Pathogen manipulation of chloroplast function triggers a light-dependent immune recognition

Abstract

In plants and animals, nucleotide-binding leucine-rich repeat (NLR) proteins are intracellular immune sensors that recognize and eliminate a wide range of invading pathogens. NLR-mediated immunity is known to be modulated by environmental factors. However, how pathogen recognition by NLRs is influenced by environmental factors such as light remains unclear. Here, we show that the agronomically important NLR Rpi-vnt1.1 requires light to confer disease resistance against races of the Irish potato famine pathogen Phytophthora infestans that secrete the effector protein AVRvnt1. The activation of Rpi-vnt1.1 requires a nuclear-encoded chloroplast protein, glycerate 3-kinase (GLYK), implicated in energy production. The pathogen effector AVRvnt1 binds the full-length chloroplast-targeted GLYK isoform leading to activation of Rpi-vnt1.1. In the dark, Rpi-vnt1.1–mediated resistance is compromised because plants produce a shorter GLYK—lacking the intact chloroplast transit peptide—that is not bound by AVRvnt1. The transition between full-length and shorter plant GLYK transcripts is controlled by a light-dependent alternative promoter selection mechanism. In plants that lack Rpi-vnt1.1, the presence of AVRvnt1 reduces GLYK accumulation in chloroplasts counteracting GLYK contribution to basal immunity. Our findings revealed that pathogen manipulation of chloroplast functions has resulted in a light-dependent immune response.

Chloroplast immunity illuminated

“…Light is required for expression of full-length tomato and potato glycerate 3kinase (GLYK) transcripts encoding a chloroplast transit sequence. AVRvnt1 binds to this chloroplast-targeting sequence and activates resistance (independent of GLYK kinase activity), impairing accumulation of GLYK in both total and chloroplast fractions of potato (Gao et al, 2020). This is somewhat analogous to the TMV N-NRIP1 interaction described above (Caplan et al, 2008), but in this case AVRvnt1 intercepts GLYK's trafficking to the chloroplast, the depletion of which (probably via proteasomal degradation) is indirectly sensed by Rpi-vnt1.1 activating ETI (Fig.…”

“…Chloroplast lipids and cROS appear to be central to generation of SAR inducing signal(s) following ETI‐activated HR (Wendehenne et al ., 2014; Shine et al ., 2019), supported by the SAR‐deficient phenotypes of fatty acid desaturase ( sfd2 ; SUPPRESSOR OF FATTY ACID DESATURASE DEFICIENCY2) mutants. The chloroplast galactolipid mutants mgd1 and dgd1 ( monogalactosyl synthase 1 , digalactosyl synthase 1 ), responsible for monogalactosyldiacylglycerol (MGDG) and digalactosyldiacylglycerol (DGDG) synthesis respectively, function nonredundantly in initial SAR signal perception (Gao et al ., 2014; Shah et al ., 2014). As noted above, ETI‐generated ROS modify fatty acids on chloroplast galactolipids leading to rapid JA accumulation (Andersson et al ., 2006; Zoeller et al ., 2012).…”

The Histological, Effectoromic, and Transcriptomic Analyses of Solanum pinnatisectum Reveal an Upregulation of Multiple NBS-LRR Genes Suppressing Phytophthora infestans Infection

“…Moreover, co-expression of Avrvnt1 and Rpi-vnt1 or single Avrvnt1 failed to induce HR in S. pinnatisectum, suggesting that specific interacting proteins are needed for Avrvnt1-Rpi-vnt1 recognition. As Gao C et al pointed out [31], glycerate 3-kinase (GLYK) is involved in activation of of Rpi-vnt1. Similarly, Avrblb1 and Rpi-blb1 only triggered typical HR in N. benthamiana but not in Arabidopsis thaliana, indicating that species-specific interactors are involved in cell death induction [32].…”

Weighted Gene Co-Expression Network Coupled with a Critical-Time-Point Analysis during Pathogenesis for Predicting the Molecular Mechanism Underlying Blast Resistance in Rice

“…Previously, it has been reported that both pathogen-associated molecular pattern (PAMP) -triggered immunity (PTI) and effector-triggered immunity (ETI) contribute to the resistance response to rice blast (Boller and Felix 2009 ), and NLR -mediated immunity is known to be modulated by many environmental factors such as light (Gao et al 2020 ). In the present study, nine SEP between Piz-t-KJ201 and NPB-KJ201 were found, especially green-yellow module, in which the photosystem plays a vital role.…”