8 The Nuclear Pore Complex in Symbiosis and Pathogen Defence
Annual Plant Reviews book series, Volume 46: Plant Nuclear Structure, Genome Architecture and Gene Regulation
Andreas Binder,
Martin Parniske,
Andreas Binder
Faculty of Biology, Genetics, University of Munich (LMU), Großhaderner Straße 2-4, Martinsried, 82152 Germany
Search for more papers by this authorMartin Parniske
Faculty of Biology, Genetics, University of Munich (LMU), Großhaderner Straße 2-4, Martinsried, 82152 Germany
Search for more papers by this authorAndreas Binder,
Martin Parniske,
Andreas Binder
Faculty of Biology, Genetics, University of Munich (LMU), Großhaderner Straße 2-4, Martinsried, 82152 Germany
Search for more papers by this authorMartin Parniske
Faculty of Biology, Genetics, University of Munich (LMU), Großhaderner Straße 2-4, Martinsried, 82152 Germany
Search for more papers by this authorFirst published: 19 April 2018
This article was originally published in 2013 in Plant Nuclear Structure, Genome Architecture and Gene Regulation, Volume 46 (ISBN 9781118472453) of the Annual Plant Reviews book series, this volume edited by David Evans, Katja Graumann and John A. Bryant. The article was republished in Annual Plant Reviews online in April 2018.
Abstract
Nuclear pores mediate all transport in and out of the nucleus. While nuclear pore complexes (NPCs) have been intensively studied in yeast and animals, they are not well characterized in plants. Nevertheless, forward and reverse genetic screens have identified plant nucleoporins with functions in various plant processes, including plant-microbe interactions. This indicates that signalling between cytoplasm and nucleus is a key event in the corresponding pathways. Loss of function mutants of Lotus japonicus NUCLEOPORIN85 (NUP85), NUP133 and NENA are impaired in arbuscular mycorrhiza and root nodule symbiosis and unable to induce symbiotic calcium oscillations in the nucleus. Arabidopsis thaliana NUP96 and NUP88 are required in both pathogen-associated molecular pattern (PAMP)-triggered and disease-resistance (R) gene-mediated defence signalling. In comparison to the yeast and animal systems, this review discusses possible specific and general functions and targets of plant nucleoporins with a focus on the role of the NPC in plant-microbe interactions.
References
- Aarts, N., Metz, M., Holub, E. et al. (1998) Different requirements for EDS1 and NDR1 by disease resistance genes define at least two R gene-mediated signalling pathways in Arabidopsis . Proceedings of the National Academy of Sciences 95, 10306–10311.
- Akhtar, A. and Gasser, S.M. (2007) The nuclear envelope and transcriptional control. Nature Review Genetics 8, 507–517.
- Alber, F., Dokudovskaya, S., Veenhoff, L.M. et al. (2007) The molecular architecture of the nuclear pore complex. Nature 450, 695–701.
- Allen, R.S., Li, J., Stahle, M.I. et al. (2007) Genetic analysis reveals functional redundancy and the major target genes of the Arabidopsis miR159 family. Proceedings of the National Academy of Sciences 104, 16371–16376.
- Ané, J.-M., Kiss, G.B., Riely, B.K. et al. (2004) Medicago truncatula DMI1 required for bacterial and fungal symbioses in legumes. Science 303, 1364–1367.
- Bai, S.W., Rouquette, J., Umeda, M. et al. (2004) The fission yeast Nup107-120 complex functionally interacts with the small GTPase Ran/Spi1 and is required for mRNA export, nuclear pore distribution, and proper cell division. Molecular and Cellular Biology 24, 6379–6392.
- Banerjee, H., Gibbs, J., Jordan, T. and Blackshear, M. (2010) Depletion of a single nucleoporin, Nup107, induces apoptosis in eukaryotic cells. Molecular and Cellular Biochemistry 343, 21–25.
- Bapteste, E., Charlebois, R., Macleod, D. and Brochier, C. (2005) The two tempos of nuclear pore complex evolution: highly adapting proteins in an ancient frozen structure. Genome Biology 6, R85.
- Belgareh, N., Rabut, G., Baï, S.W. et al. (2001) An evolutionarily conserved NPC subcomplex, which redistributes in part to kinetochores in mammalian cells. The Journal of Cell Biology 154, 1147–1160.
