The important role of chloroplasts in plant immunity

Abstract

In nature, plants are under attack by a range of pathogens. To cope with these pathogens, plants have evolved a sophisticated immune system, including pattern-triggered immunity (PTI) initiated by pattern recognition receptors on the cell surface and effector-triggered immunity (ETI) activated by intracellular nucleotide-binding and leucine-rich repeat receptors. In recent years, increasing evidence has demonstrated that organelles such as the chloroplast play crucial roles in complete activation of plant immunity. In this review, we focus on the chloroplast and summarize its role in regulating the activation of immune events, including influx of calcium (Ca²⁺), accumulation of reactive oxygen species (ROS), biosynthesis of phytohormones, and expression of defense-related genes. Because information exchange between the chloroplast and the nucleus is very important during plant immunity, we also highlight the importance of chloroplast-nucleus communication via stromules in plant immunity. This review reveals the function of the chloroplast in maintaining the trade-off between plant growth and immunity, and expands our understanding of how chloroplasts enable complete activation of plant immunity.

Keywords: Ca(2+); ROS; chloroplast; plant immunity; retrograde signals; stromule.

Figure 1

Cytoplasmic Ca²⁺ influxes in plant cells. As a second messenger, intracellular Ca²⁺ plays a crucial role in communication among various cellular organelles. Ca²⁺ and Ca²⁺ sensors across multiple organelles, together with downstream reactors, form the Ca²⁺ signaling pathway to enhance plant immunity. Ca²⁺ channels are activated after the perception of pathogen-associated molecular patterns (PAMPs) or effectors, leading to an influx of cytoplasmic Ca²⁺. Ca²⁺ channels in the chloroplast membrane also contribute to the increase in cytoplasmic Ca²⁺ levels, although the specific component involved remains unclear. Cytoplasmic Ca²⁺ is sensed by Ca²⁺ decoders such as calmodulins (CAMs), calmodulin-like proteins (CMLs), and calcium-dependent protein kinases (CDPKs), and downstream immune responses are subsequently activated. Changes in chloroplastic Ca²⁺ concentrations are also triggered by PAMPs and are subsequently sensed by chloroplastic Ca²⁺ sensors such as Ca²⁺-SENSING RECEPTOR (CAS), which regulate plant immunity in conjunction with other Ca²⁺ decoders that translocate from the PM or cytoplasm to the chloroplasts. MPKs, mitogen-activated protein kinases; PRR, pattern recognition receptor; ROS, reactive oxygen species; SA, salicylic acid; TFs, transcription factors.

Figure 2

ROS signaling in chloroplasts. Photosystems I (PS I) and II on the thylakoid membrane are activated in the light and perform photoreactions and electron transfer. Large amounts of ROS, such as singlet oxygen (¹O₂), superoxide anion radicals (O₂^·−), and hydroxyl radicals (·OH), are produced, resulting in changes in chloroplast redox state and the occurrence of cell death. Enzymes can convert high-energy ROS into lower-energy types such as hydrogen peroxide (H₂O₂), which still causes damage to cells. Excess excitation energy can be converted into heat through nonphotochemical quenching (NPQ) and dissipated. ROS can also be eliminated by ROS-scavenging systems, which are composed of enzymes such as superoxide dismutase (SOD), catalase (CAT), and ascorbate peroxidase (APX), together with the nonenzymatic ascorbate–glutathione system. Pathogens impair the function of proteins involved in these processes, disrupt the redox state, and reduce the level of chloroplastic ROS (cROS) to promote pathogenesis. During pathogen invasion, stromules, special tubular protrusions of the chloroplast, are induced by PAMPs, H₂O₂, and SA in a cytoskeleton-dependent manner. Signal molecules are delivered to the nucleus via stromules to activate immune responses. Although the specific signaling molecules involved remain to be determined, proteins such as N RECEPTOR INTERACTING PROTEIN 1 (NRIP1) and WHIRLY1 (WHY1) and metabolites such as methylerythritol cyclodiphosphate (MEcPP), β-cyclocitral, H₂O₂, and phosphonucleotide 3′-phosphoadenosine 5′-phosphate (PAP) are possible candidates. DCMU, 3-(3,4-dichlorophenyl)-1,1-dimethylurea; EEE, excess excitation energy; KIS1, KINESIN REQUIRED FOR INDUCING STROMULES 1; LHC II, light-harvesting complex II; PC, plastocyanin; PQ, plastoquinone.

Figure 3

Strategies used by pathogens to inhibit chloroplast function. To inhibit the function of chloroplasts, viral proteins and pathogen effectors are released to hijack chloroplast-localized proteins. The strategies used by pathogens include preventing chloroplast proteins in the cytoplasm from targeting chloroplasts (Pst_4/5 and Pi22926), reducing callose deposition, reducing SA concentrations (AvrPto, C4, and ITL), reducing cROS levels (HC-pro, Svp2, Pst_12806, Pi22922, and RXLR31154), and translocating host proteins (MP and p50). CAS, Ca²⁺-SENSING RECEPTOR; CPCK2, CASEIN KINASE 2; FC II, FERROCHELATASE 2; FD, FERREDOXIN; ISP, IRON-SULFUR PROTEIN; MP, movement protein; NRIP1, N RECEPTOR INTERACTING PROTEIN 1; PsbP, photosystem II subunit P; SABP3, SA BINDING PROTEIN 3.