Pathogen overcome physical and biochemical defense, neutralize inducible defense responses to obtain plant nutrient. Sugar forms the primary substrate providing energy and structural material for defense responses in plants. The expression of defense and tolerance traits requires changes both in primary and secondary metabolism (Schwachtje and Baldwin 2008). During photosynthesis plant harvest light energy to generate adenosine triphosphate (ATP) and reducing power in the form of nicotinamide adenine dinucleotide phosphate hydrogen (NADPH) that can be utilized in the production of assimilates for various biological function. In plants photosynthesis and key step in the synthesis of defense-related hormone occur in chloroplasts (Lu and Yao 2018).
The absorption of light by chlorophyll, much of which is located in the light harvesting complexes (LHCs) of photosystem II (PSII) and photosystem I (PSI) within the thylakoid membrane of chloroplast (Murchie and Niyogi 2011). Photosynthesis proceed through two phase, one a light phase that produces ATP and NADPH in the chloroplast thylakoid and is released in stroma and second the carbon di oxide reduction phase in presence of water in stroma and that consumes ATP and NADPH to produce triose phosphate through Calvin-Benson cycle (Selvaraj and Fofana 2012). Plant pathogens interfere with source-sink interaction (Biemelt and Sonnewald 2006). Pathogens are believed to reprogram a plant’s metabolism for their own benefit. The lower rate of photosynthesis is not only due to the cell death but also to an alteration in source-sink relation and carbon utilization. Plants infected with biotrophic fungal pathogens exhibit reduced photosynthetic rate and mobilizing nutrient towards infection site (Walters and McRoberts 2006).
Scharte et al. (2005) propose that in photoautotrophic leaves, photosynthesis and defense reaction were localized processes required for defense. Activation of cascade of defense reaction require energy. Thus a localized increase in sink strength by an elevated invertase activity can satisfy the increased demand for carbohydrates as an energy source for the tissues invaded by a pathogen. The increase in carbohydrates will generate a metabolic signal that induces the expression of defense-related genes and repression of photosynthesis in addition to the signal derived from the pathogen (Roitsch et al., 2003). The fungal elicitor induces a source/sink transition and activation of defense related genes.
Photosynthesis provides electron NADPH, ATP and carbon skeleton for biosynthesis of defense hormone and signals. Phytohormone abscisic acid (ABA), ethylene (ET), jasmonic acid (JA) and salicylic acid (SA), reactive oxygen species (ROS), nitric oxide (NO) and Ca2+ directly or indirectly participate in plant defense against pathogen. NO induces SA accumulation promoting NONEXPRESSOR OF PATHOGENESIS-RELATED GENES1 (NPR1) monomerization and translocation from the cytoplasm to the nucleus (Lu and Yao 2018). The rate of photosynthesis could increase to supply of carbon skeleton, energy and reducing equivalents required to support the plant defense (Bolton 2009). Chloroplast are the generator of ROS and nitric oxide and also a site for calcium signaling. The chloroplast generated ROS triggers hypersensitive response (Liu et al., 2007). ROS influences the production and signaling of phytohormone. ROS signaling is proposed to spread from plastids to the apoplast through activation of NADPH oxidases and from there to adjacent cell leading to cell death in the infected region (Zurbriggen et al., 2010).
Chloroplast have a role in plant immunity as a site for the production for SA and JA. The pathogen-associated molecular pattern (PAMP) signals are relayed to chloroplast to evoke Ca2+ in stroma. Nomura et al. (2012) demonstrated that a chloroplast-localized protein CAS (calcium-sensing receptor) is involved in stromal Ca2+ transient and responsible for both PAMP-induced basal resistance and R gene-mediated hypersensitive cell death. The study reveals chloroplast-mediated signaling pathway linking chloroplast to cytoplasmic-nuclear immune response.
Stromules (stroma-filled tubules) extend from the surface of all plastid types including proplastids, chloroplasts, etioplasts, leucoplasts, amyloplasts and chromoplasts. The primary function of stromules is to increase plastid surface area potentially increasing transport to and from the cytosol (Natesan et al., 2005). Chloroplast being the main production site of pro-defense molecules, communicate and coordinate with other organelles during defense. Chloroplast send out tubular extension called stromules, these stromules aid in amplification and transport of pro-defense signals into the nucleus and to other subcellular compartments during immunity (Caplan et al., 2015). Induction of stromules within the infection site suggest pro-defence signaling molecule may play a role in cell to cell signaling during stromulae formation (Serrano et al., 2016). The stromules develop abundant connections with nuclei during HR inducing effector triggered immunity (ETI) tightly tethering the chloroplast outer membrane and the nuclear envelope (Caplan et al., 2015). This association of chloroplast and nuclei correlate with increased nuclear accumulation to NRIP1 (N Receptor Interacting Protein1) that moves from chloroplast and accumulate in nuclei during immune signaling. After induction of the immune response followed by burst of hydrogen per oxide (H2O2) production in the chloroplast, H2O2 moves from the chloroplast to nucleus connection (Serrano et al., 2016; Caplan et al., 2015). The oxidative burst drives cross-linking of the cell wall, induces several plant genes involved in cellular protection and defense and initiates host cell death (Delledonne et al., 1998).
