Selectable marker-free co-expression of Nicotiana rustica CN and Nicotiana tabacum HAK1 genes improves resistance to tobacco mosaic virus in tobacco
Li-Jun Qin A B , Dan Zhao A , Yi Zhang B and De-Gang Zhao A CA The Key Laboratory of Plant Resources Conservation and Germplasm Innovation in Mountainous Region (Ministry of Education), Institute of Agro-Bioengineering and College of Life Sciences, Guizhou University, Guiyang 550025, Guizhou Province, People’s Republic of China.
B The State Key Laboratory Breeding Base of Green Pesticide and Agricultural Biological Engineering, Guizhou University, Guiyang, 550025, Guizhou Province, People’s Republic of China.
C Corresponding author. Email: dgzhao@gzu.edu.cn
Functional Plant Biology 42(8) 802-815 https://doi.org/10.1071/FP14356
Submitted: 17 December 2014 Accepted: 29 April 2015 Published: 4 June 2015
Abstract
The viral disease caused by tobacco mosaic virus (TMV) is the most prevalent viral disease in many tobacco production areas. A breeding strategy based on resistance genes is an effective method for improving TMV resistance in tobacco. Also, the physiological status of plants is also critical to disease resistance improvement. Potassium ion is one of the most abundant inorganic nutrients in plant cells, and mediates plant responses to abiotic and biotic stresses. Improving K+ content in soil by fertilising can enhance diseases resistance of crops. However, the K+ absorption in plants depends mostly on K+ transporters located in cytoplasmic membrane. Therefore, the encoding genes for K+ transporters are putative candidates to target for improving tobacco mosaic virus resistance. In this work, the synergistic effect of a N-like resistance gene CN and a tobacco putative potassium transporter gene HAK1 was studied. The results showed that TMV-resistance in CN-HAK1-containing tobaccos was significantly enhanced though a of strengthening leaf thickness and reduction in the size of necrotic spots compared with only CN-containing plants, indicating the improvement of potassium nutrition in plant cells could increase the tobacco resistance to TMV by reducing the spread of the virus. Quantitative real-time polymerase chain reaction (qRT–PCR) analysis for TMV-CP expression in the inoculated leaf of the transgenic and wild-type plants also supported the conclusion. Further, the results of defence-related determination including antioxidative enzymes (AOEs) activity, salicylic acid (SA) content and the expression of resistance-related genes demonstrated CN with HAK1 synergistically enhanced TMV-resistance in transgenic tobaccos. Additionally, the HAK1- overexpression significantly improved the photosynthesis and K+-enriching ability in trans-CN-HAK1 tobaccos, compared with other counterparts. Finally, this work provides a method for screening new varieties of marker-free and safe transgenic antiviral tobacco.
Additional keywords: TMV resistance, potassium-enrichment, co-transformation, tobaccos.
References
Amtmann A, Armengaud P, Volkov V (2004) Potassium nutrition and salt stress. In ‘Membrane transport in plants’. (Ed. MR Blatt) pp. 293–339. (Blackwell Press: Oxford)Amtmann A, Troufflard S, Armengaud P (2008) The effect of potassium nutrition on pest and disease resistance in plants. Physiologia Plantarum 133, 682–691.
| The effect of potassium nutrition on pest and disease resistance in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXps1Oit7s%3D&md5=4d6cfc34ad2ef3dea010e8ed53d4b325CAS | 18331404PubMed |
Auh CK, Murphy TM (1995) Plasma membrane redox enzyme is involved in the synthesis of O2•–and H2O2 by phytophthora elicitor-stimulated rose cells. Plant Physiology 107, 1241–1247.
Azevedo C, Sadanandom A, Kitagawa K, Freialdenhoven A, Shirasu K, Schulze-Lefert P (2002) The RAR1 interactor SGT1, an essential component of R gene-triggered disease resistance. Science 295, 2073–2076.
| The RAR1 interactor SGT1, an essential component of R gene-triggered disease resistance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xit1Ohs70%3D&md5=f0a49b7a7f06cf4650ccfdedb730fa22CAS | 11847307PubMed |
Bacsó R, Hafez YM, Király Z, Király L (2011) Inhibition of virus replication and symptom expression by reactive oxygen species in tobacco infected with tobacco mosaic virus. Acta Phytopathologica et Entomologica Hungarica 46, 1–10.
