Analysis of differentially expressed genes in leaf rust infected bread wheat involving seedling resistance gene Lr28
Raman Dhariwal A , Shailendra Vyas B , Govindraj R. Bhaganagare C , Shailendra K. Jha C , Jitendra P. Khurana B , Akhilesh K. Tyagi D , Kumble V. Prabhu C , Harindra S. Balyan A and Pushpendra K. Gupta A EA Molecular Biology Laboratory, Department of Genetics and Plant Breeding, Ch. Charan Singh University, Meerut-250004, UP, India.
B Interdisciplinary Centre for Plant Genomics and Department of Plant Molecular Biology, University of Delhi South Campus, New Delhi, India.
C National Phytotron Facility, Division of Genetics, Indian Agricultural Research Institute, New Delhi, India.
D National Institute of Plant Genome Research, Aruna Asaf Ali Marg, New Delhi-110067, India.
E Corresponding author. Email: pkgupta36@gmail.com
Functional Plant Biology 38(6) 479-492 https://doi.org/10.1071/FP10246
Submitted: 18 December 2010 Accepted: 24 March 2011 Published: 3 June 2011
Abstract
Genome-wide transcriptome analysis of seedling resistance to leaf rust conferred by Lr28 gene in wheat (Triticum aestivum L.) was conducted to identify differentially expressed genes during incompatible interaction. A virulent leaf rust race 77–5 was used for inoculation of resistant (HD2329 + Lr28) and susceptible (HD2329 – Lr28) wheat NILs and cDNA-AFLP analyses was carried out. As many as 223 differential transcripts appeared following leaf rust inoculation; these included 122 transcripts that appeared exclusively in resistant NIL, whereas 39 transcripts appeared both in resistant and susceptible NILs. Sequence analyses of 37 transcripts, which appeared in the resistant NIL revealed that 15 transcripts had homology with genes involved in protein synthesis, signal transduction, transport, disease resistance and metabolism. The functions of remaining 22 transcripts could not be determined; these included six novel genes reported for the first time in wheat. Specific primers could be designed for 18 of the 37 transcripts, which included genes with putative and unknown functions. Quantitative real time PCR analysis was conducted using these 18 pairs of primers. A majority (13) of these transcripts appeared within 48 h reaching a peak value at 96 h in resistant NIL signifying their role in providing leaf rust resistance.
Additional keywords: cDNA-AFLP analysis, compatible interaction, defense, incompatible interaction, Puccinia triticina, qRT-PCR analysis, TDFs.
References
Bachem CWB, van der Hoeven RS, de Bruijn SM, Vreugdenhil D, Zabeau M, Visser RGF (1996) Visualisation of differential gene expression using a novel method of RNA fingerprinting based on AFLP: analysis of gene expression during potato tuber development. The Plant Journal 9, 745–753.| Visualisation of differential gene expression using a novel method of RNA fingerprinting based on AFLP: analysis of gene expression during potato tuber development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XjvVSlsro%3D&md5=17e5b55ca1c180330cd1bc129c5898b3CAS | 8653120PubMed |
Bolton MD (2009) Primary metabolism and plant defense – fuel for the fire. Molecular Plant-Microbe Interactions 22, 487–497.
| Primary metabolism and plant defense – fuel for the fire.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXks1Wnsrk%3D&md5=3ddcb2108031c2384057b98afd73b0b8CAS | 19348567PubMed |
Bolton MD, Kolmer JA, Xu WW, Garvin DF (2008) Lr34-mediated leaf rust resistance in wheat: transcript profiling reveals a high energetic demand supported by transient recruitment of multiple metabolic pathways. Molecular Plant-Microbe Interactions 21, 1515–1527.
| Lr34-mediated leaf rust resistance in wheat: transcript profiling reveals a high energetic demand supported by transient recruitment of multiple metabolic pathways.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVaru7bK&md5=7b824c1b5dba482eb882304c56b03369CAS | 18986248PubMed |
Caldo RA, Nettleton D, Wise RP (2004) Interaction-dependent gene expression in Mla-specified response to barley powdery mildew. The Plant Cell 16, 2514–2528.
