Plant E3 Ligases and Their Role in Abiotic Stress Response

Abstract

Plants, as sessile organisms, have limited means to cope with environmental changes. Consequently, they have developed complex regulatory systems to ameliorate abiotic stresses im-posed by environmental changes. One such system is the ubiquitin proteasome pathway, which utilizes E3 ligases to target proteins for proteolytic degradation via the 26S proteasome. Plants ex-press a plethora of E3 ligases that are categorized into four major groups depending on their structure. They are involved in many biological and developmental processes in plants, such as DNA repair, photomorphogenesis, phytohormones signaling, and biotic stress. Moreover, many E3 ligase targets are proteins involved in abiotic stress responses, such as salt, drought, heat, and cold. In this review, we will provide a comprehensive overview of E3 ligases and their substrates that have been connected with abiotic stress in order to illustrate the diversity and complexity of how this pathway enables plant survival under stress conditions.

Keywords: E3 ligase; abiotic stress; drought stress; heavy metal stress; oxidative stress; salt stress; temperature stress.

Figure 1

The ubiquitin proteasome pathway. Ubiquitin binds to E1, and E1 transfers the ubiquitin to E2, which binds with E3. E3 facilitates the transfer of ubiquitin from E2 to the substrate. Once the substrate is polyubiquitinated, it becomes a target for 26S proteasome for subsequent degradation.

Figure 2

The role of A. thaliana RING DOMAIN LIGASE1 (AtRGLG1) in drought stress tolerance. AtRGLG1 targets three proteins critical for improving drought tolerance for proteasomal degradation: ETHYLENE RESPONSE FACTOR53 (AtERF53), MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE 18 (MAPKKK18), and PROTEIN PHOSPHATASE 2CA (PP2CA).

Figure 3

The role of PLANT U-BOX E3 ligases (PUBs) in drought stress tolerance. Both A. thaliana PUB46 and PUB48 positively regulate drought tolerance by targeting unknown substrates, which are suggested to be negative regulators of drought tolerance. On the other hand, AtPUB11 negatively regulates drought tolerance by targeting both LEUCINE RICH REPEAT PROTEIN 1 (LRR1) and KINASE 7 (KIN7), which are known as positive regulators of drought tolerance. Also, O. sativa PUB41 is considered to be a negative regulator of drought tolerance by targeting CHLORIDE CHANNEL 6 (OsCLC6).

Figure 4

The role of O. sativa SALT-INDUCED RING PROTEIN family (SIRPs) in salt stress tolerance. OsSIRP1 negatively regulates salt tolerance by targeting unknown substrates that are suggested to be positive regulators of salt tolerance. Also, OsSIRP3 negatively regulates salt tolerance by triggering degradation of two salt-induced proteins, O. sativa MADS-BOX GENE 70 (OsMADS70) and an ABC DOMAIN CONTAINING PROTEIN (OsABC1P11). Moreover, OsSIRP4 is a negative regulator of salt stress tolerance by targeting O. sativa PEROXISOMAL BIOGENESIS FACTOR 11-1 (OsPEX11-1), which has an unknown function related to salt stress regulation. On the other hand, OsSIRP2 is considered to be a positive regulator of salt tolerance by targeting its only known target substrate, TRANSKETOLASE 1 (OsTKL1).

Figure 5

The role of A. thaliana PARAQUAT TOLERANCE 3 (PQT3) in oxidative stress tolerance. AtPQT3 negatively regulates oxidative stress tolerance by triggering degradation of PROTEIN ARGININE METHYLTRANSFERASE 4B (AtPRMT4B), which promotes ASCORBATE PEROXIDASE 1 (APX1) and GLUTATHIONE PEROXIDASE 1 (GPX1) expression. Both APX1 and GPX1 play major roles in oxidative stress tolerance by acting as antioxidants that catalyze the reduction of H₂O₂ to water and oxygen.

Figure 6

The role of E3 ligases in temperature stress tolerance. (A) Arabidopsis thaliana PROTEIN WITH THE RING DOMAIN AND TMEMB1 (AtPPRT1) positively regulates heat tolerance by triggering the degradation of unknown substrates, which is likely a negative regulator of HEAT SHOCK PROTEIN 21 (AtHSP21), HEAT SHOCK TRANSCRIPTION FACTOR A7A (AtHSFA7a), and ZINC-FINGER PROTEIN 12 (AtZAT12). The role of A. thaliana HIGH EXPRESSION OF OSMOTICALLY RESPONSIVE GENES 1 (HOS1) in cold stress tolerance. (B) Oryza sativa HEAT-INDUCED RING FINGER PROTEIN 1 (OsHIRP1) positively regulates heat tolerance by triggering degradation of ALDO/KETO REDUCTASE 4 (OsAKR4) and HIRP1-REGULATED KINASE1 (OsHRK1), which is highly likely a negative regulator of heat stress tolerance. (C) Arabidopsis thaliana HIGH EXPRESSION OF OSMOTICALLY RESPONSIVE GENES 1 (HOS1) negatively regulates cold tolerance by triggering degradation of INDUCER OF CBF EXPRESSION 1 (ICE1), which is a positive regulator of C-REPEAT BINDING FACTORS (CBF) transcription factors. CBFs play major roles in cold stress tolerance by promoting transcription of cold tolerance related genes.

Figure 7

The role of T. aestivum PLANT U-BOX 1 (TaPUB1) in heavy metal (HMs) stress tolerance. TaPUB1 positively regulates HM tolerance by triggering degradation of both IRON-REGULATED TRANSPORTER 1 (TaIRT1) and INDOLE-3-ACETIC ACID INDUCIBLE 17 (TaIAA17), which act as negative regulators of HM stress tolerance.