‘Candidatus Liberibacter asiaticus’ peroxiredoxin (LasBCP) suppresses oxylipin-mediated defense signaling in citrus

Abstract

The Lasbcp (CLIBASIA_RS00445) 1-Cys peroxiredoxin gene is conserved among all 13 sequenced strains of Candidatus Liberibacter asiaticus, the causal agent of Huanglongbing or "citrus greening" disease. LasBCP was previously characterized as a secreted peroxiredoxin with substrate specificity for organic peroxides, and as a potential pathogenicity effector. Agrobacterium-mediated transient expression of LasBCP in citrus leaves provided significant protection against peroxidation of free and membrane-bound lipids, thereby preserving the molecular integrity of the chlorophyll apparatus and reducing accumulation of lipid peroxidation products (oxylipins) following exposure to tert-butyl hydroperoxide (tBOOH, an organic peroxide). Oxylipins extracted from GUS-expressing citrus leaves reduced viability of L. crescens, the only Liberibacter species cultured to date. However, similar extracts obtained from LasBCP-expressing leaves were less inhibitory to L. crescens growth and viability in culture. Quantitative RT-PCR analyses showed coordinated transcriptional downregulation of oxylipin biosynthetic (CitFAD, CitLOX, CitAOS and CitAOC), and jasmonic acid (JA) (CitJAR1, CitCOI1 and CitJIN1) and salicylic acid (SA) (CitPAL, CitICS and CitPR1) signaling pathway genes in citrus leaves expressing LasBCP and treated with tBOOH. The negative response regulator of jasmonic acid CitJAZ1 was upregulated in LasBCP-expressing citrus leaves under similar conditions. These data clearly demonstrated a protective role of secreted LasBCP in favor of Las survival and colonization by alleviating ROS-induced lipid peroxidation in citrus host, preventing accumulation of antimicrobial oxylipins, and suppressing both localized and systemic immune responses in planta.