Exocyst components promote an incompatible interaction between Glycine max (soybean) and Heterodera glycines (the soybean cyst nematode).
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
14 09 2020
14 09 2020
Historique:
received:
05
12
2019
accepted:
17
08
2020
entrez:
15
9
2020
pubmed:
16
9
2020
medline:
13
2
2021
Statut:
epublish
Résumé
Vesicle and target membrane fusion involves tethering, docking and fusion. The GTPase SECRETORY4 (SEC4) positions the exocyst complex during vesicle membrane tethering, facilitating docking and fusion. Glycine max (soybean) Sec4 functions in the root during its defense against the parasitic nematode Heterodera glycines as it attempts to develop a multinucleate nurse cell (syncytium) serving to nourish the nematode over its 30-day life cycle. Results indicate that other tethering proteins are also important for defense. The G. max exocyst is encoded by 61 genes: 5 EXOC1 (Sec3), 2 EXOC2 (Sec5), 5 EXOC3 (Sec6), 2 EXOC4 (Sec8), 2 EXOC5 (Sec10) 6 EXOC6 (Sec15), 31 EXOC7 (Exo70) and 8 EXOC8 (Exo84) genes. At least one member of each gene family is expressed within the syncytium during the defense response. Syncytium-expressed exocyst genes function in defense while some are under transcriptional regulation by mitogen-activated protein kinases (MAPKs). The exocyst component EXOC7-H4-1 is not expressed within the syncytium but functions in defense and is under MAPK regulation. The tethering stage of vesicle transport has been demonstrated to play an important role in defense in the G. max-H. glycines pathosystem, with some of the spatially and temporally regulated exocyst components under transcriptional control by MAPKs.
Identifiants
pubmed: 32929168
doi: 10.1038/s41598-020-72126-z
pii: 10.1038/s41598-020-72126-z
pmc: PMC7490361
doi:
Substances chimiques
Soybean Proteins
0
Mitogen-Activated Protein Kinases
EC 2.7.11.24
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
15003Références
Jones, J. D. & Dangl, J. L. The plant immune system. Nature 444, 323–329 (2006).
pubmed: 17108957
doi: 10.1038/nature05286
Flor, H. H. The complementary genic systems in flax and flax rust. Adv. Genet. 8, 29–54 (1956).
doi: 10.1016/S0065-2660(08)60498-8
Flor, H. H. Current status of the gene-for-gene concept. Annu. Rev. Phytopathol. 9, 275–296 (1971).
doi: 10.1146/annurev.py.09.090171.001423
Scofield, S. R. et al. Molecular basis of gene-for-gene specificity in bacterial speck disease of tomato. Science 274, 2063 (1996).
pubmed: 8953034
doi: 10.1126/science.274.5295.2063
Tang, X. et al. Initiation of plant disease resistance by physical interaction of AvrPto and Pto kinase. Science 274, 2060 (1996).
pubmed: 8953033
doi: 10.1126/science.274.5295.2060
Collins, N. C. et al. SNARE-protein-mediated disease resistance at the plant cell wall. Nature 425, 973–977 (2003).
pubmed: 14586469
doi: 10.1038/nature02076
Robatzek, S., Chinchilla, D. & Boller, T. Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis. Genes Dev. 20, 537–542 (2006).
pubmed: 16510871
pmcid: 1410809
doi: 10.1101/gad.366506
Novick, P., Field, C. & Schekman, R. Identification of 23 complementation groups required for post-translational events in the yeast secretory pathway. Cell 21, 205–215 (1980).
pubmed: 6996832
doi: 10.1016/0092-8674(80)90128-2
Clary, D. O., Griff, I. C. & Rothman, J. E. SNAPs, a family of NSF attachment proteins involved in intracellular membrane fusion in animals and yeast. Cell 61, 709–721 (1990).
pubmed: 2111733
doi: 10.1016/0092-8674(90)90482-T
Lauber, M. H. et al. The Arabidopsis KNOLLE protein is a cytokinesis-specific syntaxin. J. Cell Biol. 139, 1485–1493 (1997).
pubmed: 9396754
pmcid: 2132613
doi: 10.1083/jcb.139.6.1485
Assaad, F. F. et al. The PEN1 syntaxin defines a novel cellular compartment upon fungal attack and is required for the timely assembly of papillae. Mol. Biol. Cell 15, 5118–5129 (2004).
