Mp10 and Mp42 from the Aphid Species <i>Myzus persicae</i> Trigger Plant Defenses in <i>Nicotiana benthamiana</i> Through Different Activities

Rodríguez, Patricia; Stam, Remco; Warbroek, Tim; Bos, Jorunn I. B.

doi:10.1094/mpmi-05-13-0156-r

Cited by 99 publications

(86 citation statements)

References 42 publications

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“…It has to be noted that the MpMIFs also induced callose apposition and PR gene expression to some extent in control (cry À) N. benthamiana leaves (Figures 3B and 3C). Dual activities in activating and suppressing host defense responses were also shown for the salivary M. persicae protein of unknown function, Mp10 [3,23].…”

Section: Aphid Mifs Interfere With the Plant Immune Systemmentioning

confidence: 86%

A Secreted MIF Cytokine Enables Aphid Feeding and Represses Plant Immune Responses

et al. 2015

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Aphids attack virtually all plant species and cause serious crop damages in agriculture. Despite their dramatic impact on food production, little is known about the molecular processes that allow aphids to exploit their host plants. To date, few aphid salivary proteins have been identified that are essential for aphid feeding, and their nature and function remain largely unknown. Here, we show that a macrophage migration inhibitory factor (MIF) is secreted in aphid saliva. In vertebrates, MIFs are important pro-inflammatory cytokines regulating immune responses. MIF proteins are also secreted by parasites of vertebrates, including nematodes, ticks, and protozoa, and participate in the modulation of host immune responses. The finding that a plant parasite secretes a MIF protein prompted us to question the role of the cytokine in the plant-aphid interaction. We show here that expression of MIF genes is crucial for aphid survival, fecundity, and feeding on a host plant. The ectopic expression of aphid MIFs in leaf tissues inhibits major plant immune responses, such as the expression of defense-related genes, callose deposition, and hypersensitive cell death. Functional complementation analyses in vivo allowed demonstrating that MIF1 is the member of the MIF protein family that allows aphids to exploit their host plants. To our knowledge, this is the first report of a cytokine that is secreted by a parasite to modulate plant immune responses. Our findings suggest a so-far unsuspected conservation of infection strategies among parasites of animal and plant species.

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Section: Aphid Mifs Interfere With the Plant Immune Systemmentioning

confidence: 86%

A Secreted MIF Cytokine Enables Aphid Feeding and Represses Plant Immune Responses

et al. 2015

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“…Broadly speaking, effectors are proteins or other molecules produced by pathogens or insects that can alter host structures and functions (Hogenhout et al, 2009). Several insect effectors with diverse effects have been identified in aphids in recent years (Bos et al, 2010;Atamian et al, 2013;Rodriguez et al, 2014;Naessens et al, 2015). For example, expression of the aphid protein effector C002 in host plants increases the fecundity of green peach aphid, while another effector, Mp10, reduces aphid fecundity (Bos et al, 2010).…”

mentioning

confidence: 99%

“…For example, expression of the aphid protein effector C002 in host plants increases the fecundity of green peach aphid, while another effector, Mp10, reduces aphid fecundity (Bos et al, 2010). Moreover, transient in planta expression of Mp10 activates jasmonic acid (JA) and salicylic acid (SA) signaling pathways (Rodriguez et al, 2014) and triggers chlorosis in Nicotiana benthamiana (Bos et al, 2010). Similarly, the expression of two candidate effectors, Me10 and Me23, from the potato aphid in host N. benthamiana plants increases aphid fecundity (Atamian et al, 2013), and MpMIF (a MIF cytokine secreted in aphid watery saliva during feeding) plays an important role in aphid survival and can affect both the SA and JA signaling pathways (Naessens et al, 2015).…”