| Inhibition of virus replication and symptom expression by reactive oxygen species in tobacco infected with tobacco mosaic virus.Crossref | GoogleScholarGoogle Scholar |
Banuelos MA, Sychrova H, Bleykasten-Grosshans C, Souciet JL, Potier S (1998) The Nha1 antiporter of Saccharomyces cerevisiae mediates sodium and potassium efflux. Microbiology 144, 2749–2758.
| The Nha1 antiporter of Saccharomyces cerevisiae mediates sodium and potassium efflux.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXntFSmtLo%3D&md5=74f73b1045fe2237defbf9f89120e42fCAS | 9802016PubMed |
Barney PE, Bush LP (1985) Interaction of nitrate and sulfate reduction in tobacco. 1. Influence of availability of nitrate and sulfate 1. Journal of Plant Nutrition 8, 505–515.
| Interaction of nitrate and sulfate reduction in tobacco. 1. Influence of availability of nitrate and sulfate 1.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXlsVSru7Y%3D&md5=3c083979e98a549dc5d50655177bb66cCAS |
Battraw MJ, Hall TC (1990) Histochemical analysis of CaMV 35S promoter-β-glucuronidase gene expression in transgenic rice plants. Plant Molecular Biology 15, 527–538.
| Histochemical analysis of CaMV 35S promoter-β-glucuronidase gene expression in transgenic rice plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXls1Kntg%3D%3D&md5=3ea16bed60e1336cd16ff7ee7db3f78aCAS | 2102372PubMed |
Beekwilder KM (1999) The inheritance of resistance to tobacco mosaic virus in tobacco introductions. Masters thesis. Virginia Polytechnic Institute and State University, Blacksburg, Virginia.
Cakmak I (2005) The role of potassium in alleviating detrimental effects of abiotic stresses in plants. Journal of Plant Nutrition and Soil Science 168, 521–530.
| The role of potassium in alleviating detrimental effects of abiotic stresses in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXpsFCntL8%3D&md5=5c41619fb0563c91b09a532e860dafcfCAS |
Cao H, Bowling SA, Gordon AS, Dong X (1994) Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell Online 6, 1583–1592.
| Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXitl2lsb8%3D&md5=ddc44172e6bf008516001082dcd53498CAS |
Chen Z, Silva H, Klessig DF (1993) Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid. Science 262, 1883–1886.
| Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXhtVWqu7o%3D&md5=4cc84c409664ea1e1c28a18fe5730781CAS | 8266079PubMed |
Cooper RB, Blaser RE, Brown RH (1967) Potassium nutrition effects on net photosynthesis and morphology of alfalfa. Soil Science Society of America Journal 31, 231–235.
| Potassium nutrition effects on net photosynthesis and morphology of alfalfa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF2sXksVaqtr0%3D&md5=0e476dcaafd24ea4beb188f1dc342db0CAS |
Cornelissen BJC, van Huijsduijnen RAMH, Van Loon LC, Bol JF (1986) Molecular characterization of messenger RNAs for pathogenesis-related proteins 1a, 1b and 1c, induced by TMV infection of tobacco. EMBO Journal 5, 37–40.
Daley M, Knauf VC, Summerfelt KR, Turner JC (1998) Co-transformation with one Agrobacterium tumefaciens strain containing two binary plasmids as a method for producing marker-free transgenic plants. Plant Cell Reports 17, 489–496.
| Co-transformation with one Agrobacterium tumefaciens strain containing two binary plasmids as a method for producing marker-free transgenic plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXisFWkt7s%3D&md5=60589ae248b4f559b3ea49621ffaa5b0CAS |
Dangl JL, Dietrich RA, Richberg MH (1996) Death don’t have no mercy: cell death programs in plant–microbe interactions. The Plant Cell 8, 1793–1807.
| Death don’t have no mercy: cell death programs in plant–microbe interactions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xmsl2mur4%3D&md5=2b817a382fef4ee74cd2ae38fcf9fcf8CAS | 12239362PubMed |
De Gara L, de Pinto MC, Tommasi F (2003) The antioxidant systems vis-à-vis reactive oxygen species during plant–pathogen interaction. Plant Physiology and Biochemistry 41, 863–870.
| The antioxidant systems vis-à-vis reactive oxygen species during plant–pathogen interaction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXnvVOntbo%3D&md5=f06673898bcb2335d2ff3a8d645aba69CAS |
Despres C, Chubak C, Rochon A, Clark R, Bethune T, Desveaux D, Fobert PR (2003) The Arabidopsis NPR1 disease resistance protein is a novel cofactor that confers redox regulation of DNA binding activity to the basic domain/leucine zipper transcription factor TGA1. The Plant Cell 15, 2181–2191.
