Identification and analysis of bZIP family genes in Citrus sinensis and the role of CsbZIP24 in response to Huanglongbing

Abstract

Citrus Huanglongbing (HLB) is one of the most destructive citrus diseases worldwide, mainly caused by ‘Candidatus Liberibacter asiaticus’ (CLas). HLB plants commonly present zinc deficiency chlorosis, which is evidenced with decreased zinc content and upregulation of genes encoding zinc transport proteins (ZIPs). However, the mechanism of how ZIPs are activated in response to CLas infection is unknown. Herein, the phylogenetic analysis was done for ZIPs and its potential upstream regulator bZIPs on the genome-wide level. Fifty-six bZIP transcription factor members classified into thirteen groups and twelve ZIP members were identified from C. sinensis. CsbZIP23 and CsbZIP24 harboring Zinc-sensor motif (ZSM) were characterized as the homologues of Arabidopsis thaliana bZIP19/23 in regulation of zinc homeostasis, and both were highly expressed in leaves compared to stems and roots. CsbZIP24 was further demonstrated in activation of CsZIP3 gene expression by binding to its promoter containing Zinc Deficiency Response Elements (ZDRE) rather than CsbZIP23. Additionally, the induction of both CsbZIP24 and CsZIP3 was observed in HLB diseased plants. Taken together, zinc sensor members were firstly identified in citrus and CsbZIP24 was proposed as the key factor in regulation of CsZIP3 gene expression to accommodate zinc-deficient conditions that caused by CLas colonization.