pubmed: 15342780
pmcid: 524786
doi: 10.1091/mbc.e04-02-0140
Wilson, D. W., Whiteheart, S. W., Wiedmann, M., Brunner, M. & Rothman, J. E. A multisubunit particle implicated in membrane fusion. J. Cell Biol. 117, 531–538 (1992).
pubmed: 1315316
doi: 10.1083/jcb.117.3.531
Söllner, T., Bennett, M. K., Whiteheart, S. W., Scheller, R. H. & Rothman, J. E. A protein assembly-disassembly pathway in vitro that may correspond to sequential steps of synaptic vesicle docking, activation, and fusion. Cell 75, 409–418 (1993).
pubmed: 8221884
doi: 10.1016/0092-8674(93)90376-2
Söllner, T. et al. SNAP receptors implicated in vesicle targeting and fusion. Nature 362, 318–324 (1993).
pubmed: 8455717
doi: 10.1038/362318a0
Lipka, V. et al. Pre- and postinvasion defenses both contribute to nonhost resistance in Arabidopsis. Science 310, 1180–1183 (2005).
pubmed: 16293760
doi: 10.1126/science.1119409
Stein, M. et al. Arabidopsis PEN3/PDR8, an ATP binding cassette transporter, contributes to nonhost resistance to inappropriate pathogens that enter by direct penetration. Plant Cell 18, 731–746 (2006).
pubmed: 16473969
pmcid: 1383646
doi: 10.1105/tpc.105.038372
Humphry, M. et al. A regulon conserved in monocot and dicot plants defines a functional module in antifungal plant immunity. Proc. Natl. Acad. Sci. USA 107, 21896–21901 (2010).
pubmed: 21098265
doi: 10.1073/pnas.1003619107
pmcid: 3003077
Du, Y., Mpina, M. H., Birch, P. R., Bouwmeester, K. & Govers, F. Phytophthora infestans RXLR Effector AVR1 interacts with exocyst component Sec5 to manipulate plant immunity. Plant Physiol. 169, 1975–1990 (2015).
pubmed: 26336092
pmcid: 4634092
Du, Y., Overdijk, E. J. R., Berg, J. A., Govers, F. & Bouwmeester, K. Solanaceous exocyst subunits are involved in immunity to diverse plant pathogens. J. Exp. Bot. 69, 655–666 (2018).
pubmed: 29329405
pmcid: 5853398
doi: 10.1093/jxb/erx442
van den Hoogen, J. et al. Soil nematode abundance and functional group composition at a global scale. Nature 572, 194–198 (2019).
pubmed: 31341281
doi: 10.1038/s41586-019-1418-6
Niblack, T. L., Lambert, K. N. & Tylka, G. L. A model plant pathogen from the kingdom Animalia: Heterodera glycines, the soybean cyst nematode. Annu. Rev. Phytopathol. 44, 283–303 (2006).
pubmed: 16704359
doi: 10.1146/annurev.phyto.43.040204.140218
Wrather, J. A. & Koenning, S. R. Estimates of disease effects on soybean yields in the United States 2003 to 2005. J. Nematol. 38, 173–180 (2006).
pubmed: 19259444
pmcid: 2586459
Wang, J. et al. Soybean cyst nematode reduces soybean yield without causing obvious aboveground symptoms. Plant Dis. 87, 623–628 (2003).
pubmed: 30812850
doi: 10.1094/PDIS.2003.87.6.623
Golden, A. et al. Terminology and identity of infraspecific forms of the soybean cyst nematode (Heterodera glycines). Plant Dis. Rep. 54, 544–546 (1970).
Riggs, R. D. & Schmitt, D. P. Complete characterization of the race scheme for Heterodera glycines. J. Nematol. 20, 392–395 (1988).
pubmed: 19290228
pmcid: 2618837
Niblack, T. L. et al. A revised classification scheme for genetically diverse populations of Heterodera glycines. J. Nematol. 34, 279–288 (2002).
pubmed: 19265945
pmcid: 2620582
Lauritis, J. A., Rebois, R. V. & Graney, L. S. Development of Heterodera glycines ichinohe on soybean, Glycine max (L.) Merr., under gnotobiotic conditions. J. Nematol. 15, 272–281 (1983).
pubmed: 19295802
pmcid: 2618278
Endo, B. Histological responses of resistant and susceptible soybean varieties and backcross progeny to entry and development of Heterodera glycines. Phytopathology 55, 375–381 (1965).