| The Arabidopsis NPR1 disease resistance protein is a novel cofactor that confers redox regulation of DNA binding activity to the basic domain/leucine zipper transcription factor TGA1.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXnsV2gurY%3D&md5=2eb06dcd9ce2a779f7ca33f449f681adCAS | 12953119PubMed |
Devoto A, Nieto-Rostro M, Xie D, Ellis C, Harmston R, Patrick E, Davis J, Sherratt L, Coleman M, Turner JG (2002) COI1 links jasmonate signalling and fertility to the SCF ubiquitin-ligase complex in Arabidopsis. The Plant Journal 32, 457–466.
| COI1 links jasmonate signalling and fertility to the SCF ubiquitin-ligase complex in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xps1Krurs%3D&md5=bc6afde98c36caee4c4781457ffa2dc5CAS | 12445118PubMed |
Dinesh-Kumar SP, Whitham S, Choi D, Hehl R, Corr C, Baker B (1995) Transposon tagging of tobacco mosaic virus resistance gene N: its possible role in the TMV-N-mediated signal transduction pathway. Proceedings of the National Academy of Sciences of the United States of America 92, 4175–4180.
| Transposon tagging of tobacco mosaic virus resistance gene N: its possible role in the TMV-N-mediated signal transduction pathway.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2M3ntlehug%3D%3D&md5=940a44f7e048ab2d750845c097006189CAS | 7753780PubMed |
Dinesh-Kumar SP, Tham WH, Baker BJ (2000) Structure-function analysis of the tobacco mosaic virus resistance gene N. Proceedings of the National Academy of Sciences of the United States of America 97, 14789–14794.
| Structure-function analysis of the tobacco mosaic virus resistance gene N.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXitVGntA%3D%3D&md5=ef13fcb5d336c0cb8b6f4ee26e957885CAS | 11121079PubMed |
Egilla JN, Davies FT, Boutton TW (2005) Drought stress influences leaf water content, photosynthesis, and water-use efficiency of Hibiscus rosa-sinensis at three potassium concentrations. Photosynthetica 43, 135–140.
| Drought stress influences leaf water content, photosynthesis, and water-use efficiency of Hibiscus rosa-sinensis at three potassium concentrations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjtlehur4%3D&md5=5721b2162c0fe1fccf867415bfd8c6fcCAS |
Feder N, O’Brien TP (1968) Plant microtechnique: some principles and new methods. American Journal of Botany 55, 123–142.
| Plant microtechnique: some principles and new methods.Crossref | GoogleScholarGoogle Scholar |
Flor HH (1971) Current status of the gene-for-gene concept. Annual Review of Phytopathology 9, 275–296.
| Current status of the gene-for-gene concept.Crossref | GoogleScholarGoogle Scholar |
Foyer CH, Noctor G (2005) Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant, Cell & Environment 28, 1056–1071.
| Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXpslSgs70%3D&md5=9d07143db9af0464deceac1927f043baCAS |
Fuchs WH, Grossmann F (1972) ‘Nutrition and resistance of crop plants against pathogens and pests.’ (Springer-Verlag: Vienna, Austria)
Gao JS, Meng Y, Sasaki N, Kanegae H, Hayashi N, Nyunoya H (2010) Characterization and cloning of TMV resistance gene N homologues from Nicotiana tabacum. African Journal of Biotechnology 9, 7998–8006.
Gechev TS, Hille J (2005) Hydrogen peroxide as a signal controlling plant programmed cell death. Journal of Cell Biology 168, 17–20.
| Hydrogen peroxide as a signal controlling plant programmed cell death.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXltlSqsA%3D%3D&md5=759088f868761c873895feb0aca629c8CAS | 15631987PubMed |
Gierth M, Mäser P, Schroeder JI (2005) The potassium transporter AtHAK5 functions in K+ deprivation-induced high-affinity K+ uptake and AKT1 K+ channel contribution to K+ uptake kinetics in Arabidopsis roots. Plant Physiology 137, 1105–1114.
| The potassium transporter AtHAK5 functions in K+ deprivation-induced high-affinity K+ uptake and AKT1 K+ channel contribution to K+ uptake kinetics in Arabidopsis roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXislOqs7o%3D&md5=925bbf2095a5315fd8dc0ec8ad85ca0cCAS | 15734909PubMed |
Gooding GV, Hebert TT (1967) A simple technique for purification of tobacco mosaic virus in large quantities. Phytopathology 57, 1285
Green MR, Sambrook J (2012) ‘Molecular cloning: a laboratory manual.’ (Cold Spring Harbor Laboratory Press: Cold Spring Harbor, NY, USA)
Greenberg JT (1997) Programmed cell death in plant–pathogen interactions. Annual Review of Plant Biology 48, 525–545.