| Interaction-dependent gene expression in Mla-specified response to barley powdery mildew.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnvVarur4%3D&md5=7fa95a6ae27d3d206794d1d556199a25CAS | 15319481PubMed |
Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host–microbe interactions: shaping the evolution of the plant immune response. Cell 124, 803–814.
| Host–microbe interactions: shaping the evolution of the plant immune response.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xit1Kltbw%3D&md5=59ba3b4d9be46beefb8318fd15cb5208CAS | 16497589PubMed |
Cloutier S, McCallum BD, Loutre C, Banks TW, Wicker T, Feuillet C, Keller B, Jordan MC (2007) Leaf rust resistance gene Lr1, isolated from bread wheat (Triticum aestivum L.) is a member of the large psr567 gene family. Plant Molecular Biology 65, 93–106.
| Leaf rust resistance gene Lr1, isolated from bread wheat (Triticum aestivum L.) is a member of the large psr567 gene family.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXovFSqs7w%3D&md5=a7d7d09da74deac118d8bc4fd8b7deb9CAS | 17611798PubMed |
Coram TE, Wang MN, Chen XM (2008) Transcriptome analysis of wheat–Puccinia striiformis f. sp. tritici interaction. Molecular Plant Pathology 9, 157–169.
| Transcriptome analysis of wheat–Puccinia striiformis f. sp. tritici interaction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXksFSltbw%3D&md5=4943864dd24c5dbde79cc3f89a390cccCAS | 18705849PubMed |
de Torres M, Sanchez P, Fernandez-Delmond I, Grant M (2003) Expression profiling of the host response to bacterial infection: the transition from basal to induced defense responses in RPM1-mediated resistance. The Plant Journal 33, 665–676.
| Expression profiling of the host response to bacterial infection: the transition from basal to induced defense responses in RPM1-mediated resistance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXislWiurs%3D&md5=a695df1cf2907f246c30530dd5a12e7aCAS | 12609040PubMed |
Diévart A, Clark SE (2003) Using mutant alleles to determine the structure and function of leucine-rich repeat receptor-like kinases. Current Opinion in Plant Biology 6, 507–516.
| Using mutant alleles to determine the structure and function of leucine-rich repeat receptor-like kinases.Crossref | GoogleScholarGoogle Scholar | 12972053PubMed |
Feuillet C, Travella S, Stein N, Albar L, Nublat A, Keller B (2003) Map-based isolation of the leaf rust disease resistance gene Lr10 from the hexaploid wheat (Triticum aestivum L.) genome. Proceedings of the National Academy of Sciences of the United States of America 100, 15 253–15 258.
| Map-based isolation of the leaf rust disease resistance gene Lr10 from the hexaploid wheat (Triticum aestivum L.) genome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpvFejsrg%3D&md5=1b3470eeb1dde3f8ceb1cb126a2b2516CAS |
Fofana B, Banks TW, McCallum B, Strelkov SE, Cloutier S (2007) Temporal gene expression profiling of the wheat leaf rust pathosystem using cDNA microarray reveals differences in compatible and incompatible defence pathways. International Journal of Plant Genomics 17 542
Golkari S, Gilbert J, Prashar S, Procunier JD (2007) Microarray analysis of Fusarium graminearum-induced wheat genes: identification of organ-specific and differentially expressed genes. Plant Biotechnology Journal 5, 38–49.
| Microarray analysis of Fusarium graminearum-induced wheat genes: identification of organ-specific and differentially expressed genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXitV2jtbs%3D&md5=3a7edc1364c0ade23af5146508960edaCAS | 17207255PubMed |
Häweker H, Rips S, Koiwa H, Salomon S, Saijo Y, Chinchilla D, Robatzek S, Schaewen A (2010) Pattern recognition receptors require N-glycosylation to mediate plant immunity. Journal of Biological Chemistry 285, 4629–4636.
