https://eutils.ncbi.nlm.nih.gov/entrez/eutils/efetch.fcgi?db=pubmed&id=29312363&retmode=xml&tool=Litmetric&email=readroberts32@gmail.com&api_key=61f08fa0b96a73de8c900d749fcb997acc09 2931236320220409
1664-462X82017Frontiers in plant scienceFront Plant SciIdentification, Validation and Utilization of Novel Nematode-Responsive Root-Specific Promoters in Arabidopsis for Inducing Host-Delivered RNAi Mediated Root-Knot Nematode Resistance.20492049204910.3389/fpls.2017.02049The root-knot nematode (RKN), Meloidogyne incognita, is an obligate, sedentary endoparasite that infects a large number of crops and severely affects productivity. The commonly used nematode control strategies have their own limitations. Of late, RNA interference (RNAi) has become a popular approach for the development of nematode resistance in plants. Transgenic crops capable of expressing dsRNAs, specifically in roots for disrupting the parasitic process, offer an effective and efficient means of producing resistant crops. We identified nematode-responsive and root-specific (NRRS) promoters by using microarray data from the public domain and known conserved cis-elements. A set of 51 NRRS genes was identified which was narrowed down further on the basis of presence of cis-elements combined with minimal expression in the absence of nematode infection. The comparative analysis of promoters from the enriched NRRS set, along with earlier reported nematode-responsive genes, led to the identification of specific cis-elements. The promoters of two candidate genes were used to generate transgenic plants harboring promoter GUS constructs and tested in planta against nematodes. Both promoters showed preferential expression upon nematode infection, exclusively in the root in one and galls in the other. One of these NRRS promoters was used to drive the expression of splicing factor, a nematode-specific gene, for generating host-delivered RNAi-mediated nematode-resistant plants. Transgenic lines expressing dsRNA of splicing factor under the NRRS promoter exhibited upto a 32% reduction in number of galls compared to control plants.KakranaAtulAICAR-National Research Centre on Plant Biotechnology, New Delhi, India.Center for Bioinformatics and Computational Biology, University of Delaware, Newark, DE, United States.KumarAnilAICAR-National Research Centre on Plant Biotechnology, New Delhi, India.Department of Biotechnology, Faculty of Science, Centre for Transgenic Plant Development, Jamia Hamdard University, New Delhi, India.SatheeshViswanathanVICAR-National Research Centre on Plant Biotechnology, New Delhi, India.AbdinM ZMZDepartment of Biotechnology, Faculty of Science, Centre for Transgenic Plant Development, Jamia Hamdard University, New Delhi, India.SubramaniamKuppuswamyKDepartment of Biotechnology, Indian Institute of Technology Madras, Chennai, India.BhattacharyaR CRCICAR-National Research Centre on Plant Biotechnology, New Delhi, India.SrinivasanRamamurthyRICAR-National Research Centre on Plant Biotechnology, New Delhi, India.SirohiAnilADivision of Nematology, ICAR-Indian Agricultural Research Institute, New Delhi, India.JainPradeep KPKICAR-National Research Centre on Plant Biotechnology, New Delhi, India.engJournal Article20171212
