Not Just a Cycle: Three <i>gab</i> Genes Enable the Non-Cyclic Flux Toward Succinate via GABA Shunt in ‘ <i>Candidatus</i> Liberibacter asiaticus’–Infected Citrus

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Abstract

Although the mitochondria retain all required enzymes for an intact tricarboxylic acid (TCA) cycle, plants might shift the cyclic flux from the TCA cycle to an alternative noncyclic pathway via γ-aminobutyric acid (GABA) shunt under specific physiological conditions. We hypothesize that several genes may ease this noncyclic flux and contribute to the citrus response to the phytopathogenic bacterium ‘Candidatus Liberibacter asiaticus’, the causal agent of Huanglongbing in citrus. To test this hypothesis, we used multiomics techniques (metabolomics, fluxomics, and transcriptomics) to investigate the potential roles of putative gab homologies from Valencia sweet orange (Citrus sinensis). Our findings showed that ‘Ca. L. asiaticus’ significantly increased the endogenous GABA and succinate content but decreased ketoglutarate in infected citrus plants. Citrus genome harbors three putative gab genes, including amino-acid permease (also known as GABA permease; CsgabP), GABA transaminase (CsgabT), and succinate-semialdehyde dehydrogenase (also known as GABA dehydrogenase; CsgabD). The transcript levels of CsgabP, CsgabT, and CsgabD were upregulated in citrus leaves upon the infection with ‘Ca. L. asiaticus’ and after the exogenous application of GABA or deuterium-labeled GABA isotope (GABA-D ₆). Moreover, our finding showed that exogenously applied GABA is quickly converted to succinate and fed into the TCA cycle. Likewise, the fluxomics study showed that GABA-D ₆ is rapidly metabolized to succinate-D ₄. Our work proved that GABA shunt and three predicated gab genes from citrus, support the upstream noncyclic flux toward succinate rather than an intact TCA cycle and contribute to citrus defense responses to ‘Ca. L. asiaticus’.

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A vast number of plant pathogens from viroids of a few hundred nucleotides to higher plants cause diseases in our crops. Their effects range from mild symptoms to catastrophes in which large areas planted to food crops are destroyed. Catastrophic plant disease exacerbates the current deficit of food supply in which at least 800 million people are inadequately fed. Plant pathogens are difficult to control because their populations are variable in time, space, and genotype. Most insidiously, they evolve, often overcoming the resistance that may have been the hard-won achievement of the plant breeder. In order to combat the losses they cause, it is necessary to define the problem and seek remedies. At the biological level, the requirements are for the speedy and accurate identification of the causal organism, accurate estimates of the severity of disease and its effect on yield, and identification of its virulence mechanisms. Disease may then be minimized by the reduction of the pathogen's inoculum, inhibition of its virulence mechanisms, and promotion of genetic diversity in the crop. Conventional plant breeding for resistance has an important role to play that can now be facilitated by marker-assisted selection. There is also a role for transgenic modification with genes that confer resistance. At the political level, there is a need to acknowledge that plant diseases threaten our food supplies and to devote adequate resources to their control.

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Author and article information

Contributors

Nabil Killiny: (View ORCID Profile)

Journal

Title: Molecular Plant-Microbe Interactions®

Abbreviated Title: MPMI

Publisher: Scientific Societies

ISSN (Print): 0894-0282

ISSN (Electronic): 1943-7706

Publication date Created: March 2022

Publication date (Print): March 2022

Volume: 35

Issue: 3

Pages: 200-214

Affiliations

[1 ]Department of Plant Pathology, Citrus Research and Education Center, University of Florida, 700 Experiment Station Rd., Lake Alfred, FL 33850, U.S.A.

[2 ]Department of Agricultural Botany, Faculty of Agriculture, Tanta University, Tanta, Egypt

Article

DOI: 10.1094/MPMI-09-21-0241-R

PubMed ID: 34775834

SO-VID: 65534aea-6395-4800-95b5-7c9572d00eec

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