| Pattern recognition receptors require N-glycosylation to mediate plant immunity.Crossref | GoogleScholarGoogle Scholar | 20007973PubMed |
Higuchi R, Fockler C, Dollinger G, Watson R (1993) Kinetic PCR analysis: real time monitoring of DNA amplification reactions. Biotechnology 11, 1026–1030.
| Kinetic PCR analysis: real time monitoring of DNA amplification reactions.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3sznvVOjsg%3D%3D&md5=c2230d9dfdaea46321380c0781361e82CAS | 7764001PubMed |
Hong SW, Jon JH, Kwak JM, Nam HG (1997) Identification of a receptor-like protein kinase gene rapidly induced by abscisic acid, dehydration, high salt and cold treatments in Arabidopsis thaliana. Plant Physiology 113, 1203–1212.
| Identification of a receptor-like protein kinase gene rapidly induced by abscisic acid, dehydration, high salt and cold treatments in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXis1GksLc%3D&md5=b86de08114170a2d6bf44ac6126f1fafCAS | 9112773PubMed |
Huang L, Brooks SA, Li W, Fellers JP, Trick HN, Gill BS (2003) Map-based cloning of leaf rust resistance gene Lr21 from the large and polyploid genome of bread wheat. Genetics 164, 655–664.
Hulbert SH, Bai J, Fellers JP, Pacheco MG, Bowden RL (2007) Gene expression patterns in near isogenic lines for wheat rust resistance gene Lr34/Yr18. Phytopathology 97, 1083–1093.
| Gene expression patterns in near isogenic lines for wheat rust resistance gene Lr34/Yr18.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVOms7nN&md5=0969bba6867f85fdba0a35a865b9223fCAS | 18944173PubMed |
Ishitani M, Liu J, Halfter U, Kim CS, Shi W, Zhu JK (2000) SOS3 function in plant salt tolerance requires N-myristoylation and calcium binding. The Plant Cell 12, 1667–1677.
Jain M, Nijhawan A, Arora R, Agarwal P, Ray S, Sharma P, Kapoor S, Tyagi AK, Khurana JP (2007) F-box proteins in rice. Genome-wide analysis, classification, temporal and spatial gene expression during panicle and seed development, and regulation by light and abiotic stress. Plant Physiology 143, 1467–1483.
| F-box proteins in rice. Genome-wide analysis, classification, temporal and spatial gene expression during panicle and seed development, and regulation by light and abiotic stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXksFWjtrk%3D&md5=48a2a087a11bbc29245f9f988e6f1a48CAS | 17293439PubMed |
Jammes F, Lecomte P, Almeida EJ, Bitton F, Martin MML, Renou JP, Abad P, Favery B (2005) Genome-wide expression profiling of the host response to root-knot nematode infection in Arabidopsis. The Plant Journal 44, 447–458.
| Genome-wide expression profiling of the host response to root-knot nematode infection in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1alsbnL&md5=667ba48824db5d406f67bcb72be81f7aCAS | 16236154PubMed |
Jones JD, Dangl JL (2006) The plant immune system. Nature 444, 323–329.
| The plant immune system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1SgtbzO&md5=289500416c19947efd96d3e4aedb7bf5CAS | 17108957PubMed |
Krattinger SG, Lagudah ES, Spielmeyer W, Singh RP, Huerta-Espino J, McFadden H, Bossolini E, Selter LL, Keller B (2009) A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science 323, 1360–1363.
| A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXisFemtbg%3D&md5=19275afd2d9d75f8d620bfce838ef393CAS | 19229000PubMed |
Kruger WM, Pritsch C, Chao S, Muehlbauer GJ (2002) Functional and comparative bioinformatic analysis of expressed genes from wheat spikes infected with Fusarium graminearum. Molecular Plant-Microbe Interactions 15, 445–455.
