Roles of E3 Ubiquitin Ligases in Plant Responses to Abiotic Stresses

Abstract

Plants are frequently exposed to a variety of abiotic stresses, such as those caused by salt, drought, cold, and heat. All of these stressors can induce changes in the proteoforms, which make up the proteome of an organism. Of the many different proteoforms, protein ubiquitination has attracted a lot of attention because it is widely involved in the process of protein degradation; thus regulates many plants molecular processes, such as hormone signal transduction, to resist external stresses. Ubiquitin ligases are crucial in substrate recognition during this ubiquitin modification process. In this review, the molecular mechanisms of plant responses to abiotic stresses from the perspective of ubiquitin ligases have been described. This information is critical for a better understanding of plant molecular responses to abiotic stresses.

Keywords: abscisic acid; drought stress; salt stress; temperature stress; ubiquitin ligase; ubiquitination.

Figure 1

Schematic diagram of E3 ubiquitin ligases in different signaling pathways involved in plant responses to salt stress. The salt-stress pathways crosstalk with the ABA and MAPK pathways. E3 functions by ubiquitination of downstream target proteins. +P—phosphorylation; +U—ubiquitination; +MA—N-myristoylation; +M—methylation; ABA—abscisic acid; SOS—salt overly sensitive; GI—GIGANTEA; IbATL38—Ipomoea batatas Arabidopsis Toxicos en Levadura 38; SiGRF1—Setaria italica growtn-regulating factor1; EST1—Ever shorter Telomeres 1; SiRNF1/2—Setaria italica RING finger protein 1/2; RGLG—RING domain ligase; FT—Flowering Locus T; LFY—LEAFY; PRMT4b—protein arginine methyltransferase 4b; AtAPX1—Arabidopsis thaliana ascorbate peroxidase 1; GPX1—glutathione peroxidase 1; PQT3—paraquat tolerance 3; MfSTMIR—Medicago falcata salt tunicamycin-induced RING finger protein; MtUBC32—ubiquitin-conjugating enzyme 32; ROS—reactive oxygen species; MAPK—mitogen-activated protein kinase. A solid arrow shows a promoting effect or positive regulation; a dotted arrow shows that the specific mechanism of action is unclear; a horizontal line shows inhibition or negative regulation; a double arrow shows interacting proteins.

Figure 2

Schematic diagram of E3 ubiquitin ligases in signaling pathways involved in plant responses to drought stress. E3 functions by ubiquitination of downstream target proteins. +P—phosphorylation; +U—ubiquitination; +MA—N-myristoylation; +M—methylation; ABA—abscisic acid; DREB2A—dehydration-responsive element-binding protein 2A; DRIP1—DREB2A interacting protein 1; TaSAP5—Triticum aestivum stress-associated protein; AtAIRP1—A. thaliana ABA-insensitive RING 1; LOG2—loss of glutamine dumper 2; HSP90C—chloroplast heat shock protein 90; RGLG—RING domain ligase; PIN2—pin-formed 2; UBC13—ubiquitin-conjugating enzyme UBC13; RD21—responsive to desiccation 21; TaDIS1—Triticum aestivum drought-induced SINA protein 1; TaSTP—Triticum aestivum salt tolerant protein; CHYR1—CHY zinc-finger and RING protein1; SARD1—SAR deficient 1; CBF60g—calmodulin-binding protein 60-like g; SA—salicylic acid; ICS1—isochorismate synthase 1; PR genes—pathogenesis-related genes; JA—jasmonic acid; SNC2—suppressor of NPR1, constitutive 2; MAPK—mitogen-activated protein kinase. A solid arrow shows a promoting effect or positive regulation; a dotted arrow shows that the specific mechanism of action is unclear; a horizontal line shows inhibition or negative regulation; a double arrow shows interacting proteins.

Figure 3

Schematic diagram of E3 ubiquitin ligases in signaling pathways involved in plant responses to cold stress. +P—phosphorylation; +U—ubiquitination; +MA—N-myristoylation; CORs—cold-regulated genes; CBF—C-repeat binding factor; COLD1—chilling-tolerance divergence 1; CBLs—calcineurin B-like proteins; CIPKs—CBL-interacting protein kinases; ICE1—CBF expression 1; OST1—open stomata1; EGR2:—lade-E growth-regulating 2; NMT1—myristoyltransferase; CO—constans; COP1—constitutive photomorphogenic 1. A solid arrow shows a promoting effect or positive regulation; a dotted arrow shows that the specific mechanism of action is unclear; a horizontal line shows inhibition or negative regulation.

Figure 4

Schematic diagram of E3 ubiquitin ligases in signaling pathways involved in plant responses to heat stress. +U—ubiquitination; ROS—reactive oxygen species; HSFs—heat shock TFs; HSPs—heat shock proteins; SlCHIP—Solanum lycopersicum carboxyl terminus of the HSC70-interacting proteins; OsHTAS—Oryza sativa heat tolerance at seedling stage; H₂O₂—hydrogen peroxide. A solid arrow shows a promoting effect or positive regulation; a horizontal line shows inhibition or negative regulation; a double arrow shows interacting proteins.