A host-pathogen interactome uncovers phytopathogenic strategies to manipulate plant ABA responses.
Abscisic Acid
/ metabolism
Arabidopsis
/ genetics
Arabidopsis Proteins
/ genetics
Bacterial Proteins
/ genetics
Gene Expression Regulation
/ drug effects
Host-Pathogen Interactions
/ drug effects
Plant Diseases
/ genetics
Plant Growth Regulators
/ metabolism
Protein Interaction Maps
/ drug effects
Pseudomonas syringae
/ genetics
Virulence
/ genetics
Arabidopsis thaliana
Nicotiana benthamiana
Pseudomonas syringae
ERF transcriptions factors
ERF8
abscisic acid
interactome
type III effectors
Journal
The Plant journal : for cell and molecular biology
ISSN: 1365-313X
Titre abrégé: Plant J
Pays: England
ID NLM: 9207397
Informations de publication
Date de publication:
10 2019
10 2019
Historique:
received:
05
04
2018
revised:
05
04
2018
accepted:
22
05
2019
pubmed:
31
5
2019
medline:
1
7
2020
entrez:
1
6
2019
Statut:
ppublish
Résumé
The phytopathogen Pseudomonas syringae delivers into host cells type III secreted effectors (T3SEs) that promote virulence. One virulence mechanism employed by T3SEs is to target hormone signaling pathways to perturb hormone homeostasis. The phytohormone abscisic acid (ABA) influences interactions between various phytopathogens and their plant hosts, and has been shown to be a target of P. syringae T3SEs. In order to provide insight into how T3SEs manipulate ABA responses, we generated an ABA-T3SE interactome network (ATIN) between P. syringae T3SEs and Arabidopsis proteins encoded by ABA-regulated genes. ATIN consists of 476 yeast-two-hybrid interactions between 97 Arabidopsis ABA-regulated proteins and 56 T3SEs from four pathovars of P. syringae. We demonstrate that T3SE interacting proteins are significantly enriched for proteins associated with transcription. In particular, the ETHYLENE RESPONSIVE FACTOR (ERF) family of transcription factors is highly represented. We show that ERF105 and ERF8 displayed a role in defense against P. syringae, supporting our overall observation that T3SEs of ATIN converge on proteins that influence plant immunity. In addition, we demonstrate that T3SEs that interact with a large number of ABA-regulated proteins can influence ABA responses. One of these T3SEs, HopF3
Substances chimiques
Arabidopsis Proteins
0
Bacterial Proteins
0
Plant Growth Regulators
0
Abscisic Acid
72S9A8J5GW
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
187-198Informations de copyright
© 2019 The Authors The Plant Journal © 2019 John Wiley & Sons Ltd.
Références
Abramovitch, R.B., Kim, Y.J., Chen, S., Dickman, M.B. and Martin, G.B. (2003) Pseudomonas type III effector AvrPtoB induces plant disease susceptibility by inhibition of host programmed cell death. EMBO J. 22, 60-69.
Allu, A.D., Brotman, Y., Xue, G.P. and Balazadeh, S. (2016) Transcription factor ANAC032 modulates JA/SA signalling in response to Pseudomonas syringae infection. EMBO Rep. 17, 1578-1589.
Anandalakshmi, R., Pruss, G.J., Ge, X., Marathe, R., Mallory, A.C., Smith, T.H. and Vance, V.B. (1998) A viral suppressor of gene silencing in plants. Proc. Natl Acad. Sci. USA 95, 13 079-13 084.
Bolt, S., Zuther, E., Zintl, S., Hincha, D.K. and Schmülling, T. (2017) ERF105 is a transcription factor gene of Arabidopsis thaliana required for freezing tolerance and cold acclimation. Plant Cell Environ. 40, 108-120.
Buttner, D. (2016) Behind the lines-actions of bacterial type III effector proteins in plant cells. FEMS Microbiol. Rev. 40, 894-937.
Canonne, J. and Rivas, S. (2012) Bacterial effectors target the plant cell nucleus to subvert host transcription. Plant Signal. Behav. 7, 217-221.
Cao, F.Y., Yoshioka, K. and Desveaux, D. (2011) The roles of ABA in plant-pathogen interactions. J. Plant. Res. 124, 489-499.
