplasts and its frequency is regulated in response to the chloroplast redox status (Brunkard et al., 2015;  de Torres Zabala et al., 2015). Photosynthetic activity provides NADPH, ATP and carbon skeleton which fuels the initiation of responses against the external stress. The Arabidopsis thaliana chloroplast protein ACCELERATED CELL DEATH2 (ACD2) modulated programmed cell death   (Yao and Greenberg 2006).

Hydrogen per oxide is produced via superoxide and superoxide dismutase, by electron transport in chloroplast and mitochondria, plasma membrane NADPH oxidases, peroxisomal oxidases, type III peroxidases and other apoplastic oxidases (Smirnoff and Arnaud 2018). Aquaporin facilitate H2O2 into guard cell, suggesting a signaling role of aquaporin in context involving H2O2 (Rodrigues et al., 2017).  In plasma membrane NADPH oxidases (NOX) transfer electrons from NADPH to oxygen, leading to the generation of superoxide and hydrogen peroxide in the apoplast (Sagi and Fluhr 2006). In plant NOX homologs have been named respiratory burst oxidase homologs (Rboh) and are also involved in production of ROS in response to pathogens (Sagi and Fluhr 2001; Torres et al., 2002).

Chloroplast metabolism results in the production of reactive oxygen species and nitric oxide as defense molecules (Kretschmer et al., 2020). Changes in chloroplast redox signaling pathway and reactive oxygen species metabolism mediates local and systemic signal modulating plant resistance to disease and light stress (Trotta et al., 2014). The major source of ROS is plasma membrane localized NADPH/NADPH oxidases that generate superoxide or cell wall localized peroxidases that generate H2O2 or both system operating in tandem (Bolwell 1999; Daudi et al., 2012). The ROS H2O2 during hypersensitive response-programmed cell death (HR-PCD) can also originate from plasma membrane localized Rboh of NADPH oxidase (Zhou et al., 2019; Torres et al., 2006).

Chloroplast is a central component in plant immunity. On recognition of pathogen- or microbe-associated molecular patterns (PAMPs/ MAMPs) by the plasma membrane receptor kinases leading to activation of mitogen-activated protein kinase (MAPK), followed by changes in cytoplasmic calcium concentration, activating calcium-dependent protein kinase (CDPK) cascades leading to rapid NADPH oxidase-driven burst of reactive oxygen species in apoplast. Thus together these processes provide protection to plant against plant pathogens (Boudsocq et al., 2010; Trotta et al., 2014). CDPK and MAPK cascades act differentially in four MAMP-mediated regulatory program to control early genes involved in synthesis of defense peptides and metabolites, cell wall modification and redox signaling (Boudsocq et al., 2010).

Calcium-sensing receptor (CAS) is a calcium-binding protein located on the thylakoid membrane in the chloroplast. Recognition of PAMPs by pattern recognition receptor leads to PAMP- triggered immunity (PTI) (induces basal defense); while recognition by resistance (R) gene leads to effector- triggered immunity (ETI) (induces hypersensitive response leading to cell death).  Once the PTI or ETI signal is relayed to the chloroplast, Ca2+ from thylakoid lumen, containing high concentration of Ca2+ are transported to the stroma by CAS and the signal is then transduced from the chloroplast to the nucleus through the singlet oxygen (1O2)-mediated retrograde signaling pathway (Nomura et al., 2012; Kim and Apel2013) regulating the defense response through transcriptional reprogramming of defense related genes (Nomura et al., 2012; Yang et al., 2021).


Bolwell, G. P. 1999 Role of Active Oxygen Species and NO in Plant Defence Responses. Curr. Opin. Plant Biol. 2(4): 287 – 294

Boudsocq, M., Willmann, M. R., McCormack, M., Lee, H., Shan, L., He, P., Bush, J., Cheng, S-H. and Sheen, J. 2010 Differential Innate Immune Signaling via Ca 2+ Sensor Protein Kinases. Nature 464(7287): 418 – 422

doi: 10.1038/nature08794

Brunkard, J. O., Runkel, A. M. and Zambryski, P. 2015 Chloroplasts Extends Stromules Independently and in Response to Internal Redox Signals. PNAS 112(32): 10044 – 10049

Caplan, J. L., Kumar, A. S., Park, E., Padmanabhan, M. S., Hoban, K., Modla, S., Czymmek, K. and Dinesh-Kumar, S. P. 2015  Chloroplast Stromules Function during Innate Immunity      Dev. Cell 34(1): 45 – 57

doi: 10.1016/j.devcel.2015.05.011

Daudi, A., Cheng, Z., O’Brien, J. A., Mamarella, N., Khan, S., Ausubel, F. M. and Bolwell, G. P. 2012 The apoplastic Oxidative Burst Peroxidase in Arabidopsis is .a Major Component of Pattern-Triggered Immunity. Plant Cell 24(1): 275 – 287