| Functional and comparative bioinformatic analysis of expressed genes from wheat spikes infected with Fusarium graminearum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjslSit7g%3D&md5=8c0433b46266cad5406932eb9bd1229bCAS | 12036275PubMed |
Liang P, Pardee AB (1992) Differential display of eukaryotic messenger RNA by means of the polymerase chain reaction. Science 257, 967–971.
| Differential display of eukaryotic messenger RNA by means of the polymerase chain reaction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38Xls1Cqt70%3D&md5=66ad45a0e9a4b3ae6d91a2fb95f0e734CAS | 1354393PubMed |
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔ C T method. Methods 25, 402–408.
| Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔ C T method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtFelt7s%3D&md5=fb7f5980d7bf4d62f797a1988cd8f193CAS | 11846609PubMed |
Manickavelu A, Kawaura K, Oishi K, Shin-I T, Kohara Y, Yahiaoui N, Keller B, Suzuki A, Yano K, Ogihara Y (2010) Comparative gene expression analysis of susceptible and resistant near-isogenic lines in common wheat infected by Puccinia triticina. DNA Research 17, 211–222.
| Comparative gene expression analysis of susceptible and resistant near-isogenic lines in common wheat infected by Puccinia triticina.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVanurfJ&md5=7ef7afa34f99d62ef4387d9dd5b0161fCAS | 20360266PubMed |
McIntosh RA, Miller TE, Chapman V (1982) Cytogenetical studies in wheat XII. Lr28 for resistance to Puccinia recondita and Sr34 for resistance to P. graminis tritici. Zeitschrift für Pflanzenzüchtung 89, 295–306.
McIntosh RA, Dubcovsky J, Rogers WJ, Morris C, Appels R, Xia XC (2009) Catalogue of gene symbols for wheat: supplement 2009. Available at: http://www.shigen.nig.ac.jp/wheat/komugi/genes/macgene/supplement2009.pdf [Accessed 5 May 2010]
Montoya-García L, Muñoz-Ocotero V, Aguilar R, de Jimenez ES (2002) Regulation of acidic ribosomal protein expression and phosphorylation in maize. Biochemistry 41, 10 166–10 172.
| Regulation of acidic ribosomal protein expression and phosphorylation in maize.Crossref | GoogleScholarGoogle Scholar |
Nguyen HP, Chakravarthy S, Velásquez AC, McLane HL, Zeng L, Nakayashiki H, Park DH, Collmer A, Martin GB (2010) Methods to study PAMP-triggered immunity using tomato and Nicotiana benthamiana. Molecular Plant-Microbe Interactions 23, 991–999.
| Methods to study PAMP-triggered immunity using tomato and Nicotiana benthamiana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpsFegtb4%3D&md5=e29e5ecafe1910e87abe1c5ba3f1b7efCAS | 20615110PubMed |
Ouyang SQ, Liu YF, Liu P, Lei G, He SJ, Ma B, Zhang WK, Zhang JS, Chen SY (2010) Receptor-like kinase OsSIK1 improves drought and salt stress tolerance in rice (Oryza sativa) plants. The Plant Journal 62, 316–329.
| Receptor-like kinase OsSIK1 improves drought and salt stress tolerance in rice (Oryza sativa) plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlslShsLc%3D&md5=4eb6fbdf828a2e01ba87c31d31ea9852CAS | 20128882PubMed |
Patton EE, Willems AR, Tyers M (1998) Combinatorial control in ubiquitin-dependent proteolysis: don’t skip the F-box hypothesis. Trends in Genetics 14, 236–243.
| Combinatorial control in ubiquitin-dependent proteolysis: don’t skip the F-box hypothesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjslanur4%3D&md5=2361772077b729aae9f618098857048dCAS | 9635407PubMed |
Romeis T, Ludwig AA, Martin R, Jones JDG (2001) Calcium-dependent protein kinases play an essential role in a plant defence response. EMBO Journal 20, 5556–5567.