Cao, F.Y., DeFalco, T.A., Moeder, W. et al. (2018) Arabidopsis ETHYLENE RESPONSE FACTOR 8 (ERF8) has dual functions in ABA signalling and immunity. BMC Plant Biol. 18, 211-227.
Chang, J.H., Urbach, J.M., Law, T.F., Arnold, L.W., Hu, A., Gombar, S., Grant, S.R., Ausubel, F.M. and Dangl, J.L. (2005) A high-throughput, near-saturating screen for type III effector genes from Pseudomonas syringae. Proc. Natl Acad. Sci. USA 102, 2549-2554.
Clough, S.J. and Bent, A.F. (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
Coll, N.S., Epple, P. and Dangl, J.L. (2011) Programmed cell death in the plant immune system. Cell Death Differ. 18, 1247-1256.
Couto, D. and Zipfel, C. (2016) Regulation of pattern recognition receptor signalling in plants. Nat. Rev. Immunol. 16, 537-552.
Ding, Y., Dommel, M. and Mou, Z. (2016) Abscisic acid promotes proteasome-mediated degradation of the transcription coactivator NPR1 in Arabidopsis thaliana. Plant J. 86, 20-34.
Dong, S., Lau, V., Song, R. et al. (2019) Proteome-wide, structure-based prediction of protein-protein interactions/New molecular interactions viewer. Plant Physiology. 179, 1893-1907.
Earley, K.W., Haag, J.R., Pontes, O., Opper, K., Juehne, T., Song, K. and Pikaard, C.S. (2006) Gateway-compatible vectors for plant functional genomics and proteomics. Plant J. 45, 616-629.
Fan, J., Hill, L., Crooks, C., Doerner, P. and Lamb, C. (2009) Abscisic acid has a key role in modulating diverse plant-pathogen interactions. Plant Physiol. 150, 1750-1761.
Finkelstein, R.R. and Lynch, T.J. (2000) Abscisic acid inhibition of radicle emergence but not seedling growth is suppressed by sugars. Plant Physiol. 122, 1179-1186.
Fuglsang, A.T., Guo, Y., Cuin, T.A. et al. (2007) Arabidopsis protein kinase PKS5 inhibits the plasma membrane H+-ATPase by preventing interaction with 14-3-3 protein. Plant Cell, 19, 1617-1634.
Goel, A.K., Lundberg, D., Torres, M.A., Matthews, R., Akimoto-Tomiyama, C., Farmer, L., Dangl, J.L. and Grant, S.R. (2008) The Pseudomonas syringae type III effector HopAM1 enhances virulence on water-stressed plants. Mol. Plant Microbe Interact. 21, 361-370.
Goritschnig, S., Weihmann, T., Zhang, Y.L., Fobert, P., McCourt, P. and Li, X. (2008) A novel role for protein farnesylation in plant innate immunity. Plant Physiol. 148, 348-357.
Guttman, D.S., Vinatzer, B.A., Sarkar, S.F., Ranall, M.V. and Greenberg, J.T. (2002) A functional screen for the type III (Hrp) secretome of the plant pathogen Pseudomonas syringae. Science 295, 1722-1726.
Hillmer, R.A., Tsuda, K., Rallapalli, G., Asai, S., Truman, W., Papke, M.D., Sakakibara, H., Jones, J.D.G., Myers, C.L. and Katagiri, F. (2017) The highly buffered Arabidopsis immune signaling network conceals the functions of its components. PLoS Genet. 13, e1006639.
Ho, Y., Tan, C.M., Li, M., Lin, H., Deng, W. and Yang, J. (2013) The AvrB _ AvrC domain of AvrXccC of Xanthomonas campestris pv. campestris is required to elicit plant defense responses and manipulate ABA homeostasis. Mol. Plant Microbe Interact. 26, 419-430.
Huang, P.Y., Catinot, J. and Zimmerli, L. (2016) Ethylene response factors in Arabidopsis immunity. J. Exp. Bot. 67, 1231-1241.
Hurley, B., Subramaniam, R., Guttman, D.S. and Desveaux, D. (2014) The Pseudomonas syringae type III effector HopF2 suppresses Arabidopsis stomatal immunity. PLoS ONE 9, e114921.
Huysmans, M., Lema, A.S., Coll, N.S. and Nowack, M.K. (2017) Dying two deaths - programmed cell death regulation in development and disease. Curr. Opin. Plant Biol. 35, 37-44.