SwitzerlandFront Plant Sci1015682001664-462XArabidopsisHD-RNAiin silico analysisnematode-responsive genespromoter analysisroot-specific genes201761520171115201811060201811060201811061201711epublish29312363PMC573300910.3389/fpls.2017.02049Abad P., Gouzy J., Aury J. M., Castagnone-Sereno P., Danchin E. G., Deleury E., et al. . (2008). Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita. Nat. Biotechnol. 26, 909–915. 10.1038/nbt.148210.1038/nbt.148218660804Alkharouf N. W., Klink V. P., Chouikha I. B., Beard H. S., MacDonald M. H., Meyer S., et al. . (2006). Timecourse microarray analyses reveal global changes in gene expression of susceptible Glycine max (soybean) roots during infection by Heterodera glycines (soybean cyst nematode). Planta 224, 838–852. 10.1007/s00425-006-0270-810.1007/s00425-006-0270-816575592Bakhetia M., Charlton W., Atkinson H. J., McPherson M. J. (2005). RNA interference of dual oxidase in the plant nematode Meloidogyne incognita. Mol. Plant Microbe Interact. 18, 1099–1106. 10.1094/MPMI-18-109910.1094/MPMI-18-109916255249Banerjee S., Banerjee A., Gill S. S., Gupta O. P., Dahuja A., Jain P. K., et al. . (2017). RNA Interference: a novel source of resistance to combat plant parasitic nematodes. Front. Plant Sci. 8:834. 10.3389/fpls.2017.0083410.3389/fpls.2017.00834PMC543737928580003Barcala M., García A., Cabrera J., Casson S., Lindsey K., Favery B., et al. . (2010). Early transcriptomic events in microdissected Arabidopsis nematode-induced giant cells. Plant J. 61, 698–712. 10.1111/j.1365-313X.2009.04098.x10.1111/j.1365-313X.2009.04098.x20003167Bar-Or C., Kapulnik Y., Koltai H. (2005). A broad characterization of the transcriptional profile of the compatible tomato response to the plant parasitic root-knot nematode Meloidogyne javanica. Eur. J. Plant Pathol. 111, 181–192. 10.1007/s10658-004-2134-z10.1007/s10658-004-2134-zBertioli D. J., Smoker M., Burrows P. R. (1999). Nematode-responsive activity of the cauliflower mosaic virus 35S promoter and its subdomains. Mol. Plant Microbe Interact. 12, 189–196. 10.1094/MPMI.1999.12.3.18910.1094/MPMI.1999.12.3.189Cabrera J., Bustos R., Favery B., Fenoll C., Escobar C. (2014). Technical advance NEMATIC : a simple and versatile tool for the in silico analysis of plant – nematode interactions. Mol. Plant Pathol. 15, 627–636. 10.1111/mpp.1211410.1111/mpp.12114PMC663870824330140Clough S. J., Bent A. F. (1998). Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735–743. 10.1046/j.1365-313x.1998.00343.x10.1046/j.1365-313x.1998.00343.x10069079Coutu C., Brandle J., Brown D., Miki B., Simmonds J. (2007). PORE: a modular binary vector series suited for both monocot and dicot plant transformation. Transgenic Res. 16, 771–781. 10.1007/s11248-007-9066-210.1007/s11248-007-9066-217273915Davuluri R. V., Sun H., Palaniswamy S. K., Matthews N., Molina C., Kurtz M., et al. . (2003). AGRIS: Arabidopsis gene regulatory information server, an information resource of Arabidopsis cis-regulatory elements and transcription factors. BMC Bioinformatics 4:25. 10.1186/1471-2105-4-2510.1186/1471-2105-4-25PMC16615212820902Dinh P. T. Y., Brown C. R., Elling A. A. (2014). RNA Interference of effector gene Mc16D10L confers resistance against Meloidogyne chitwoodi in Arabidopsis and Potato. Phytopathology 104, 1098–1106. 10.1094/PHYTO-03-14-0063-R10.1094/PHYTO-03-14-0063-R24835223Dong L., Xu J., Chen S., Li X., Zuo Y. (2016). Mi-flp-18 and Mi-mpk-1 genes are potential targets for Meloidogyne incognita control. J. Parasitol. 102, 20–213. 10.1645/15-76810.1645/15-76826785173Dutta T. K., Banakar P., Rao U. (2015). The status of RNAi- based transgenic research in plant nematology. Front. Micrbiol. 5:760. 10.3389/fmicb.2014.0076010.3389/fmicb.2014.00760PMC429061825628609Elling A. A. (2013). Major emerging problems with minor Meloidogyne species. Phytopathology 103, 1092–1102. 