Burton, Y. Ultrastructure of initial responses of susceptible and resistant soybean roots to infection by Heterodera glycines. Revue Nétnatol. 4, 73–94 (1991).
Ross, J. Host-parasite relationship of the soybean cyst nematode in resistant soybean roots. Phytopathology 48, 578–579 (1958).
Matsye, P. D. et al. Mapping cell fate decisions that occur during soybean defense responses. Plant Mol. Biol. 77, 513–528 (2011).
pubmed: 21986905
doi: 10.1007/s11103-011-9828-3
Matsye, P. D. et al. The expression of a naturally occurring, truncated allele of an α-SNAP gene suppresses plant parasitic nematode infection. Plant Mol. Biol. 80, 131–155 (2012).
pubmed: 22689004
doi: 10.1007/s11103-012-9932-z
Pant, S. R. et al. Syntaxin 31 functions in Glycine max resistance to the plant parasitic nematode Heterodera glycines. Plant Mol. Biol. 85, 107–121 (2014).
pubmed: 24452833
doi: 10.1007/s11103-014-0172-2
Sharma, K., Pant, S. R., McNeece, B. T., Lawrence, G. W. & Klink, V. P. Co-regulation of the Glycine max soluble N-ethylmaleimide-sensitive fusion protein attachment protein receptor (SNARE)-containing regulon occurs during defense to a root pathogen. J. Plant Interact. 11, 74–93 (2016).
doi: 10.1080/17429145.2016.1195891
Bekal, S. et al. A SNARE-like protein and biotin are implicated in soybean cyst nematode virulence. PLoS ONE 10, e0145601 (2015).
pubmed: 26714307
pmcid: 4699853
doi: 10.1371/journal.pone.0145601
Schiavo, G. et al. Tetanus and botulinum-B neurotoxins block neurotransmitter release by proteolytic cleavage of synaptobrevin. Nature 359, 832–835 (1992).
pubmed: 1331807
doi: 10.1038/359832a0
Klink, V. P. et al. Components of the SNARE-containing regulon are co-regulated in root cells undergoing defense. Plant Signal. Behav. 12, e1274481 (2017).
pubmed: 28010187
doi: 10.1080/15592324.2016.1274481
Guo, W., Roth, D., Walch-Solimena, C. & Novick, P. The exocyst is an effector for Sec4p, targeting secretory vesicles to sites of exocytosis. EMBO J. 18, 1071–1080 (1999).
pubmed: 10022848
pmcid: 1171198
doi: 10.1093/emboj/18.4.1071
Mizuno-Yamasaki, E., Rivera-Molina, F. & Novick, P. GTPase networks in membrane traffic. Annu. Rev. Biochem. 81, 637–659 (2012).
pubmed: 22463690
pmcid: 3708692
doi: 10.1146/annurev-biochem-052810-093700
TerBush, D. R. & Novick, P. Sec6, Sec8, and Sec15 are components of a multisubunit complex which localizes to small bud tips in Saccharomyces cerevisiae. J. Cell Biol. 130, 299–312 (1995).
pubmed: 7615633
doi: 10.1083/jcb.130.2.299
TerBush, D. R., Maurice, T., Roth, D. & Novick, P. The exocyst is a multiprotein complex required for exocytosis in Saccharomyces cerevisiae. EMBO J. 15, 6483–6494 (1996).
pubmed: 8978675
pmcid: 452473
doi: 10.1002/j.1460-2075.1996.tb01039.x
Hsu, S.-C., TerBush, D., Abraham, M. & Guo, W. The exocyst complex in polarized exocytosis. Int. Rev. Cytol. 233, 243 (2004).
pubmed: 15037366
doi: 10.1016/S0074-7696(04)33006-8
Lipschutz, J. H. & Mostov, K. E. Exocytosis: the many masters of the exocyst. Curr. Biol. 12, R212-214 (2002).
pubmed: 11909549
doi: 10.1016/S0960-9822(02)00753-4
He, B. & Guo, W. The exocyst complex in polarized exocytosis. Curr. Opin. Cell Biol. 21, 537–542 (2009).