de Torres Zabala, M., Littlejohn, G., Jayaraman, S., Studholme, D., Bailey, T., Lawson, T., Tillich, M., Licht, D., Bolter, B., Delfino, L., Truman, W., Mansfield, J., Smirnoff, N. and Grant, M. 2015 Chloroplast Play a Central Role in Plant Defense and are Targeted by Pathogen Effectors. Nat. Plants 1: 15074

doi: 10.1038/nplants.2015.74

Ding, X., Jimenez-Gongora, T., Krenz, B. and Lozano-Duran, R. 2019 Chloroplast Clustering around the Nucleus is a Feneral Response to Pathogen Perception in Nicotiana benthamiana Mol. Plant Pathol. 20(9):1298 – 1306

doi: 10.1111/mpp.12840

Kim, C. and Apel, K. 2013 1O2-mediated and EXECUTER-Dependent Retrograde Plastid-to-Nucleus Signaling in Norflurazon-Treated Seedlings of Arabidopsis thaliana. Mol. Plant 6(5): 1580- 1591

doi: 10.1093/mp/sst020

Kretschmer, M., Damoo, D., Djamei, A. and Kronstad, J. 2020 Chloroplasts and Plant Immunity: Where are the Fungal Effectors?   Pathogens 9(1): 19

doi: 10.3390/pathogens9010019

Kumar, A. S., Park, E., Nedo, A., Alqarni, A., Ren, L., Hoban, K., Modla, S., McDonald, J. H., Kambhamettu, C., Dinesh-Kumar, S. P. and  Caplan, J. L. 2018 Stromule Extension along Microtubules Coordinated with Actin-Mediated Anchoring Guides Perinuclear Chloroplast Movement during Innate Immunity. Elife. 7:e23625

doi: 10.7554/eLife.23625

Natesan, S. K., Sullivan, J. A. and Gray, J. C. 2005 Stromules: A Characteristic Cell-Specific Feature of Plastid Morphology. J. Exp. Bot. 56(413): 787 – 797

doi: 10.1093/jxb/eri088

Nomura, H., Komori, T., Uemura, S. Kanada, Y., Shimotani, K., Nakai, K., Furuichi, T., Takebayashi, K., Sugimoto, T., Sano, S., Suwastika, I. N., Fukusaki, E., Yoshioka, H., Nakahira, Y. and Shiina, T. 2012 Chloroplast Mediated Activation of Plant Immune Signaling in Arabidopsis. Nat. Commun. 3: 926

doi: 10.1038/ncomms1926

Rodrigues, O., Reshetnyak, G., Grondin, A. and Verdouca, L. 2017 Aquaporins Facilitate Hydrogen Peroxide Entry into Guard Cells to Mediate ABA- and Pathogen-Triggered Stomatal Closure. PNAS USA 114(34): 9200 – 9205

Sagi, M. and Fluhr, R. 2006. Production of Reactive Oxygen Species by Plant NADPH Oxidases. Plant Physiol. 141(2): 336 – 340

doi: 10.1104/pp.106.078089

Sagi, M. and Fluhr, R. 2001 Superoxide Production by Plant Homologues of the gp91phox NADPH Oxidase. Modulation of Activity by Calcium and by Tobacco Mosaic Virus Infection. Plant Physiol. 126(3): 1281 – 1290

doi: 10.1104/pp.126.3.1281

Smirnoff, N. and Arnaud, D. 2018 Hydrogen Peroxide Metabolism and Functions in Plants. New Phytologist 221(3): 1197 – 1214

Torres. M. A., Jones, J. D. and   Dangl, J. L. 2006 Reactive Oxygen Species Signaling in Response to Pathogen. Plant Physiol. 141(2): 373 – 378

Torres, M. A., Dangl, J. L., Jones, J. D. 2002 Arabidopsis gp91phox homologues Atrboh D and Artboh F are required for Accumulation of Reactive Oxygen Intermediates in Plant Defense Response. Proc. Natl. Acad. Sci. USA 99(1): 517 – 522

doi: 10.1073/pnas.012452499

Trotta, A., Rahikainen, M., Konert, G., Finazzi, G. and Kangasjarvi, S. 2014 Signaling Crosstalk in Light Stress and Immune Reactions in Plants.  Philos. Trans. R. Soc. Lond. B. Biol. Sci. 369(1640): 20130235

doi: 10.1098/rstb.2013.0235

Yang, F., Xiao, K., Pan, H. and Liu, J. 2021 Chloroplast: The Emerging Battlefield in Plant-Microbe Interaction. Front. Plant Sci.

Yao, N. and Greenberg, J. T. 2006 Arabidopsis ACCELERATED CELL DEATH2 Modulates Programmed Cell Death. Plant Cell 18(2): 397 – 411

doi: 10.1105/tpc.105.036251

Zhou, Z., Zhao, Y., Bi, G., Liang, X. and Zhou, J-M. 2019 Early Signaling Mechanisms Underlying Receptor Kinase-Mediated Immunity in Plants. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 374(1767): 20180310

doi: 10.1098/rstb.2018.0310

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