| Calcium-dependent protein kinases play an essential role in a plant defence response.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnvVeksbo%3D&md5=4a907c7c7b98b314cdb918ac5cee28bdCAS | 11597999PubMed |
Sambrook J, Fitsch EF, Maniatis T (1989) ‘Molecular cloning: a laboratory manual.’ (Cold Spring Harbor Press: Woodbury, NY)
Sayre KD, Singh RP, Huerta-Espino J, Rajaram S (1998) Genetic progress in reducing losses to leaf rust in CIMMYT-derived Mexican spring wheat cultivars. Crop Science 38, 654–659.
| Genetic progress in reducing losses to leaf rust in CIMMYT-derived Mexican spring wheat cultivars.Crossref | GoogleScholarGoogle Scholar |
Song WY, Wang GL, Chen L, Zhai W, Kim HS, Holsten T, Zhu L, Ronald P (1995) A receptor-like protein kinase encoded by the rice disease resistance gene, Xa21. Science 270, 1804–1806.
| A receptor-like protein kinase encoded by the rice disease resistance gene, Xa21.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXhtVSiurnI&md5=2f4565a1eb224125ab4f8c8af466b392CAS | 8525370PubMed |
Tao Y, Xie ZY, Chen WQ, Glazebrook J, Chang HS, Han B, Zhu T, Zou GZ, Katagiri F (2003) Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae. The Plant Cell 15, 317–330.
| Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtlOmtLY%3D&md5=bb1f54da7caa78c29290e3470d612abeCAS | 12566575PubMed |
Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G, Nomura K, He SY, Howe GA, Browse J (2007) JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling. Nature 448, 661–665.
| JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXos1yks7k%3D&md5=6354393e8ce90e8390864f3ffdb7bdf8CAS | 17637677PubMed |
Tsantrizos YS, Xu XJ (1993) Novel quinazolinones and enniatins from Fusarium lateritium Nees. Canadian Journal of Chemistry 71, 1362–1367.
| Novel quinazolinones and enniatins from Fusarium lateritium Nees.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXms1KjtbY%3D&md5=05123a4cd34c5e5066010b9499b44f4dCAS |
Valentines MC, Vilaplana R, Torres R, Usall J, Larrigaudiere C (2005) Specific roles of enzymatic browning and lignification in apple disease resistance. Postharvest Biology and Technology 36, 227–234.
van der Knaap E, Song WY, Ruan DL, Sauter M, Ronald PC, Kende H (1999) Expression of a gibberellin-induced leucine-rich repeat receptor-like protein kinase in deepwater rice and its interaction with kinase-associated protein phosphatase. Plant Physiology 120, 559–570.
| Expression of a gibberellin-induced leucine-rich repeat receptor-like protein kinase in deepwater rice and its interaction with kinase-associated protein phosphatase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXktFWqs78%3D&md5=e9c6a2a78f567a08fcd35fcc0a769162CAS | 10364408PubMed |
van Esse HP, van’t Klooster JW, Bolton MD, Yadeta KA, van Baarlen P, Boeren S, Vervoort J, de Wit PJGM, Thomma BPHJ (2008) The Cladosporium fulvum virulence protein Avr2 inhibits host proteases required for basal defense. The Plant Cell 20, 1948–1963.
| The Cladosporium fulvum virulence protein Avr2 inhibits host proteases required for basal defense.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVyrsbfI&md5=05ba2a9f68cb4003414887594b093259CAS | 18660430PubMed |
Vij S, Giri J, Dansana PK, Kapoor S, Tyagi AK (2008) The receptor-like cytoplasmic kinase (OsRLCK) gene family in rice: organization, phylogenetic relationship, and expression during development and stress. Molecular Plant 1, 732–750.
| The receptor-like cytoplasmic kinase (OsRLCK) gene family in rice: organization, phylogenetic relationship, and expression during development and stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlWiu7fE&md5=6b36497eef63145c678ef713fdab03dcCAS | 19825577PubMed |
Vos P, Hogers R, Bleeker M, Reijans M, de Lee TV, Hornes M, Frijters A, Pot J, Peleman J, Kuiper M, Zabeau M (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Research 23, 4407–4414.