10.1094/PHYTO-01-13-0019-RVW10.1094/PHYTO-01-13-0019-RVW23777404Escobar C., Barcala M., Portillo M., Almoguera C., Jordano J., Fenoll C. (2003). Induction of the Hahsp17.7G4 promoter by root-knot nematodes: involvement of heat-shock elements in promoter activity in giant cells. Mol. Plant Microbe Interact. 16, 1062–1068. 10.1094/MPMI.2003.16.12.106210.1094/MPMI.2003.16.12.106214651339Escobar C., De Meutter J., Aristizábal F. A., Sanz-Alférez S., del Campo F. F., Barthels N., et al. . (1999). Isolation of the LEMMI9 gene and promoter analysis during a compatible plant-nematode interaction. Mol. Plant Microbe Interact. 12, 440–449. 10.1094/MPMI.1999.12.5.44010.1094/MPMI.1999.12.5.44010226377Fairbairn D. J., Cavallaro A. S., Bernard M., Mahalinga-Iyer J., Graham M. W., Botella J. R. (2007). Host-delivered RNAi: an effective strategy to silence genes in plant parasitic nematodes. Planta 226, 1525–1533. 10.1007/s00425-007-0588-x10.1007/s00425-007-0588-x17653759Favery B., Chelysheva L. A., Lebris M., Jammes F., Marmagne A., De Almeida-Engler J., et al. . (2004). Arabidopsis formin AtFH6 is a plasma membrane-associated protein upregulated in giant cells induced by parasitic nematodes. Plant Cell 16, 2529–2540. 10.1105/tpc.104.02437210.1105/tpc.104.024372PMC52095015319477Fudali S., Janakowski S., Sobczak M., Griesser M., Grundler F. M., Golinowski W., et al. (2008). Two tomato alpha-expansins show distinct spatial and temporal expression patterns during development of nematode-induced syncytia. Physiol. Plant 132, 370–383. 10.1111/j.1399-3054.2007.01017.x10.1111/j.1399-3054.2007.01017.x18275468Fuller V. L., Lilley C. J., Atkinson H. J., Urwin P. E. (2007). Differential gene expression in Arabidopsis following infection by plant-parasitic nematodes Meloidogyne incognita and Heterodera schachtii. Mol. Plant Pathol. 8, 595–609. 10.1111/j.1364-3703.2007.00416.x10.1111/j.1364-3703.2007.00416.x20507524Gal T. Z., Aussenberg E. R., Burdman S., Kapulnik Y., Koltai H. (2006). Expression of a plant expansin is involved in the establishment of root-knot nematode parasitism in tomato. Planta 224, 155–162. 10.1007/s00425-005-0204-x10.1007/s00425-005-0204-x16395582Gheysen G., Mitchum M. (2009). Molecular insights in the susceptible plant response to nematode infection, in Cell Biology of Plant Nematode Parasitism, eds Berg R. H., Taylor C. (Berlin: Springer; ), 45–81.Goddijn O. J., Lindsey K., van der Lee F. M., Klap J. C., Sijmons P. C. (1993). Differential gene expression in nematode-induced feeding structures of transgenic plants harbouring promoter-gusA fusion constructs. Plant J. 4, 863–873. 10.1046/j.1365-313X.1993.04050863.x10.1046/j.1365-313X.1993.04050863.x8275103Grunewald W., Cannoot B., Friml J., Gheysen G. (2009). Parasitic nematodes modulate PIN-mediated auxin transport to facilitate infection. PLoS Pathog. 5:e1000266. 10.1371/journal.ppat.100026610.1371/journal.ppat.1000266PMC261352919148279Grunewald W., Karimi M., Wieczorek K., Van de Cappelle E., Wischnitzki E., Grundler F., et al. . (2008). A role for AtWRKY23 in feeding site establishment of plant-parasitic nematodes. Plant Physiol. 148, 358–368. 10.1104/pp.108.11913110.1104/pp.108.119131PMC252809818599655Hammes U. Z., Schachtman D. P., Berg R. H., Nielsen E., Koch W., McIntyre L. M., et al. . (2005). Nematode-induced changes of transporter gene expression in Arabidopsis roots. Mol. Plant Microbe Interact. 18, 1247–1257. 10.1094/MPMI-18-124710.1094/MPMI-18-124716478044Higo K., Ugawa Y., Iwamoto M., Korenaga T. (1999). Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res. 27, 297–300. 