Molecular Plant Pathology

ABSTRACTCitrus huanglongbing (HLB), caused by “Candidatus Liberibacter” spp., is one of the most disastrous citrus diseases worldwide. HLB‐affected citrus fruits are significantly more acidic than healthy fruits. However, the molecular mechanism behind this phenomenon remains to be elucidated. Here, we report that HLB‐affected fruits have higher levels of citric acid (CA) than healthy fruits. Moreover, Citrus PH4 (CitPH4), which encodes a MYB transcription factor that functions as a key regulator of CA accumulation, was upregulated in HLB‐affected fruits relative to healthy fruits. Heterologous overexpression of CitPH4 in tobacco (Nicotiana tabacum) plants enhanced tolerance to HLB. Subsequently, overexpression and gene‐editing experiments indicated that CitPH4 can affect the salicylic acid (SA) pathway, which directly binds to and activates the promoter of CsPBS3, a key gene of SA biosynthesis. HLB‐affected fruits had higher SA levels than healthy fruits. Furthermore, application of SA activated CA biosynthesis and application of CA activated SA biosynthesis and signalling in citrus fruits and decreased “Candidatus Liberibacter asiaticus” (CLas) titres in infected leaves. This work suggests that CitPH4 is a key node between CA and SA, thus revealing crosstalk between defence responses and fruit quality in citrus.

AbstractCitrus huanglongbing (HLB) has been causing enormous damage to the global citrus industry. As the main causal agent, ‘Candidatus Liberibacter asiaticus’ (CLas) delivers a set of effectors to modulate host responses, while the modes of action adopted remain largely unclear. Here, we demonstrated that CLIBASIA_00185 (CLas0185) could attenuate reactive oxygen species (ROS)‐mediated cell death in Nicotiana benthamiana. Transgenic expression of CLas0185 in Citrus sinensis ‘Wanjincheng’ enhanced plant susceptibility to CLas. We found that methionine sulphoxide reductase B1 (CsMsrB1) was targeted by the effector, and its abundance was elevated in CLas0185‐transgenic citrus plants. Their interaction promoted CLas proliferation. We then determined that CsMsrB1 sustained redox state and enzymatic activity of ascorbate peroxidase 1 (CsAPX1) under oxidative stress. The latter reduced H2O2 accumulation and was associated with host susceptibility to CLas infection. Consistently, citrus plants expressing CLas0185 and CsMsrB1 conferred enhanced APX activity and decreased H2O2 content. Taken together, these findings revealed how CLas0185 benefits CLas colonization by targeting CsMsrB1, which facilitated the antioxidant activity and depressed ROS during pathogen infection.