| AFLP: a new technique for DNA fingerprinting.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXpslensbo%3D&md5=103639968fc5070aa8e76f4291783164CAS | 7501463PubMed |
Walker JC (1994) Structure and function of the receptor-like kinases of higher plants. Plant Molecular Biology 26, 1599–1609.
| Structure and function of the receptor-like kinases of higher plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXjvFeks74%3D&md5=9161b3a1b654602f5b25a0e1badf5a92CAS | 7858206PubMed |
Wang XJ, Tang CL, Zhang G, Li YC, Wang CF, Liu B, Qu ZP, Zhao J, Han QM, Huang LL, Chen XM, Kang ZS (2009) cDNA-AFLP analysis reveals differential gene expression in compatible interaction of wheat challenged with Puccinia striiformis f. sp. tritici. BMC Genomics 10, 289
| cDNA-AFLP analysis reveals differential gene expression in compatible interaction of wheat challenged with Puccinia striiformis f. sp. tritici.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXit1SgtLo%3D&md5=00d52122e004a2cd90ad29ee5808ae15CAS | 19566949PubMed |
Wang X, Liu W, Chen X, Tang C, Dong Y, Ma J, Huang X, Wei G, Han Q, Huang L, Kang Z (2010) Differential gene expression in incompatible interaction between wheat and stripe rust fungus revealed by cDNA-AFLP and comparison to compatible interaction. BMC Plant Biology 10, 9
| Differential gene expression in incompatible interaction between wheat and stripe rust fungus revealed by cDNA-AFLP and comparison to compatible interaction.Crossref | GoogleScholarGoogle Scholar | 20067621PubMed |
Xiao W, Jang JC (2000) F-box proteins in Arabidopsis. Trends in Plant Science 5, 454–457.
| F-box proteins in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M%2FmtFSnug%3D%3D&md5=aeab320e1f218aea76ff1d5daaca461bCAS | 11077244PubMed |
Xie D, Feys BF, James S, Nieto-Rostro M, Tumes JG (1998) COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility. Science 280, 1091–1094.
| COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjt1egsbk%3D&md5=80570bae9530b0fa2f4c6977dfb0e342CAS | 9582125PubMed |
Yang C, Guo R, Jie F, Nettleton D, Peng J, Carr T, Yeakley JM, Fan JB, Whitham SA (2007) Spatial analysis of Arabidopsis thaliana gene expression in response to turnip mosaic virus infection. Molecular Plant-Microbe Interactions 20, 358–370.
| Spatial analysis of Arabidopsis thaliana gene expression in response to turnip mosaic virus infection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjsVyksL4%3D&md5=a6de8cc41294a2b4656d44d2f2a0ab0bCAS | 17427806PubMed |
Zhang GY, Chen M, Guo JM, Xu T, 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=de22726ddfc87e4d2f789afb2af2168cCAS | 19191020PubMed |
Zhang L, Meakin H, Dickinson M (2003) Isolation of genes expressed during compatible interactions between leaf rust (Puccinia triticina) and wheat using cDNA-AFLP. Molecular Plant Pathology 4, 469–477.
| Isolation of genes expressed during compatible interactions between leaf rust (Puccinia triticina) and wheat using cDNA-AFLP.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpvVygsro%3D&md5=58d2d30b050d4d5c8f085e3fab84004eCAS | 20569406PubMed |
Zhou H, Li S, Deng Z, Wang X, Chen T, Zhang J, Chen S, Ling H, Zhang A, Wang D, Zhang X (2007) Molecular analysis of three new receptor-like kinase genes from hexaploid wheat and evidence for their participation in the wheat hypersensitive response to stripe rust fungus infection. The Plant Journal 52, 420–434.
| Molecular analysis of three new receptor-like kinase genes from hexaploid wheat and evidence for their participation in the wheat hypersensitive response to stripe rust fungus infection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtl2jtbfN&md5=634e3b5794ee78a3e603867823a6fbabCAS | 17764502PubMed |