- Bernad, R., Van Der Velde, H., Fornerod, M. and Pickersgill, H. (2004) Nup358/RanBP2 attaches to the nuclear pore complex via association with Nup88 and Nup214/CAN and plays a supporting role in CRM1-mediated nuclear protein export. Molecular and Cellular Biology 24, 2373–2384.
- Boehmer, T., Enninga, J., Dales, S. et al. (2003) Depletion of a single nucleoporin, Nup107, prevents the assembly of a subset of nucleoporins into the nuclear pore complex. Proceedings of the National Academy of Sciences 100, 981–985.
- Bollman, K.M., Aukerman, M.J., Park, M.-Y. et al. (2003) HASTY, the Arabidopsis ortholog of exportin 5/MSN5, regulates phase change and morphogenesis. Development 130, 1493–1504.
- Bootman, M.D., Fearnley, C., Smyrnias, I. et al. (2009) An update on nuclear calcium signalling. Journal of Cell Science 122, 2337–2350.
- Brown, C.R., Kennedy, C.J., Delmar, V.A. et al. (2008) Global histone acetylation induces functional genomic reorganization at mammalian nuclear pore complexes. Genes and Development 22, 627–639.
- Burch-Smith, T.M., Schiff, M., Caplan, J.L. et al. (2007) A novel role for the TIR domain in association with pathogen-derived elicitors. PloS Biology 5, e68.
- Bustamante, J.O. (2006) Current concepts in nuclear pore electrophysiology. Canadian Journal of Physiology and Pharmacology 84, 347–365.
- Cao, H., Glazebrook, J., Clarke, J.D. et al. (1997) The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell 88, 57–63.
- Capelson, M. and Hetzer, M.W. (2009) The role of nuclear pores in gene regulation, development and disease. EMBO Reports 10, 697–705.
- Capelson, M., Liang, Y., Schulte, R. et al. (2010) Chromatin-bound nuclear pore components regulate gene expression in higher eukaryotes. Cell 140, 372–383.
- Caplan, J., Padmanabhan, M. and Dinesh-Kumar, S.P. (2008) Plant NB-LRR Immune receptors: from recognition to transcriptional reprogramming. Cell Host and Microbe 3, 126–135.
- Capoen, W., Sun, J., Wysham, D. et al. (2011) Nuclear membranes control symbiotic calcium signalling of legumes. Proceedings of the National Academy of Sciences 108, 14348–14353.
- Chabaud, M., Genre, A., Sieberer, B.J. et al. (2011) Arbuscular mycorrhizal hyphopodia and germinated spore exudates trigger Ca2+ spiking in the legume and nonlegume root epidermis. New Phytologist 189, 347–355.
- Charpentier, M., Bredemeier, R., Wanner, G. et al. (2008) Lotus japonicus CASTOR and POLLUX are ion channels essential for perinuclear calcium spiking in legume root endosymbiosis. Plant Cell 20, 3467–3479.
- Chatel, G. and Fahrenkrog, B. (2011) Nucleoporins: Leaving the nuclear pore complex for a successful mitosis. Cellular Signalling 23, 1555–1562.
- Cheng, Y.T., Germain, H., Wiermer, M. et al. (2009) Nuclear pore complex component MOS7/Nup88 is required for innate immunity and nuclear accumulation of defense regulators in Arabidopsis . Plant Cell 21, 2503–2516.
- D'Angelo, M.A. and Hetzer, M.W. (2008) Structure, dynamics and function of nuclear pore complexes. Trends in Cell Biology 18, 456–466.
- Danker, T., Shahin, V., Schlune, A. et al. (2001) Electrophoretic plugging of nuclear pores by using the nuclear hourglass technique. Journal of Membrane Biology 184, 91–99.
- Deslandes, L. and Rivas, S. (2011) The plant cell nucleus: a true arena for the fight between plants and pathogens. Plant Signaling and Behavior 6, 42.
- Després, C., Delong, C., Glaze, S. et al. (2000) The Arabidopsis NPR1/NIM1 protein enhances the DNA binding activity of a subgroup of the TGA family of bZIP transcription factors. Plant Cell 12, 279–290.
- Dharmasiri, N. and Estelle, M. (2004) Auxin signalling and regulated protein degradation. Trends in Plant Science 9, 302–308.
- Dong, C.-H., Hu, X., Tang, W. et al. (2006) A putative Arabidopsis nucleoporin, AtNUP160, is critical for RNA export and required for plant tolerance to cold stress. Molecular and Cellular Biology 26, 9533–9543.
