Amino acid permease 6 modulates host response to cyst nematodes in wheat and Arabidopsis
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Summary
Cyst nematodes are plant parasites that cause significant crop loss in wheat and other crops. Infective juveniles invade roots and induce syncytial feeding structures as the only source of nutrients throughout their life. A previous genome-wide association study in wheat identified amino acid permease 6 (TaAAP6) to be linked to susceptibility to the cereal cyst nematode Heterodera filipjevi. To characterise the role of AAP6 during nematode parasitism, we analysed the expression of TaAAP6 and the Arabidopsis orthologue AtAAP6. TaAAP6 was found to be highly expressed in nematode-infected roots of susceptible wheat, whereas it was not upregulated in nematode-infected roots of resistant accessions. AtAAP6 was also found to be highly upregulated in nematode-induced syncytia compared with non-infected roots. Infection assays with an AtAAP6 knock-out mutant revealed reduction in developing females, female size, and size of female-associated syncytia, thus indicating the importance of AAP6 in cyst nematode parasitism.
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-
Acedo, J.R., Dropkin, V.H. & Luedders, V.D. (1984). Nematode population attrition and histopathology of Heterodera glycines-soybean associations. Journal of Nematology 16, 48-57.
-
Alonso, J.M., Stepanova, A.N., Leisse, T.J., Kim, C.J., Chen, H., Shinn, P., Stevenson, D.K., Zimmerman, J., Barajas, P. & Cheuk, R. (2003). Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301, 653-657. DOI: 10.1126/science.1086391
-
Barcala, M., García, A., Cabrera, J., Casson, S., Lindsey, K., Favery, B., García-Casado, G., Solano, R., Fenoll, C. & Escobar, C. (2010). Early transcriptomic events in micro dissected Arabidopsis nematode-induced giant cells. Plant Journal 61, 698-712. DOI: 10.1111/j.1365-313X.2009.04098.x
-
Barrett, J.C., Fry, B., Maller, J. & Daly, M. (2005). Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21, 263-265. DOI: 10.1093/bioinformatics/bth457
-
Betka, M., Grundler, F.M.W. & Wyss, U. (1991). Influence of changes in the nurse cell system (syncytium) on the development of the cyst nematode Heterodera schachtii: single amino acids. Phytopathology 81, 75-79. DOI: 10.1094/Phyto-81-75
-
Blümel, M., Dally, N. & Jung, C. (2015). Flowering time regulation in crops – what did we learn from Arabidopsis? Current Opinion in Biotechnology 32, 121-129. DOI: 10.1016/j.copbio.2014.11.023
-
Böckenhoff, A. & Grundler, F.M.W. (1994). Studies on the nutrient uptake by the beet cyst nematode Heterodera schachtii by in situ microinjection of fluorescent probes into the feeding structures in Arabidopsis thaliana. Parasitology 109, 249-255. DOI: 10.1017/S003118200007637X
-
Böckenhoff, A., Prior, D.A., Grundler, F.M.W. & Oparka, K.J. (1996). Induction of phloem unloading in Arabidopsis thaliana roots by the parasitic nematode Heterodera schachtii. Plant Physiology 112, 1421-1427. DOI: 10.1104/pp.112.4.1421
-
Clarke, B., Lambrecht, M. & Rhee, S.Y. (2003). Arabidopsis genomic information for interpreting wheat EST sequences. Functional Integrative Genomics 3, 33-38. DOI: 10.1007/s10142-002-0075-1
-
Dubcovsky, J. & Dvorak, J. (2007). Genome plasticity a key factor in the success of polyploidy wheat under domestication. Science 316, 1862-1866. DOI: 10.1126/science.1143986
-
Elashry, A., Okumoto, S., Siddique, S., Koch, W., Kreil, D.P. & Bohlmann, H. (2013). The AAP gene family for amino acid permeases contributes to development of the cyst nematode Heterodera schachtii in roots of Arabidopsis. Plant Physiological Biochemistry 70, 379-386. DOI: 10.1016/j.plaphy.2013.05.016