10.1093/nar/27.1.29710.1093/nar/27.1.297PMC1481639847208Hruz T., Laule O., Szabo G., Wessendorp F., Bleuler S., Oertle L., et al. . (2008). Genevestigator V3: a reference expression database for the meta-analysis of transcriptomes. Adv. Bioinformatics 2008:420747. 10.1155/2008/42074710.1155/2008/420747PMC277700119956698Huang G., Allen R., Davis E. L., Baum T. J., Hussey R. S. (2006). Engineering broad root-knot resistance in transgenic plants by RNAi silencing of a conserved and essential root-knot nematode parasitism gene. Proc. Natl. Acad. Sci. U.S.A. 103, 14302–14306. 10.1073/pnas.060469810310.1073/pnas.0604698103PMC157018416985000Ithal N., Recknor J., Nettleton D., Maier T., Baum T. J., Mitchum M. G. (2007). Developmental transcript profiling of cyst nematode feeding cells in soybean roots. Mol. Plant Microbe Interact. 20, 510–525. 10.1094/MPMI-20-5-051010.1094/MPMI-20-5-051017506329Jammes F., Lecomte P., de Almeida-Engler J., Bitton F., Martin-Magniette M. L., Renou J. P., et al. . (2005). Genome-wide expression profiling of the host-response to root-knot nematode infection in Arabidopsis. Plant J. 44, 447–458. 10.1111/j.1365-313X.2005.02532.x10.1111/j.1365-313X.2005.02532.x16236154Jefferson R. A. (1989). The GUS reporter gene system. Nature 342, 837–838. 10.1038/342837a010.1038/342837a02689886Jiao Y., Ma L., Strickland E., Deng X. W. (2005). Conservation and divergence of light-regulated genome expression patterns during seedling development in rice and Arabidopsis. Plant Cell 17, 3239–3256. 10.1105/tpc.105.03584010.1105/tpc.105.035840PMC131536716284311Kankainen M., Pehkonen P., Rosenstöm P., Törönen P., Wong G., Holm L. (2006). POXO: A web-enabled tool series to discover transcription factor binding sites. Nucleic Acids Res. 34, 534–540. 10.1093/nar/gkl29610.1093/nar/gkl296PMC153877316845065Klink V. P., Overall C. C., Alkharouf N. W., MacDonald M. H., Matthews B. F. (2007). A time-course comparative microarray analysis of an incompatible and compatible response by Glycine max (soybean) to Heterodera glycines (soybean cyst nematode) infection. Planta 226, 1423–1447. 10.1007/s00425-007-0581-410.1007/s00425-007-0581-417653570Kumar A., Joshi I., Kohli D., Satheesh V., Abdin M. Z., Sirohi A., et al. (2016). Characterization of root-knot nematode responsive and root-specific promoter containing PIN domain from Arabidopsis thaliana (L.) Heynh. Indian J. Genet. Plant Breed. 76, 75–83. 10.5958/0975-6906.2016.00011.010.5958/0975-6906.2016.00011.0Kumar A., Kakrana A., Sirohi A., Subramaniam K., Srinivasan R., Abdin M. Z., et al. (2017). Host-delivered RNAi-mediated root-knot nematode resistance in Arabidopsis by targeting splicing factor and integrase genes. J. Gen. Plant Pathol. 83, 91–97. 10.1007/s10327-017-0701-310.1007/s10327-017-0701-3Liu Q., Kasuga M., Sakuma Y., Abe H., Miura S., Yamaguchi-Shinozaki K., et al. . (1998). Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10, 1391–1406. 10.1105/tpc.10.8.139110.1105/tpc.10.8.1391PMC1443799707537Livak K. J., Schmittgen T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25, 402–408. 10.1006/meth.2001.126210.1006/meth.2001.126211846609Lilley C. J., Urvin P. E., Johnston K. A., Atkinson H. J. (2004). Preferential expression of a plant cystatin at nematode feeding sites confers resistance to Meloidogyne incognita and Globodera pallida. Plant Biotechnol. J. 2, 3–12. 10.1046/j.1467-7652.2003.00037.x10.1046/j.1467-7652.2003.00037.x17166138Mahony S., Benos P. V. (2007). STAMP: a web tool for exploring DNA-binding motif similarities. Nucleic Acids Res. 35, 253–258. 