Fungal infection of leaf tissue causes a reduced rate of photosynthesis. A sugar deficit and energy may be observed at the infection site. The biotrophic fungi such as Albugo candida, Pucccinia coronata and Blumeria graminis causes decrease in the rate of photosynthesis (Chou et al., 2000; Scholes and Rolfe 1996; Swarbrick et al., 2006). Decreased photosynthetic rates possibly may be due to inhibition of protein synthesis which may anticipate the need to redirect resources to defensive function (Schwachtje and Baldwin 2008). Whereas, an increased photosynthetic rate may be due to increased demand for energy and carbon (C)-based resources that the production of defensive compounds require.
Reference:
Biemelt, S. and Sonnewald, U. 2006 Plant-Microbe Interactions to Probe Regulation of Plant Carbon Metabolism. Plant Physiol. 163(3): 307 – 318
doi.org/10.1016/j.jplph.2005.10.011
Bolton, M. D. 2009 Primary Metabolism and Plant Defense-Fuel for the Fire. MPMI 22(5): 487 – 497
doi.org/10.1094/MPMI-22-5-0487
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. Developmental Cell 34(1): 45 – 57
doi: 10.1016/j.devcel.2015.05.011
Chou, H. M., Bundock, N., Rolfe, S. A. and Scholes, J. D. 2000 Infection of Arabidopsis thaliana Leaves with Albugo candida (White Blister Rust) Causes a Reprogramming of Host Metabolism. Mol. Plant Pathol. 1(2): 99 – 113
doi.org/10.1046/j.1364-3703.2000.00013.x
Delledonne, M., Xia, Y., Dixon, R. A. and Lamb, C. 1998 Nitric Oxide Functions as a Signal in Plant Disease Resistance. Nature 394(6693): 585 – 588
doi.org/10.1038/29087
Liu, Y., Ren, D., Pike, S., Pallardy, S., Gassmann, W. and Zhang, S. 2007 Chloroplast-Generated Reactive Oxygen Species are Involved in Hypersensitive Response-like Cell Death Mediated by a Mitogen-activated Protein Kinase Cascade. Plant J. 51(6): 941 – 954
doi.org/10.1111/j.1365-313X.2007.03191.x.
Lu, Y. and Yao, J. 2018 Chloroplasts at the Crossroad of Photosynthesis, Pathogen Infection and Plant Defense. Int. J. Mol. Sci. 19(12): 3900
doi.org/10.3390/ijms19123900
Murchie, E. H. and Niyogi, K. K. 2011 Manipulation of Photoprotection to Improve Plant Photosynthesis. Plant Physiol. 155: 86 – 92
doi.org/10.1104/pp.110.168831
Natesan, S. K. A., 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.org/10.1093/jxb/eri088
Nomura, H., Komori, T., Uemura, S., Kanda, 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 Siganling in Arabidopsis. Nat. Commun. 3: 926
doi.org/10.1038/ncomms1926
Roitsch, T., Balibrea, M. E., Hofmann, M., Proels, R. and Sinha, A. K. 2003 Extracellular Invertase: Key Metabolic Enzyme and PR Protein. J. Exp. Bot. 54(382): 513 – 524
doi.org/10.1093/jxb/erg050
Scharte, J., Schon, H. and Weis, E. 2005 Photosynthesis and Carbohydrate Metabolism in Tobacco Leaves during an Incompatible Interaction with Phytophthora nicotianae. Plant Cell Environ. 28(11): 1421 – 1435
doi.org/10.1111/j.1365-3040.2005.01380.x
Scholes, J. D. and Rolfe, S. A. 1996 Photosynthesis in Localised Regions of Oat Leaves Infected with Crown Rust (Puccinia coronate): Quantitative Imaging of Chlorophyll Fluorescence. Planta 199(4): 573 – 582
doi.org/10.1007/BF00195189
Schwachtje, J. and Baldwin, I. T. 2008 Why Does Herbivore Attack Reconfigure Primary Metabolism? Plant Physiol. 146: 845 – 851
doi.org/10.1104/pp.107.112490
Selvaraj, K. and Fofana, B. 2012 An Overview of Plant Photosynthesis Modulation by Pathogen Attack. In “Advances in Photosynthesis-Fundamental Aspects” Najafpour, M. (ed.). Chapter 22: 465 – 486
doi: 10.5772/27124
Serrano, I., Audran, C. and Rivas, S. 2016 Chloroplasts at Work during Plant Innate Immunity. Journ. Exp. Bot. 67(13): 3845 – 3854
doi.org/10.1093/jxb/erw088
Swarbrick, P. J., Schulze-Lefert, P. and Scholes, J. D. 2006 Metabolic Consequences of Susceptibility and Resistance (Race-specific and broad spectrum) in Barley Leaves Challenged with Powdery Mildew. Plant Cell Environ. 29(6): 1061 – 1076
doi: 10.1111/j.1365-3040.2005.01472.x
Walters, D. R. and McRoberts, N. 2006 Plants and Biotrophs: A Pivotal Role for Cytokinins? Trends Plant Sci. 11(12): 581 – 586
doi: 10.1016/j.tplants.2006.10.003
Zurbriggen, M. D., Carrillo, N. and Hajirezaei, M-R. 2010 ROS Signaling in the Hypersensitive Response: When, Where and What For? Plant Signal Behav. 5(4): 393 – 396
doi.org/10.4161/psb.5.4.10793
BIOLOGICAL PROCESSES- A NATURE'S GIFT 