The overexpression of OsACBP5 protects transgenic rice against necrotrophic, hemibiotrophic and biotrophic pathogens

Abstract

The most devastating diseases in rice (Oryza sativa) are sheath blight caused by the fungal necrotroph Rhizoctonia solani, rice blast by hemibiotrophic fungus Magnaporthe oryzae, and leaf blight by bacterial biotroph Xanthomonas oryzae (Xoo). It has been reported that the Class III acyl-CoA-binding proteins (ACBPs) such as those from dicots (Arabidopsis and grapevine) play a role in defence against biotrophic pathogens. Of the six Arabidopsis (Arabidopsis thaliana) ACBPs, AtACBP3 conferred protection in transgenic Arabidopsis against Pseudomonas syringae, but not the necrotrophic fungus, Botrytis cinerea. Similar to Arabidopsis, rice possesses six ACBPs, designated OsACBPs. The aims of this study were to test whether OsACBP5, the homologue of AtACBP3, can confer resistance against representative necrotrophic, hemibiotrophic and biotrophic phytopathogens and to understand the mechanisms in protection. Herein, when OsACBP5 was overexpressed in rice, the OsACBP5-overexpressing (OsACBP5-OE) lines exhibited enhanced disease resistance against representative necrotrophic (R. solani & Cercospora oryzae), hemibiotrophic (M. oryzae & Fusarium graminearum) and biotrophic (Xoo) phytopathogens. Progeny from a cross between OsACBP5-OE9 and the jasmonate (JA)-signalling deficient mutant were more susceptible than the wild type to infection by the necrotroph R. solani. In contrast, progeny from a cross between OsACBP5-OE9 and the salicylic acid (SA)-signalling deficient mutant was more susceptible to infection by the hemibiotroph M. oryzae and biotroph Xoo. Hence, enhanced resistance of OsACBP5-OEs against representative necrotrophs appears to be JA-dependent whilst that to (hemi)biotrophs is SA-mediated.

In silico Analysis of Acyl-CoA-Binding Protein Expression in Soybean

“…Inoculation of cultivar Conrad with P. sojae revealed that most members of Classes I, III, and IV exhibited slight downregulation in expression from the control. This situation appeared to differ from ACBPs of other plants such as Arabidopsis, grapevine and rice, in which Class III ACBPs, AtACBP3 ( Xiao and Chye, 2011 ), VvACBP ( Takato et al, 2013 ), and OsACBP5 ( Panthapulakkal Narayanan et al, 2020 ) respectively, respond to plant pathogens. In transgenic Arabidopsis, AtACBP3 -overexpressors and acbp3 showed contrasting reactions to biotrophic and necrotrophic pathogens.…”

“…tomato DC3000, but was susceptible to infection by necrotrophic fungus Botrytis cinerea ( Xiao and Chye, 2011 ). In contrast, transgenic rice OsACBP5 -overexpressors displayed disease resistance toward biotrophic ( Xanthomonas oryzae ), hemibiotrophic ( Magnaporthe oryzae and Fusarium graminearum ) and necrotrophic ( Rhizoctonia solani and Cercospora oryzae ) pathogens via both jasmonic acid (JA)- and salicylic acid (SA)-mediated pathways ( Panthapulakkal Narayanan et al, 2020 ). Also transgenic Arabidopsis overexpressing V. vinifera Class III ACBP was tolerant to P. syringae and Colletotrichum higginsianum , a pathogenic hemibiotrophic ascomycetous fungus ( Takato et al, 2013 ).…”

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

“…It binds long-chain acyl-CoA esters [ 83 ], participates in acyl-CoA transport [ 84 ], maintains acyl-CoA pool [ 85 ], and regulates the activities of various enzymes including glycerol-3-phosphate acyltransferase [ 83 ], lysophosphatidylcholine acyltransferase [ 85 ] and lysophosphatidic acid acyltransferase [ 86 ]. The transport of acyl-CoA esters is important for the biosynthesis of lipids such as glycerolipids, ceramides and phospholipids, and studies have shown that the binding of phospholipids to ACBPs plays a role in plant growth and development as well as stress responses [ 76 , 78 , 87 , 88 , 89 , 90 , 91 , 92 , 93 , 94 ]. Following the discovery of BnACBP, similar 10-kDa ACBPs emerged in Arabidopsis thaliana [ 95 ], Gossypium hirsutum (cotton) [ 96 ], Ricinus communis (castor bean) [ 97 ], Digitalis lanata Ehrh.…”

“…Thus far, only AtACBP2 interacts with FARNESYLATED PROTEIN6 (AtFP6) which may be involved in phospholipid repair following heavy metal-induced lipid peroxidation [ 75 ]. Lipid binding of ACBPs and their protein-protein interactions are now known to be important in regulating abiotic and biotic stress responses [ 74 , 75 , 76 , 78 , 80 , 87 , 88 , 93 , 120 , 121 , 122 , 123 , 124 , 125 , 126 , 127 , 128 ], as well as plant development including embryogenesis [ 81 , 116 , 119 ], seed dormancy [ 78 ], seed germination and development [ 78 , 80 , 129 , 130 , 131 ], cuticle development [ 25 , 26 ], pollen growth [ 132 ] and senescence [ 112 , 117 ].…”

“…Under the natural environment, plants are always exposed to a variety of bacterial and fungal pathogens. Several AtACBPs, such as AtACBP1, AtACBP3, AtACBP4 and AtACBP6, and Class III OsACBP5, have been reported to participate in plant defence against infections caused by bacterial and fungal pathogens ( Figure 2 ) [ 25 , 26 , 93 , 121 , 127 ]. AtACBP3 expression was induced in wild-type Arabidopsis following pathogen infection ( Pseudomonas syringae pv tomato DC3000 and Botrytis cinerea ) and treatments using pathogen elicitors (arachidonic acid) and defence-related phytohormones [1-aminocyclopropane-1-carboxylic acid (ACC), MeJA and salicylic acid (SA)] [ 121 ].…”