-
Fischer, W.N., André, B., Rentsch, D., Krolkiewicz, S., Tegeder, M., Breitkreuz, K. & Frommer, W.B. (1998). Amino acid transport in plants. Trends in Plant Science 3, 188-195. DOI: 10.1016/S1360-1385(98)01231-X
-
Gill, K.S. & Gill, B.S. (1994). Mapping in the realm of polyploidy: the wheat model. BioEssays 16, 841-846. DOI: 10.1002/bies.950161111
-
Giménez, M.J., Pistón, F. & Atienza, S.G. (2011). Identification of suitable reference genes for normalization of qPCR data in comparative transcriptomic analyses in the Triticeae. Planta 233, 163-173. DOI: 10.1007/s00425-010-1290-y
-
Golinowski, W., Grundler, F.M.W. & Sobczak, M. (1996). Changes in the structure of Arabidopsis thaliana during female development of the plant-parasitic nematode Heterodera schachtii. Protoplasma 194, 103-116. DOI: 10.1007/BF01273172
-
Hammes, U.Z., Schachtman, D.P., Berg, R.H., Nielsen, E., Koch, W., McIntyre, L.M. & Taylor, C.G. (2005). Nematode-induced changes of transporter gene expression in Arabidopsis roots. Molecular Plant-Microbe Interactions 18, 1247-1257. DOI: 10.1094/MPMI-18-1247
-
Hofmann, J., Wieczorek, K., Blochl, A. & Grundler, F.M.W. (2007). Sucrose supply to nematode-induced syncytia depends on the apoplasmic and symplasmic pathways. Journal of Experimental Botany 58, 1591-1601. DOI: 10.1093/jxb/erl285
-
Hofmann, J., Elashry, A.E.N., Anwar, S., Erban, A., Kopka, J. & Grundler, F.M.W. (2010). Metabolic profiling reveals local and systemic responses of host plants to nematode parasitism. Plant Journal 62, 1058-1071. DOI: 10.1111/j.1365-313X.2010.04217.x
-
Hoth, S., Stadler, R., Sauer, N. & Hammes, U.Z. (2008). Differential vascularization of nematode-induced feeding sites. Proceedings of the National Academy of Sciences of the United States of America 105, 12617-12622. DOI: 10.1073/pnas.0803835105
-
Huang, X., Börner, A., Röder, M. & Ganal, M. (2002). Assessing genetic diversity of wheat (Triticum aestivum L.) germplasm using microsatellite markers. Theoretical and Applied Genetics 105, 699-707. DOI: 10.1007/s00122-002-0959-4
-
Hunt, E., Gattolin, S., Newbury, H.J., Bale, J.S., Tseng, H.M., Barrett, D.A. & Pritchard, J.A. (2010). Mutation in amino acid permease AAP6 reduces the amino acid content of the Arabidopsis sieve elements but leaves aphid herbivores unaffected. Journal of Experimental Botany 61, 55-64. DOI: 10.1093/jxb/erp274
-
Krasileva, K.V., Buffalo, V., Bailey, P., Pearce, S., Ayling, S., Tabbita, F., Soria, M., Wang, S., Akhunov, E. & Uauy, C. (2013). Separating homologs by phasing in the tetraploid wheat transcriptome. Genome Biology 14, R66. DOI: 10.1186/gb-2013-14-6-r66
-
Lalonde, S., Wipf, D. & Frommer, W.B. (2004). Transport mechanisms for organic forms of carbon and nitrogen between source and sink. Annual Review of Plant Biology 55, 341-372. DOI: 10.1146/annurev.arplant.55.031903.141758
-
Marella, H.H., Nielsen, E., Schachtman, D.P. & Taylor, C.G. (2013). The amino acid permeases AAP3 and AAP6 are involved in root-knot nematode parasitism of Arabidopsis. Molecular Plant-Microbe Interactions 26, 44-54. DOI: 10.1094/MPMI-05-12-0123-FI
-
Matsuoka, Y. (2011). Evolution of polyploid Triticum wheats under cultivation: the role of domestication, natural hybridization and allopolyploid speciation in their diversification. Plant Cell Physiology 52, 750-764. DOI: 10.1093/pcp/pcr018
-
Murray, M. & Thompson, W.F. (1980). Rapid isolation of high molecular weight plant DNA. Nucleic Acids Research 8, 4321-4326. DOI: 10.1093/nar/8.19.4321
