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 [ Candidatus Liberibacter asiaticus ( C Las)] 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 with C Las-infected vectors caused SA-associated upregulation of PR-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 ( BMST and DMR6 ). Similarly, transcriptional responses and metabolite (SA and its analytes) accumulation in citrus exposed to a continuously reproducing population of D. citri exhibited 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 of C. sinensis , whether or not those trees were coincidentally infected with C Las. Our results indicate that prevention of feeding injury inflicted by D. citri from the tritrophic interaction may allow citrus plants to better cope with the consequences of C Las infection, highlighting the importance of vector suppression as a component of managing this cosmopolitan disease.

中文翻译：

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水杨酸介导的柑橘对不同频率的食草和病原体接种的免疫反应

植物对病原体和害虫的免疫力由复杂的机制组成，这些机制由植物激素[水杨酸（SA）和茉莉酸（JA）]调控的信号传导途径精心设计。植物对植物病原体和韧皮部喂食者的免疫反应的研究表明，SA在通过翻译后修饰修饰转录调节子的活性和/或定位中起着至关重要的作用。我们研究了植物病原体载体[亚洲柑橘木虱，桔黄]和病原体[亚洲假丝酵母]的食草对甜橙[Citrus sinensis（L.）Osbeck]感染的反应，并采用了针对性的处理措施模仿柑桔种植者面对黄龙病（HLB）病菌种植柑桔时遇到的侵染/感染类型。用Las感染的载体进行的一次（7 d）接种时间段会导致SA相关的PR-1上调，在长期无草食感染（270天和330天）后刺激防御反应。相反，虽然重复（每月一次）7 d的木虱觅食性伤害的“脉冲”通过最初（长达120 d）叶片中[SA]的增加而刺激了CLas感染的柑橘的免疫力，但长期（270和330天）重复食草导致[SA]下降，与SA代谢相关基因（BMST和DMR6）的上调同时发生。同样，转录反应和代谢产物（SA及其分析物）在暴露于连续繁殖的D群体的柑橘中积累。柠檬酸在120天时表现出与SA信号相关的基因的短暂上调，而长期木虱（成年和若虫）摄食（270天和330天）后后表达下调。食草在调节中华绒螯蟹成熟叶片中SA积累中起着重要作用，无论这些树木是否同时感染了C Las。我们的研究结果表明，预防由三养相互作用引起的柑橘D. citrior造成的进食伤害可能使柑橘类植物更好地应对C Las感染的后果，从而突出了载体抑制作为管理这种国际性疾病的组成部分的重要性。这些树木是否同时感染了C Las。我们的研究结果表明，预防由三养相互作用引起的柑橘D. citrior造成的进食伤害可能使柑橘类植物更好地应对C Las感染的后果，从而突出了载体抑制作为管理这种国际性疾病的组成部分的重要性。这些树木是否同时感染了C Las。我们的研究结果表明，预防由三养相互作用引起的柑橘D. citrior造成的进食伤害可能使柑橘类植物更好地应对C Las感染的后果，从而突出了载体抑制作为管理这种国际性疾病的组成部分的重要性。