Early Arabidopsis root hair growth stimulation by pathogenic strains of Pseudomonas syringae
Jazyk angličtina Země Velká Británie, Anglie Médium print
Typ dokumentu časopisecké články
PubMed
28911019
PubMed Central
PMC5591418
DOI
10.1093/aob/mcx073
PII: 3980127
Knihovny.cz E-zdroje
- Klíčová slova
- Arabidopsis, Flg22, Pseudomonas, Root hair, dde2/ein2/pad4/sid2, exocyst, vesicle trafficking,
- MeSH
- Arabidopsis genetika růst a vývoj mikrobiologie MeSH
- genový knockout MeSH
- interakce hostitele a patogenu * MeSH
- kořeny rostlin růst a vývoj mikrobiologie MeSH
- mutace MeSH
- proteinkinasy genetika MeSH
- proteiny huseníčku genetika MeSH
- Pseudomonas syringae * MeSH
- receptory buněčného povrchu genetika MeSH
- regulace genové exprese u rostlin MeSH
- signální transdukce MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- EIN2 protein, Arabidopsis MeSH Prohlížeč
- EXO70A1 protein, Arabidopsis MeSH Prohlížeč
- FLS2 protein, Arabidopsis MeSH Prohlížeč
- proteinkinasy MeSH
- proteiny huseníčku MeSH
- receptory buněčného povrchu MeSH
BACKGROUND AND AIMS: Selected beneficial Pseudomonas spp. strains have the ability to influence root architecture in Arabidopsis thaliana by inhibiting primary root elongation and promoting lateral root and root hair formation. A crucial role for auxin in this long-term (1week), long-distance plant-microbe interaction has been demonstrated. METHODS: Arabidopsis seedlings were cultivated in vitro on vertical plates and inoculated with pathogenic strains Pseudomonas syringae pv. maculicola (Psm) and P. syringae pv. tomato DC3000 (Pst), as well as Agrobacterium tumefaciens (Atu) and Escherichia coli (Eco). Root hair lengths were measured after 24 and 48h of direct exposure to each bacterial strain. Several Arabidopsis mutants with impaired responses to pathogens, impaired ethylene perception and defects in the exocyst vesicle tethering complex that is involved in secretion were also analysed. KEY RESULTS: Arabidopsis seedling roots infected with Psm or Pst responded similarly to when infected with plant growth-promoting rhizobacteria; root hair growth was stimulated and primary root growth was inhibited. Other plant- and soil-adapted bacteria induced similar root hair responses. The most compromised root hair growth stimulation response was found for the knockout mutants exo70A1 and ein2. The single immune pathways dependent on salicylic acid, jasmonic acid and PAD4 are not directly involved in root hair growth stimulation; however, in the mutual cross-talk with ethylene, they indirectly modify the extent of the stimulation of root hair growth. The Flg22 peptide does not initiate root hair stimulation as intact bacteria do, but pretreatment with Flg22 prior to Psm inoculation abolished root hair growth stimulation in an FLS2 receptor kinase-dependent manner. These early response phenomena are not associated with changes in auxin levels, as monitored with the pDR5::GUS auxin reporter. CONCLUSIONS: Early stimulation of root hair growth is an effect of an unidentified component of living plant pathogenic bacteria. The root hair growth response is triggered in the range of hours after bacterial contact with roots and can be modulated by FLS2 signalling. Bacterial stimulation of root hair growth requires functional ethylene signalling and an efficient exocyst-dependent secretory machinery.
Zobrazit více v PubMed
Balmer D, Mauch-Mani B. 2013. More beneath the surface? Root versus shoot antifungal plant defenses. Frontiers in Plant Science 4: 256. doi:10.3389/fpls.2013.00256. PubMed PMC
Bates TR, Lynch JP. 1996. Stimulation of root hair elongation in Arabidopsis thaliana by low phosphorus availability. Plant, Cell & Environment 19: 529–538.