| Programmed cell death in plant–pathogen interactions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjs1emtLg%3D&md5=b0cc7d81d607569497b5c1f602c5c1b6CAS |
Grüner R, Strompen G, Pfitzner AJP, Pfitzner UM (2003) Salicylic acid and the hypersensitive response initiate distinct signal transduction pathways in tobacco that converge on the as-1-like element of the PR-1a promoter. European Journal of Biochemistry 270, 4876–4886.
| Salicylic acid and the hypersensitive response initiate distinct signal transduction pathways in tobacco that converge on the as-1-like element of the PR-1a promoter.Crossref | GoogleScholarGoogle Scholar | 14653814PubMed |
Hammond-Kosack KE, Jones DG (1996) Resistance gene-dependent plant defense responses. The Plant Cell 8, 1773–1791.
| Resistance gene-dependent plant defense responses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xmsl2mtbY%3D&md5=cfa5fc63ea5a7ee82d5ac6434b649c81CAS | 8914325PubMed |
Harper JR, Balke NE (1981) Characterization of the inhibition of K+ absorption in oat roots by salicylic acid. Plant Physiology 68, 1349–1353.
| Characterization of the inhibition of K+ absorption in oat roots by salicylic acid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38Xjtl2gtA%3D%3D&md5=fd18c1e8bf9f11c8408dccd17990c858CAS | 16662106PubMed |
Heath MC (1998) Apoptosis, programmed cell death and the hypersensitive response. European Journal of Plant Pathology 104, 117–124.
| Apoptosis, programmed cell death and the hypersensitive response.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjtV2lu7s%3D&md5=3739385f13671cf42bb6d09279469fcdCAS |
Hoekema A, Hirsch PR, Hooykaas PJJ, Schilperoort RA (1983) A binary plant vector strategy based on separation of vir-and T-region of the Agrobacterium tumefaciens Ti plasmid. Nature 303, 179–180.
| A binary plant vector strategy based on separation of vir-and T-region of the Agrobacterium tumefaciens Ti plasmid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXktVWhsrY%3D&md5=22f08b11475aabe2a237ac540a172252CAS |
Horsch RB, Fry JE, Hoffmann NL, Eichholtz D, Rogers SA, Fraley RT (1985) A simple and general method for transferring genes into plants. Science 227, 1229–1231.
| A simple and general method for transferring genes into plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXhtFSjsLc%3D&md5=2a9695de141c444f44078c0291d97ca0CAS |
Huber DM, Arny DC (1985) Interactions of potassium with plant disease. In ‘Potassium in agriculture’. (Ed. RD Munson) pp. 467–488. (ASA CSSA: Madison, WI)
Huber DM, Graham RD, Rengel Z (1999) The role of nutrition in crop resistance and tolerance to diseases. In ‘Mineral nutrition of crops: fundamental mechanisms and implications’. pp. 169–204. (Food Products Press: Binghamton, NY, USA)
Kapusi E, Hensel G, Coronado MJ, Broeders S, Marthe C, Otto I, Kumlehn J (2013) The elimination of a selectable marker gene in the doubled haploid progeny of co-transformed barley plants. Plant Molecular Biology 81, 149–160.
| The elimination of a selectable marker gene in the doubled haploid progeny of co-transformed barley plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvV2ks7rE&md5=e9703aef91a89e6fe76535e706c9e14fCAS | 23180016PubMed |
Keen NT (2000) A century of plant pathology: a retrospective view on understanding host-parasite interactions. Annual Review of Phytopathology 38, 31–48.
| A century of plant pathology: a retrospective view on understanding host-parasite interactions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXot1Sjur4%3D&md5=5464b0230c1e5571b4e8aba267b25214CAS | 11701835PubMed |
Ketchum KA, Joiner WJ, Sellers AJ, Kaczmarek LK, Goldstein SA (1995) A new family of outwardly rectifying potassium channel proteins with two pore domains in tandem. Nature 376, 690–695.
| A new family of outwardly rectifying potassium channel proteins with two pore domains in tandem.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXnslagtbs%3D&md5=4d8c516895fa024adfc967caf8ce0286CAS | 7651518PubMed |
Khan RS, Ntui VO, Chin DP, Nakamura I, Mii M (2011) Production of marker-free disease-resistant potato using isopentenyl transferase gene as a positive selection marker. Plant Cell Reports 30, 587–597.
