Salicylic acid mediated immune response ofCitrus Sinensisto varying frequencies of herbivory and pathogen inoculation
Authors: Ibanez Freddy , Suh Joon Hyuk , Wang Yu , Rivera Monique , Setamou Mamoudou , Stelinski Lukasz L. 
Published: August 2020

Plant immunity against pathogens and pests is comprised of complex mechanisms orchestrated by signaling pathways regulated by plant hormones [Salicylic acid (SA) and Jasmonic acid (JA)]. Investigations of plant immune response to phytopathogens and phloem-feeders have revealed that SA plays a critical role in reprogramming of the activity and/or localization of transcriptional regulators via post-translational modifications. We explored the contributing effects of herbivory by a phytopathogen vector [Asian citrus psyllid,Diaphorina citri] and pathogen [CandidatusLiberibacter asiaticus (CLas)] infection on response of sweet orange [Citrus sinensis(L.) Osbeck] using manipulative treatments designed to mimic the types of infestations/infections that citrus growers experience when cultivating citrus in the face of Huanglongbing (HLB) disease. A one-time (7 d) inoculation access period withCLas-infected vectors caused SA-associated upregulation ofPR-1, stimulating defense response after a long period of infection without herbivory (270 and 330 days). In contrast, while repeated (monthly) ‘pulses’ of 7 d psyllid feeding injury stimulated immunity in CLas-infected citrus by increasing [SA] in leaves initially (up to 120 d), long-term (270 and 330 days) repeated herbivory caused [SA] to decrease coincident with upregulation of genes associated with SA metabolism (BMSTandDMR6). Similarly, transcriptional responses and metabolite (SA and its analytes) accumulation in citrus exposed to a continuously reproducing population ofD. citriexhibited a transitory upregulation of genes associated with SA signaling at 120 days and a posterior downregulation after long-term psyllid (adults and nymphs) feeding (270 and 330 days). Herbivory played an important role in regulation of SA accumulation in mature leaves ofC. sinensis, whether or not those trees were coincidentally infected withCLas. Our results indicate that prevention of feeding injury inflicted byD. citrifrom the tritrophic interaction may allow citrus plants to better cope with the consequences ofCLas infection, highlighting the importance of vector suppression as a component of managing this cosmopolitan disease.

Author Summary

We explored tritrophic interactions among an insect vector (Diaphorina citri) – phytopathogen (CandidatusLiberibacter asiaticus) – and cultivated fruit crop [sweet orange,Citrus sinensis(L) Osbeck]. Transcriptional and metabolic responses of plants were analyzed over an extended time-course of disease progression after various frequencies of herbivore feeding and durations of pathogen infection using manipulative treatments designed to mimic the types of infestations/infections that citrus growers experience when cultivating citrus in the presence of the devastating citrus disease, huanglongbing. We found that in the absence of coincident psyllid feeding damage, citrus trees could mount a defense response against the pathogen by activating the salicylic acid (SA) pathway. Repeated, monthly ‘pulses’ of herbivory led to pronounced stimulation of SA transcription that was coincident with diminished pathogen titers in plants. Although insect injury initially activated SA-dependent defense responses, continuous and/or long-term (≥ 270 d) herbivory shut downPR-1-dependent defense responses against the pathogen. Our results provide a mechanism explaining how vector suppression contributes to maintaining health of cultivated citrus in areas where huanglongbing is endemic. Our results also point to specific gene targets that may yield novel genotypes expressing tolerance againstCLas after appropriate manipulations.