Bauer Z, Gómez-Gómez L, Boller T, Felix G. 2001. Sensitivity of different ecotypes and mutants of Arabidopsis thaliana toward the bacterial elicitor flagellin correlates with the presence of receptor-binding sites. The Journal of Biological Chemistry 276: 45669–45676. doi:10.1074/jbc.M102390200 PubMed
Beck M, Zhou J, Faulkner C, MacLean D, Robatzek S. 2012. Spatio-temporal cellular dynamics of the Arabidopsis flagellin receptor reveal activation status-dependent endosomal sorting. The Plant Cell 24: 4205–4219. doi:10.1105/tpc.112.100263. PubMed PMC
Brands A, Ho TD. 2002. Function of a plant stress-induced gene, HVA22. Synthetic enhancement screen with its yeast homolog reveals its role in vesicular traffic. Plant Physiology 130: 1121–1131. doi:10.1104/pp.007716 PubMed PMC
Cao H, Bowling SA, Gordon AS, Dong X. 1994. Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. The Plant Cell 6: 1583–1592. doi:10.1105/tpc.6.11.1583 PubMed PMC
Chinchilla D, Zipfel C, Robatzek S. et al. 2007. A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448: 497–500. doi:10.1038/nature05999 PubMed
Cui H, Gobbato E, Kracher B, Qiu J, Bautor J, Parker JE. 2017. A core function of EDS1 with PAD4 is to protect the salicylic acid defense sector in Arabidopsis immunity. New Phytologist 213: 1802–1817. doi:10.1111/nph.14302. PubMed
Dolan L. 2001. The role of ethylene in root hair growth in Arabidopsis. Journal of Plant Nutrition and Soil Science 164: 141–145.
Dong X, Mindrinos M, Davis KR, Ausubel FM. 1991. Induction of Arabidopsis defense genes by virulent and avirulent Pseudomonas syringae strains and by a cloned avirulence gene. The Plant Cell 3: 61–72. doi:10.1105/tpc.3.1.61 PubMed PMC
Dörmann P, Kim H, Ott T. et al. 2014. Cell-autonomous defense, re-organization and trafficking of membranes in plant-microbe interactions. New Phytologist 204: 815–822. doi:10.1111/nph.12978. PubMed
Du Y, Mpina MH, Birch PRJ, Bouwmeester K, Govers F. 2015. Phytophthora infestans RXLR effector AVR1 interacts with exocyst component Sec5 to manipulate plant immunity. Plant Physiology 169: 1975–1990. doi:10.1104/pp.15.01169 PubMed PMC
Glazebrook J. 2005. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annual Review of Phytopathology 43: 205–227. doi:10.1146/annurev.phyto.43.040204.135923 PubMed
Gómez-Gómez L, Felix G, Boller T. 1999. A single locus determines sensitivity to bacterial flagellin in Arabidopsis thaliana. The Plant Journal 18: 277–284. PubMed
Guo W, Roth D, Walch-Solimena C, Novick P. 1999. The exocyst is an effector for Sec4p, targeting secretory vesicles to sites of exocytosis. The EMBO Journal 18: 1071–1080. doi:10.1093/emboj/18.4.1071 PubMed PMC
Guzmán P, Ecker JR. 1990. Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. The Plant Cell 2: 513–523. doi:10.1105/tpc.2.6.513 PubMed PMC
Hála M, Cole R, Synek L. et al. 2008. An exocyst complex functions in plant cell growth in Arabidopsis and tobacco. The Plant Cell 20: 1330–1345. doi:10.1105/tpc.108.059105 PubMed PMC
Hsu S-C, TerBush D, Abraham M, Guo W. 2004. The exocyst complex in polarized exocytosis. International Review of Cytology 233: 243–265. doi:10.1016/S0074-7696(04)33006-8 PubMed
Janda M, Ruelland E. 2015. Magical mystery tour: salicylic acid signaling. Environmental and Experimental Botany, 114:117–128. doi:10.1016/j.envexpbot.2014.07.003