pubmed: 19473826
pmcid: 2725219
doi: 10.1016/j.ceb.2009.04.007
Žárský, V., Kulich, I., Fendrych, M. & Pečenková, T. Exocyst complexes multiple functions in plant cells secretory pathways. Curr. Opin. Plant Biol. 16, 726–733 (2013).
pubmed: 24246229
doi: 10.1016/j.pbi.2013.10.013
Hála, M. et al. An exocyst complex functions in plant cell growth in Arabidopsis and tobacco. Plant Cell 20, 1330–1345 (2008).
pubmed: 18492870
pmcid: 2438459
doi: 10.1105/tpc.108.059105
Heider, M. R. & Munson, M. Exorcising the exocyst complex. Traffic 13, 898–907 (2012).
pubmed: 22420621
pmcid: 3374049
doi: 10.1111/j.1600-0854.2012.01353.x
Finger, F. P. & Novick, P. Sec3p is involved in secretion and morphogenesis in Saccharomyces cerevisiae. Mol. Biol. Cell 8, 647–662 (1997).
pubmed: 9247645
pmcid: 276116
doi: 10.1091/mbc.8.4.647
Finger, F. P., Hughes, T. E. & Novick, P. Sec3p is a spatial landmark for polarized secretion in budding yeast. Cell 92, 559–571 (1998).
pubmed: 9491896
doi: 10.1016/S0092-8674(00)80948-4
McNeece, B. T., Sharma, K., Lawrence, G. W., Lawrence, K. S. & Klink, V. P. The mitogen activated protein kinase (MAPK) gene family functions as a cohort during the Glycine max defense response to Heterodera glycines. Plant Physiol. Biochem. 137, 25–41 (2019).
pubmed: 30711881
doi: 10.1016/j.plaphy.2019.01.018
Austin, H. W. et al. An expanded role of the SNARE-containing regulon as it relates to the defense process that Glycine max has to Heterodera glycines. J. Plant Interact. 14, 276–283 (2019).
doi: 10.1080/17429145.2019.1622043
Wang, W., Liu, N., Gao, C., Rui, L. & Tang, D. The Pseudomonas syringae effector AvrPtoB associates with and ubiquitinates arabidopsis exocyst subunit EXO70B1. Front. Plant Sci. 10, 1027 (2019).
pubmed: 31555308
pmcid: 6726739
doi: 10.3389/fpls.2019.01027
Synek, L. et al. AtEXO70A1, a member of a family of putative exocyst subunits specifically expanded in land plants, is important for polar growth and plant development. Plant J. 48, 54–72 (2006).
pubmed: 16942608
pmcid: 2865999
doi: 10.1111/j.1365-313X.2006.02854.x
Synek, L. et al. EXO70C2 is a key regulatory factor for optimal tip growth of pollen. Plant Physiol. 174, 223–240 (2017).
pubmed: 28356503
pmcid: 5411130
doi: 10.1104/pp.16.01282
Haarer, B. K. et al. SEC3 mutations are synthetically lethal with profilin mutations and cause defects in diploid-specific bud-site selection. Genetics 144, 495–510 (1996).
pubmed: 8889515
pmcid: 1207545
doi: 10.1093/genetics/144.2.495
Croteau, N. J., Furgason, M. L., Devos, D. & Munson, M. Conservation of helical bundle structure between the exocyst subunits. PLoS ONE 4, e4443 (2009).
pubmed: 19214222
pmcid: 2635961
doi: 10.1371/journal.pone.0004443
Yamashita, M. et al. Structural basis for the Rho- and phosphoinositide-dependent localization of the exocyst subunit Sec3. Nat. Struct. Mol. Biol. 17, 180–186 (2010).
pubmed: 20062059
doi: 10.1038/nsmb.1722
Picco, A. et al. The in vivo architecture of the exocyst provides structural basis for exocytosis. Cell 168, 400–412 (2017).
pubmed: 28129539
doi: 10.1016/j.cell.2017.01.004
Roth, D., Guo, W. & Novick, P. Dominant negative alleles of SEC10 reveal distinct domains involved in secretion and morphogenesis in yeast. Mol. Biol. Cell 9, 1725–1739 (1998).
pubmed: 9658167
pmcid: 25411
doi: 10.1091/mbc.9.7.1725
Boyd, C., Hughes, T., Pypaert, M. & Novick, P. Vesicles carry most exocyst subunits to exocytic sites marked by the remaining two subunits, Sec3p and Exo70p. J. Cell Biol. 167, 889–901 (2004).