10.1093/nar/gkm27210.1093/nar/gkm272PMC193320617478497Mitchum M., Sukno S., Shani Z., Shoseyov O., Davis E. L. (2004). The promoter of the Arabidopsis thaliana cel1 endo-1,4-β-glucanase gene is differentially expressed in plant feeding cells induced by root-knot and cyst nematodes. Mol. Plant Pathol. 5, 175–181. 10.1111/j.1364-3703.2004.00216.x10.1111/j.1364-3703.2004.00216.x20565607Niu J., Liu P., Liu Q., Chen C., Guo Q., Yin J., et al. (2016). Msp40 effector of root-knot nematode manipulates plant immunity to facilitate parasitism. Sci. Rep. 6:19443 10.1038/srep1944310.1038/srep19443PMC472642326797310Ono A., Izawa T., Chua N. H., Shimamoto K. (1996). The rab16B promoter of rice contains two distinct abscisic acid-responsive elements. Plant Physiol. 112, 483–491. 10.1104/pp.112.2.48310.1104/pp.112.2.483PMC1579718883374Onyango S. O., Roderick H., Tripathi J. N., Collins R., Atkinson H. J., Oduor R. O., et al. . (2016). The ZmRCP-1 promoter of maize provides root tip specific expression of transgenes in plantain. J. Biol. Res. Thessaloniki 23:4. 10.1186/s40709-016-0041-z10.1186/s40709-016-0041-zPMC481264527030819Opperman C. H., Taylor C. G., Conkling M. A. (1994). Root-knot nematode-directed expression of a plant root-specific gene. Science 263, 221–223. 10.1126/science.263.5144.22110.1126/science.263.5144.22117839183Portillo M., Cabrera J., Lindsey K., Topping J., Andrés M. F., Emiliozzi M., et al. . (2013). Distinct and conserved transcriptomic changes during nematode-induced giant cell development in tomato compared with Arabidopsis: a functional role for gene repression. New Phytol. 197, 1276–1290. 10.1111/nph.1212110.1111/nph.1212123373862Puzio P., Lausen J., Heinen P., Grundler F. (2000). Promoter analysis of pyk20, a gene from Arabidopsis thaliana. Plant Sci. 157, 245–255. 10.1016/S0168-9452(00)00287-910.1016/S0168-9452(00)00287-910960738Rosso M. N., Jones J. T., Abad P. (2009). RNAi and functional genomics in plant parasitic nematodes. Annu. Rev. Phytopathol. 47, 207–232. 10.1146/annurev.phyto.112408.13260510.1146/annurev.phyto.112408.13260519400649Rozen S., Skaletsky H. (2000). Primer3 on the WWW for general users and for biologist programmers. Methods Mol. Biol. 132, 365–386. 10.1385/1-59259-192-2:36510.1385/1-59259-192-2:36510547847Saha D., Kumar V., Bhat S. R., Srinivasan R. (2007). Characterization of upstream sequences of the LOJ gene leads to identification of a novel enhancer element conferring lateral organ junction-specific expression in Arabidopsis thaliana. Plant Mol. Biol. Rep. 29, 265–277. 10.1007/s11105-010-0229-610.1007/s11105-010-0229-6Sambrook J., Fritsch E. F., Maniatis T. (1989). Molecular Cloning: A Laboratory Manual. New York, NY: Cold Spring Harbor Laboratory Press.Schaff J. E., Nielsen D. M., Smith C. P., Scholl E. H., Bird D. M. (2007). Comprehensive transcriptome profiling in tomato reveals a role for glycosyltransferase in Mi-mediated nematode resistance. Plant Physiol. 144, 1079–1092. 10.1104/pp.106.09024110.1104/pp.106.090241PMC191419817434994Severino F. E., Brandalise M., Costa C. S., et al. . (2012). CaPrx, a Coffea arabica gene encoding a putative class III peroxidase induced by root-knot nematode infection. Plant Sci. 191–192, 35–42. 10.1016/j.plantsci.2012.04.01210.1016/j.plantsci.2012.04.01222682563Smith E. F., Townsend C. O. (1907). A plant-tumor of Bacterial origin. Science 25, 671–673. 10.1126/science.25.643.67110.1126/science.25.643.67117746161Smyth G. K. (2004). Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3:3. 10.2202/1544-6115.102710.2202/1544-6115.102716646809Sukno S., Shimerling O., McCuiston J., Tsabary G., Shani Z., Shoseyov O., et al. . (2006). Expression and regulation of the Arabidopsis thaliana cel1 endo 1,4 beta glucanase gene during compatible plant-nematode interactions. J. Nematol. 