A viral protein orchestrates rice ethylene signaling to coordinate viral infection and insect vector-mediated transmission

Zhao, Yue; Cao, Xue; Zhong, Wang; Zhou, Shunkang; Li, Zhanbiao; An, Hong; Liu, Xiahua; Wu, Ruifeng; Bohora, Surakshya; Wu, Yan; Liang, Zu‐Pei; Yang, Xin; Zhou, Guohui; Zhang, Tong

doi:10.1016/j.molp.2022.01.006

Cited by 24 publications

(17 citation statements)

References 54 publications

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“…The interactions among host plants, plant viruses, and insect vectors are multiple and complex [ 3 , 27 , 28 ]. Plant virus infection could alter chemical cues and behavioral changes in its host plants and insect vectors that enhance virus epidemic and dispersal [ 4 , 10 , 29 , 30 ].…”

Section: Discussionmentioning

confidence: 99%

“…Plant viruses are most often transmitted by insect vectors including thrips, whiteflies, planthoppers, leafhoppers, and aphids [ 1 ], and they seriously threaten crop yield and lead to major economic losses [ 2 ]. Insect vectors, plant viruses, and host plants form complex multilevel interactions that affect virus dispersal [ 3 ]. For persistent plant viruses transmitted by insect vectors, studies have found that non-viruliferous insect vectors initially preferred virus-infected plants, but once the virus was acquired by the vectors, they showed a predilection for virus-free plants, and this phenomenon may accelerate the outbreak of virus [ 4 ].…”

Section: Introductionmentioning

confidence: 99%

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Virus-Induced Plant Volatiles Promote Virus Acquisition and Transmission by Insect Vectors

Chang

Guo

Ren

et al. 2023

IJMS

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Rice dwarf virus (RDV) is transmitted by insect vectors Nephotettix virescens and Nephotettix cincticeps (Hemiptera: Cicadellidae) that threatens rice yield and results in substantial economic losses. RDV induces two volatiles ((E)-β-caryophyllene (EBC) and 2-heptanol) to emit from RDV-infected rice plants. However, the effects of the two volatiles on the olfactory behavior of both non-viruliferous and viruliferous N. virescens are unknown, and whether the two volatiles could facilitate the spread and dispersal of RDV remains elusive. Combining the methods of insect behavior, chemical ecology, and molecular biology, we found that EBC and 2-heptanol influenced the olfactory behavior of non-viruliferous and viruliferous N. virescens, independently. EBC attracted non-viruliferous N. virescens towards RDV-infected rice plants, promoting virus acquisition by non-viruliferous vectors. The effect was confirmed by using oscas1 mutant rice plants (repressed EBC synthesis), but EBC had no effects on viruliferous N. virescens. 2-heptanol did not attract or repel non-viruliferous N. virescens. However, spraying experiments showed that 2-heptanol repelled viruliferous N. virescens to prefer RDV-free rice plants, which would be conducive to the transmission of the virus. These novel results reveal that rice plant volatiles modify the behavior of N. virescens vectors to promote RDV acquisition and transmission. They will provide new insights into virus–vector–plant interactions, and promote the development of new prevention and control strategies for disease management.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Virus-Induced Plant Volatiles Promote Virus Acquisition and Transmission by Insect Vectors

Chang

Guo

Ren

et al. 2023

IJMS

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“…However, upon RBSDV infection, the induction of OsGSK2 positively regulates the JA antiviral response to RBSDV by promoting the phosphorylation and degradation of OsJAZ4, a repressor of the JA signaling [ 105 ]. During the early stage of SRBSDV infection, SRBSDV P6 activates ethylene signaling via interacting with OsRTH2 in the cytoplasm, thus leading to enhanced SRBSDV proliferation [ 106 ]. These findings imply positive roles of JA and auxin for antiviral defense, but ethylene contributes to virus proliferation.…”

Section: The Complex Interactions Between Rice Viruses and Their Hostsmentioning

confidence: 99%

“…Emerging evidence has proven that rice viruses can manipulate their vectors either directly or by inducing changes in host plants to promote the spread of viral pathogens. For example, during the late infection of SRBSDV in rice plants, SRBSDV P6 enters the nucleus and interacts with OsEIL2 to suppress ethylene signaling by blocking the dimerization of OsEIL2, thus promoting virus spread via attracting the insect vector [ 106 ]. It implies more complex interactions among insect vectors, viruses, and host plants contribute the transmission of viruses by balancing all organizational levels, from molecules to populations.…”