- Doucet, C.M., Talamas, J.A. and Hetzer, M.W. (2010) Cell cycle-dependent differences in nuclear pore complex assembly in metazoa. Cell 141, 1030–1041.
- Durrant, W.E. and Dong, X. (2004) Systemic acquired resistance. Annual Review of Phytopathology 42, 185–209.
- Ehrhardt, D.W., Wais, R. and Long, S.R. (1996) Calcium spiking in plant root hairs responding to rhizobium nodulation signals. Cell 85, 673–681.
- Endre, G., Kereszt, A., Kevei, Z. et al. (2002) A receptor kinase gene regulating symbiotic nodule development. Nature 417, 962–966.
- Enninga, J., Levy, D.E., Blobel, G.N. and Fontoura, B.M.A. (2002) Role of nucleoporin induction in releasing an mRNA nuclear export block. Science 295, 1523–1525.
- Faria, A.M.C., Levay, A., Wang, Y. et al. (2006) The nucleoporin Nup96 is required for proper expression of interferon-regulated proteins and functions. Immunity 24, 295–304.
- Felle, H.H., Kondorosi, É., Kondorosi, Á. and Schultze, M. (1998) The role of ion fluxes in Nod factor signalling in Medicago sativa . The Plant Journal 13, 455–463.
- Fernandez-Martinez, J. and Rout, M.P. (2009) Nuclear pore complex biogenesis. Current Opinion in Cell Biology 21, 603–612.
- Feys, B.J., Wiermer, M., Bhat, R.A. et al. (2005) Arabidopsis SENESCENCE-ASSOCIATED GENE101 stabilizes and signals within an ENHANCED DISEASE SUSCEPTIBILITY1 complex in plant innate immunity. Plant Cell 17, 2601–2613.
- Fiserova, J., Kiseleva, E. and Goldberg, M.W. (2009) Nuclear envelope and nuclear pore complex structure and organization in tobacco BY-2 cells. The Plant Journal 59, 243–255.
- Frey, S. and Görlich, D. (2007) A saturated FG-repeat hydrogel can reproduce the permeability properties of nuclear pore complexes. Cell 130, 512–523.
- Gaffney, T., Friedrich, L., Vernooij, B. et al. (1993) Requirement of salicylic acid for the induction of systemic acquired resistance. Science 261, 754–756.
- García, A.V., Blanvillain-Baufumé, S., Huibers, R.P. et al. (2010) Balanced nuclear and cytoplasmic activities of EDS1 are required for a complete plant innate immune response. PLoS Pathogens 6, e1000970.
- Genre, A., Chabaud, M., Faccio, A. et al. (2008) Prepenetration apparatus assembly precedes and predicts the colonization patterns of arbuscular mycorrhizal fungi within the root cortex of both Medicago truncatula and Daucus carota . Plant Cell 20, 1407–1420.
- Gong, Z., Dong, C.-H., Lee, H. et al. (2005) A DEAD box RNA helicase is essential for mRNA export and important for development and stress responses in Arabidopsis . Plant Cell 17, 256–267.
- Gong, Z., Lee, H., Xiong, L. et al. (2002) RNA helicase-like protein as an early regulator of transcription factors for plant chilling and freezing tolerance. Proceedings of the National Academy of Sciences 99, 11507–11512.
- Goormachtig, S., Capoen, W. and Holsters, M. (2004) Rhizobium infection: lessons from the versatile nodulation behaviour of water-tolerant legumes. Trends in Plant Science 9, 518–522.
- Greenberg, J.T. and Yao, N. (2004) The role and regulation of programmed cell death in plant–pathogen interactions. Cellular Microbiology 6, 201–211.
- Groth, M., Takeda, N., Perry, J. et al. (2010) NENA, a Lotus japonicus homolog of Sec13, is required for rhizodermal infection by arbuscular mycorrhiza fungi and rhizobia but dispensable for cortical endosymbiotic development. Plant Cell 22, 2509.
- Harel, A., Orjalo, A.V., Vincent, T. et al. (2003) Removal of a single pore subcomplex results in vertebrate nuclei devoid of nuclear pores. Molecular Cell 11, 853–864.
- Hayashi, T., Banba, M., Shimoda, Y. et al. (2010) A dominant function of CCaMK in intracellular accommodation of bacterial and fungal endosymbionts. The Plant Journal 63, 141–154.