Jacomy, M., Venturini, T., Heymann, S. and Bastian, M. (2014) ForceAtlas2, a continuous graph layout algorithm for handy network visualization designed for the Gephi Software. PLoS ONE 9, e98679.
Jamir, Y., Guo, M., Oh, H.S., Petnicki-Ocwieja, T., Chen, S., Tang, X., Dickman, M.B., Collmer, A. and Alfano, J.R. (2004) Identification of Pseudomonas syringae type III effectors that can suppress programmed cell death in plants and yeast. Plant J. 37, 554-565.
Johansen, L.K. and Carrington, J.C. (2001) Silencing on the spot. Induction and suppression of RNA silencing in the Agrobacterium-mediated transient expression system. Plant Physiol. 126, 930-938.
Johnson, C.D., Chary, S.N., Chernoff, E.A., Zeng, Q., Running, M.P. and Crowell, D.N. (2005) Protein geranylgeranyltransferase I is involved in specific aspects of abscisic acid and auxin signaling in Arabidopsis. Plant Physiol. 139, 722-733.
Jones, J.D.G., Vance, R.E. and Dangl, J.L. (2016) Intracellular innate immune surveillance devices in plants and animals. Science 354, aaf6395.
Kay, S., Hahn, S., Marois, E., Hause, G. and Bonas, U. (2007) A bacterial effector acts as a plant transcription factor and induces a cell size regulator. Science, 318, 648-651.
Kazan, K. and Lyons, R. (2014) Intervention of phytohormone pathways by pathogen effectors. Plant Cell, 26, 2285-2309.
Khan, M., Seto, D., Subramaniam, R. and Desveaux, D. (2018) Oh, the places they'll go! A survey of phytopathogen effectors and their host targets. Plant J. 93, 651-663.
König, K., Vaseghi, M.J., Dreyer, A. and Dietz, K.J. (2018) The significance of glutathione and ascorbate in modulating the retrograde high light response in Arabidopsis thaliana leaves. Physiol. Plant. 162, 262-273.
de Lange, O., Schreiber, T., Schandry, N., Radeck, J., Braun, K.H., Koszinowski, J., Heuer, H., Strauß, A. and Lahaye, T. (2013) Breaking the DNA-binding code of Ralstonia solanacearum TAL effectors provides new possibilities to generate plant resistance genes against bacterial wilt disease. New Phytol. 199, 773-786.
Lee, S.J., Jung, H.J., Kang, H. and Kim, S.Y. (2012) Arabidopsis zinc finger proteins AtC3H49/AtTZF3 and AtC3H20/AtTZF2 are involved in ABA and JA responses. Plant Cell Physiol. 53, 673-686.
Lewis, J.D., Guttman, D.S. and Desveaux, D. (2009) The targeting of plant cellular systems by injected type III effector proteins. Semin. Cell Dev. Biol. 20, 1055-1063.
Lim, C.W. and Lee, S.C. (2015) Arabidopsis abscisic acid receptors play an important role in disease resistance. Plant Mol. Biol. 88, 313-324.
Lim, C.W., Luan, S. and Lee, S.C. (2014) A prominent role for RCAR3-mediated ABA signaling in response to Pseudomonas syringae pv. tomato DC3000 infection in Arabidopsis. Plant Cell Physiol. 55, 1691-1703.
Liu, J., Elmore, J.M., Fuglsang, A.T., Palmgren, M.G., Staskawicz, B.J. and Coaker, G. (2009) RIN4 functions with plasma membrane H+-ATPases to regulate stomatal apertures during pathogen attack. PLoS Biol. 7, e1000139.
Lo, T., Koulena, N., Seto, D., Guttman, D.S. and Desveaux, D. (2016) The HopF family of Pseudomonas syringae type III secreted effectors. Mol. Plant Pathol. 8, 457-468.
Lumba, S., Toh, S., Handfield, L.F. et al. (2014) A mesoscale abscisic acid hormone interactome reveals a dynamic signaling landscape in Arabidopsis. Dev. Cell, 29, 360-372.
Ma, K.-W., Flores, C. and Ma, W. (2011) Chromatin configuration as a battlefield in plant-bacteria interactions. Plant Physiol. 157, 535-543.