Section: The Complex Interactions Between Rice Viruses and Their Hostsmentioning

confidence: 99%

A Review of Vector-Borne Rice Viruses

Wang

Liu

Lyu

et al. 2022

Viruses

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Rice (Oryza sativa L.) is one of the major staple foods for global consumption. A major roadblock to global rice production is persistent loss of crops caused by plant diseases, including rice blast, sheath blight, bacterial blight, and particularly various vector-borne rice viral diseases. Since the late 19th century, 19 species of rice viruses have been recorded in rice-producing areas worldwide and cause varying degrees of damage on the rice production. Among them, southern rice black-streaked dwarf virus (SRBSDV) and rice black-streaked dwarf virus (RBSDV) in Asia, rice yellow mottle virus (RYMV) in Africa, and rice stripe necrosis virus (RSNV) in America currently pose serious threats to rice yields. This review systematizes the emergence and damage of rice viral diseases, the symptomatology and transmission biology of rice viruses, the arm races between viruses and rice plants as well as their insect vectors, and the strategies for the prevention and control of rice viral diseases.

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“…For instance, the potyviral protein NIa-Pro from turnip mosaic virus (TuMV) resides in the nucleus primarily during infection, but it relocalizes outside of the nucleus to enhance aphid vector fecundity, and inhibits aphid induction of ethylene-dependent defences when expressed in plants [6][7][8]. The viral protein P6 of southern rice black-streaked dwarf virus (SRBSDV) interacts with the rice host transcription factor OsEIL2 and increases vector planthopper attraction to plants expressing P6 [9]. Many other viral proteins also have a similar function, such as the 2b protein from cucumber mosaic virus (CMV), which prevents the degradation of JAZ proteins and the induction of downstream volatiles, increasing aphid vector attraction to infected plants [10,11].…”

Section: Introductionmentioning

confidence: 99%

Engineering aphid transmission of foxtail mosaic virus in the presence of potyvirus helper component proteinase through coat protein modifications

Jiang

Nihranz

et al. 2023

Journal of General Virology

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Biotechnologies that use plant viruses as plant enhancement tools have shown great potential to flexibly engineer crop traits, but field applications of these technologies are still limited by efficient dissemination methods. Potyviruses can be rapidly inoculated into plants by aphid vectors due to the presence of the potyviral helper component proteinase (HC-Pro), which binds to the DAG motif of the coat protein (CP) of the virion. Previously it was determined that a naturally occurring DAG motif in the non-aphid-transmissible potexvirus, potato aucuba mosaic virus (PAMV), is functional when a potyviral HC-Pro is provided to aphids in plants. The DAG motif of PAMV was successfully transferred to the CP of another non-aphid-transmissible potexvirus, potato virus X, to convey aphid transmission capabilities in the presence of HC-Pro. Here, we demonstrate that DAG-containing segments of the CP from two different potyviruses (sugarcane mosaic virus and turnip mosaic virus), and from the previously used potexvirus, PAMV, can make the potexvirus, foxtail mosaic virus (FoMV), aphid-transmissible when fused with the FoMV CP. We show that DAG-containing FoMVs are transmissible by aphids that have prior access to HC-Pro through potyvirus-infected plants or ectopic expression of HC-Pro. The transmission efficiency of the DAG-containing FoMVs varied from less than 10 % to over 70 % depending on the length and composition of the surrounding amino acid sequences of the DAG-containing segment, as well as due to the recipient plant species. Finally, we show that the engineered aphid-transmissible FoMV is still functional as a plant enhancement resource, as endogenous host target genes were silenced in FoMV-infected plants after aphid transmission. These results suggest that aphid transmission could be engineered into non-aphid-transmissible plant enhancement viral resources to facilitate their field applications.

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A viral protein orchestrates rice ethylene signaling to coordinate viral infection and insect vector-mediated transmission

Cited by 24 publications

References 54 publications

Virus-Induced Plant Volatiles Promote Virus Acquisition and Transmission by Insect Vectors

Virus-Induced Plant Volatiles Promote Virus Acquisition and Transmission by Insect Vectors

A Review of Vector-Borne Rice Viruses

Engineering aphid transmission of foxtail mosaic virus in the presence of potyvirus helper component proteinase through coat protein modifications

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