- Heidrich, K., Wirthmueller, L., Tasset, C. et al. (2011) Arabidopsis EDS1 connects pathogen effector recognition to cell compartment-specific immune responses. Science 334, 1401–1404.
- Hoelz, A., Debler, E.W. and Blobel, G. (2011) The structure of the nuclear pore complex. Annual Review of Biochemistry 80, 613–643.
- Hohn, T. and Vazquez, F. (2011) RNA silencing pathways of plants: silencing and its suppression by plant DNA viruses. Biochimica et Biophysica Acta (BBA) – Gene Regulatory Mechanisms 1809, 588–600.
- Iglesias, N. and Stutz, F.O. (2008) Regulation of mRNP dynamics along the export pathway. FEBS Letters 582, 1987–1996.
- Imaizumi-Anraku, H., Takeda, N., Charpentier, M. et al. (2005) Plastid proteins crucial for symbiotic fungal and bacterial entry into plant roots. Nature, 433, 527–531.
- Jacob, Y., Mongkolsiriwatana, C., Veley, K.M. et al. (2007) The nuclear pore protein AtTPR is required for RNA homeostasis, flowering time, and auxin signaling. Plant Physiology 144, 1383–1390.
- Jones, J.D.G. and Dangl, J.L. (2006) The plant immune system. Nature 444, 323–329.
- Kaló, P., Gleason, C., Edwards, A. et al. (2005) Nodulation signaling in legumes requires NSP2, a member of the GRAS family of transcriptional regulators. Science 308, 1786–1789.
- Kalverda, B., Pickersgill, H., Shloma, V.V. and Fornerod, M. (2010) Nucleoporins directly stimulate expression of developmental and cell-cycle genes inside the nucleoplasm. Cell 140, 360–371.
- Kanamori, N., Madsen, L., Radutoiu, S. et al. (2006) A nucleoporin is required for induction of Ca2+ spiking in legume nodule development and essential for rhizobial and fungal symbiosis. Proceedings of the National Academy of Sciences 103, 359.
- Kim, S.-H., Arnold, D., Lloyd, A. and Roux, S.J. (2001) Antisense expression of an Arabidopsis Ran binding protein renders transgenic roots hypersensitive to auxin and alters auxin-induced root growth and development by arresting mitotic progress. Plant Cell 13, 2619–2630.
- Kinkema, M., Fan, W. and Dong, X. (2000) Nuclear localization of NPR1 is required for activation of PR gene expression. Plant Cell 12, 2339.
- Kistner, C. and Parniske, M. (2002) Evolution of signal transduction in intracellular symbiosis. Trends in Plant Science 7, 511–518.
- Kistner, C., Winzer, T., Pitzschke, A. et al. (2005) Seven Lotus japonicus genes required for transcriptional reprogramming of the root during fungal and bacterial symbiosis. Plant Cell 17, 2217–2229.
- Kodiha, M., Tran, D., Qian, C. et al. (2008) Oxidative stress mislocalizes and retains transport factor importin-α and nucleoporins Nup153 and Nup88 in nuclei where they generate high molecular mass complexes. Biochimica et Biophysica Acta (BBA) – Molecular Cell Research 1783, 405–418.
- Kosuta, S., Hazledine, S., Sun, J. et al. (2008) Differential and chaotic calcium signatures in the symbiosis signalling pathway of legumes. Proceedings of the National Academy of Sciences 105, 9823–9828.
- Kudla, J., Batistic, O. and Hashimoto, K. (2010) Calcium signals: the lead currency of plant information processing. Plant Cell 22, 541–563.
- Lecourieux, D., Lamotte, O., Bourque, S.P. et al. (2005) Proteinaceous and oligosaccharidic elicitors induce different calcium signatures in the nucleus of tobacco cells. Cell Calcium 38, 527–538.
- Lecourieux, D., Ranjeva, R. and Pugin, A. (2006) Calcium in plant defence-signalling pathways. New Phytologist 171, 249–269.
- Lee, J.-Y., Lee, H.-S., Wi, S.-J. et al. (2009) Dual functions of Nicotiana benthamiana Rae1 in interphase and mitosis. The Plant Journal 59, 278–291.
- Lévy, J., Bres, C., Geurts, R. et al. (2004) A putative Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 303, 1361–1364.