38, 354–361.PMC258670919259541Tamilarasan S., Rajam M. V. (2013). Engineering crop plants for nematode resistance through host-derived RNA interference. Cell Dev. Biol. 2:114 10.4172/2168-9296.100011410.4172/2168-9296.1000114Thomas-Chollier M., Sand O., Turatsinze J. V., Janky R., Defrance M., Vervisch E., et al. . (2008). RSAT: regulatory sequence analysis tools. Nucleic Acids Res. 36, 119–127. 10.1093/nar/gkn30410.1093/nar/gkn304PMC244777518495751Thurau T., Kifle S., Jung C., Cai D. (2003). The promoter of the nematode resistance gene Hs1pro-1 activates a nematode-responsive and feeding site-specific gene expression in sugar beet (Beta vulgaris L.) and Arabidopsis thaliana. Plant Mol. Biol. 52, 643–660.12956533Urwin P. E., Lilley C. J., McPherson M. J., Atkinson H. J. (1997). Resistance to both cyst and root-knot nematodes conferred by transgenic Arabidopsis expressing a modified plant cystatin. Plant J. 12, 455–461. 10.1046/j.1365-313X.1997.12020455.x10.1046/j.1365-313X.1997.12020455.x9301094Vaughan S. P., James D. J., Lindsey K., Massiah A. J. (2006). Characterization of FaRB7, a near root-specific gene from strawberry (Fragaria x ananassa Duch.) and promoter activity analysis in homologous and heterologous hosts. J. Exp. Bot. 57, 3901–3910. 10.1093/jxb/erl18510.1093/jxb/erl18517032728Vercauteren I., Van Der Schueren E., Van Montagu M., Gheysen G. (2001). Arabidopsis thaliana genes expressed in the early compatible interaction with root-knot nematodes. Mol. Plant Microbe Interact. 14, 288–299. 10.1094/MPMI.2001.14.3.28810.1094/MPMI.2001.14.3.28811277426Weigel D., Glazebrook J. (2006). Transformation of Agrobacterium using the freeze–thaw method. Cold Spring Harb. Protoc. 7, 1031–1036. 10.1101/pdb.prot466610.1101/pdb.prot466622484682Wieczorek K., Hofmann J., Blöchl A., Szakasits D., Bohlmann H., Grundler F. M. W. (2008). Arabidopsis endo-1,4-β-glucanases are involved in the formation of root syncytia induced by Heterodera schachtii. Plant J. 53, 336–351. 10.1111/j.1365-313X.2007.03340.x10.1111/j.1365-313X.2007.03340.x18069944Xiao F. H., Xue G. P. (2001). Analysis of the promoter activity of late embryogenesis abundant protein genes in barley seedlings under conditions of water deficit. Plant Cell Rep. 20, 667–673. 10.1007/s00299010038410.1007/s002990100384Yadav B. C., Veluthambi K., Subramaniam K. (2006). Host-generated double stranded RNA induces RNAi in plant-parasitic nematodes and protects the host from infection. Mol. Biochem. Parasitol. 148, 219–222. 10.1016/j.molbiopara.2006.03.01310.1016/j.molbiopara.2006.03.01316678282Yamaguchi-Shinozaki K., Shinozaki K. (2001). Improving plant drought, salt and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Novartis Found Symp. 236, 176–186. 10.1002/9780470515778.ch1310.1002/9780470515778.ch1311387979Yamamoto Y. T., Taylor C. G., Acedo G. N., Cheng C. L., Conkling M. A. (1991). Characterization of cis-acting sequences regulating root-specific gene expression in tobacco. Plant Cell 3, 371–382.PMC1600071840917Yu D., Chen C., Chen Z. (2001). Evidence for an important role of WRKY DNA binding proteins in the regulation of NPR1 gene expression. Plant Cell 13, 1527–1540. 10.1105/tpc.13.7.152710.1105/tpc.13.7.1527PMC13955011449049Zimmermann P., Hirsch-Hoffmann M., Hennig L., Gruissem W. (2004). Genevestigator. Arabidopsis microarray database and analysis toolbox. Plant Physiol. 136, 2621–2632. 10.1104/pp.104.04636710.1104/pp.104.046367PMC52332715375207