Plant Acyl-CoA-Binding Proteins-Their Lipid and Protein Interactors in Abiotic and Biotic Stresses

Abstract

Plants are constantly exposed to environmental stresses during their growth and development. Owing to their immobility, plants possess stress-sensing abilities and adaptive responses to cope with the abiotic and biotic stresses caused by extreme temperatures, drought, flooding, salinity, heavy metals and pathogens. Acyl-CoA-binding proteins (ACBPs), a family of conserved proteins among prokaryotes and eukaryotes, bind to a variety of acyl-CoA esters with different affinities and play a role in the transport and maintenance of subcellular acyl-CoA pools. In plants, studies have revealed ACBP functions in development and stress responses through their interactions with lipids and protein partners. This review summarises the roles of plant ACBPs and their lipid and protein interactors in abiotic and biotic stress responses.

Keywords: abiotic stress; acyl-CoA-binding proteins; biotic stress; lipids; protein interactors; stress signalling.

Figure 1

Signalling pathways associated with acyl-CoA-binding proteins (ACBPs) following abiotic stresses in Arabidopsis thaliana. In transgenic Arabidopsis Class II AtACBP1-overexpressors (OEs), PLDα1 was induced upon cold stress, causing a decrease in the ratio of PC to PA leading to membrane instability and freezing sensitivity [88]. In contrast, transgenic Arabidopsis Class I AtACBP6-OEs were conferred freezing tolerance via the PLDδ-mediated pathway in rosettes and the ABA-mediated pathway in flowers, resulting in changes in lipids, sugars and stress-related genes [87,123]. During drought, transgenic Arabidopsis Class II AtACBP2-OEs exhibited elevated AtAREB1 and AtRBOHF expression which led to ROS production, subsequent stomatal closure and reduced water loss [90]. Proper stem cuticle development conferred by Class I AtACBP6, Class III AtACBP3 or Class IV AtACBP4 protects wild-type Arabidopsis from water loss [25]. Under high salinity, AtACBP1 and AtAREB1 expression were upregulated in wild-type seeds [80]. The overexpression of AtACBP1 in transgenic Arabidopsis triggers nuclear translocation of AtAREB1, leading to the induction of stress marker genes (RD22 and RD29B) and AtAREB1 target genes (PKS5 and RAB18), thereby promoting stronger ABA responses during seed germination and seedling establishment [80]. When wild-type Arabidopsis undergoes hypoxia, the RAP2.12 transcription factor bound to AtACBP1 or AtACBP2, translocates to the nucleus and activates hypoxia-responsive gene transcription, conferring hypoxic protection [77,128,134,139]. Another hypoxic tolerance pathway involves the interaction of unsaturated VLC ceramide and the CTR1 protein with subsequent nuclear translocation of EIN2, resulting in the activation of CTR1-mediated ethylene signalling [137]. AtACBP1 is involved in phytoremediation and its overexpression in transgenic Arabidopsis confers Pb(II) tolerance [135]. AtACBP2 can interact with AtFP6 or LYSOPL2, mediating heavy metal transport and phospholipid repair respectively, and hence transgenic Arabidopsis AtACBP2-OEs were resistant to Cd(II) and Cd(II)-induced oxidative stress [75,76,82]. On wounding, the up-regulation of AtACBP3 and AtACBP6 expression in the wild type suggested their involvement in JA-mediated local and systemic wound responses [125,126]. Orange and yellow boxes indicate transgenic Arabidopsis AtACBP-OEs and wild-type Arabidopsis AtACBPs respectively, used in studies on abiotic stress. Blue boxes represent the signalling pathways. White boxes indicate the molecular events that occur along the signalling pathway. Red and blue arrows indicate increase and a decrease, respectively. Black arrows denote the flow of events. ABA, abscisic acid; ACBP, acyl-CoA-binding protein; AREB1, ABA-RESPONSIVE ELEMENT BINDING PROTEIN1; FP6, FARNESYLATED PROTEIN6; COR, COLD-RESPONSIVE; CTR1, CONSTITUTIVE TRIPLE RESPONSE1; EIN2, ETHYLENE-INSENSITIVE2; JA, jasmonic acid; LYSOPL2, LYSOPHOSPHOLIPASE2; MGDG, monogalactosyldiacylglycerol; PA, phosphatidic acid; PC, phosphatidylcholine; PKS5, PROTEIN KINASE SOS2-LIKE5; PLD, PHOSPHOLIPASE D; RAB18, RESPONSIVE TO ABA18; RAP2.12, RELATED TO APETALA2.12; RBOHF, RESPIRATORY BURST OXIDASE HOMOLOG F; RD, RESPONSIVE TO DESSICATION; ROS, reactive oxygen species; VLC, very-long-chain.

Figure 2

Biotic stress-related signalling pathways associated with acyl-CoA-binding proteins (ACBPs) in plants. Upon pathogen infection, the overexpression of Class III AtACBP3 in transgenic Arabidopsis thaliana led to constitutive activation of pathogenesis-related (PR) genes including PR1, PR2 and PR5, elevated H₂O₂ production and eventually cell death [121]. AtACBP3 plays a distinct role in the plant defence response against necrotrophic and biotrophic pathogens as transgenic Arabidopsis AtACBP3-overexpressors (OEs) were protected against the biotrophic pathogen (Pseudomonas syringae pv tomato DC3000) but not the necrotrophic pathogen (Botrytis cinerea) [121]. In wild-type Arabidopsis, the expression of Class IV AtACBP4 and AtEBP encoding a protein interactor of AtACBP4 were reported to be induced by B. cinerea infection, and ethylene precursor 1-aminocyclopropane-1-carboxylic acid (ACC) and methyl jasmonate (MeJA) treatments, suggesting that AtACBP4 and AtEBP are mediated by ethylene and/or JA signalling [74]. Rice Class III OsACBP5 protects transgenic Arabidopsis and rice plants against hemibiotrophs and biotrophs via NPR1-dependent SA signalling, and necrotrophs by JA signalling [93,127]. The OsACBP5 5′-flanking region contains W-boxes which were verified in pathogen-responsiveness of OsACBP5 [93]. Proteomic studies showed that eleven biotic stress-related proteins were upregulated by Rhizoctonia solani infection in transgenic Arabidopsis OsACBP5-OEs [127]. Grape Class III VvACBP conferred resistance to P. syringae and Colletotrichum higginsianum in transgenic Arabidopsis, possibly through the NPR1-mediated pathway following induction of PDF1.2, the gene encoding plant defensin [100]. Orange boxes represent the named ACBPs involved in the pathogen response. White boxes indicate the molecular events that occur along the signalling pathway. Black arrows denote the flow of signalling events. ACBP, acyl-CoA-binding protein; EBP, ETHYLENE-RESPONSIVE BINDING PROTEIN; JA, jasmonic acid; NPR1, NONEXPRESSOR OF PR-1; PR, pathogenesis-related; SA, salicylic acid.