- Li, O., Heath, C.V., Amberg, D.C. et al. (1995) Mutation or deletion of the Saccharomyces cerevisiae RAT3/NUP133 gene causes temperature-dependent nuclear accumulation of poly(A)+ RNA and constitutive clustering of nuclear pore complexes. Molecular Biology of the Cell 6, 401–417.
- Li, X., Clarke, J.D., Zhang, Y. and Dong, X. (2001) Activation of an EDS1-mediated R-gene pathway in the snc1 mutant leads to constitutive, NPR1-independent pathogen resistance. Molecular Plant–Microbe Interactions 14, 1131–1139.
- Loïodice, I., Alves, A., Rabut, G. et al. (2004) The entire Nup107-160 complex, including three new members, is targeted as one entity to kinetochores in mitosis. Molecular Biology of the Cell 15, 3333–3344.
- Lu, Q., Tang, X., Tian, G. et al. (2010) Arabidopsis homolog of the yeast TREX-2 mRNA export complex: components and anchoring nucleoporin. The Plant Journal 61, 259–270.
- Lupu, F., Alves, A., Anderson, K. et al. (2008) Nuclear pore composition regulates neural stem/progenitor cell differentiation in the mouse embryo. Developmental Cell 14, 831–842.
- Lusk, C.P., Blobel, G. and King, M.C. (2007) Highway to the inner nuclear membrane: rules for the road. Nature Reviews Molecular Cell Biology, 8, 414–420.
- Lutzmann, M., Kunze, R., Buerer, A. et al. (2002) Modular self-assembly of a Y-shaped multiprotein complex from seven nucleoporins. EMBO Journal 21, 387–397.
- Madsen, E.B., Madsen, L.H., Radutoiu, S. et al. (2003) A receptor kinase gene of the LysM type is involved in legumeperception of rhizobial signals. Nature 425, 637–640.
- Madsen, L.H., Tirichine, L., Jurkiewicz, A. et al. (2010) The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus . Nature Communications 1, 10.
- Maillet, F., Poinsot, V., Andre, O. et al. (2011) Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469, 58–63.
- Mazars, C., Bourque, S., Mithöfer, A. et al. (2009) Calcium homeostasis in plant cell nuclei. New Phytologist 181, 261–274.
- Meier, I. and Brkljacic, J. (2009) The nuclear pore and plant development. Current Opinion in Plant Biology 12, 87–95.
- Meinema, A.C., Laba, J.K., Hapsari, R.A. et al. (2011) Long unfolded linkers facilitate membrane protein import through the nuclear pore complex. Science 333, 90–93.
- Messinese, E., Mun, J.-H., Yeun, L.H., et al. (2007) A novel nuclear protein interacts with the symbiotic DMI3 calcium- and calmodulin-dependent protein kinase of Medicago truncatula . Molecular Plant-Microbe Interactions 20, 912–921.
- Mitra, R.M., Gleason, C.A., Edwards, A. et al. (2004) A Ca2+/calmodulin-dependent protein kinase required for symbiotic nodule development: Gene identification by transcript-based cloning. Proceedings of the National Academy of Sciences of the United States of America 101, 4701–4705.
- Miwa, H., Sun, J., Oldroyd, G.E.D. and Downie, J.A. (2006) Analysis of nod-factor-induced calcium signaling in root hairs of symbiotically defective mutants of Lotus japonicus . Molecular Plant-Microbe Interactions 19, 914–923.
- Monaghan, J., Germain, H., Weihmann, T. and Li, X. (2010) Dissecting plant defence signal transduction: modifiers of snc1 in Arabidopsis . Canadian Journal of Plant Pathology 32, 35–42.
- Ohba, T., Schirmer, E.C., Nishimoto, T. and Gerace, L. (2004) Energy- and temperature-dependent transport of integral proteins to the inner nuclear membrane via the nuclear pore. The Journal of Cell Biology 167, 1051–1062.
- Oldroyd, G.E.D. and Downie, J.A. (2008) Coordinating nodule morphogenesis with rhizobial infection in legumes. Annual Review of Plant Biology 59, 519–546.
- Oldroyd, G.E.D., Murray, J.D., Poole, P.S. and Downie, J.A. (2011) The rules of engagement in the legume-rhizobial symbiosis. Annual Review of Genetics 45, 119–145.
