Abstract
Environments such as light condition influence the spread of infectious diseases by affecting insect vector behavior. However, whether and how light affects the host defense which further affects insect preference and performance, remains unclear, nor has been demonstrated how pathogens co-adapt light condition to facilitate vector transmission. We previously showed that begomoviral βC1 inhibits MYC2-mediated jasmonate signaling to establish plant-dependent mutualism with its insect vector. Here we show red-light as an environmental catalyzer to promote mutualism of whitefly-begomovirus by stabilizing βC1, which interacts with PHYTOCHROME-INTERACTING FACTORS (PIFs) transcription factors. PIFs positively control plant defenses against whitefly by directly binding to the promoter of terpene synthase genes and promoting their transcription. Moreover, PIFs interact with MYC2 to integrate light and jasmonate signaling and regulate the transcription of terpene synthase genes. However, begomovirus encoded βC1 inhibits PIFs' and MYC2' transcriptional activity via disturbing their dimerization, thereby impairing plant defenses against whitefly-transmitted begomoviruses. Our results thus describe how a viral pathogen hijacks host external and internal signaling to enhance the mutualistic relationship with its insect vector.
Highlights
Climate change affects the emergence and spread of vector-borne infectious disease such as malaria, West Nile virus, Zika virus, and viral disease in staple crops via many ways [1,2]
Red-light is essential for mutualism between virus and its vector herbivore found in Genebank/EMBL or The Arabidopsis Information Resource under the following accession numbers: AtPIF1 (AT2G20180), AtPIF3 (AT1G09530), AtPIF4 (AT2G43010), AtPIF5 (AT3G59060), AtMYC2 (At1G32640), AtTPS10 (At2G24210), AtTPS14 (AT1G61680), AtTPS21 (AT5G23960), Tomato yellow leaf curl China virus (TYLCCNV) βC1 (AJ421621).Whiteflies were collected in the field in Chaoyang District, Beijing, China and were identified as Bemisia tabaci MEAM1, B biotype
To detect whether light affects the natural begomoviral transmission process, we performed whitefly two-choice experiments using Nicotiana benthamiana (Nb) plants and Nb plants infected with TYLCCNV and its associated betasatellite (TYLCCNB) (TA+β) in white light and dark conditions (Fig 1A)
Summary
Climate change affects the emergence and spread of vector-borne infectious disease such as malaria, West Nile virus, Zika virus, and viral disease in staple crops via many ways [1,2]. The distribution and population size of disease vectors can be heavily affected by local climate and light conditions. Besides of direct effecting fitness of their vectors, plant pathogens confer indirect effects on their vectors often by manipulating the plant defenses against the vector, e.g. volatile chemical components. These volatile substances act as olfactory clues, and host-finding cues, defensive substances even sex pheromones [6,7]. Many of insect-borne plant pathogens, e.g. arboviruses of the families Geminiviridae, are capable of achieving indirect mutualistic relationships with vectors via their shared host plant [8,9,10]
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