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. 2019 Jul 11;14(9):1640566. doi: 10.1080/15592324.2019.1640566

Nitric oxide is a suppressor of aluminum-induced mitochondria and caspase-like protease-dependent programmed cell death in plants

Huyi He a,b, Long-Fei He a,✉
PMCID: PMC6768225  PMID: 31291833

ABSTRACT

Aluminum (Al) promotes programmed cell death (PCD) in plants. Although a lot of knowledge about the mechanisms of Al tolerance has been learned, how Al-induced PCD is regulated by nitric oxide (NO) is poorly understood. Mitochondrion is the regulatory center for PCD. We found that Al reduced the level of mitochondrial NO/H2O2, promoted the opening of mitochondrial permeability transition pore, decreased mitochondrial inner membrane potential (∆ψm), and increased caspase-like protease activity. NO-specific scavenger cPTIO enhanced these effects that were reversed by NO donor sodium nitroprusside. Our data suggest that NO suppresses Al-induced PCD by improving mitochondrial physiological properties.

KEYWORDS: Nitric oxide, programmed cell death, mitochondria, aluminum stress

Introduction

Acidic soil accounts for 43% of the arable lands in the world.1 When soil pH drops below 5.5, trivalent aluminum (Al) dissolved from the acidic soil inhibits root elongation growth of crops. Some studies have shown that Al could also promote programmed cell death (PCD) in plants. Al-induced PCD may be a mechanism of Al toxicity in plants.2 PCD is involved in Al toxicity in yeast.3 Al-induced PCD is a process of accelerated senescence, as evidenced by the function of AhSAG.4 The results of DNA ladder, DAPI staining, and caspase 3-like protease activity show that Al-induced cell death is a typical PCD in peanut root tips.5 Al rapidly induced PCD in Al-sensitive peanut cultivar, indicating that there is a negative relationship between Al tolerance and Al-induced PCD.6 The negative modulation can enhance Al tolerance in plants.

NO is a suppressor of PCD

As a signal molecule, nitric oxide (NO) is involved in plant growth and development as well as environmental response. The role of NO in environmental stress is dependent on its concentration. Al treatment can increase NO concentration or reduce endogenous NO content in plants. To resist Al toxicity, plants have evolved Al tolerance mechanisms, including external exclusion and internal tolerance.7 Although much has been learned about the mechanisms of Al tolerance, how Al-induced PCD is regulated by NO is poorly understood. Al-induced PCD through a reactive oxygen species (ROS)-activated signal transduction pathway.2 Al stress induced ROS burst and PCD occurrence. Exogenous H2O2 accelerated PCD production, which was reversed by the ROS scavengers catalase and ascorbic acid.8 NO delays PCD in barley aleurone layers by acting as an antioxidant.9 Al stress reduced the production of endogenous NO in Hibiscus moscheutos.10 By mitigating Al-induced mitochondrial respiratory dysfunction, NO donor alleviated Al toxicity in wheat root tips.11 Under the condition of Al-induced PCD, exogenous NO inhibited PCD production, while NO-specific scavenger aggravated PCD occurrence.5 NO is a negative regulator of Al-induced PCD in plants.

Mitochondrion is the regulatory center of PCD

The cell wall is the first barrier for Al3+ entry into plant cells. After Al3+ is absorbed in the cell wall, the loss of cell wall extensibility further enhances the Al binding capacity of the cell wall with the increase of pectin methylesterase (PME) activity and the decrease of xyloglucan endotransglucosylase/hydrolase (XTH-32) expression. However, exogenous NO inhibited Al adsorption in the cell wall by increasing XTH-32 expression and decreasing PME activity.12 Mitochondrion is responsible for electron transport and oxidative phosphorylation in plant cells. Moreover, mitochondria play a significant role in Al-induced PCD in peanut. Al induced mitochondria-dependent PCD in Arabidopsis thaliana.13 The alterations of mitochondria also contribute to the regulation of PCD, including lipid peroxidation of mitochondrial membrane, opening of mitochondrial permeability transition pore (MPTP), reduction of mitochondrial inner membrane potential (∆ψm), Cyt c release, and mitochondrial respiratory dysfunction.14 Oxidative stress promoted ROS production, MPTP opening, protease activation, leading to PCD induction in Arabidopsis.15 In heat shock-induced PCD in tobacco Bright-Yellow 2 cells, ROS production and impairment of mitochondrial metabolism were early events.16 ROS initiated the release of Cyt c.17 Mitochondria produced NO through anoxic reduction of nitrite in barley roots.18 Al-induced cell death is mitochodria-dependent PCD. The occurrence of PCD was associated with the level of mitochondrial NO/H2O2. Therefore, it is suggested that NO/H2O2 may be a trigger signal for mitochondria-dependent PCD. By inhibiting the opening of MPTP and increasing ∆ψm, exogenous NO suppressed Al-induced PCD in the root tips of peanut.19 So mitochondrion is considered to be the regulatory center of PCD.

Caspase-like proteases are involved in al-induced PCD

The cysteine protease mcll-Pa executes PCD during plant embryogenesis.20 Metacaspase-8 was involved in the modulation of UV and H2O2-induced PCD in Arabidopsis.21 The existence of caspase protease activities in plant PCD indicated that caspase-like proteases may play an important role in the mechanisms of PCD occurrence in plants. Among different caspase-like proteases in peanut root tips, caspase-3-like protease may be a critical executor in Al-induced PCD.22

Based on all the results, a mechanism of NO involved in Al-induced PCD is proposed in Figure 1. Al3+ not only affects the physiological properties of the cell wall and plasma membrane, but also enters mitochondrial membrane. Al3+ in mitochondria affects the electron transmission chain and then triggers NO production and H2O2 burst. The integrative signal of NO/H2O2 opens MPTP and accelerates the collapse of ∆ψm. Subsequently, PCD is induced with the release of cytochrome c and activation of caspase-like proteases. NO may act as a suppressor that plays a negative role in Al-induced PCD in plants.

Figure 1.

Figure 1.

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Proposed model for mitochondria and caspase-like protease dependent PCD induced by Al in plants. Al, aluminum; ETC, electron transmission chain; MPTP, mitochondrial mermeability transition pore; NO, nitric oxide; PCD, programmed cell death; PM, plasma membrane.

Funding Statement

This work was supported by the National Natural Science Foundation of China (Nos. 31660350, 31660352, 31860334).

Disclosure of Potential Conflicts of Interest

No potential conflicts of interest were disclosed.

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