| Production of marker-free disease-resistant potato using isopentenyl transferase gene as a positive selection marker.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjtFagt7k%3D&md5=d1b3565b5d1a2b322d73dbb2d6817dd2CAS | 21184230PubMed |
Kim EJ, Kwak JM, Uozumi N, Schroeder JI (1998) AtKUP1: an Arabidopsis gene encoding high-affinity potassium transport activity. Plant Cell Online 10, 51–62.
| AtKUP1: an Arabidopsis gene encoding high-affinity potassium transport activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXoslGjtA%3D%3D&md5=684a42b7865323dcd8566766afb4bfceCAS |
Klug A (1999) The tobacco mosaic virus particle: structure and assembly. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 354, 531–535.
| The tobacco mosaic virus particle: structure and assembly.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXisFagtLk%3D&md5=bf0e2ddab810720685042ddd072637afCAS | 10212932PubMed |
Krauss A (2001) Potassium and biotic stress. In ‘Potassium in Argentina’s agricultural systems, Fauba-Fertilizar-IPI Workshop on Press’. pp. 20–21. (Buenos Aires, Argentina)
Lamb C, Dixon RA (1997) The oxidative burst in plant disease resistance. Annual Review of Plant Biology 48, 251–275.
| The oxidative burst in plant disease resistance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjs1entr8%3D&md5=95e325f64ae2e82e185fcb6599b7928bCAS |
León J, Lawton MA, Raskin I (1995) Hydrogen peroxide stimulates salicylic acid biosynthesis in tobacco. Plant Physiology 108, 1673–1678.
Les Erickson F, Holzberg S, Calderon-Urrea A, Handley V, Axtell M, Corr C, Baker B (1999) The helicase domain of the TMV replicase proteins induces the N-mediated defence response in tobacco. The Plant Journal 18, 67–75.
| The helicase domain of the TMV replicase proteins induces the N-mediated defence response in tobacco.Crossref | GoogleScholarGoogle Scholar |
Li J, Brader G, Palva ET (2004) The WRKY70 transcription factor: a node of convergence for jasmonate-mediated and salicylate-mediated signals in plant defence. The Plant Cell 16, 319–331.
| The WRKY70 transcription factor: a node of convergence for jasmonate-mediated and salicylate-mediated signals in plant defence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhsFKisrY%3D&md5=af35434d9082985e0b2951be8c93d7c4CAS | 14742872PubMed |
Lin CY, Yeh DM (2008) Potassium nutrition affects leaf growth, anatomy, and macroelements of Guzmania. HortScience 43, 146–148.
Liu Y, Zhang S, Klessig DF (2000) Molecular cloning and characterization of a tobacco MAP kinase kinase that interacts with SIPK. Molecular Plant-Microbe Interactions 13, 118–124.
| Molecular cloning and characterization of a tobacco MAP kinase kinase that interacts with SIPK.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXislSgug%3D%3D&md5=12eb5ad981c76cc87f906ff67a3ae735CAS | 10656593PubMed |
Liu Y, Schiff M, Marathe R, Dinesh-Kumar SP (2002) Tobacco Rar1, EDS1 and NPR1/NIM1 like genes are required for N-mediated resistance to tobacco mosaic virus. The Plant Journal 30, 415–429.
| Tobacco Rar1, EDS1 and NPR1/NIM1 like genes are required for N-mediated resistance to tobacco mosaic virus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XltFaqsbg%3D&md5=fbb63b169f00c0e042fd2515b9d79946CAS | 12028572PubMed |
Liu Y, Burch-Smith T, Schiff M, Feng S, Dinesh-Kumar SP (2004a) Molecular chaperone Hsp90 associates with resistance protein N and its signaling proteins SGT1 and Rar1 to modulate an innate immune response in plants. Journal of Biological Chemistry 279, 2101–2108.
| Molecular chaperone Hsp90 associates with resistance protein N and its signaling proteins SGT1 and Rar1 to modulate an innate immune response in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXis1ShsQ%3D%3D&md5=b9919f0e3560e2ce6064302bbde17746CAS | 14583611PubMed |
Liu Y, Schiff M, Dinesh-Kumar SP (2004b) Involvement of MEK1 MAPKK, NTF6 MAPK, WRKY/MYB transcription factors, COI1 and CTR1 in N-mediated resistance to tobacco mosaic virus. The Plant Journal 38, 800–809.
