Editor-in-charge | Yi Fan
Hypoxia is one of the most common abiotic stresses affecting plant growth, development and yield. Flooding or stagnant water caused by flooding reduces the oxygen concentration in the environment in which the plant is located, leaving the cells in a state of hypoxia, thereby affecting the normal physiological metabolism and growth and development of the plant, resulting in crop yield reduction or even harvest failure, threatening agricultural safety. Therefore, studying the perception and signal transduction mechanism of plants on hypoxic stress is of great scientific and practical significance for in-depth understanding of plant flooding adaptability and ensuring stable crop yield after flood disasters. At present, the physiological adaptation mechanism of plant hypoxia response has been relatively clear, and the regulatory mechanism of plant hypoxia perception and signal transduction is poorly understood.
Studies have shown that the ethylene reaction transcription factor ERF-VII family proteins interact with membrane-associated ACBPs proteins anchored on the plasma membrane. Under flooded conditions, plants induced polyunsaturated acyl-CoA signaling molecules by hypoxia and relied on ubiquitin-like N-terminal protein degradation mechanisms to achieve dynamic perception and response to hypoxic stress, which opened up new ideas for the study of plant lipid metabolism or lipid signaling molecules involved in regulating hypoxia response (Licausi et al., 2011; Xie et al., 2021; Zhou et al., 2020）。 Previous studies have revealed that another lipid signaling molecule, phosphatidic acid (PA), accumulates significantly in the hypoxic response (Xie et al., 2015), but how PA participates in the plant hypoxia signaling pathway is unclear.
Recently, Xiao Shi's research group of plant stress biology team of Sun Yat-sen University published a research paper entitled "Phosphatidic acid modulates MPK3- and MPK6-mediated hypoxia signaling in Arabidopsis" online at The Plant Cell (Zhou et al., 2022). The molecular mechanism of phosphatidic acid (PA) molecularly regulated protein kinases MPK3 and MPK6 mediates for plant hypoxia signal transduction was deeply analyzed.
The study found that phospholipase PLDα1 and PLDδ are activated by flooding stress, and the hydrolyzed substrate phosphatidylethanolamine (PE) produces PA, which binds to protein kinases MPK3 and MPK6 as signaling molecules and activates their kinase activity. Further, MPK3 and MPK6 rely on the upstream unknown MAPKKK and MKK5 to phosphorylate the plant hypoxic response core transcription factor RAP2.12, regulating their transcriptional activity and hypoxic signal transduction pathway (Figure 1). At the same time, the excessive production of PA caused by long-term flooding will cause reactive oxygen species (ROS) outbreaks, cell death, and cell membrane integrity to be destroyed, which is not conducive to the resumption of plant growth in the re-oxygenation process after flooding removal. In-depth research has found that MPK3 and MPK6 kinases regulate their protein levels by interacting directly with PLDα1 and PLDδ proteins, phosphorylation and negative feedback, thereby maintaining suitable PA levels and intracellular homeostasis under low oxygen, and protecting the normal growth and development of plants during re-oxygenation (Figure 1). This study reveals for the first time a new mechanism of plant hypoxia signal chain mediated by PA-MPK3/6-RAP2.12 module, which is of great significance for improving the transduction mechanism of plant hypoxia signal and the genetic and molecular improvement of crop waterlogging resistance.
Figure 1. Pattern diagram of PA regulation of hypoxic signal transduction in plants by phosphatidic acid.
Zhou Ying, a postdoctoral fellow of Xiao Shi's research group, is the first author of the paper, Professor Xiao Shi and Associate Professor Xie Lijuan of South China Agricultural University are the co-corresponding authors of the paper, and Professor Li Jianfeng and Professor Yao Nan of Sun Yat-sen University are co-authors, and participated in part of the research. The work has been funded by the National Natural Science Foundation of China Jieqing Project, the Surface Project, the Youth Science Foundation Project, and the Guangdong Provincial Key R&D Program Project.
Key references
Licausi F, Kosmacz M, Weits DA, Giuntoli B, Giorgi FM, Voesenek LACJ, Perata P, and van Dongen JT (2011) Oxygen sensing in plants is mediated by an N-end rule pathway for protein destabilization. Nature 479: 419-422.
Xie LJ, Zhou Y, Chen QF*, and Xiao S. (2021) New insights into the role of lipids in plant hypoxia responses. Progress in Lipid Research 81: 101072.
Xie LJ, Chen QF, Chen MX, Yu LJ, Huang L, Chen L, Wang FZ, Xia FN, Zhu TR, Wu JX, Yin J, Liao B, Shi JX, Zhang JH, Aharoni A, Yao N, Shu W, and Xiao S. (2015) Unsaturation of very-long-chain ceramides protects plant from hypoxia-induced damages by modulating ethylene signaling in Arabidopsis. PLoS Genetics 11(3): e1005143.
Zhou Y, Tan WJ, Xie LJ, Qi H, Yang YC, Huang LP, Lai YX, Tan YF, Zhou DM, Yu LJ, Chen QF, Chye ML, and Xiao S. (2020) Polyunsaturated linolenoyl-CoA modulates ERF-VII-mediated hypoxia signaling in Arabidopsis. Journal of Integrative Plant Biology 62: 330-348.
Zhou Y, Zhou DM, Yu WW, Shi LL, Lai YX, Huang LP, Chen QF, Yao N, Li JF, Xie LJ, and Xiao S. (2022) Phosphatidic acid modulates MPK3- and MPK6-mediated hypoxia signaling in Arabidopsis. Plant Cell doi: 10.1093/plcell/koab289.
Thesis Link:
https://academic.oup.com/plcell/advance-article/doi/10.1093/plcell/koab289/6446039?searchresult=1
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