Gamma-Aminobutyric Acid Supplementation Boosts the Phytohormonal Profile in ‘Candidatus Liberibacter asiaticus’-Infected Citrus

Abstract

The devastating citrus disease, Huanglongbing (HLB), is associated with ‘Candidatus Liberibacter sp.’ and transmitted by citrus psyllids. Unfortunately, HLB has no known sustainable cure yet. Herein, we proposed γ-aminobutyric acid (GABA) as a potential eco-friendly therapeutic solution to HLB. Herein, we used GC/MS-based targeted metabolomics combined with gene expression to investigate the role of GABA in citrus response against HLB and to better understand its relationship(s) with different phytohormones. GABA supplementation via root drench boosts the accumulation of endogenous GABA in the leaves of both healthy and ‘Ca. L. asiaticus’-infected trees. GABA accumulation benefits the activation of a multi-layered defensive system via modulating the phytohormone levels and regulating the expression of their biosynthesis genes and some pathogenesis-related proteins (PRs) in both healthy and ‘Ca. L. asiaticus’-infected plants. Moreover, our findings showed that GABA application stimulates auxin biosynthesis in ‘Ca. L. asiaticus’-infected plants via the activation of the indole-3-pyruvate (I3PA) pathway, not via the tryptamine (TAM)-dependent pathway, to enhance the growth of HLB-affected trees. Likewise, GABA accumulation was associated with the upregulation of SA biosynthesis genes, particularly the PAL-dependent route, resulting in higher SA levels that activated CsPR1, CsPR2, CsPR5, and CsWRKY70, which are prominent to activation of the SA-mediated pathway. Additionally, higher GABA levels were correlated with an enhanced JA profile and linked with both CsPR3 and CsPR4, which activates the JA-mediated pathway. Collectively, our findings suggest that exogenous GABA application might be a promising alternative and eco-friendly strategy that helps citrus trees battle HLB.

Non-proteinogenic amino acids mitigate oxidative stress and enhance the resistance of common bean plants against Sclerotinia sclerotiorum

“…Therefore, it is necessary to introduce some eco-friendly alternatives to control S. sclerotiorum particularly, and soil-borne phytopathogens in general. NPAAs have emerged as potent fungistatic agents that could be promising eco-friendly alternatives to control fungal phytopathogens ( Marcucci et al., 2010 ; Justyna and Ewa, 2013 ; de Oliveira et al., 2019 ; Guo et al., 2022 ), as well as bacterial ones ( Nehela and Killiny, 2019 ; Nehela and Killiny, 2023a , b ).…”

“…However, GABA was reported to be accumulated as a part of the metabolomic responses of soybean plants against S. sclerotiorum ( de Oliveira et al., 2019 ), as well as grapevine response against Neofusicoccum parvum . Additionally, GABA plays a positive role in the host response to bacterial phytopathogens such as Agrobacterium tumefaciens ( Chevrot et al., 2006 ), Pseudomonas syringae ( Park et al., 2010 ; Deng et al., 2020 ), and ‘ Candidatus Liberibacter Asiaticus’ ( Killiny and Nehela, 2017 ; Nehela and Killiny, 2019 , 2022 ; Nehela and Killiny, 2023a , b ). In other words, augmented GABA shunt activity was reported to be associated with plant defense against Agrobacterium in tobacco ( Chevrot et al., 2006 ), Botrytis cinerea in tomato ( Seifi et al., 2013 ), and ‘ Candidatus Liberibacter Asiaticus’ in citrus ( Killiny and Nehela, 2017 ; Nehela and Killiny, 2019 , 2022 ; Nehela and Killiny, 2023a , b ).…”

“…For instance, the tolerance of citrus plants against the bacterial pathogen ‘ Ca . Liberibacter asiaticus’ was enhanced by the positive regulation of the GABA shunt and associated pathways such as amino acids ( Killiny and Nehela, 2017 ; Nehela and Killiny, 2023a ), polyamines ( Nehela and Killiny, 2020 ; Nehela and Killiny, 2023a ), TCA cycle, phytohormones ( Nehela and Killiny, 2023b ), and other stress-associated metabolites ( Nehela and Killiny, 2020 ; Nehela and Killiny, 2023a ). The dual function of GABA as a metabolite and as a signaling component enables plants to cope with different conditions.…”

“…Moreover, GABA and BABA prime defense responses against several fungal and bacterial pathogens ( Li et al., 2019 ; Deng et al., 2020 ; van Rensburg and Van den Ende, 2020 ; Nehela and Killiny, 2023a , b ; Li et al., 2024 ). For example, priming with GABA enhanced the response of mango ( Mangifera indica ) fruits to Colletotrichum gloeosporioides as well as the responses of Arabidopsis thaliana plants ( van Rensburg and Van den Ende, 2020 ) and tomato ( Solanum lycopersicum ) fruits to Botrytis cinerea ( Li et al., 2024 ).…”

“…Similarly, GABA contributes to the defense of A. thaliana and sweet orange ( Citrus sinensis ) to the bacterial pathogens Pseudomonas syringae ( Deng et al., 2020 ) and ‘Ca. Liberibacter Asiaticus’, respectively ( Nehela and Killiny, 2023a , b ). The priming effect of GABA against phytopathogens might be due to the modulation of phytohormones and their signaling pathways ( Nehela and Killiny, 2023b ; Li et al., 2024 ) and/or maintaining of redox status and buffering the antioxidant machinery ( van Rensburg and Van den Ende, 2020 ; Nehela and Killiny, 2023a ).…”