- Op Den Camp, R., Streng, A., De Mita, S. et al. (2011) LysM-type mycorrhizal receptor recruited for rhizobium symbiosis in nonlegume Parasponia . Science 331, 909–912.
- Orjalo, A.V., Arnaoutov, A., Shen, Z. et al. (2006) The Nup107-160 nucleoporin complex is required for correct bipolar spindle assembly. Molecular Biology of the Cell 17, 3806–3818.
- Palma, K., Zhang, Y. and Li, X. (2005) An importin alpha homolog, MOS6, plays an important role in plant innate immunity. Current Biology 15, 1129–1135.
- Park, M.Y., Wu, G., Gonzalez-Sulser, A. et al. (2005) Nuclear processing and export of microRNAs in Arabidopsis . Proceedings of the National Academy of Sciences of the United States of America 102, 3691–3696.
- Parniske, M. (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nature Reviews Microbiology 6, 763–775.
- Parry, G., Ward, S., Cernac, A. et al. (2006) The Arabidopsis SUPPRESSOR OF AUXIN RESISTANCE proteins are nucleoporins with an important role in hormone signalling and development. Plant Cell 18, 1590–1603.
-
Pawlowski, K. and Sprent, J.I. (2008) Comparison between actinorhizal and legume symbiosis nitrogen-fixing actinorhizal symbioses. In: K. Pawlowski and W.E. Newton (eds) Nitrogen-Fixing Actinorhizal Symbioses, Springer, Dordrecht.
10.1007/978-1-4020-3547-0 Google Scholar
- Perry, J., Brachmann, A., Welham, T. et al. (2009) TILLING in Lotus japonicus identified large allelic series for symbiosis genes and revealed a bias in functionally defective ethyl methanesulfonate alleles toward glycine replacements. Plant Physiology 151, 1281–1291.
- Radutoiu, S., Madsen, L.H., Madsen, E.B., et al. (2003) Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature 425, 585–592.
- Reeves, P.H., Murtas, G., Dash, S. and Coupland, G. (2002) Early in short days 4, a mutation in Arabidopsis that causes early flowering and reduces the mRNA abundance of the floral repressor FLC . Development 129, 5349–5361.
- Ribbeck, K., Lipowsky, G., Kent, H.M. et al. (1998) NTF2 mediates nuclear import of Ran. EMBO Journal 17, 6587–6598.
- Rodrigues, M.A., Gomes, D.A., Nathanson, M.H. and Leite, M.F. (2009) Nuclear calcium signalling: a cell within a cell. Brazilian Journal of Medical and Biological Research 42, 17–20.
- Roth, P., Xylourgidis, N., Sabri, N. et al. (2003) The Drosophila nucleoporin DNup88 localizes DNup214 and CRM1 on the nuclear envelope and attenuates NES-mediated nuclear export. The Journal of Cell Biology 163, 701–706.
- Saito, K., Yoshikawa, M., Yano, K. et al. (2007) NUCLEOPORIN85 is required for calcium spiking, fungal and bacterial symbioses, and seed production in Lotus japonicus . Plant Cell 19, 610–624.
- Schüßler, A., Schwarzott, D. and Walker, C. (2001) A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycological Research 105, 1413–1421.
- Schüßler, A. and Walker, C. (2010) The Glomeromycota: A species list with new families and genera. Edinburgh & Kew, UK: The Royal Botanic Garden; Munich, Germany: Botanische Staatssammlung Munich; Oregon, USA: Oregon State University. URL: http://www.amf-phylogeny.com. ISBN-13: 9781466388048; ISBN-10: 1466388048.
- Scott, I.M., Clarke, S.M., Wood, J.E. and Mur, L. (2004) Salicylate accumulation inhibits growth at chilling temperature in Arabidopsis . Plant Physiology 135, 1040–1049.
- Shahin, V., Danker, T., Enss, K. et al. (2001) Evidence for Ca2+- and ATP-sensitive peripheral channels in nuclear pore complexes. The FASEB Journal 15, 1895–1901.
- Shaw, S.L. and Long, S.R. (2003) Nod factor elicits two separable calcium responses in Medicago truncatula root hair cells. Plant Physiology 131, 976–984.
- Shen, Q.-H., Saijo, Y., Mauch, S. et al. (2007) Nuclear activity of MLA immune receptors links isolate-specific and basal disease-resistance responses. Science 315, 1098–1103.
