Programmed cell death (PCD), a genetically controlled process of cell suicide, is important for proper growth, development and biotic/abiotic stress responses in animals and plants. Although Chloroplasts and mitochondria have been reported to play important roles in plant PCD, fundamental challenges remain to be addressed, such as whether a plant PCD requires the communication between the two organelles and what is the nature of the signaling molecule(s) transduced between them.
Recently, Prof. LI Jiayang’s group from the Institute of Genetics and Developmental Biology, Chinese Academy of Sciences uncovered a conserved malate-induced PCD pathway in plant and animal systems, revolutionizing people’s understanding of the communication between organelles.
Prof. LI Jiayang’s group has long-term interests in the molecular mechanism of PCD in plants. They identified an Arabidopsis thaliana cell death mutant, mosaic death 1 (mod1), and found that MOD1, an enoyl-acyl carrier protein (ACP) reductase, is essential for fatty acid biosynthesis in chloroplasts (Mou et al., Plant Cell, 2000). By screening and investigating of the suppressors of mod1 (som), they found that mod1 plants accumulate high levels of reactive oxygen species (ROS) and that the deficiency of mitochondrial electron transport chain (mETC) complex I can inhibit both ROS accumulation and cell death in mod1 (Wu et al., Cell Res, 2015). These results indicate that the PCD in mod1 may involve the communication between chloroplasts and mitochondria.
In a recent study, by investigation of soms which do not alter mETC complex I activities, they have identified 3 new genes: PLASTIDIAL NAD-DEPENDENT MALATE DEHYDROGENASE (plNAD-MDH), chloroplastic DICARBOXYLATE TRANSPORTER 1 (DiT1), and MITOCHONDRIAL MALATE DEHYDROGENASE 1 (mMDH1). These three genes are all key components of the malate-oxaloacetate (OAA) shuttle in plants, the deficiency of which can each suppress the ROS accumulation and cell death in mod1. The deficiency in MOD1 will favorably lead to the accumulation of the reducing equivalent NADH in chloroplasts and then drive the transport of reducing power in the form of malate from chloroplasts to mitochondria by malate-OAA shutttle to trigger ROS generation and initiate PCD.
Further study shows that this pathway plays crucial roles in the regulation of ROS generation and oxidative stress responses in continuous light condition. Moreover, the malate treatment of HeLa cells can induce ROS generation and cell death, and mitochondrial MDH plays a key role in this process.
These findings demonstrate the existence of a long suspected Chloroplast-To-Mitochondrion communication pathway in plants and a conserved cytosol-mitochondrion ROS- and cell death-inducing mechanism in animals.
This work entitled “Malate transported from chloroplast to mitochondrion triggers production of ROS and PCD in
Arabidopsis thaliana” has been published online in
Cell Research on March 14, 2018 (
DOI: 10.1038/s41422-018-0024-8), with Dr. ZHAO Yannan and Dr. LUO Lilan from Prof. LI Jiayang group and Dr. XU Jiesi from Prof. HUANG Xun group as the co-first authors. Prof. LI Jiayang, Prof. HUANG Xun and associate Prof. YU Hong are the co-corresponding authors. The main collaborators include Dr. CHU Jinfang, Prof. ZUO Jianru and Prof. WANG Guodong from the Institute of Genetics and Developmental Biology, Chinese Academy of Sciences.
This work was supported by the National Natural Science Foundation of China, and the Strategic Priority Research Program of Chinese Academy of Sciences.
Figure. A proposed model of programmed cell death in plant and animal cells (Image by IGDB)
Contact:
Dr. LI Jiayang