pubmed: 15583031
pmcid: 2172445
doi: 10.1083/jcb.200408124
He, B., Xi, F., Zhang, X., Zhang, J. & Guo, W. Exo70 interacts with phospholipids and mediates the targeting of the exocyst to the plasma membrane. EMBO J. 26, 4053–4065 (2007).
pubmed: 17717527
pmcid: 2230670
doi: 10.1038/sj.emboj.7601834
Liu, J., Zuo, X., Yue, P. & Guo, W. Phosphatidylinositol 4,5-bisphosphate mediates the targeting of the exocyst to the plasma membrane for exocytosis in mammalian cells. Mol. Biol. Cell 18, 4483–4492 (2007).
pubmed: 17761530
pmcid: 2043555
doi: 10.1091/mbc.e07-05-0461
Zhang, X. et al. Membrane association and functional regulation of Sec3 by phospholipids and Cdc42. J. Cell Biol. 180, 145–158 (2008).
pubmed: 18195105
pmcid: 2213614
doi: 10.1083/jcb.200704128
Salminen, A. & Novick, P. J. A ras-like protein is required for a post-Golgi event in yeast secretion. Cell 49, 527–538 (1987).
pubmed: 3552249
doi: 10.1016/0092-8674(87)90455-7
Bourne, H. R. Do GTPases direct membrane traffic in secretion?. Cell 53, 669–671 (1988).
pubmed: 2836065
doi: 10.1016/0092-8674(88)90081-5
Goud, B., Salminen, A., Walworth, N. C. & Novick, P. J. A GTP-binding protein required for secretion rapidly associates with secretory vesicles and the plasma membrane in yeast. Cell 53, 753–768 (1988).
pubmed: 3131018
doi: 10.1016/0092-8674(88)90093-1
Walworth, N. C., Goud, B., Kabcenell, A. K. & Novick, P. J. Mutational analysis of SEC4 suggests a cyclical mechanism for the regulation of vesicular traffic. EMBO J. 8, 1685–1693 (1989).
pubmed: 2504585
pmcid: 401010
doi: 10.1002/j.1460-2075.1989.tb03560.x
Alshehri, H. A., Alkharouf, N. W., Darwish, O., McNeece, B. T. & Klink, V. P. MAPKDB: a MAP kinase database for signal transduction element identification. Bioinformation 15, 338–341 (2019).
pubmed: 31249436
doi: 10.6026/97320630015338
Livak, K. J. & Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25, 402–408 (2001).
pubmed: 11846609
doi: 10.1006/meth.2001.1262
Yuan, J. S., Reed, A., Chen, F. & Stewart, C. N. Statistical analysis of real-time PCR data. BMC Bioinform. 7, 85 (2006).
doi: 10.1186/1471-2105-7-85
Mann, H. B. & Whitney, D. R. On a test of whether one of two random variables is stochastically larger than the other. Ann. Math. Stat. 18, 50–60 (1947).
doi: 10.1214/aoms/1177730491
Goodstein, D. M. et al. Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res. 40, D1178-1186 (2012).
pubmed: 22110026
doi: 10.1093/nar/gkr944
Cvrčková, F. et al. Evolution of the land plant exocyst complexes. Front. Plant Sci. 3, 159 (2012).
pubmed: 22826714
pmcid: 3399122
doi: 10.3389/fpls.2012.00159
Schmutz, J. et al. Genome sequence of the palaeopolyploid soybean. Nature 463, 178–183 (2010).
pubmed: 20075913
doi: 10.1038/nature08670
Sturgill, T. W. & Ray, L. B. Muscle proteins related to microtubule associated protein-2 are substrates for an insulin-stimulatable kinase. Biochem. Biophys. Res. Commun. 134, 565–571 (1986).
pubmed: 3511906
doi: 10.1016/S0006-291X(86)80457-0
Jonak, C., Okrész, L., Bögre, L. & Hirt, H. Complexity, cross talk and integration of plant MAP kinase signalling. Curr. Opin. Plant Biol. 5, 415–424 (2002).
pubmed: 12183180
doi: 10.1016/S1369-5266(02)00285-6
MAPK Group. Mitogen-activated protein kinase cascades in plants: a new nomenclature. Trends Plant Sci. 7, 301–308 (2002).
