Integrated Analysis of the miRNAome and Transcriptome Reveals miRNA–mRNA Regulatory Networks in Catharanthus roseus Through Cuscuta campestris-Mediated Infection With “Candidatus Liberibacter asiaticus”

Abstract

Citrus Huanglongbing (HLB) is the most devastating disease of citrus caused by the Gram-negative phloem-limited bacterium “Candidatus Liberibacter asiaticus” (CLas). It can be transmitted by the Asian citrus psyllid “Diaphorina citri,” by grafting, and by the holoparasitic dodder. In this study, the non-natural host periwinkle (Catharanthus roseus) was infected via dodder (Cuscuta campestris) from CLas-infected citrus plants, and the asymptomatic leaves (AS) were subjected to transcriptomic and small-RNA profiling. The results were analyzed together with a transcriptome dataset from the NCBI repository that included leaves for which symptoms had just occurred (S) and yellowing leaves (Y). There were 3,675 differentially expressed genes (DEGs) identified in AS, and 6,390 more DEGs in S and further 2109 DEGs in Y. These DEGs were commonly enriched in photosystem, chloroplast, membrane, oxidation-reduction process, metal/zinc ion binding on GO. A total of 14,974 DEGs and 336 DE miRNAs (30 conserved and 301 novel) were identified. Through weighted gene co-expression network and nested network analyses, two critical nested miRNA–mRNA regulatory networks were identified with four conserved miRNAs. The primary miR164-NAC1 network is potentially involved in plant defense responses against CLas from the early infection stage to symptom development. The secondary network revealed the regulation of secondary metabolism and nutrient homeostasis through miR828-MYB94/miR1134-HSF4 and miR827-ATG8 regulatory networks, respectively. The findings discovered new potential mechanisms in periwinkle–CLas interactions, and its confirmation can be done in citrus–CLas system later on. The advantages of periwinkle plants in facilitating the quick establishment and greater multiplication of CLas, and shortening latency for disease symptom development make it a great surrogate for further studies, which could expedite our understanding of CLas pathogenesis.

Pathogenicity and Transcriptomic Analyses of Two “ Candidatus Liberibacter asiaticus” Strains Harboring Different Types of Phages

“…Liberibacter asiaticus” pathogenic effectors ( 14 ), and analyses of “ Ca . Liberibacter asiaticus”-host interaction ( 15 , 16 ).…”

Bidirectional mRNA transfer between Cuscuta australis and its hosts

“…Given the rapid establishment and multiplication of CLas, and shortening latency for symptoms development induced by CLas, periwinkle is commonly used for studies of CLas ( Zheng et al, 2014 ; Li et al, 2021 ; Killiny, 2022 ). A recent study found that the miRNA–mRNA regulatory mechanism involved in plant defense responses, regulation of secondary metabolism, and nutrient homeostasis plays an important role in periwinkle–CLas interaction ( Zeng et al, 2022 ). In addition to acting as a transmission tool for CLas, dodder can be also used as an appropriate plant host for CLas multiplication ( Li et al, 2021 ).…”

Candidatus Liberibacter solananearum-tomato as an experimental system for the study of genes associated with Huanglongbing in Mexican lime

“…A pesar de los esfuerzos por mitigar la enfermedad, hasta la fecha no hay variedades con resistencia real, ni tratamientos efectivos para eliminar el HLB en ninguna especie de cítricos (Gao et al, 2018). Por ello, se han buscado estrategias para elucidar el mecanismo regulatorio de la enfermedad, siendo las aproximaciones "ómicas" (genómica, transcriptómica, metabolómica) las más utilizadas en los últimos años (Ventura-Medina et al, 2019;Zeng et al, 2022). Con la ayuda de tecnologías como RNA-Seq, actualmente es posible caracterizar el transcriptoma de plantas de manera rápida y con una mayor sensibilidad, lo que ha supuesto un cambio relevante en el estudio de plantas no modelo ante el estrés biótico y abiótico.…”