Jung J-Y, Shin R, Schachtman DP. 2009. Ethylene mediates response and tolerance to potassium deprivation in Arabidopsis. The Plant Cell 21: 607–621. doi:10.1105/tpc.108.063099 PubMed PMC
Katagiri F, Thilmony R, He SY. 2002. The Arabidopsis thaliana-Pseudomonas syringae interaction. Arabidopsis Book 1: e0039. doi:10.1199/tab.0039 PubMed PMC
Kim Y, Tsuda K, Igarashi D. et al. 2014. Mechanisms underlying robustness and tunability in a plant immune signaling network. Cell Host & Microbe 15: 84–94. doi:10.1016/j.chom.2013.12.002 PubMed PMC
Kinkema M, Fan W, Dong X. 2000. Nuclear localization of NPR1 is required for activation of PR gene expression. The Plant Cell 12: 2339–2350. PubMed PMC
Kremer RJ, Begonia MF, Stanley L, Lanham ET. 1990. Characterization of rhizobacteria associated with weed seedlings. Applied and Environmental Microbiology 56: 1649–1655. PubMed PMC
Kulich I, Pečenková T, Sekereš J. et al. 2013. Arabidopsis exocyst subcomplex containing subunit EXO70B1 is involved in autophagy-related transport to the vacuole. Traffic 14: 1155–1165. doi:10.1111/tra.12101 PubMed
Lamesch P, Dreher K, Swarbreck D, Sasidharan R, Reiser L, Huala E. 2010. Using the Arabidopsis information resource (TAIR) to find information about Arabidopsis genes. Current Protocols in Bioinformatics Suppl. 30: Chapter 1, Unit1.11. doi:10.1002/0471250953.bi0111s30 PubMed
López-Bucio J, Campos-Cuevas JC, Hernández-Calderón E. et al. 2007. Bacillus megaterium rhizobacteria promote growth and alter root-system architecture through an auxin- and ethylene-independent signaling mechanism in Arabidopsis thaliana. Molecular Plant-Microbe Interactions 20: 207–217. doi:10.1094/MPMI-20-2-0207 PubMed
Lugtenberg B, Kamilova F. 2009. Plant-growth-promoting rhizobacteria. Annual Review of Microbiology 63: 541–556. doi:10.1146/annurev.micro.62.081307.162918 PubMed
Maketon C, Fortuna A, Okubara PA. 2012. Cultivar-dependent transcript accumulation in wheat roots colonized by Pseudomonas fluorescens Q8r1-96 wild type and mutant strains. Biological Control 60: 216-224.
Millet YA, Danna CH, Clay NK. et al. 2010. Innate immune responses activated in Arabidopsis roots by microbe-associated molecular patterns. The Plant Cell 22: 973–990. doi:10.1105/tpc.109.069658 PubMed PMC
Mine A, Nobori T, Salazar‐Rondon MC. et al. 2017. An incoherent feed‐forward loop mediates robustness and tunability in a plant immune network. EMBO Reports 18: 464–476. doi:10.15252/embr.201643051 PubMed PMC
Niu Y, Chai R, Liu L. et al. 2014. Magnesium availability regulates the development of root hairs in Arabidopsis thaliana (L.) Heynh. Plant, Cell & Environment 37: 2795–2813. doi:10.1111/pce.12362 PubMed
Ortíz-Castro R, Martínez-Trujillo M, López-Bucio J. 2008. N-acyl-L-homoserine lactones: a class of bacterial quorum-sensing signals alter post-embryonic root development in Arabidopsis thaliana. Plant, Cell & Environment 31: 1497–1509. doi:10.1111/j.1365-3040.2008.01863.x PubMed
Ortíz-Castro R, Pelagio-Flores R, Méndez-Bravo A, Ruiz-Herrera LF, Campos-García J, López-Bucio J. 2014. Pyocyanin, a virulence factor produced by Pseudomonas aeruginosa, alters root development through reactive oxygen species and ethylene signaling in Arabidopsis. Molecular Plant-Microbe Interactions 27: 364–378. doi:10.1094/MPMI-08-13-0219-R PubMed