doi: 10.1016/S1360-1385(02)02302-6
Cao, H., Bowling, S. A., Gordon, A. S. & Dong, X. Characterization of an arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell 6, 1583–1592 (1994).
pubmed: 12244227
pmcid: 160545
doi: 10.2307/3869945
Century, K. S., Holub, E. B. & Staskawicz, B. J. NDR1, a locus of Arabidopsis thaliana that is required for disease resistance to both a bacterial and a fungal pathogen. Proc. Natl. Acad. Sci. USA 92, 6597–6601 (1995).
pubmed: 11607554
doi: 10.1073/pnas.92.14.6597
pmcid: 41565
Century, K. S. et al. NDR1, a pathogen-induced component required for Arabidopsis disease resistance. Science 278, 1963–1965 (1997).
pubmed: 9395402
doi: 10.1126/science.278.5345.1963
Falk, A. et al. EDS1, an essential component of R gene-mediated disease resistance in Arabidopsis has homology to eukaryotic lipases. Proc. Natl. Acad. Sci. USA 96, 3292–3297 (1999).
pubmed: 10077677
doi: 10.1073/pnas.96.6.3292
pmcid: 15935
Coppinger, P. et al. Overexpression of the plasma membrane-localized NDR1 protein results in enhanced bacterial disease resistance in Arabidopsis thaliana. Plant J. 40, 225–237 (2004).
pubmed: 15447649
doi: 10.1111/j.1365-313X.2004.02203.x
Aljaafri, W. A. R. et al. A harpin elicitor induces the expression of a coiled-coil nucleotide binding leucine rich repeat (CC-NB-LRR) defense signaling gene and others functioning during defense to parasitic nematodes. Plant Physiol. Biochem. 121, 161–175 (2017).
pubmed: 29107936
doi: 10.1016/j.plaphy.2017.10.004
McNeece, B. T. et al. A Glycine max homolog of NON-RACE SPECIFIC DISEASE RESISTANCE 1 (NDR1) alters defense gene expression while functioning during a resistance response to different root pathogens in different genetic backgrounds. Plant Physiol. Biochem. 114, 60–71 (2017).
pubmed: 28273511
doi: 10.1016/j.plaphy.2017.02.022
Kunkel, B. N., Bent, A. F., Dahlbeck, D., Innes, R. W. & Staskawicz, B. J. RPS2, an Arabidopsis disease resistance locus specifying recognition of Pseudomonas syringae strains expressing the avirulence gene avrRpt2. Plant Cell 5, 865–875 (1993).
pubmed: 8400869
pmcid: 160322
Mindrinos, M., Katagiri, F., Yu, G. L. & Ausubel, F. M. The A. thaliana disease resistance gene RPS2 encodes a protein containing a nucleotide-binding site and leucine-rich repeats. Cell 78, 1089–1099 (1994).
pubmed: 7923358
doi: 10.1016/0092-8674(94)90282-8
Grant, M. R. et al. Structure of the arabidopsis RPM1 gene enabling dual specificity disease resistance. Science 269, 843–846 (1995).
pubmed: 7638602
doi: 10.1126/science.7638602
van der Biezen, E. A. & Jones, J. D. The NB-ARC domain: a novel signalling motif shared by plant resistance gene products and regulators of cell death in animals. Curr. Biol. 8, R226-227 (1998).
pubmed: 9545207
doi: 10.1016/S0960-9822(98)70145-9
Mackey, D., Holt, B. F. 3rd., Wiig, A. & Dangl, J. L. RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell 108, 743–754 (2002).
pubmed: 11955429
doi: 10.1016/S0092-8674(02)00661-X
Mackey, D., Belkhadir, Y., Alonso, J. M., Ecker, J. R. & Dangl, J. L. Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell 112, 379–389 (2003).
pubmed: 12581527
doi: 10.1016/S0092-8674(03)00040-0
Day, B., Dahlbeck, D. & Staskawicz, B. J. NDR1 interaction with RIN4 mediates the differential activation of multiple disease resistance pathways in Arabidopsis. Plant Cell 18, 2782–2791 (2006).
pubmed: 17012600
pmcid: 1626609
doi: 10.1105/tpc.106.044693
Sabol, P., Kulich, I. & Žárský, V. RIN4 recruits the exocyst subunit EXO70B1 to the plasma membrane. J. Exp. Bot. 68, 3253–3265 (2017).