| Involvement of MEK1 MAPKK, NTF6 MAPK, WRKY/MYB transcription factors, COI1 and CTR1 in N-mediated resistance to tobacco mosaic virus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXltlCrs7o%3D&md5=fb084c24f0e1851d12da5ce0d0af37daCAS | 15144381PubMed |
Malamy J, Carr JP, Klessig DF, Raskin I (1990) Salicylic acid: a likely endogenous signal in the resistance response of tobacco to viral infection. Science 250, 1002–1004.
| Salicylic acid: a likely endogenous signal in the resistance response of tobacco to viral infection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXjvFelug%3D%3D&md5=e6f3bc2d933f14552fde8e3e82ecd5c1CAS | 17746925PubMed |
Martínez-Cordero MA, Martínez V, Rubio F (2004) Cloning and functional characterization of the high-affinity K+ transporter HAK1 of pepper. Plant Molecular Biology 56, 413–421.
| Cloning and functional characterization of the high-affinity K+ transporter HAK1 of pepper.Crossref | GoogleScholarGoogle Scholar | 15604753PubMed |
Menke FLH, Kang HG, Chen Z, Park JM, Kumar D, Klessig DF (2005) Tobacco transcription factor WRKY1 is phosphorylated by the MAP kinase SIPK and mediates HR-like cell death in tobacco. Molecular Plant-Microbe Interactions 18, 1027–1034.
| Tobacco transcription factor WRKY1 is phosphorylated by the MAP kinase SIPK and mediates HR-like cell death in tobacco.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVCgsbfI&md5=2c1ea942e65d945a227fd114a8b1b36cCAS |
Miki B, McHugh S (2004) Selectable marker genes in transgenic plants: applications, alternatives and biosafety. Journal of Biotechnology 107, 193–232.
| Selectable marker genes in transgenic plants: applications, alternatives and biosafety.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXltVGrtg%3D%3D&md5=1baaac526e55e309677eaec46d420ad3CAS | 14736458PubMed |
Mullins GL, Burmester CH (1990) Dry matter, nitrogen, phosphorus, and potassium accumulation by four cotton varieties. Agronomy Journal 82, 729–736.
| Dry matter, nitrogen, phosphorus, and potassium accumulation by four cotton varieties.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXit12rug%3D%3D&md5=6c1c05812db15ee641aa07ed6d1bbadcCAS |
O’Neill LA (2002) Wanted: a molecular basis for specificity in toll-like receptor signal transduction. Molecular Cell 10, 969–971.
| Wanted: a molecular basis for specificity in toll-like receptor signal transduction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xptl2ksL8%3D&md5=e657801444d0e6df55e883d6964c3eeaCAS | 12453406PubMed |
Padgett HS, Watanabe Y, Beachy RN (1997) Identification of the TMV replicase sequence that activates the N gene-mediated hypersensitive response. Molecular Plant-Microbe Interactions 10, 709–715.
| Identification of the TMV replicase sequence that activates the N gene-mediated hypersensitive response.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXkvFeqtrw%3D&md5=58a05283c14a36f407cfa1cbb4c81f4aCAS |
Peart JR, Mestre P, Lu R, Malcuit I, Baulcombe DC (2005) NRG1, a CC-NB-LRR protein, together with N, a TIR-NB-LRR protein, mediates resistance against tobacco mosaic virus. Current Biology 15, 968–973.
| NRG1, a CC-NB-LRR protein, together with N, a TIR-NB-LRR protein, mediates resistance against tobacco mosaic virus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXks1GjtL8%3D&md5=4ce09aff3bec131c6d0a419ed7dd5478CAS | 15916955PubMed |
Perrenoud S (1977) ‘Potassium and plant health. IPI Research Topics.’ pp. 218. (International Potash Institute Press: Bern-Worblaufen, Switzerland)
Pettigrew WT, Meredith WR (1997) Dry matter production, nutrient uptake, and growth of cotton as affected by potassium fertilization. Journal of Plant Nutrition 20, 531–548.
| Dry matter production, nutrient uptake, and growth of cotton as affected by potassium fertilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjtFWlu7o%3D&md5=ac5813cef8ec066371b0eac8d6faf61aCAS |
Prabhu AS, Fageria NK, Huber DM (2007) Potassium nutrition and plant diseases. In ‘Mineral nutrition and plant disease’. (Eds LE Datnoff, WH Elmer, DM Huber) pp. 122–278. (The American Phytopathological Society Press, Saint Paul, MN, USA)
Premachandra GS, Saneoka H, Ogata S (1991) Cell membrane stability and leaf water relations as affected by potassium nutrition of water-stressed maize. Journal of Experimental Botany 42, 739–745.
| Cell membrane stability and leaf water relations as affected by potassium nutrition of water-stressed maize.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXkslSms74%3D&md5=5d57bc0fc4e4da57ea3b7b67bb70a853CAS |
Purohit VK, Tamta S, Chandra S, Vyas P, Palni LMS, Nandi SK (2002) In vitro multiplication of Quercus leucotrichophora and Q. glauca: important Himalayan oaks. Plant Cell, Tissue and Organ Culture 69, 121–133.
| In vitro multiplication of Quercus leucotrichophora and Q. glauca: important Himalayan oaks.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XksFSqtLs%3D&md5=63cffab9d92f25a1692de9b086ff76aaCAS |
Radke SE, Turner JC, Facciotti D (1992) Transformation and regeneration of Brassica rapa using Agrobacterium tumefaciens. Plant Cell Reports 11, 499–505.
| Transformation and regeneration of Brassica rapa using Agrobacterium tumefaciens.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2c7ltlarsA%3D%3D&md5=72fc9b95e5fb8a2eb939a2cf25cfd9c7CAS | 24213157PubMed |
Raskin I (1992) Role of salicylic acid in plants. Annual Review of Plant Biology 43, 439–463.
| Role of salicylic acid in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38Xks1Knu74%3D&md5=134b88a07a18ecf3039ff86adfdf2520CAS |
Römheld V, Kirkby EA (2010) Research on potassium in agriculture: needs and prospects. Plant and Soil 335, 155–180.
| Research on potassium in agriculture: needs and prospects.Crossref | GoogleScholarGoogle Scholar |
Rouquié D, Tournaire-Roux C, Szponarski W, Rossignol M, Doumas P (1998) Cloning of the V-ATPase subunit G in plant: functional expression and subcellular localization. FEBS Letters 437, 287–292.
Rubio F, Gassmann W, Schroeder JI (1995) Sodium-driven potassium uptake by the plant potassium transporter HKT1 and mutations conferring salt tolerance. Science 270, 1660–1663.
| Sodium-driven potassium uptake by the plant potassium transporter HKT1 and mutations conferring salt tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXpvVCisbw%3D&md5=3479de8cb71623069b350bec0b307517CAS | 7502075PubMed |
Ryals JA, Neuenschwander UH, Willits MG, Molina A, Steiner HY, Hunt MD (1996) Systemic acquired resistance. The Plant Cell 8, 1809–1819.
| Systemic acquired resistance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xmsl2murw%3D&md5=c975c01e83f627770f8af9aef5850bb8CAS | 12239363PubMed |
Sánchez-Casas P, Klessig DF (1994) A salicylic acid-binding salicylic acid-inhibitable catalase activity and a activity are present in a variety of plant species. Plant Physiology 106, 1675–1679.
Santa-María GE, Rubio F, Dubcovsky J, Rodríguez-Navarro A (1997) The HAK1 gene of barley is a member of a large gene family and encodes a high-affinity potassium transporter. Plant Cell Online 9, 2281–2289.
| The HAK1 gene of barley is a member of a large gene family and encodes a high-affinity potassium transporter.Crossref | GoogleScholarGoogle Scholar |
Schachtman DP, Schroeder JI (1994) Structure and transport mechanism of a high-affinity potassium uptake transporter from higher plant. Nature 370, 655–658.
| Structure and transport mechanism of a high-affinity potassium uptake transporter from higher plant.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXmt1Cguro%3D&md5=0203a591306df53458875f64b1bb8443CAS | 8065452PubMed |
Shulaev V, León J, Raskin I (1995) Is salicylic acid a translocated signal of systemic acquired resistance in tobacco? Plant Cell Online 7, 1691–1701.
| Is salicylic acid a translocated signal of systemic acquired resistance in tobacco?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXovFCqurc%3D&md5=f9913c5a34dcb444ae0b3b3ccaefe11eCAS |
Stange C, Matus JT, Elorza A, Arce-Johnson P (2004) Identification and characterization of a novel tobacco mosaic virus resistance N gene homologue in Nicotiana tabacum plants. Functional Plant Biology 31, 149–158.
