Panax notoginseng Root Cell Death Caused by the Autotoxic Ginsenoside Rg1 Is Due to Over-Accumulation of ROS, as Revealed by Transcriptomic and Cellular Approaches

Abstract

Panax notoginseng is a highly valuable medicinal herb, but its culture is strongly hindered by replant failure, mainly due to autotoxicity. Deciphering the response mechanisms of plants to autotoxins is critical for overcoming the observed autotoxicity. Here, we elucidated the response of P. notoginseng to the autotoxic ginsenoside Rg1 via transcriptomic and cellular approaches. Cellular analyses demonstrated that Rg1 inhibited root growth by disrupting the cell membrane and wall. Transcriptomic analyses confirmed that genes related to the cell membrane, cell wall decomposition and reactive oxygen species (ROS) metabolism were up-regulated by Rg1 stress. Further cellular analyses revealed that Rg1 induced ROS (O2·- and H2O2) accumulation in root cells by suppressing ascorbate peroxidase (APX) and the activities of enzymes involved in the ascorbate-glutathione (ASC-GSH) cycle. Exogenous antioxidants (ASC and gentiobiose) helped cells scavenge over-accumulated ROS by promoting superoxide dismutase (SOD) activity and the ASC-GSH cycle. Collectively, the autotoxin Rg1 caused root cell death by inducing the over-accumulation of ROS, and the use of exogenous antioxidants could represent a strategy for overcoming autotoxicity.

Light Quality Affected the Growth and Root Organic Carbon and Autotoxin Secretions of Hydroponic Lettuce

“…This indicated that the lettuce with the same root surface area or same accumulation in shoot dry weight secreted more autotoxins into the nutrient solution under white light, especially benzoic acid and salicylic acid. Autotoxins led to the disorder of plant metabolism, the inhibition of water and nutrients absorption, and to the accumulation of reactive oxygen species in plants [ 52 , 53 ]. The membrane structure of the plant was then destroyed by autotoxicity, the permeability of membrane increased, the electrolyte inside the cell extravasated, and, in severe cases, the root tip cell would die [ 53 ].…”

“…Autotoxins led to the disorder of plant metabolism, the inhibition of water and nutrients absorption, and to the accumulation of reactive oxygen species in plants [ 52 , 53 ]. The membrane structure of the plant was then destroyed by autotoxicity, the permeability of membrane increased, the electrolyte inside the cell extravasated, and, in severe cases, the root tip cell would die [ 53 ]. In addition, autotoxins not only directly affected the root system of lettuce, but also indirectly inhibited the photosystem function and photosynthesis by destroying the structure of chloroplast [ 54 ].…”

Complete Genome Sequence and Biodegradation Characteristics of Benzoic Acid-Degrading Bacterium Pseudomonas sp. SCB32

“…Allelochemicals, metabolites produced by living organisms that have a detrimental effect on other species when released into the environment, significantly inhibit plant growth [11,37]. The use of microorganisms to degrade allelochemicals such as benzoic acid and for soil remediation has proven to be effective [38,39].…”

Planting Density Affects Panax notoginseng Growth and Ginsenoside Accumulation by Balancing Primary and Secondary Metabolism

“…Previous reports have found that stress conditions can induce the burst of reactive oxygen species (ROS) (Jorge et al, 2016). In this study, intraspecific competition among P. notoginseng at the high planting densities caused environmental stress, and the relative content of the antioxidants gentiobiose (Yang et al, 2018b), dehydroascorbic acid (Dewhirst and Fry, 2018), and oxalic acid (Martínez-Esplá et al, 2019) were significantly increased at the high planting densities (Figure 4D). These increased metabolites may be involved in eliminating excessive ROS.…”