Pečenková T, Hála M, Kulich I. et al. 2011. The role for the exocyst complex subunits Exo70B2 and Exo70H1 in the plant-pathogen interaction. Journal of Experimental Botany 62: 2107–2116. doi:10.1093/jxb/erq402 PubMed PMC
Pieterse CM, Leon-Reyes A, Van der Ent S, Van Wees SC. 2009. Networking by small-molecule hormones in plant immunity. Nature Chemical Biology 5: 308–16. doi:10.1038/nchembio.164 PubMed
Rahman A, Hosokawa S, Oono Y, Amakawa T, Goto N, Tsurumi S. 2002. Auxin and ethylene response interactions during Arabidopsis root hair development dissected by auxin influx modulators. Plant Physiology 130: 1908–1917. doi:10.1104/pp.010546 PubMed PMC
Rietz S, Stamm A, Malonek S. et al. 2011. Different roles of Enhanced Disease Susceptibility1 (EDS1) bound to and dissociated from Phytoalexin Deficient4 (PAD4) in Arabidopsis immunity. New Phytologist 191: 107–119. doi:10.1111/j.1469-8137.2011.03675.x. PubMed
Rothman JE, Warren G. 1994. Implications of the SNARE hypothesis for intracellular membrane topology and dynamics. Current Biology 4: 220–233. PubMed
Rudrappa T, Bais HP. 2008. Rhizospheric pseudomonads: Friends or foes? Plant Signaling and Behavior 3: 1132–1133. PubMed PMC
Schikora A, Schmidt W, 2001. Iron stress-induced changes in root epidermal cell fate are regulated independently from physiological responses to low iron availability. Plant Physiology 125: 1679–1687. PubMed PMC
Schneider CA, Rasband WS, Eliceiri KW. 2012. NIH Image to ImageJ: 25years of image analysis. Nature Methods 9: 671–675. PubMed PMC
Smith JM, Salamango DJ, Leslie ME, Collins CA, Heese A. 2014. Sensitivity to Flg22 is modulated by ligand-induced degradation and de novo synthesis of the endogenous flagellin-receptor FLAGELLIN-SENSING2. Plant Physiology 164: 440–454. doi:10.1104/pp.113.229179 PubMed PMC
Stefano G, Renna L, Moss T, McNew JA, Brandizzi F. 2012. In Arabidopsis, the spatial and dynamic organization of the endoplasmic reticulum and Golgi apparatus is influenced by the integrity of the C-terminal domain of RHD3, a non-essential GTPase. Plant Journal 69: 957–966. doi:10.1111/j.1365-313X.2011.04846.x PubMed
Stegmann M, Anderson RG, Ichimura K. et al. 2012. The ubiquitin ligase PUB22 targets a subunit of the exocyst complex required for PAMP-triggered responses in Arabidopsis. The Plant Cell 24: 4703–4716. doi:10.1105/tpc.112.104463 PubMed PMC
Synek L, Schlager N, Eliás M, Quentin M, Hauser M-T, Zárský V. 2006. AtEXO70A1, a member of a family of putative exocyst subunits specifically expanded in land plants, is important for polar growth and plant development. Plant Journal 48: 54–72. doi:10.1111/j.1365-313X.2006.02854.x PubMed PMC
Tanaka N, Kato M, Tomioka R. et al. 2014. Characteristics of a root hair-less line of Arabidopsis thaliana under physiological stresses. Journal of Experimental Botany 65: 1497–1512. doi:10.1093/jxb/eru014. PubMed PMC
TerBush DR, Maurice T, Roth D, Novick P. 1996. The Exocyst is a multiprotein complex required for exocytosis in Saccharomyces cerevisiae. EMBO Journal 15: 6483–6494. PubMed PMC
Trapet P, Avoscan L, Klinguer A. et al. 2016. The Pseudomonas fluorescens siderophore pyoverdine weakens Arabidopsis thaliana defense in favour of growth in iron-deficient conditions. Plant Physiology 171: 675–693. doi:10.1104/pp.15.01537 PubMed PMC