- Sieberer, B.J., Chabaud, M., Timmers, A.C. et al. (2009) A nuclear-targeted cameleon demonstrates intranuclear Ca2+ spiking in Medicago truncatula root hairs in response to rhizobial nodulation factors. Plant Physiology 151, 1197–1206.
- Siniossoglou, S., Wimmer, C., Rieger, M. et al. (1996) A novel complex of nucleoporins, which includes Sec13p and a Sec13p homolog, is essential for normal nuclear pores. Cell 84, 265–275.
- Smith, S.E. and Read, D.J. (2008) Mycorrhizal symbiosis, London, Academic Press.
- Smith, S.E. and Smith, F.A. (2011) Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annual Review of Plant Biology 62, 227–250.
- Soltis, D.E., Soltis, P.S., Chase, M.W., et al. (2000) Angiosperm phylogeny inferred from 18S rDNA, rbcL, and atpB sequences. Botanical Journal of the Linnean Society 133, 381–461.
- Sprent, J.I. (2007) Evolving ideas of legume evolution and diversity: a taxonomic perspective on the occurrence of nodulation. New Phytologist 174, 11–25.
- Stockinger, H., Walker, C. and Schüßler, A. (2009) ‘ Glomus intraradices DAOM197198’, a model fungus in arbuscular mycorrhiza research, is not Glomus intraradices . New Phytologist 183, 1176–1187.
- Stracke, S., Kistner, C., Yoshida, S. et al. (2002) A plant receptor-like kinase required for both bacterial and fungal symbiosis. Nature 417, 959–962.
- Strambio-De-Castillia, C., Niepel, M. and Rout, M.P. (2010) The nuclear pore complex: bridging nuclear transport and gene regulation. Nature Reviews Molecular Cell Biology 11, 490–501.
- Sunkar, R. and Zhu, J.-K. (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis . Plant Cell 16, 2001–2019.
- Tamura, K., Fukao, Y., Iwamoto, M. et al. (2010) Identification and characterization of nuclear pore complex components in Arabidopsis thaliana . Plant Cell 22, 4084–4097.
- Tirichine, L., Imaizumi-Anraku, H., Yoshida, S., et al. (2006) Deregulation of a Ca2+/calmodulin-dependent kinase leads to spontaneous nodule development. Nature 441, 1153–1156.
- Uv, A.E., Roth, P., Xylourgidis, N. et al. (2000) Members only encodes a Drosophila nucleoporin required for Rel protein import and immune response activation. Genes and Development 14, 1945–1957.
- Vasu, S., Shah, S., Orjalo, A. et al. (2001) Novel vertebrate nucleoporins Nup133 and Nup160 play a role in mRNA export. The Journal of Cell Biology 155, 339–354.
- Venugopal, S.C., Jeong, R.-D., Mandal, M.K. et al. (2009) Enhanced disease susceptibility 1 and salicylic acid act redundantly to regulate resistance gene-mediated signaling. PlOS Genetics 5, e1000545.
- Walter, A., Mazars, C., Maitrejean, M. et al. (2007) Structural requirements of jasmonates and synthetic analogues as inducers of Ca2+ signals in the nucleus and the cytosol of plant cells. Angewandte Chemie International Edition 46, 4783–4785.
- Walther, T.C., Alves, A., Pickersgill, H. et al. (2003) The conserved Nup107-160 complex is critical for nuclear pore complex assembly. Cell 113, 195–206.
- Wente, S.R. (2000) Gatekeepers of the nucleus. Science 288, 1374–1377.
- Wente, S.R. and Rout, M.P. (2010) The nuclear pore complex and nuclear transport. Cold Spring Harbor Perspectives in Biology 2.
- White, J., Prell, J., James, E. and Poole, P. (2007) Nutrient sharing between symbionts. Plant Physiology 144, 604–614.
- Wiermer, M., Cheng, Y.T., Imkampe, J. et al. (2012) Putative members of the Arabidopsis Nup107-160 nuclear pore sub-complex contribute to pathogen defense. The Plant Journal 70, 796–808.
- Wiermer, M., Palma, K., Zhang, Y. and Li, X. (2007) Should I stay or should I go? Nucleocytoplasmic trafficking in plant innate immunity. Cellular Microbiology 9, 1880–1890.
