Chloroplast Activity and 3′phosphadenosine 5′phosphate Signaling Regulate Programmed Cell Death in Arabidopsis

Abstract

Programmed cell death (PCD) is a crucial process both for plant development and responses to biotic and abiotic stress. There is accumulating evidence that chloroplasts may play a central role during plant PCD as for mitochondria in animal cells, but it is still unclear whether they participate in PCD onset, execution, or both. To tackle this question, we have analyzed the contribution of chloroplast function to the cell death phenotype of the myoinositol phosphate synthase1 (mips1) mutant that forms spontaneous lesions in a light-dependent manner. We show that photosynthetically active chloroplasts are required for PCD to occur in mips1, but this process is independent of the redox state of the chloroplast. Systematic genetic analyses with retrograde signaling mutants reveal that 39-phosphoadenosine 59-phosphate, a chloroplast retrograde signal that modulates nuclear gene expression in response to stress, can inhibit cell death and compromises plant innate immunity via inhibition of the RNA-processing 59-39 exoribonucleases. Our results provide evidence for the role of chloroplast-derived signal and RNA metabolism in the control of cell death and biotic stress response.

Mitochondrial Energy Signaling and Its Role in the Low-Oxygen Stress Response of Plants

“…As many of these commonly regulated genes are ANAC017 dependent, it was recently suggested that the PAP and ANAC017 pathways are mechanistically linked (Van Aken and Pogson, 2017). At least part of this common pathway appears capable of suppressing cell death and lesion formation, potentially by suppressing, e.g., extrusion of toxic compounds such as chlorophyll degradation products (Bruggeman et al, 2016;Van Aken and Pogson, 2017).…”

Signaling interactions between mitochondria and chloroplasts in Nicotiana tabacum leaf

“…Besides their central role in carbon and energy metabolism, both mitochondria and chloroplasts have also been implicated as key players in various plant cell death signaling pathways (Mühlenbock et al , Zurbriggen et al , van Doorn et al , Pattanayak et al , Bruggeman et al , Huang et al , Dickman et al , Dogra et al ). This influence likely relates to the critical role of these organelles in energy metabolism, as well as their capacity to engage various and likely interconnected signaling pathways, some of which promote cell death (Baena‐González and Sheen , Green et al , Van Aken and Pogson ).…”

Ties that bind: the integration of plastid signalling pathways in plant cell metabolism

“…ex1 ex2 double mutants cannot rescue the ROS-dependent necrotic phenotype of fc2 mutants (discussed at length below) nor the lesion mimic phenotype of mips1 ( myoinositol phosphate synthase1 ) mutants. Like several other lesion mimic mutants, mips1 lesion formation is light- and chlorophyll-dependent [13], and can be suppressed in the dark or in mutant backgrounds defective in chlorophyll biosynthesis (including mutants defective in Mg chelatase activity, gun4 and gun5 , and a mutant defective in divinyl protochlorophyllide 8-vinyl reductase activity, pcb2 ) [14]. A reverse genetic screen for suppressors of the mips1 lesion formation identified sal1/fiery1 as a strong suppressor of mips1 PCD [14].…”

“…Like several other lesion mimic mutants, mips1 lesion formation is light- and chlorophyll-dependent [13], and can be suppressed in the dark or in mutant backgrounds defective in chlorophyll biosynthesis (including mutants defective in Mg chelatase activity, gun4 and gun5 , and a mutant defective in divinyl protochlorophyllide 8-vinyl reductase activity, pcb2 ) [14]. A reverse genetic screen for suppressors of the mips1 lesion formation identified sal1/fiery1 as a strong suppressor of mips1 PCD [14]. SAL1 localizes to chloroplasts and mitochondria, where it dephosphorylates PAP (3′ phosphoadenosine 5′ phosphate) into AMP, but sal1 mutants hyperaccumulate PAP without dramatic effects on the levels of PAP precursors [15] (Figure 1C).…”

“…Through the suppression of gene silencing, and perhaps other transcripts that are sensitive to XRN activity, PAP causes increased expression of high light- and drought-inducible genes. Supporting this model, mips1 xrn2 xrn3 xrn4 quadruple mutants, which lack all Arabidopsis XRN enzymes (there is no Arabidopsis orthologue of eukaryotic XRN1 ), also suppresses the mips1 light-dependent cell death phenotype [14]. Thus, loss of XRN activity by either PAP inhibition in the sal1 background or genetic mutation prevents PCD in the mips1 background.…”