Tsuda K, Katagiri F. 2010. Comparing signaling mechanisms engaged in pattern-triggered and effector-triggered immunity. Current Opinion in Plant Biology 13: 459–465. doi:10.1016/j.pbi.2010.04.006. PubMed
Tsuda K, Sato M, Stoddard T, Glazebrook J, Katagiri F. 2009. Network properties of robust immunity in plants. PLoS Genetics 5(12), doi:10.1371/journal.pgen.1000772 PubMed PMC
Ulmasov T, Murfett J, Hagen G, Guilfoyle TJ. 1997. Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. The Plant Cell 9: 1963–1971. doi:10.1105/tpc.9.11.1963 PubMed PMC
Vacheron J, Desbrosses G, Bouffaud ML. et al. 2013. Plant growth-promoting rhizobacteria and root system functioning. Frontiers in Plant Science 4: 356. doi:10.3389/fpls.2013.00356. PubMed PMC
van Loon LC, Bakker PAHM, van der Heijdt WHW, Wendehenne D, Pugin A. 2008. Early responses of tobacco suspension cells to rhizobacterial elicitors of induced systemic resistance. Molecular Plant-Microbe Interactions 21: 1609–1621. doi:10.1094/MPMI-21-12-1609 PubMed
Vansuyt G, Robin A, Briat J-F, Curie C, Lemanceau P. 2007. Iron acquisition from Fe-pyoverdine by Arabidopsis thaliana. Molecular Plant-Microbe Interactions 20: 441–447. doi:10.1094/MPMI-20-4-0441 PubMed
von Malek B, van der Graaff E, Schneitz K, Keller B, 2002. The Arabidopsis male-sterile mutant dde2-2 is defective in the ALLENE OXIDE SYNTHASE gene encoding one of the key enzymes of the jasmonic acid biosynthesis pathway. Planta 216: 187–192. doi:10.1007/s00425-002-0906-2 PubMed
Wen T-J, Hochholdinger F, Sauer M, Bruce W, Schnable PS. 2005. The roothairless1 gene of maize encodes a homolog of sec3, which is involved in polar exocytosis. Plant Physiology 138: 1637–1643. doi:10.1104/pp.105.062174 PubMed PMC
Wildermuth MC, Dewdney J, Wu G, Ausubel FM, 2001. Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414: 562–565. doi:10.1038/35107108 PubMed
Xin XF, He SY. 2013. Pseudomonas syringae pv. tomato DC3000: a model pathogen for probing disease susceptibility and hormone signaling in plants. Annual Review of Phytopathology 51: 473-498. doi:10.1146/annurev-phyto-082712-102321 PubMed
Yang TJW, Perry PJ, Ciani S, Pandian S, Schmidt W. 2008. Manganese deficiency alters the patterning and development of root hairs in Arabidopsis. Journal of Experimental Botany 59: 3453–3464. doi:10.1093/jxb/ern195 PubMed PMC
Zamioudis C, Pieterse CMJ. 2012. Modulation of host immunity by beneficial microbes. Molecular Plant-Microbe Interactions 25: 139–150. doi:10.1094/MPMI-06-11-0179 PubMed
Zamioudis C, Mastranesti P, Dhonukshe P, Blilou I, Pieterse CMJ. 2013. Unraveling root developmental programs initiated by beneficial Pseudomonas spp. bacteria. Plant Physiology 162: 304–318. doi:10.1104/pp.112.212597 PubMed PMC
Zárský V, Cvrčková F, Potocký M, Hála M. 2009. Exocytosis and cell polarity in plants – exocyst and recycling domains. New Phytologist 183: 255–272. doi:10.1111/j.1469-8137.2009.02880.x PubMed
Zárský V, Kulich I, Fendrych M, Pečenková T. 2013. Exocyst complexes multiple functions in plant cells secretory pathways. Current Opinion in Plant Biology 16: 726–733. doi:10.1016/j.pbi.2013.10.013 PubMed
Zipfel C, Robatzek S, Navarro L. et al. 2004. Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428: 764–767. doi:10.1038/nature02485 PubMed
Plasma membrane phospholipid signature recruits the plant exocyst complex via the EXO70A1 subunit