- Wirthmueller, L., Zhang, Y., Jones, J.D.G. and Parker, J.E. (2007) Nuclear accumulation of the Arabidopsis immune receptor RPS4 is necessary for triggering EDS1-dependent defense. Current Biology 17, 2023–2029.
- Xiong, T.C., Jauneau, A., Ranjeva, R. and Mazars, C. (2004) Isolated plant nuclei as mechanical and thermal sensors involved in calcium signalling. The Plant Journal 40, 12–21.
- Xu, X.M. and Meier, I. (2008) The nuclear pore comes to the fore. Trends in Plant Science 13, 20–27.
- Xu, X.M., Rose, A., Muthuswamy, S. et al. (2007) NUCLEAR PORE ANCHOR, the Arabidopsis homolog of Tpr/Mlp1/Mlp2/megator, is involved in mRNA export and SUMO homeostasis and affects diverse aspects of plant development. Plant Cell 19, 1537.
- Xylourgidis, N., Roth, P., Sabri, N., et al. (2006) The nucleoporin Nup214 sequesters CRM1 at the nuclear rim and modulates NFκB activation in Drosophila . Journal of Cell Science 119, 4409–4419.
- Yano, K., Yoshida, S., Müller, J. et al. (2008) CYCLOPS, a mediator of symbiotic intracellular accommodation. Proceedings of the National Academy of Sciences 105, 20540–20545.
- Zhang, Y., Fan, W., Kinkema, M. et al. (1999) Interaction of NPR1 with basic leucine zipper protein transcription factors that bind sequences required for salicylic acid induction of the PR-1 gene. Proceedings of the National Academy of Sciences 96, 6523–6528.
- Zhang, Y., Goritschnig, S., Dong, X. and Li, X. (2003) A gain-of-function mutation in a plant disease resistance gene leads to constitutive activation of downstream signal transduction pathways in suppressor of npr1-1, constitutive 1 . Plant Cell 15, 2636–2646.
- Zhang, Y. and Li, X. (2005) A putative Nucleoporin 96 is required for both basal defense and constitutive resistance responses mediated by suppressor of npr1-1,constitutive 1 . Plant Cell 17, 1306–1316.
- Zhao, Q., Brkljacic, J. and Meier, I. (2008) Two distinct interacting classes of nuclear envelope-associated coiled-coil proteins are required for the tissue-specific nuclear envelope targeting of Arabidopsis RanGAP. Plant Cell 20, 1639–1651.
- Zhao, Q., Leung, S., Corbett, A.H. and Meier, I. (2006) Identification and characterization of the Arabidopsis orthologs of nuclear transport Factor 2, the nuclear import factor of Ran. Plant Physiology 140, 869–878.
- Zhao, Q. and Meier, I. (2011) Identification and characterization of the Arabidopsis FG-repeat nucleoporin Nup62. Plant Signaling and Behavior 6, 330–334.
- Zhou, G.-K., Kubo, M., Zhong, R. et al. (2007) Overexpression of miR165 affects apical Meristem formation, organ polarity establishment and vascular development in Arabidopsis . Plant and Cell Physiology 48, 391–404.
- Zhou, J.-M., Trifa, Y., Silva, H. et al. (2000) NPR1 differentially interacts with members of the TGA/OBF family of transcription factors that bind an element of the PR-1 gene required for induction by salicylic acid. Molecular Plant-Microbe Interactions 13, 191–202.
- Zhu, S., Jeong, R.-D., Venugopal, S.C. et al. (2011) SAG101 forms a ternary complex with EDS1 and PAD4 and is required for resistance signaling against turnip crinkle virus. PLOS Pathogens 7, e1002318.
- Zhu, Z., Xu, F., Zhang, Y. et al. (2010) Arabidopsis resistance protein SNC1 activates immune responses through association with a transcriptional corepressor. Proceedings of the National Academy of Sciences of the United States of America 107, 13960–13965.
- Zipfel, C. and Felix, G. (2005) Plants and animals: a different taste for microbes? Current Opinion in Plant Biology, 8, 353–360.
- Zuccolo, M., Alves, A., Galy, V. et al. (2007) The human Nup107-160 nuclear pore subcomplex contributes to proper kinetochore functions. EMBO Journal 26, 1853–1864.
- Zuleger, N., Korfali, N. and Schirmer, E. (2008) Inner nuclear membrane protein transport is mediated by multiple mechanisms. Biochemical Society Transactions 36, 1373–1377.
Browse other articles of this reference work:
