Expression of a Nicotiana tabacum pathogen-induced gene is involved in the susceptibility to black shank
Roxana Portieles A , Eduardo Canales A , Osmani Chacon B , Yussuan Silva B , Ingrid Hernández A , Yunior López A , Mayra Rodríguez A , Ryohei Terauchi C , Hideo Matsumura D , Carlos Borroto E , Jonathan D. Walton F , Ramon Santos G and Orlando Borrás-Hidalgo A HA Centre for Genetic Engineering and Biotechnology, PO Box 6162, Havana, 10 600, Cuba.
B Tobacco Research Institute, Carretera de Tumbadero 8, PO Box 6063, Havana, Cuba.
C Iwate Biotechnology Research Centre, Kitakami, Iwate, 024-0003, Japan.
D Gene Research Center, Shinshu University, Ueda 386-8567, Japan.
E Centro de Investigación Científica de Yucatán, Calle 43 No. 130, Colonia Chuburná de Hidalgo, 97200 Mérida, Yucatán, México.
F Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, USA 48824.
G Centro de Bioplantas, Carretera de Morón Km 9, Ciego de Avila, C. P. 69450, Cuba.
H Corresponding author. Email: orlando.borras@cigb.edu.cu
Functional Plant Biology 43(6) 534-541 https://doi.org/10.1071/FP15350
Submitted: 11 November 2015 Accepted: 22 March 2016 Published: 9 May 2016
Abstract
Many host genes induced during compatible plant–pathogen interactions constitute targets of pathogen virulence factors that act to suppress host defenses. In order to identify Nicotiana tabacum L. genes for pathogen-induced proteins involved in susceptibility to the oomycete Phytophthora parasitica var. nicotianae, we used SuperSAGE technology combined with next-generation sequencing to identify transcripts that were differentially upregulated during a compatible interaction. We identified a pathogen-induced gene (NtPIP) that was rapidly induced only during the compatible interaction. Virus-induced gene silencing of NtPIP reduced the susceptibility of N. tabacum to P. parasitica var. nicotianae. Additionally, transient expression of NtPIP in the resistant species Nicotiana megalosiphon Van Heurck & Mull. Arg. compromised the resistance to P. parasitica var. nicotianae. This pathogen-induced protein is therefore a positive regulator of the susceptibility response against an oomycete pathogen in tobacco.
Additional keywords: oomycete, SuperSAGE.
References
Bai Y, Pavan S, Zheng Z, Zappel NF, Reinstädler A, Lotti C, De Giovanni C, Ricciardi L, Lindhout P, Visser R, Theres K, Panstruga R (2008) Naturally occurring broad-spectrum powdery mildew resistance in a Central American tomato accession is caused by loss of Mlo function. Molecular Plant-Microbe Interactions 21, 30–39.| Naturally occurring broad-spectrum powdery mildew resistance in a Central American tomato accession is caused by loss of Mlo function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsVOrtr3J&md5=481e03c7eb60c52ce33b67a7d13141c4CAS | 18052880PubMed |
Borrás-Hidalgo O, Caprari C, De Lorenzo G, Cervone F (2012) A gene for plant protection: expression of a bean polygalacturonase inhibitor in tobacco confers a strong resistance against fungi and oomycetes. Frontiers in Plant Science 3, 268
| A gene for plant protection: expression of a bean polygalacturonase inhibitor in tobacco confers a strong resistance against fungi and oomycetes.Crossref | GoogleScholarGoogle Scholar | 23264779PubMed |
Büschges R, Hollricher K, Panstruga R, Simons G, Wolter M, Frijters A, van Daelen R, van der Lee T, Diergaarde P, Groenendijk J, Töpsch S, Vos P, Salamini F, Schulze-Lefert P (1997) The barley Mlo gene: a novel control element of plant pathogen resistance. Cell 88, 695–705.
| The barley Mlo gene: a novel control element of plant pathogen resistance.Crossref | GoogleScholarGoogle Scholar | 9054509PubMed |
Chacón O, Hernández I, Portieles R, López Y, Pujol M, Borrás-Hidalgo O (2009) Identification of defense-related genes in tobacco responding to black shank disease. Plant Science 177, 175–180.
| Identification of defense-related genes in tobacco responding to black shank disease.Crossref | GoogleScholarGoogle Scholar |
Chen L, Shiotani K, Togashi T, Miki D, Aoyama M, Wong HL, Kawasaki T, Shimamoto K (2010) Analysis of the Rac/Rop small GTPase family in rice: expression, subcellular localization and role in disease resistance. Plant & Cell Physiology 51, 585–595.
| Analysis of the Rac/Rop small GTPase family in rice: expression, subcellular localization and role in disease resistance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXks1Khtbg%3D&md5=c61515493c4ac315bce6cfaa2457b923CAS |
Collazo C, Ramos PL, Chacon O, Borroto CJ, López Y, Pujol M, Thomma B, Hein I, Borrás-Hidalgo O (2006) Phenotypical and molecular characterization of the tomato mottle Taino virus – Nicotiana megalosiphon interaction. Physiological and Molecular Plant Pathology 67, 231–236.
| Phenotypical and molecular characterization of the tomato mottle Taino virus – Nicotiana megalosiphon interaction.Crossref | GoogleScholarGoogle Scholar |
Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21, 3674–3676.
| Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXpvFGqt70%3D&md5=4bc0173f2ee147ee5aa71537bef70069CAS | 16081474PubMed |
Consonni C, Humphry ME, Hartmann HA, Livaja M, Durner J, Westphal L, Vogel J, Lipka V, Kemmerling B, Schulze-Lefert P, Somerville SC, Panstruga R (2006) Conserved requirement for a plant host cell protein in powdery mildew pathogenesis. Nature Genetics 38, 716–720.
| Conserved requirement for a plant host cell protein in powdery mildew pathogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XltVOhurs%3D&md5=155d0c4f89e67f0cd644571c1ef11043CAS | 16732289PubMed |
Craddock C, Lavagi I, Yang Z (2012) New insights into Rho signaling from plant ROP/Rac GTPases. Trends in Cell Biology 22, 492–501.
| New insights into Rho signaling from plant ROP/Rac GTPases.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtlWqtLrF&md5=e2906e5b8beebcdf3b3a3c9d0e2f3803CAS | 22795444PubMed |
Csinos AS (1999) Stem and root resistance to tobacco black shank. Plant Disease 83, 777–780.
| Stem and root resistance to tobacco black shank.Crossref | GoogleScholarGoogle Scholar |
Espino E, Rey X, García V (1997) Habana 92 y Habana 2000: dos nuevas variedades de tabaco negro resistentes al moho azul Peronospora tabacina. Revista Cubana de Agricultura 1, 15–24.
Fernandez-Pozo N, Menda N, Edwards JD, Saha S, Tecle IY, Strickler SR, Bombarely A, Fisher-York T, Pujar A, Foerster H, Yan A, Mueller LA (2015) The Sol Genomics Network (SGN)—from genotype to phenotype to breeding. Nucleic Acids Research 43, D1036–D1041.
| The Sol Genomics Network (SGN)—from genotype to phenotype to breeding.Crossref | GoogleScholarGoogle Scholar | 25428362PubMed |
Hellens RP, Edwards AE, Leyland NR, Bean S, Mullineaux MP (2000) pGreen: a versatile and flexible binary Ti vector for Agrobacterium mediated plant transformation. Plant Molecular Biology 42, 819–832.
| pGreen: a versatile and flexible binary Ti vector for Agrobacterium mediated plant transformation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXks12jsL0%3D&md5=912f34c966d95198f387ba9ad182ed29CAS | 10890530PubMed |
Hok S, Danchin EG, Allasia V, Panabières F, Attard A, Keller H (2011) An Arabidopsis (malectin-like) leucine-rich repeat receptor-like kinase contributes to downy mildew disease. Plant, Cell & Environment 34, 1944–1957.
| An Arabidopsis (malectin-like) leucine-rich repeat receptor-like kinase contributes to downy mildew disease.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsVyls7%2FF&md5=c415d77449af649d6e9853c65f2d13dcCAS |
Jones JDG, Dangl JL (2006) The plant immune system. Nature 444, 323–329.
| The plant immune system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1SgtbzO&md5=8c3478940ede75d28698c9946ce7d46eCAS |
Jones L, Hamilton AJ, Voinnet O, Thomas CL, Maule AJ, Baulcombe DC (1999) RNA–DNA interactions and DNA methylation in post-transcriptional gene silencing. The Plant Cell 11, 2291–2301.
| RNA–DNA interactions and DNA methylation in post-transcriptional gene silencing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXkt1Cgtg%3D%3D&md5=0d35fb8a3c37d9d0719443cbca16d2dfCAS | 10590159PubMed |
Jørgensen JH (1992) Discovery, characterization and exploitation of Mlo powdery mildew resistance in barley. Euphytica 63, 141–152.
| Discovery, characterization and exploitation of Mlo powdery mildew resistance in barley.Crossref | GoogleScholarGoogle Scholar |
Kim DS, Hwang BK (2012) The pepper MLO gene, CaMLO2, is involved in the susceptibility cell-death response and bacterial and oomycete proliferation. The Plant Journal 72, 843–855.
| The pepper MLO gene, CaMLO2, is involved in the susceptibility cell-death response and bacterial and oomycete proliferation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhslelur3L&md5=7522dcc763207a62fb8880dd37ac644bCAS | 22913752PubMed |
Lapin D, Van den Ackerveken G (2013) Susceptibility to plant disease: more than a failure of host immunity. Trends in Plant Science 18, 546–554.
| Susceptibility to plant disease: more than a failure of host immunity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXpslKltb4%3D&md5=41ff76971f27be040b6a2706fe13c752CAS | 23790254PubMed |
Li Y, Wu MY, Song HH, Hu X, Qiu BS (2005) Identification of a tobacco protein interacting with tomato mosaic virus coat protein and facilitating long-distance movement of virus. Archives of Virology 150, 1993–2008.
| Identification of a tobacco protein interacting with tomato mosaic virus coat protein and facilitating long-distance movement of virus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVajsLbE&md5=e545d04da5b7d73b79d7e209c70aebb3CAS | 15931463PubMed |
Li BC, Bass WT, Cornelius PL (2006) Resistance to tobacco black shank in Nicotiana species. Crop Science 46, 554–560.
| Resistance to tobacco black shank in Nicotiana species.Crossref | GoogleScholarGoogle Scholar |
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method. Methods 25, 402–408.
| Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtFelt7s%3D&md5=3c52ba31a95ed35024a5c40b81df18e8CAS | 11846609PubMed |
Lu R, Martin-Hernandez AM, Peart JR, Malcuit I, Baulcombe DC (2003) Virus-induced gene silencing in plants. Methods 30, 296–303.
| Virus-induced gene silencing in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXkvVejsr0%3D&md5=eccd19466221745e9e7ec831a40c8446CAS | 12828943PubMed |
Mackey D, Holt Iii BF, Wiig A, Dangl JL (2002) RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell 108, 743–754.
| RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XisFOgsrg%3D&md5=9541c7103f47cff283d67af676ce24e9CAS | 11955429PubMed |
Matsumura H, Yoshida K, Luo S, Kimura E, Terauchi R (2010) High-throughput SuperSAGE for digital gene expression analysis of multiple samples using next generation sequencing. PLoS One 5, e12010
| High-throughput SuperSAGE for digital gene expression analysis of multiple samples using next generation sequencing.Crossref | GoogleScholarGoogle Scholar | 20700453PubMed |
Morris PF, Ward EWB (1992) Chemo-attraction of zoospores of the soybean pathogen, Phytophthora sojae, by isoflavones. Physiological and Molecular Plant Pathology 40, 17–22.
| Chemo-attraction of zoospores of the soybean pathogen, Phytophthora sojae, by isoflavones.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XitlWku7k%3D&md5=fb88306300c32b757c3029b56ca40144CAS |
Nürnberger T, Lipka V (2005) Non-host resistance in plants: new insights into an old phenomenon. Molecular Plant Pathology 6, 335–345.
| Non-host resistance in plants: new insights into an old phenomenon.Crossref | GoogleScholarGoogle Scholar | 20565662PubMed |
Park C-J, Peng Y, Chen X, Dardick C, Ruan D, Bart R, Canlas PE, Ronald PC (2008) Rice XB15, a protein phosphatase 2C, negatively regulates cell death and XA21-mediated innate immunity. PLoS Biology 6, e231
| Rice XB15, a protein phosphatase 2C, negatively regulates cell death and XA21-mediated innate immunity.Crossref | GoogleScholarGoogle Scholar | 18817453PubMed |
Pritchard L, Birch P (2011) A systems biology perspective on plant-microbe interactions: biochemical and structural targets of pathogen effectors. Plant Science 180, 584–603.
| A systems biology perspective on plant-microbe interactions: biochemical and structural targets of pathogen effectors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXisFyhs7s%3D&md5=5341270e42294afee2534c586d741f4bCAS | 21421407PubMed |
Ratcliff F, Martin-Hernandez AM, Baulcombe DC (2001) Tobacco rattle virus as a vector for analysis of gene functions by silencing. The Plant Journal 25, 237–245.
| Tobacco rattle virus as a vector for analysis of gene functions by silencing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhtlals78%3D&md5=a297f02910bc891d07aa320722b243b6CAS | 11169199PubMed |
Thomas PE (2004) Nicotiana megalosiphon, a highly susceptible, new and useful host for Potato virus. Plant Disease 88, 1160
| Nicotiana megalosiphon, a highly susceptible, new and useful host for Potato virus.Crossref | GoogleScholarGoogle Scholar |
Voegele RT, Struck C, Hahn M, Mendgen K (2001) The role of haustoria in sugar supply during infection of broad bean by the rust fungus Uromyces fabae. Proceedings of the National Academy of Sciences of the United States of America 98, 8133–8138.
| The role of haustoria in sugar supply during infection of broad bean by the rust fungus Uromyces fabae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlt1Knu7s%3D&md5=1b5d162ad81f8546f1eab460c0ff9104CAS | 11390980PubMed |
Zhang Y, Fan W, Kinkema M, Li X, Dong X (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 of the United States of America 96, 6523–6528.
| Interaction of NPR1 with basic leucine zipper protein transcription factors that bind sequences required for salicylic acid induction of the PR-1 gene.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXksFKktbY%3D&md5=74cd4eec78f6cb02ef3f6a56cf5471aaCAS | 10339621PubMed |