Chloroplasts at the Crossroad of Photosynthesis, Pathogen Infection and Plant Defense

Abstract

Photosynthesis, pathogen infection, and plant defense are three important biological processes that have been investigated separately for decades. Photosynthesis generates ATP, NADPH, and carbohydrates. These resources are utilized for the synthesis of many important compounds, such as primary metabolites, defense-related hormones abscisic acid, ethylene, jasmonic acid, and salicylic acid, and antimicrobial compounds. In plants and algae, photosynthesis and key steps in the synthesis of defense-related hormones occur in chloroplasts. In addition, chloroplasts are major generators of reactive oxygen species and nitric oxide, and a site for calcium signaling. These signaling molecules are essential to plant defense as well. All plants grown naturally are attacked by pathogens. Bacterial pathogens enter host tissues through natural openings or wounds. Upon invasion, bacterial pathogens utilize a combination of different virulence factors to suppress host defense and promote pathogenicity. On the other hand, plants have developed elaborate defense mechanisms to protect themselves from pathogen infections. This review summarizes recent discoveries on defensive roles of signaling molecules made by plants (primarily in their chloroplasts), counteracting roles of chloroplast-targeted effectors and phytotoxins elicited by bacterial pathogens, and how all these molecules crosstalk and regulate photosynthesis, pathogen infection, and plant defense, using chloroplasts as a major battlefield.

Chloroplasts and Plant Immunity: Where Are the Fungal Effectors?

“…Plastids, and more specifically chloroplasts, also make important contributions to plant defense against pathogens, including participation in the pathogen-associated molecular pattern (PAMP), triggered immunity (PTI) and effector-triggered immunity (ETI) [2][3][4][5][6][7][8]. As a basal layer of plant defense, PTI is usually triggered by conserved PAMPs on pathogens (e.g., bacterial flagellin and fungal chitin) or by damage-associated molecular patterns (DAMPs, such as oligogalacturonides or cellobiose) that may originate from the plant cell wall [2,4,5]. ETI is a second layer of plant immunity that requires the recognition of effectors by resistance (R) proteins leading to a hypersensitive response (HR) [2,4,5].…”

“…As a basal layer of plant defense, PTI is usually triggered by conserved PAMPs on pathogens (e.g., bacterial flagellin and fungal chitin) or by damage-associated molecular patterns (DAMPs, such as oligogalacturonides or cellobiose) that may originate from the plant cell wall [2,4,5]. ETI is a second layer of plant immunity that requires the recognition of effectors by resistance (R) proteins leading to a hypersensitive response (HR) [2,4,5]. Key reactions during defense include the synthesis of secondary metabolites and phytoalexins, the formation of reactive oxygen species (ROS) and nitric oxide (NO), calcium oscillations, stomatal closure, apoplastic alkalization, cell wall strengthening and the expression of plant defense proteins including pathogenesis-related proteins (PRs) [4,5,9,10].…”

“…ETI is a second layer of plant immunity that requires the recognition of effectors by resistance (R) proteins leading to a hypersensitive response (HR) [2,4,5]. Key reactions during defense include the synthesis of secondary metabolites and phytoalexins, the formation of reactive oxygen species (ROS) and nitric oxide (NO), calcium oscillations, stomatal closure, apoplastic alkalization, cell wall strengthening and the expression of plant defense proteins including pathogenesis-related proteins (PRs) [4,5,9,10]. Chloroplasts are the sites of production of ROS, calcium oscillations, and the synthesis of plant defense molecules, including jasmonic acid (JA) and salicylic acid (SA), that are critical components of the plant defense strategy against necrotrophic (JA) and biotrophic pathogens (SA).…”

“…In this review, we first briefly summarize the contributions of the chloroplast to immunity to set the stage for understanding potential targets of pathogen attack on the plastid. Our focus here is primarily on fungal pathogens, and readers are directed to several excellent recent reviews on the role of the chloroplast in interactions with viral and bacterial pathogens [4,5,11]. We initially discuss recent examples of chloroplast functions that are impacted by interactions with fungi and specifically consider chloroplast contributions to defense against fungi.…”

Plastid gene expression is required for singlet oxygen-induced chloroplast degradation and cell death

“…Photosynthesis itself involves highly reactive chemistry that leads to the formation of reactive oxygen species (ROS) such as singlet oxygen ( 1 O2) at photosystem II (PSII) and superoxide and hydrogen peroxide (H2O2) at photosystem I (PSI) (Asada 2006). Although a certain amount of ROS can be produced even under ideal conditions, many common environmental stresses (e.g., excess light (Triantaphylides et al 2008), drought (Chan et al 2016), salinity (Suo et al 2017), and pathogen attack (Lu and Yao 2018)) can drastically increase ROS production in the chloroplast.…”