Dysfunctional chloroplasts up-regulate the expression of mitochondrial genes in Arabidopsis seedlings

Abstract

Chloroplasts and mitochondria play important roles in maintaining metabolic and energy homeostasis in the plant cell. The interactions between these two organelles, especially photosynthesis and respiration, have been intensively studied. Still, little is known about the regulation of mitochondrial gene expression by chloroplasts and vice versa. The gene expression machineries in chloroplasts and mitochondria rely heavily on the nuclear genome. Thus, the interactions between nucleus and these organelles, including anterograde and retrograde regulation, have been actively investigated in the last two decades. Norflurazon (NF) and lincomycin (Lin) are two commonly used inhibitors to study chloroplast-to-nucleus retrograde signaling in plants. We used NF and Lin to block the development and functions of chloroplasts and examined their effects on mitochondrial gene expression, RNA editing and splicing. The editing of most mitochondrial transcripts was not affected, but the editing extents of nad4-107, nad6-103, and ccmFc-1172 decreased slightly in NF- and Lin-treated seedlings. While the splicing of mitochondrial transcripts was not significantly affected, steady-state mRNA levels of several mitochondrial genes increased significantly in NF- and Lin-treated seedlings. Moreover, Lin seemed to have more profound effects than NF on the expression of mitochondrial genes, indicating that signals derived from these two inhibitors might be distinct. NF and Lin also significantly induced the expression of nuclear genes encoding subunits of mitochondrial electron transport chain complexes. Thus, dysfunctional chloroplasts may coordinately up-regulate the expression of nuclear and mitochondrial genes encoding subunits of respiratory complexes.

Interference with plastome gene expression and Clp protease activity in Arabidopsis triggers a chloroplast unfolded protein response to restore protein homeostasis

“…LIN specifically inhibits chloroplast translation even though it also has secondary effects on mitochondrial gene expression at high concentrations, i.e. those causing seedling bleaching [ 29 , 30 ]. WT (Columbia) Arabidopsis plants were germinated and grown for 10 days under long-day (LD) conditions in the presence of LIN at concentrations causing from no visible symptoms (5 μM) to complete bleaching (100 μM) ( Fig 1B ).…”

“…Unlike LIN, NFZ treatment did not trigger the accumulation of chaperone transcripts ( Fig 7A ). While both inhibitors cause similar bleaching symptoms ( Fig 1 ), only LIN has a direct impact on PGE [ 28 – 30 ]. Blockage of carotenoid biosynthesis with NFZ can eventually alter PGE as it leads to decreased photoprotection and photooxidation, but LIN directly inhibits the translation of plastome-encoded proteins and has a much stronger impact on RNA transcription and processing than NFZ [ 30 , 53 ].…”

“…While both inhibitors cause similar bleaching symptoms ( Fig 1 ), only LIN has a direct impact on PGE [ 28 – 30 ]. Blockage of carotenoid biosynthesis with NFZ can eventually alter PGE as it leads to decreased photoprotection and photooxidation, but LIN directly inhibits the translation of plastome-encoded proteins and has a much stronger impact on RNA transcription and processing than NFZ [ 30 , 53 ]. In any case, the secondary effects of NFZ on PGE are not expected to be relevant in green plants at short times like those used to analyze the existence of a cpUPR after transferring WT plants to inhibitor-supplemented media ( Fig 7A ).…”

Chlorosis of Ogura-CMS Brassica rapa is due to down-regulation of genes for chloroplast proteins

“…Therefore, extensive researches on the interaction between these organelles have been carried out with respect to photosynthesis and respiration at physiological levels. But, only one paper (Liao et al 2016) has mentioned that dysfunctional chloroplast is related to the up-regulation of mitochondrial gene expression in Arabidopsis. Our results is the first report for the chloroplast gene expression change by dysfunctional mitochondria, showing accumulation of chloroplast proteins can be regulated by mitochondrial signal.…”

“…Chloroplastic retrograde signaling changes both nuclear (Fernández and Strand 2008;Liao et al 2016;Woodson 2016) and mitochondrial gene expression (Liao et al 2016). However, little is known about the regulation of chloroplast genes and nuclear genes for chloroplast proteins by mitochondrial retrograde signaling.…”