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confidence: 99%

A Mucin-Like Protein of Planthopper Is Required for Feeding and Induces Immunity Response in Plants

et al. 2017

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The brown planthopper, Nilaparvata lugens, is a pest that threatens rice (Oryza sativa) production worldwide. While feeding on rice plants, planthoppers secrete saliva, which plays crucial roles in nutrient ingestion and modulating plant defense responses, although the specific functions of salivary proteins remain largely unknown. We identified an N. lugens-secreted mucin-like protein (NlMLP) by transcriptome and proteome analyses and characterized its function, both in brown planthopper and in plants. NlMLP is highly expressed in salivary glands and is secreted into rice during feeding. Inhibition of NlMLP expression in planthoppers disturbs the formation of salivary sheaths, thereby reducing their performance. In plants, NlMLP induces cell death, the expression of defense-related genes, and callose deposition. These defense responses are related to Ca 2+ mobilization and the MEK2 MAP kinase and jasmonic acid signaling pathways. The active region of NlMLP that elicits plant responses is located in its carboxyl terminus. Our work provides a detailed characterization of a salivary protein from a piercing-sucking insect other than aphids. Our finding that the protein functions in plant immune responses offers new insights into the mechanism underlying interactions between plants and herbivorous insects.

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“…Other host targets include JAZ proteins involved in JA-signaling, which are targeted by both bacterial and fungal effectors (Jiang et al, 2013;Plett et al, 2014), but also the host proteasome (Groll et al, 2008;Üstün et al, 2013), extracellular proteases (Song et al, 2009), and the cytoskeleton and secretion pathways (Bozkurt et al, 2011;Lee et al, 2012). Also, aphids alter host physiology as reflected by their ability to affect nutrient allocation (Sandström et al, 2000;Girousse et al, 2005) and to suppress defense responses (Bos et al, 2010b;Elzinga and Jander, 2013;Rodriguez et al, 2014). With parallels emerging between plant microbe infection and aphid infestation strategies, it is likely that aphid effectors also target important host cell processes to promote virulence-or effector-triggered susceptibility (Rodriguez and Bos, 2013).…”

mentioning

confidence: 99%

An Aphid Effector Targets Trafficking Protein VPS52 in a Host-Specific Manner to Promote Virulence

2017

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Plant-and animal-feeding insects secrete saliva inside their hosts, containing effectors, which may promote nutrient release and suppress immunity. Although for plant pathogenic microbes it is well established that effectors target host proteins to modulate host cell processes and promote disease, the host cell targets of herbivorous insects remain elusive. Here, we show that the existing plant pathogenic microbe effector paradigm can be extended to herbivorous insects in that effector-target interactions inside host cells modify critical host processes to promote plant susceptibility. We showed that the effector Mp1 from Myzus persicae associates with the host Vacuolar Protein Sorting Associated Protein52 (VPS52). Using natural variants, we provide a strong link between effector virulence activity and association with VPS52, and show that the association is highly specific to M. persicae-host interactions. Also, coexpression of Mp1, but not Mp1-like variants, specifically with host VPS52s resulted in effector relocalization to vesicle-like structures that associate with prevacuolar compartments. We show that high VPS52 levels negatively impact virulence, and that aphids are able to reduce VPS52 levels during infestation, indicating that VPS52 is an important virulence target. Our work is an important step forward in understanding, at the molecular level, how a major agricultural pest promotes susceptibility during infestation of crop plants. We give evidence that an herbivorous insect employs effectors that interact with host proteins as part of an effective virulence strategy, and that these effectors likely function in a species-specific manner.

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Mp10 and Mp42 from the Aphid Species Myzus persicae Trigger Plant Defenses in Nicotiana benthamiana Through Different Activities

Cited by 99 publications

References 42 publications

A Secreted MIF Cytokine Enables Aphid Feeding and Represses Plant Immune Responses

A Secreted MIF Cytokine Enables Aphid Feeding and Represses Plant Immune Responses

A Mucin-Like Protein of Planthopper Is Required for Feeding and Induces Immunity Response in Plants

An Aphid Effector Targets Trafficking Protein VPS52 in a Host-Specific Manner to Promote Virulence

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