| Identification and characterization of a novel tobacco mosaic virus resistance N gene homologue in Nicotiana tabacum plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhsl2gtrY%3D&md5=7c6f969114b445d75d9f19d87b21e501CAS |
Steven HC (1985) Role of potassium in photosynthesis and respiration. In ‘Potassium in agriculture’. (Eds RD Munson) pp. 369–396. (ACSESS: Madison, WI)
Walters DR, Bingham IJ (2007) Influence of nutrition on disease development caused by fungal pathogens: implications for plant disease control. Annals of Applied Biology 151, 307–324.
| Influence of nutrition on disease development caused by fungal pathogens: implications for plant disease control.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXnvV2guw%3D%3D&md5=b08247c84600fb53fe36e450accdbda1CAS |
Whitham S, Dinesh-Kumar SP, Choi D, Hehl R, Corr C, Baker B (1994) The product of the tobacco mosaic virus resistance gene N: similarity to toll and the interleukin-1 receptor. Cell 78, 1101–1115.
| The product of the tobacco mosaic virus resistance gene N: similarity to toll and the interleukin-1 receptor.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXhtVamt78%3D&md5=f27c8d99cf647498ba534d3975fee648CAS | 7923359PubMed |
Whitham S, McCormick S, Baker B (1996) The N gene of tobacco confers resistance to tobacco mosaic virus in transgenic tomato. Proceedings of the National Academy of Sciences of the United States of America 93, 8776–8781.
| The N gene of tobacco confers resistance to tobacco mosaic virus in transgenic tomato.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XkvFyrtLg%3D&md5=288f753952c969f5b7d5fb8b2c5a998bCAS | 8710948PubMed |
Xie DX, Feys BF, James S, Nieto-Rostro M, Turner JG (1998) COI1: an Arabidopsis gene required for jasmonate-regulated defence and fertility. Science 280, 1091–1094.
| COI1: an Arabidopsis gene required for jasmonate-regulated defence and fertility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjt1egsbk%3D&md5=6dcc7962e789753dec369cb91247e44cCAS | 9582125PubMed |
Yalpani N, Silverman P, Wilson TM, Kleier DA, Raskin I (1991) Salicylic acid is a systemic signal and an inducer of pathogenesis-related proteins in virus-infected tobacco. Plant Cell Online 3, 809–818.
| Salicylic acid is a systemic signal and an inducer of pathogenesis-related proteins in virus-infected tobacco.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXmsFaht74%3D&md5=97f69f887a250c0fecbba221b6ba188bCAS |
Yalpani N, Shulaev V, Raskin I (1993) Endogenous salicylic acid levels correlate with accumulation of pathogenesis-related proteins and virus resistance in tobacco. Phytopathology 83, 702–708.
| Endogenous salicylic acid levels correlate with accumulation of pathogenesis-related proteins and virus resistance in tobacco.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXht12ksbY%3D&md5=a1217a433380a0894dc8b5fec47c828fCAS |
Yi SY, Yu SH, Choi D (1999) Molecular cloning of a catalase cDNA from Nicotiana glutinosa L. and its repression by tobacco mosaic virus infection. Molecules and Cells 9, 320–325.
Zhang S, Du H, Klessig DF (1998) Activation of the tobacco SIP kinase by both a cell wall-derived carbohydrate elicitor and purified proteinaceous elicitins from Phytophthora spp. The Plant Cell 10, 435–449.
Zhang GY, Chen M, Guo JM, Xu TW, Li LC, Xu ZS, Ma YZ, Chen XP (2009) Isolation and characteristics of the CN gene, a tobacco mosaic virus resistance N gene homolog from tobacco. Biochemical Genetics 47, 301–314.
| Isolation and characteristics of the CN gene, a tobacco mosaic virus resistance N gene homolog from tobacco.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjt1Siuro%3D&md5=3ad4395ebc980fe8095fc645b563f878CAS | 19191020PubMed |
Zhao D, Oosterhuis DM, Bednarz CW (2001) Influence of potassium deficiency on photosynthesis, chlorophyll content, and chloroplast ultrastructure of cotton plants. Photosynthetica 39, 103–109.
| Influence of potassium deficiency on photosynthesis, chlorophyll content, and chloroplast ultrastructure of cotton plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmtlensLw%3D&md5=83845f66fc8beca1d99619427cbadc09CAS |
Zhou L, He H, Liu R, Han Q, Shou H, Liu B (2014) Overexpression of GmAKT2 potassium channel enhances resistance to soybean mosaic virus. BMC Plant Biology 14, 154
| Overexpression of GmAKT2 potassium channel enhances resistance to soybean mosaic virus.Crossref | GoogleScholarGoogle Scholar | 24893844PubMed |