Integrative network-centric approach reveals signaling pathways associated with plant resistance and susceptibility to Pseudomonas syringae.
Plant protein kinases form redundant signaling pathways to perceive microbial pathogens and activate immunity. Bacterial pathogens repress cellular immune responses by secreting effectors, some of which bind and inhibit multiple host kinases. To understand how broadly bacterial effectors may bind pr...
| Main Authors: | , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2018-12-01
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| Series: | PLoS Biology |
| Online Access: | https://doi.org/10.1371/journal.pbio.2005956 |
| _version_ | 1819045209156091904 |
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| author | Elizabeth K Brauer George V Popescu Dharmendra K Singh Mauricio Calviño Kamala Gupta Bhaskar Gupta Suma Chakravarthy Sorina C Popescu |
| author_facet | Elizabeth K Brauer George V Popescu Dharmendra K Singh Mauricio Calviño Kamala Gupta Bhaskar Gupta Suma Chakravarthy Sorina C Popescu |
| author_sort | Elizabeth K Brauer |
| collection | DOAJ |
| description | Plant protein kinases form redundant signaling pathways to perceive microbial pathogens and activate immunity. Bacterial pathogens repress cellular immune responses by secreting effectors, some of which bind and inhibit multiple host kinases. To understand how broadly bacterial effectors may bind protein kinases and the function of these kinase interactors, we first tested kinase-effector (K-E) interactions using the Pseudomonas syringae pv. tomato-tomato pathosystem. We tested interactions between five individual effectors (HopAI1, AvrPto, HopA1, HopM1, and HopAF1) and 279 tomato kinases in tomato cells. Over half of the tested kinases interacted with at least one effector, and 48% of these kinases interacted with more than three effectors, suggesting a role in the defense. Next, we characterized the role of select multi-effector-interacting kinases and revealed their roles in basal resistance, effector-triggered immunity (ETI), or programmed cell death (PCD). The immune function of several of these kinases was only detectable in the presence of effectors, suggesting that these kinases are critical when particular cell functions are perturbed or that their role is typically masked. To visualize the kinase networks underlying the cellular responses, we derived signal-specific networks. A comparison of the networks revealed a limited overlap between ETI and basal immunity networks. In addition, the basal immune network complexity increased when exposed to some of the effectors. The networks were used to successfully predict the role of a new set of kinases in basal immunity. Our work indicates the complexity of the larger kinase-based defense network and demonstrates how virulence- and avirulence-associated bacterial effectors alter sectors of the defense network. |
| first_indexed | 2024-12-21T10:24:56Z |
| format | Article |
| id | doaj.art-798bbf3454474370b7d52bc23a153179 |
| institution | Directory Open Access Journal |
| issn | 1544-9173 1545-7885 |
| language | English |
| last_indexed | 2024-12-21T10:24:56Z |
| publishDate | 2018-12-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Biology |
| spelling | doaj.art-798bbf3454474370b7d52bc23a1531792022-12-21T19:07:21ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852018-12-011612e200595610.1371/journal.pbio.2005956Integrative network-centric approach reveals signaling pathways associated with plant resistance and susceptibility to Pseudomonas syringae.Elizabeth K BrauerGeorge V PopescuDharmendra K SinghMauricio CalviñoKamala GuptaBhaskar GuptaSuma ChakravarthySorina C PopescuPlant protein kinases form redundant signaling pathways to perceive microbial pathogens and activate immunity. Bacterial pathogens repress cellular immune responses by secreting effectors, some of which bind and inhibit multiple host kinases. To understand how broadly bacterial effectors may bind protein kinases and the function of these kinase interactors, we first tested kinase-effector (K-E) interactions using the Pseudomonas syringae pv. tomato-tomato pathosystem. We tested interactions between five individual effectors (HopAI1, AvrPto, HopA1, HopM1, and HopAF1) and 279 tomato kinases in tomato cells. Over half of the tested kinases interacted with at least one effector, and 48% of these kinases interacted with more than three effectors, suggesting a role in the defense. Next, we characterized the role of select multi-effector-interacting kinases and revealed their roles in basal resistance, effector-triggered immunity (ETI), or programmed cell death (PCD). The immune function of several of these kinases was only detectable in the presence of effectors, suggesting that these kinases are critical when particular cell functions are perturbed or that their role is typically masked. To visualize the kinase networks underlying the cellular responses, we derived signal-specific networks. A comparison of the networks revealed a limited overlap between ETI and basal immunity networks. In addition, the basal immune network complexity increased when exposed to some of the effectors. The networks were used to successfully predict the role of a new set of kinases in basal immunity. Our work indicates the complexity of the larger kinase-based defense network and demonstrates how virulence- and avirulence-associated bacterial effectors alter sectors of the defense network.https://doi.org/10.1371/journal.pbio.2005956 |
| spellingShingle | Elizabeth K Brauer George V Popescu Dharmendra K Singh Mauricio Calviño Kamala Gupta Bhaskar Gupta Suma Chakravarthy Sorina C Popescu Integrative network-centric approach reveals signaling pathways associated with plant resistance and susceptibility to Pseudomonas syringae. PLoS Biology |
| title | Integrative network-centric approach reveals signaling pathways associated with plant resistance and susceptibility to Pseudomonas syringae. |
| title_full | Integrative network-centric approach reveals signaling pathways associated with plant resistance and susceptibility to Pseudomonas syringae. |
| title_fullStr | Integrative network-centric approach reveals signaling pathways associated with plant resistance and susceptibility to Pseudomonas syringae. |
| title_full_unstemmed | Integrative network-centric approach reveals signaling pathways associated with plant resistance and susceptibility to Pseudomonas syringae. |
| title_short | Integrative network-centric approach reveals signaling pathways associated with plant resistance and susceptibility to Pseudomonas syringae. |
| title_sort | integrative network centric approach reveals signaling pathways associated with plant resistance and susceptibility to pseudomonas syringae |
| url | https://doi.org/10.1371/journal.pbio.2005956 |
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