Viral effector protein manipulates host hormone signaling to attract insect vectors

Wu, Dewei; Qi, Tiancong; Li, Wanxiang; Tian, Hao; Gao, Hua; Wang, Jiaojiao; Ge, Jin; Yao, Ruifeng; Ren, Chunmei; Wang, Xianbing; Liu, Yule; Kang, Le; Ding, Shou‐Wei; Xie, Daoxin

doi:10.1038/cr.2017.2

Cited by 126 publications

(110 citation statements)

References 50 publications

(91 reference statements)

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“…HIS-JAZb and HIS-JAZi degradation assays were performed as described (85). Flowers in the early floral stage of each genotype were used for crude protein extraction.…”

Section: Methodsmentioning

confidence: 99%

Flower-specific jasmonate signaling regulates constitutive floral defenses in wild tobacco

Wang

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Optimal defense (OD) theory predicts that within a plant, tissues are defended in proportion to their fitness value and risk of predation. The fitness value of leaves varies greatly and leaves are protected by jasmonate (JA)-inducible defenses. Flowers are vehicles of Darwinian fitness in flowering plants and are attacked by herbivores and pathogens, but how they are defended is rarely investigated. We used Nicotiana attenuata, an ecological model plant with well-characterized herbivore interactions to characterize defense responses in flowers. Early floral stages constitutively accumulate greater amounts of two well-characterized defensive compounds, the volatile (E)-α-bergamotene and trypsin proteinase inhibitors (TPIs), which are also found in herbivore-induced leaves. Plants rendered deficient in JA biosynthesis or perception by RNA interference had significantly attenuated floral accumulations of defensive compounds known to be regulated by JA in leaves. By RNA-seq, we found a JAZ gene, NaJAZi, specifically expressed in early-stage floral tissues. Gene silencing revealed that NaJAZi functions as a flower-specific jasmonate repressor that regulates JAs, (E)-α-bergamotene, TPIs, and a defensin. Flowers silenced in NaJAZi are more resistant to tobacco budworm attack, a florivore. When the defensin was ectopically expressed in leaves, performance of Manduca sexta larvae, a folivore, decreased. NaJAZi physically interacts with a newly identified NINJA-like protein, but not the canonical NINJA. This NINJA-like recruits the corepressor TOPLESS that contributes to the suppressive function of NaJAZi on floral defenses. This study uncovers the defensive function of JA signaling in flowers, which includes components that tailor JA signaling to provide flower-specific defense

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“…HIS-JAZb and HIS-JAZi degradation assays were performed as described (85). Flowers in the early floral stage of each genotype were used for crude protein extraction.…”

Section: Methodsmentioning

confidence: 99%

Flower-specific jasmonate signaling regulates constitutive floral defenses in wild tobacco

Wang

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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“…However, it did not change the attraction of M. persicae as a virus vector, but increased its feeding time on plant. By contrast, protein 2b increased immigration of M. persicae to infected Arabidopsis plants, but decreased its settling on virus-infected plants (Wu et al, 2017). Groen et al (2017) proposed that nonpersistent virus has two transmission types in different plant hosts.…”

Section: Cucumber Mosaic Virus and Barley Yellow Dwarf Luteovirus (Vimentioning

confidence: 99%

“…JA is the main hormone that regulates volatile biosynthesis in plants (Arimura & Pearse, 2017). Therefore, invaders use several strategies to control JA signaling and subsequent volatile emissions in plants (Krumm et al, 1995;Wu et al, 2017). JASMONATE ZIM DOMAIN (JAZ) is a key target of microbes in their effort to induce or suppress JA-dependent volatile biosynthesis.…”

