Dataset Information

Red-light is an environmental effector for mutualism between begomovirus and its vector whitefly.

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 ?C1 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 ?C1, 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 ?C1 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.

SUBMITTER: Zhao P

PROVIDER: S-EPMC7822537 | biostudies-literature | 2021 Jan

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

Red-light is an environmental effector for mutualism between begomovirus and its vector whitefly.

Zhao Pingzhi P Zhang Xuan X Gong Yuqing Y Wang Duan D Xu Dongqing D Wang Ning N Sun Yanwei Y Gao Lianbo L Liu Shu-Sheng SS Deng Xing Wang XW Kliebenstein Daniel J DJ Zhou Xueping X Fang Rong-Xiang RX Ye Jian J

PLoS pathogens 20210111 1

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 ...[more]

PMID: 33428670

Similar Datasets

Project description:Apoptosis is generally considered the first line of defense against viral infection. However, the role of apoptosis in the interactions between plant viruses and their insect vectors has rarely been investigated. By studying plant DNA viruses of the genus Begomovirus within the family Geminiviridae, which are transmitted by whiteflies of the Bemisia tabaci species complex in a persistent manner, we revealed that virus-induced apoptosis in insect vectors can facilitate viral accumulation and transmission. We found that infection with tomato yellow leaf curl virus activated the apoptosis pathway in B. tabaci Suppressing apoptosis by inhibitors or silencing caspase-3 significantly reduced viral accumulation, while the activation of apoptosis increased viral accumulation in vivo Moreover, the positive effect of whitefly apoptosis on virus accumulation and transmission was not due to its cross talk with the autophagy pathway that suppresses begomovirus infection in whiteflies. We further showed that viral replication, rather than the viral coat protein, is likely the critical factor in the activation of apoptosis by the virus. These novel findings indicate that similarly to many animal and a few plant RNA viruses, plant DNA viruses may activate apoptosis in their insect vectors leading to enhanced viral accumulation and transmission.IMPORTANCE Of the approximately 1,100 known plant viruses, about one-third are DNA viruses that are vectored by insects. Plant virus infections often induce cellular and molecular responses in their insect vectors, which can, in many cases, affect the spread of viruses. However, the mechanisms underlying vector responses that affect virus accumulation and transmission are poorly understood. Here, we examined the role of virus-induced apoptosis in the transmission of begomoviruses, a group of single-stranded plant DNA viruses that are transmitted by whiteflies and cause extensive damage to many crops worldwide. We demonstrated that virus infection can induce apoptosis in the insect vector conferring protection to the virions from degradation, leading to enhanced viral accumulation and transmission to host plants. Our findings provide valuable clues for designing new strategies to block the transmission of insect-vectored plant viruses, particularly plant DNA viruses.

Project description:BackgroundThe MEAM1 (B biotype) Bemisia tabaci (Gennadius) is one of the most widespread and damaging whitefly cryptic species. Our previous studies discovered that the MEAM1 whitefly indirectly benefits from interactions with the tomato yellow leaf curl China virus (TYLCCNV) via accelerated ovarian development and increased fecundity. However, the physiological mechanism of begomoviruse-infected plants acting on the reproduction of the insect vector was unknown.Methodology/principal findingsBiochemical and molecular properties of vitellogenin (Vg) and vitellin (Vt) were characterized in the MEAM1 whitefly. In addition, kinetics of Vt levels in ovary and Vg levels in hemolymph in different stages were detected using a sandwich ELISA. The level of hemolymph Vg increased rapidly after eclosion. A significantly higher level of hemolymph Vg and ovary Vt were observed in whiteflies feeding on virus-infected tobacco plants than those feeding on uninfected plants. In order to detect the levels of Vg mRNA transcription, complete vitellogenin (Vg) mRNA transcripts of 6474 bp were sequenced. Vg mRNA level in whiteflies feeding on virus-infected plants was higher than those feeding on uninfected plants. However, virus-infection of the whiteflies per se, as demonstrated using an artificial diet system, did not produce significant changes in Vg mRNA level.Conclusions/significanceIn MEAM1 whitefly, increased levels of both vitellin and vitellogenin as well as increased transcription of Vg mRNA are associated with feeding on begomovirus-infected plants, thus providing a mechanism for accelerated vitellogenesis. We conclude that MEAM1 whitefly profits from feeding on begomovirus-infected plants for yolk protein synthesis and uptake, and thereby increases its fecundity. These results not only provide insights into the molecular and physiological mechanisms underlying the elevated reproduction of a whitefly species through its association with a begomovirus-infected plant, but also provide a better understanding of the molecular mechanisms related to whitefly reproduction.

Dataset Information

Red-light is an environmental effector for mutualism between begomovirus and its vector whitefly.

Publications

Red-light is an environmental effector for mutualism between begomovirus and its vector whitefly.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets