Chloroplast redox state changes mark cell‐to‐cell signaling in the hypersensitive response

Abstract

Summary Hypersensitive response (HR)‐conferred resistance is associated with induction of programmed cell death and pathogen spread restriction in its proximity. The exact role of chloroplastic reactive oxygen species and its link with salicylic acid (SA) signaling in HR remain unexplained. To unravel this, we performed a detailed spatiotemporal analysis of chloroplast redox response in palisade mesophyll and upper epidermis to potato virus Y (PVY) infection in a resistant potato genotype and its transgenic counterpart with impaired SA accumulation and compromised resistance. Besides the cells close to the cell death zone, we detected individual cells with oxidized chloroplasts further from the cell death zone. These are rare in SA‐deficient plants, suggesting their role in signaling for resistance. We confirmed that chloroplast redox changes play important roles in signaling for resistance, as blocking chloroplast redox changes affected spatial responses at the transcriptional level. Through spatiotemporal study of stromule induction after PVY infection, we show that stromules are induced by cell death and also as a response to PVY multiplication at the front of infection. Overall induction of stromules is attenuated in SA‐deficient plants.

Calponin homology domain containing kinesin, KIS1, regulates chloroplast stromule formation and immunity

“…We demonstrated that stromules are induced during immunity and play a role in the transport of defense signals, such as H 2 O 2 or the defense protein NRIP1, potentiating immunity-induced cell death (22). Since then, accumulating evidence indicates that the stromules are an integral part of a plant immune system (14,15,(24)(25)(26)(27)(28). However, lacking genetic mutants with abolished stromule formation has severely hindered our ability to understand the direct role of stromules in immunity.…”

Effects of Poty-Potexvirus Synergism on Growth, Photosynthesis and Metabolite Status of Nicotiana benthamiana

“…A successful defense response via the production of these molecules leads to hypersensitive response (HR), a form of programmed cell death (PCD), and confinement of the pathogen to the necrotic lesion [ 74 , 75 , 76 ]. A recent study indicated that the increase in chloroplast redox state at the cell death zone is linked to PCD signaling in a SA independent manner whereas the signaling for HR-conferred resistance to the virus is SA-dependent [ 77 ]. In susceptible infection, confinement of the virus/viruses is not successful.…”

Early detection of late blight in potato by whole‐plant redox imaging

“…Increasing evidence points to the role of chloroplast in sensing and responding to pathogens. Specifically, many chloroplast‐localized effector proteins targeting chloroplast processes have been identified (de Torres Zabala et al., 2015; Gao et al., 2020; Kretschmer et al., 2020; Littlejohn et al., 2021; Lukan et al., 2023; Tang et al., 2020; Xu et al., 2019). For example, it has been demonstrated that the interaction between AVRvnt1, a host‐translocated RxLR type of effector protein, and chloroplast‐targeted glycerate 3‐kinase triggers a light‐dependent immune response to P. infestans infection (Gao et al., 2020).…”

“…Genetically encoded biosensors have also been introduced into crop plants, including potato (Chamusco et al., 2022; Hipsch et al., 2021; Huang et al., 2014; Rattanawong et al., 2021), and spatially resolved mapping of stress‐induced long‐term redox perturbations has recently been demonstrated by whole‐plant imaging of potato plants expressing roGFP2 in their chloroplasts (Hipsch et al., 2021). Additionally, in potato plants infected with the potato virus Y, chloroplast‐targeted roGFP2 has been used to demonstrate the role of chloroplast redox state in SA‐independent cell death signaling and SA‐dependent HR (Lukan et al., 2023).…”