Macho, A.P., Zumaquero, A., Goanzalez-Plaza, J.J., Ortiz-Martin, J., Rufián, J.S. and Beuzón, C.R. (2012) Genetic analysis of the individual contribution to virulence of the type III effector inventory of Pseudomonas syringae pv. phaseolicola. PLoS One, 7, e35871.
Mang, H.G., Qian, W.Q., Zhu, Y., Qian, J., Kang, H.G., Klessig, D.F. and Hua, J. (2012) Abscisic acid deficiency antagonizes high-temperature inhibition of disease resistance through enhancing nuclear accumulation of resistance proteins SNC1 and RPS4 in Arabidopsis. Plant Cell, 24, 1271-1284.
Melotto, M., Underwood, W., Koczan, J., Nomura, K. and He, S.Y. (2006) Plant stomata function in innate immunity against bacterial invasion. Cell, 126, 969-980.
Meng, X., Xu, J., He, Y., Yang, K.-Y., Mordorski, B., Liu, Y. and Zhang, S. (2013) Phosphorylation of an ERF transcription factor by Arabidopsis MPK3/MPK6 regulates plant defense gene induction and fungal resistance. Plant Cell, 25, 1126-1142.
Moffat, C.S., Ingle, R.A., Wathugala, D.L., Saunders, N.J., Knight, H. and Knight, M.R. (2012) ERF5 and ERF6 play redundant roles as positive regulators of JA/Et-mediated defense against Botrytis cinerea in Arabidopsis. PLoS ONE 7, e35995.
Mukhtar, M.S., Carvunis, A.-R., Dreze, M. et al. (2011) Independently evolved virulence effectors converge onto hubs in a plant immune system network. Science 333, 596-601.
Mukhtar, M.S., Mccormack, M.E., Argueso, C.T. and Pajerowska-Mukhtar, K.M. (2016) Pathogen tactics to manipulate plant cell death. Curr. Biol. 26, R608-R619.
Sarris, P.F., Duxbury, Z., Huh, S.U. et al. (2015) A plant immune receptor detects pathogen effectors that target WRKY transcription factors. Cell, 161, 1089-1100.
Schandry, N., de Lange, O., Prior, P. and Lahaye, T. (2016) TALE-like effectors are an ancestral feature of the Ralstonia solanacearum species complex and converge in DNA targeting specificity. Front Plant Sci. 7, 1225.
Shigenaga, A.M. and Argueso, C.T. (2016) No hormone to rule them all: interactions of plant hormones during the responses of plants to pathogens. Semin. Cell Dev. Biol. 56, 174-189.
Singh, N., Swain, S., Singh, A. and Nandi, A.K. (2018) AtOZF1 positively regulates defense against bacterial pathogens and NPR1-independent salicylic acid signaling. Mol. Plant Microbe Interact. 31, 323-333.
Son, G.H., Wan, J., Kim, H.J., Nguyen, X.C., Chung, W.S., Hong, J.C. and Stacey, G. (2012) Ethylene-responsive element-binding factor 5, ERF5, is involved in chitin-induced innate immunity response. Mol. Plant Microbe Interact. 25, 48-60.
Spoel, S.H. and Dong, X. (2008) Making sense of hormone crosstalk during plant immune responses. Cell Host Microbe 3, 348-351.
Swain, S., Singh, N. and Nandi, A.K. (2015) Identification of plant defence regulators through transcriptional profiling of Arabidopsis thaliana cdd1 mutant. J Biosci. 40, 137-146.
de Torres-Zabala, M., Truman, W., Bennett, M.H., Lafforgue, G., Mansfield, J.W., Rodriguez Egea, P., Bögre, L., Grant, M. and Egea, P.R. (2007) Pseudomonas syringae pv. tomato hijacks the Arabidopsis abscisic acid signalling pathway to cause disease. EMBO J. 26, 1434-1443.
Van den Broeck, L., Dubois, M., Vermeersch, M., Storme, V., Matsui, M. and Inzé, D. (2017) From network to phenotype: the dynamic wiring of an Arabidopsis transcriptional network induced by osmotic stress. Mol. Syst. Biol. 13, 961.
Vishwakarma, K., Upadhyay, N., Kumar, N. et al. (2017) Abscisic acid signaling and abiotic stress tolerance in plants: a review on current knowledge and future prospects. Front. Plant Sci. 8, 161.
