Protein S-nitrosylation in programmed cell death in plants

Abstract

Programmed cell death (PCD) is associated with different phases of plant life and provides resistance to different kinds of biotic or abiotic stress. The redox molecule nitric oxide (NO) is usually produced during the stress response and exerts dual effects on PCD regulation. S-nitrosylation, which NO attaches to the cysteine thiol of proteins, is a vital posttranslational modification and is considered as an essential way for NO to regulate cellular redox signaling. In recent years, a great number of proteins have been identified as targets of S-nitrosylation in plants, especially during PCD. S-nitrosylation can directly affect plant PCD positively or negatively, mainly by regulating the activity of cell death-related enzymes or reconstructing the conformation of several functional proteins. Here, we summarized S-nitrosylated proteins that are involved in PCD and provide insight into how S-nitrosylation can regulate plant PCD. In addition, both the importance and challenges of future works on S-nitrosylation in plant PCD are highlighted.

Keywords: Plants; Programmed cell death; Protein S-nitrosylation.

Fig. 1

S-nitrosylation of ROS-related proteins involved in PCD regulation. NADPH oxidase can synthesize ROS, while S-nitrosylation at Cys-890 inactivates NADPH ability, inhibiting ROS production. S-nitrosylation of two antioxidant enzymes, APX1 and PrxII E, also affect ROS accumulation. S-nitrosylation of APX1 at Cys-32 regulates APX1 activity, leading to APX1 ubiquitination and therefore leading to degradation. S-nitrosylation of PrxII E not only inhibited its activity of H₂O₂-reducing peroxidase but also reduced its ability to detoxify ONOO⁻, leading to the accumulation of toxic O²⁻ and consequently causing PCD after Pst infection. NADPH ox respiratory burst oxidase homolog, O² oxygen, O²⁻ superoxide anion, H₂O₂ hydrogen peroxide, APX1 ascorbate peroxidase 1, SOD superoxide dismutase, PrxII E peroxiredoxin II E, Ub ubiquitination

Fig. 2

S-nitrosylation of SA signaling-related and the metabolism- and photosynthesis -related proteins GSNOR and MC9 involved in PCD regulation. aS-nitrosylation regulates SA signaling (lines in blue): SABP3 can be S-nitrosylated at its Cys-280 during the SA-related defense response. Under normal conditions, S-nitrosylation is beneficial for NPR1 in an oligomeric state in the cytosol. The oligomer can be reduced to monomers by TRXs in a NO-dependent manner and then translocated to the nucleus; S-nitrosylation of TGA1 at two Cys sites results in the formation of the NPR1/TGA system, regulating the expression of downstream PR genes. bS-nitrosylation of two metabolism-related proteins (lines in black): Rubisco and GAPDH can be S-nitrosylated, and S-nitrosylated GAPDH can interact with NtOSAK to respond to stress. c GSNOR S-nitrosylation leads to GSNOR degradation via selective autophagy (lines in orange); dS-nitrosylation of MC9 (lines in gray). SA salicylic acid, SABP3 salicylic acid-binding protein 3, GSNO S-nitrosoglutathione, NPR1 nonexpresser of pathogenesis-related Genes 1, NO nitric oxide, TRXs thioredoxins, TGA1 TGACG motif binding factor1, Rubisco ribulose-1,5-bisphosphate carboxylase/oxygenase, GAPDH glyceraldehyde 3-phosphate dehydrogenase, NtOSAK Nicotiana tabacum osmotic stress-activated protein kinase, GSNOR1 S-nitrosoglutathione reductase 1, ATG8 AUTOPHAGY-RELATED8, AIM ATG8-interacting motif, AtMC9 A. thaliana metacaspase 9