Chloroplast: The Emerging Battlefield in Plant-Microbe Interactions

Abstract

Higher plants and some algae convert the absorbed light into chemical energy through one of the most important organelles, chloroplast, for photosynthesis and store it in the form of organic compounds to supply their life activities. However, more and more studies have shown that the role of chloroplasts is more than a factory for photosynthesis. In the process of light conversion to chemical energy, any damage to the components of chloroplast may affect the photosynthesis efficiency and promote the production of by-products, reactive oxygen species, that are mainly produced in the chloroplasts. Substantial evidence show that chloroplasts are also involved in the battle of plants and microbes. Chloroplasts are important in integrating a variety of external environmental stimuli and regulate plant immune responses by transmitting signals to the nucleus and other cell compartments through retrograde signaling pathways. Besides, chloroplasts can also regulate the biosynthesis and signal transduction of phytohormones, including salicylic acid and jasmonic acid, to affect the interaction between the plants and microbes. Since chloroplasts play such an important role in plant immunity, correspondingly, chloroplasts have become the target of pathogens. Different microbial pathogens target the chloroplast and affect its functions to promote their colonization in the host plants.

Keywords: CAS; chloroplast immunity; effectors; light-harvesting complex; phytohormone; retrograde signaling pathway.

FIGURE 1

Microbes interfere with chloroplast functions. (a) Activated nucleotide-binding leucine-rich repeat domain-containing receptors (NLRs) activate MPK3 and MPK6 through unknown mechanisms, regulating the immune responses by increasing the expression of immune-related genes. (b) Once pathogen-associated molecular pattern (PAMP)-triggered immune signals are transported to the chloroplast, Ca²⁺ flows out from the thylakoid lumen to the stroma through the calcium-sensing (CAS) receptor, transmitting the signals to the nucleus via the retrograde signaling pathway, eliciting immune response. SsITL interacts with CAS to inhibit salicylic acid (SA) accumulation and promotes infection. (c) Phosphorylated LHCB5 exists as a dimer or trimer instead of a monomer, which weakens the interaction with PsbS and then weakens non-photochemical quenching (NPQ), promoting the production of reactive oxygen species (ROS). S. sclerotiorum secretes oxalate during infection to acidify the host tissue and accelerates the synthesis of zeaxanthin from violaxanthin, which reduced the production of ROS and ABA. (d) The CP protein of the virus interacts with PsbS as dimers in the cytoplasm to sequestrate PsbS from functioning. (e) Proteins enter the chloroplast by interacting with the translocator located in the inner membrane (TIC)/outer membrane (TOC) on the chloroplast membrane via chloroplast transit peptide (cTP). Moreover, the cTP of cpHsp70 protein is age selective and the Bamboo mosaic virus (BaMV) virus interacts with it to preferentially enter the mature chloroplasts for more energy. (f) Pst_12806 interacts with TaISP protein in chloroplasts to reduce ROS production and thus inhibit host cells death. (g) During the infection of P. infestans, CHUP1 anchors chloroplasts to the host–pathogen interface and restricts the entry of pathogen. Meanwhile, P. infestans secretes effector AVR3a to inhibit the formation of chloroplast stromules to reduce the contact area. (h) The production of ROS in chloroplast increases under light conditions.