Vogel, M.O., Moore, M., König, K., Pecher, P., Alsharafa, K., Lee, J. and Dietz, K.J. (2014) Fast retrograde signaling in response to high light involves metabolite export, MITOGEN-ACTIVATED PROTEIN KINASE6, and AP2/ERF transcription factors in Arabidopsis. Plant Cell, 26, 1151-1165.
Wang, Y., Li, J., Hou, S., Wang, X., Li, Y., Ren, D., Chen, S., Tang, X. and Zhou, J.-M. (2010) A Pseudomonas syringae ADP-ribosyltransferase inhibits Arabidopsis mitogen-activated protein kinase kinases. Plant Cell, 22, 2033-2044.
Waese, J., Fan, J., Pasha, A. et al. (2017) ePlant: Visualizing and exploring multiple levels of data for hypothesis generation in plant biology. The Plant Cell, 29, 1806-1821.
Weßling, R., Epple, P., Altmann, S. et al. (2015) Convergent targeting of a common host protein-network by pathogen effectors from three kingdoms of life. Cell Host Microbe. 16, 364-375.
Wild, M., Daviere, J.-M., Cheminant, S., Regnault, T., Baumberger, N., Heintz, D., Baltz, R., Genschik, P. and Achard, P. (2012) The Arabidopsis DELLA RGA-LIKE3 is a direct target of MYC2 and modulates jasmonate signaling responses. Plant Cell, 24, 3307-3319.
Wilton, M., Subramaniam, R., Elmore, J., Felsensteiner, C., Coaker, G. and Desveaux, D. (2010) The type III effector HopF2Pto targets Arabidopsis RIN4 protein to promote Pseudomonas syringae virulence. Proc. Natl Acad. Sci. USA 107, 2349-2354.
Wu, S., Lu, D., Kabbage, M., Wei, H.-L., Swingle, B., Records, A.R., Dickman, M., He, P. and Shan, L. (2011) Bacterial effector HopF2 suppresses Arabidopsis innate immunity at the plasma membrane. Mol. Plant Microbe Interact. 24, 585-593.
Xie, C., Zhou, X., Deng, X. and Guo, Y. (2010) PKS5, a SNF1-related kinase, interacts with and phosphorylates NPR1, and modulates expression of WRKY38 and WRKY62. J. Genet. Genomics 37, 359-369.
Xu, J., Audenaert, K., Hofte, M. and de Vleesschauwer, D. (2013) Abscisic acid promotes susceptibility to the rice leaf blight pathogen Xanthomonas oryzae pv oryzae by suppressing salicylic acid-mediated defenses. PLoS ONE 8, e67413.
Yan, A. and Chen, Z. (2016) The pivotal role of abscisic acid signaling during transition from seed maturation to germination. Plant Cell Rep. 36, 689-703.
Yang, L., Teixeira, P.J.P.L., Biswas, S., Finkel, O.M., He, Y., Salas-Gonzalez, I., English, M.E., Epple, P., Mieczkowski, P. and Dangl, J.L. (2017) Pseudomonas syringae type III effector HopBB1 promotes host transcriptional repressor degradation to regulate phytohormone responses and virulence. Cell Host Microbe 21, 156-168.
Yoshida, T., Nishmura, N., Kitahata, N., Kuromori, T., Ito, T., Asami, T., Shinozaki, K. and Hirayama, T. (2005) ABA-hypersensitive germination3 encodes a Protein Phosphatase 2C (AtPP2CA) that strongly regulates abscisic acid signaling during germination among Arabidopsis protein Phosphatase 2Cs. Plant Physiol. 140, 115-126.
Yoshioka, K., Moeder, W., Kang, H., Kachroo, P., Masmoudi, K., Berkowitz, G. and Klessig, D.F. (2006) The chimeric Arabidopsis CYCLIC NUCLEOTIDE-GATED ION CHANNEL11/12 activates multiple pathogen resistance responses. Plant Cell, 18, 747-763.
Zhang, J., Shao, F., Li, Y. et al. (2007) A Pseudomonas syringae effector inactivates MAPKs to suppress PAMP-induced immunity in plants. Cell Host Microbe 1, 175-185.
Zipfel, C. (2014) Plant pattern-recognition receptors. Trends Immunol., 35, 345-351.