Section: Microbe-induced Signaling Cascades Conciliate Plant Volatilementioning

confidence: 99%

“…JAZ represses JA-dependent genes, but JA activation by external stimuli causes JAZ to be degraded by the 26S proteasome (Wasternack & Hause, 2013). The degradation of JAZ releases JA-dependent transcription factors from JA-dependent genes such as volatile synthase genes, allowing them to be expressed (Taniguchi et al, 2014b;Wu et al, 2017). Some pathogens actively target JAZ to modify plant volatile emissions.…”

Section: Microbe-induced Signaling Cascades Conciliate Plant Volatilementioning

confidence: 99%

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Microbe‐induced plant volatiles

2017

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Plants emit a plethora of volatile organic compounds in response to biotic and abiotic stresses. These compounds act as infochemicals for ecological communication in the phytobiome. This study reviews the role of microbe-induced plant volatiles (MIPVs) in plant-microbe interactions. MIPVs are affected by the taxonomic position of the microbe, the identity of the plant and the type of interaction. Plants also emit exclusive blends of volatiles in response to nonhost and host interactions, as well as to beneficial microbes and necrotrophic/biotrophic pathogens. These MIPVs directly inhibit pathogen growth and indirectly promote resistance/susceptibility to subsequent plant pathogen attack. Viruses and phloem-limiting bacteria modify plant volatiles to attract insect vectors. Susceptible plants can respond to MIPVs from resistant plants and become resistant. Recent advances in our understanding of the molecular mechanisms of MIPV synthesis in plants and how plant pathogen effectors manipulate their biosynthesis are discussed. This knowledge will help broaden our understanding of plant-microbe interactions and should facilitate the development of new emerging techniques for sustainable plant disease management.

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“…The rationale is that better insect survival will increase the number of vectors loaded with virus, thus promoting virus transmission. One example of a pathogen effector is CMV protein 2b that tampers with jasmonic acid signaling (Lewsey et al, 2010) to possibly promote aphid infestation and transmission (Ziebell et al, 2011;Wu et al, 2017). In another example, Casteel et al (2014) demonstrated that TuMV infection suppresses callose deposition and increases aphid fecundity on tobacco and Arabidopsis plants.…”

Section: Plant Defense-related Pathways Involved In Virus Transmissionmentioning

confidence: 99%

Insect transmission of plant viruses: Multilayered interactions optimize viral propagation

et al. 2017

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By serving as vectors of transmission, insects play a key role in the infection cycle of many plant viruses. Viruses use sophisticated transmission strategies to overcome the spatial barrier separating plants and the impediment imposed by the plant cell wall. Interactions among insect vectors, viruses, and host plants mediate transmission by integrating all organizational levels, from molecules to populations. Best-examined on the molecular scale are two basic transmission modes wherein virus-vector interactions have been well characterized. Whereas association of virus particles with specific sites in the vector's mouthparts or in alimentary tract regions immediately posterior to them is required for noncirculative transmission, the cycle of particles through the vector body is necessary for circulative transmission. Virus transmission is also determined by interactions that are associated with changes in vector feeding behaviors and with alterations in plant host's morphology and/or metabolism that favor the attraction or deterrence of vectors. A recent concept in virus-host-vector interactions proposes that when vectors land on infected plants, vector elicitors and effectors "inform" the plants of the confluence of interacting entities and trigger signaling pathways and plant defenses. Simultaneously, the plant responses may also influence virus acquisition and inoculation by vectors. Overall, a picture is emerging where transmission depends on multilayered virus-vector-host interactions that define the route of a virus through the vector, and on the manipulation of the host and the vector. These interactions guarantee virus propagation until one or more of the interactants undergo changes through evolution or are halted by environmental interventions.

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Viral effector protein manipulates host hormone signaling to attract insect vectors

Cited by 126 publications

References 50 publications

Flower-specific jasmonate signaling regulates constitutive floral defenses in wild tobacco

Flower-specific jasmonate signaling regulates constitutive floral defenses in wild tobacco

Microbe‐induced plant volatiles

Insect transmission of plant viruses: Multilayered interactions optimize viral propagation

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