pubmed: 28338727
pmcid: 5853926
doi: 10.1093/jxb/erx007
Nielsen, M. E., Feechan, A., Böhlenius, H., Ueda, T. & Thordal-Christensen, H. Arabidopsis ARF-GTP exchange factor, GNOM, mediates transport required for innate immunity and focal accumulation of syntaxin PEN1. Proc. Natl. Acad. Sci. USA 109, 11443–11448 (2012).
pubmed: 22733775
doi: 10.1073/pnas.1117596109
pmcid: 3396477
Kulich, I. et al. Arabidopsis exocyst subcomplex containing subunit EXO70B1 is involved in autophagy-related transport to the vacuole. Traffic 14, 1155–1165 (2013).
pubmed: 23944713
Ellinger, D. et al. Elevated early callose deposition results in complete penetration resistance to powdery mildew in Arabidopsis. Plant Physiol. 161, 1433–1444 (2013).
pubmed: 23335625
pmcid: 3585607
doi: 10.1104/pp.112.211011
Ellinger, D. & Voigt, C. A. The use of nanoscale fluorescence microscopic to decipher cell wall modifications during fungal penetration. Front. Plant Sci. 5, 270 (2014).
pubmed: 24995012
pmcid: 4061529
doi: 10.3389/fpls.2014.00270
Ellinger, D. et al. Interaction of the Arabidopsis GTPase RabA4c with its effector PMR4 results in complete penetration resistance to powdery mildew. Plant Cell 26, 3185–3200 (2014).
pubmed: 25056861
pmcid: 4145140
doi: 10.1105/tpc.114.127779
Ellinger, D., Sode, B., Falter, C. & Voigt, C. A. Resistance of callose synthase activity to free fatty acid inhibition as an indicator of Fusarium head blight resistance in wheat. Plant Signal. Behav. 9, e28982 (2014).
pubmed: 25763484
pmcid: 4091610
doi: 10.4161/psb.28982
Yang, L. et al. Myosins XI modulate host cellular responses and penetration resistance to fungal pathogens. Proc. Natl. Acad. Sci. USA 111, 13996–14001 (2014).
pubmed: 25201952
doi: 10.1073/pnas.1405292111
pmcid: 4183272
Leslie, M. E., Rogers, S. W. & Heese, A. Increased callose deposition in plants lacking DYNAMIN-RELATED PROTEIN 2B is dependent upon POWDERY MILDEW RESISTANT 4. Plant Signal. Behav. 11, e1244594 (2016).
pubmed: 27748639
pmcid: 5157887
doi: 10.1080/15592324.2016.1244594
Sassmann, S. et al. An immune-responsive cytoskeletal-plasma membrane feedback loop in plants. Curr. Biol. 28, 2136-2144.e7 (2018).
pubmed: 29937351
pmcid: 6041470
doi: 10.1016/j.cub.2018.05.014
De Benedictis, M. et al. The Arabidopsis thaliana knockout mutant for phytochelatin synthase1 (cad1-3) is defective in callose deposition, bacterial pathogen defense and auxin content, but shows an increased stem lignification. Front. Plant Sci. 9, 19 (2018).
pubmed: 29403524
pmcid: 5786554
doi: 10.3389/fpls.2018.00019
Klink, V., Alkharouf, N., MacDonald, M. & Matthews, B. Laser capture microdissection (LCM) and analysis of Glycine max (soybean) syncytial cells formed by the soybean cyst nematode Heterodera glycines. Plant Mol. Biol. 59, 969–983 (2005).
doi: 10.1007/s11103-005-2416-7
Klink, V. P., Overall, C. C., Alkharouf, N. W., Macdonald, M. H. & Matthews, B. F. Microarray detection call methodology as a means to identify and compare transcripts expressed within syncytial cells from Soybean (Glycine max) roots undergoing resistant and susceptible reactions to the soybean cyst nematode (Heterodera glycines). J. Biomed. Biotechnol. 2010, 491217 (2010).
pubmed: 20508855
pmcid: 2875038
doi: 10.1155/2010/491217
Murashige, T. & Skoog, F. A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol. Plant. 15, 473–497 (1962).
doi: 10.1111/j.1399-3054.1962.tb08052.x
Jenkins, W. A rapid centrifugal-flotation technique for separating nematodes from soil. Plant Dis. Rep. 48, 692 (1964).