-
Okumoto, S. & Pilot, G. (2011). Amino acid export in plants: a missing link in nitrogen cycling. Molecular Plant 4, 453-463. DOI: 10.1093/mp/ssr003
-
Okumoto, S., Schmidt, R., Tegeder, M., Fischer, W.N., Rentsch, D., Frommer, W.B. & Koch, W. (2002). High affinity amino acid transporters specifically expressed in xylem parenchyma and developing seeds of Arabidopsis. Journal of Biological Chemistry 277, 45338-45346. DOI: 10.1074/jbc.M207730200
-
Pariyar, S.R., Dababat, A.A., Sannemann, W., Erginbas-Orakci, G., Elashry, A., Siddique, S., Morgounov, A., Leon, J. & Grundler, F.M.W. (2016a). Genome-wide association study in wheat identifies resistance to the cereal cyst nematode Heterodera filipjevi. Phytopathology 106, 1128-1138. DOI: 10.1094/PHYTO-02-16-0054-FI
-
Pariyar, S.R., Dababat, A.A., Siddique, S., Erginbas-Orakci, G., Elashry, A., Morgounov, A. & Grundler, F.M.W. (2016b). Identification and characterisation of resistance to the cereal cyst nematode Heterodera filipjevi in winter wheat. Nematology 18, 377-402. DOI: 10.1163/15685411-00002964
-
Pfaffl, M.W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research 29, e45. DOI: 10.1093/nar/29.9.e45
-
Puthoff, D.P., Nettleton, D., Rodermel, S.R. & Baum, T.J. (2003). Arabidopsis gene expression changes during cyst nematode parasitism revealed by statistical analyses of microarray expression profiles. Plant Journal 33, 911-921. DOI: 10.1046/j.1365-313X.2003.01677.x
-
Rentsch, D., Boorer, K. & Frommer, W. (1998). Structure and function of plasma membrane amino acid, oligopeptide and sucrose transporters from higher plants. Journal of Membrane Biology 162, 177-190. DOI: 10.1007/s002329900355
-
Rentsch, D., Schmidt, S. & Tegeder, M. (2007). Transporters for uptake and allocation of organic nitrogen compounds in plants. FEBS Letters 581, 2281-2289. DOI: 10.1016/j.febslet.2007.04.013
-
Rice, S.L., Leadbeater, B.S.C. & Stone, A.R. (1985). Changes in cell structure in roots of resistant potatoes parasitized by potato cyst nematodes. I. Potatoes with resistance gene H1 derived from Solanum tuberosum ssp. andigena. Physiological Plant Pathology 27, 219-234. DOI: 10.1016/0048-4059(85)90069-4
-
Roberts, P.A. & Stone, A.R. (1983). Comparisons of invasion and development of Globodera spp. and European potato cyst-nematode pathotypes in roots of resistant Solanum sg. Leptostemonum spp. Nematologica 29, 95-108. DOI: 10.1163/187529283X00221
-
Saier, M.H., Yen, M.R., Noto, K., Tamang, D.G. & Elkan, C. (2009). The transporter classification database: recent advances. Nucleic Acids Research 37, D274-D278. DOI: 10.1093/nar/gkn862
-
Sambrook, J. & Russell, D. (2001). Molecular cloning, a laboratory manual, 3rd edition. Cold Spring Harbor, NY, USA, Cold Spring Harbor Laboratory Press.
-
Schmittgen, T.D. & Livak, K.J. (2008). Analyzing real-time PCR data by the comparative CT method. Nature Protocols 3, 1101-1108. DOI: 10.1038/nprot.2008.73
-
Shewry, P.R. (2009). Wheat. Journal of Experimental Botany 60, 1537-1553. DOI: 10.1093/jxb/erp058
-
Siddique, S., Endres, S., Atkins, J.M., Szakasits, D., Wieczorek, K., Hofmann, J., Blaukopf, C., Urwin, P.E., Tenhaken, R. & Grundler, F.M.W. (2009). Myo-inositol oxygenase genes are involved in the development of syncytia induced by Heterodera schachtii in Arabidopsis roots. New Phytologist 184, 457-472. DOI: 10.1111/j.1469-8137.2009.02981.x
-
Sijmons, P.C., Grundler, F.M.W., von Mende, N., Burrows, P.R. & Wyss, U. (1991). Arabidopsis thaliana as a new model host for plant-parasitic nematodes. Plant Journal 1, 245-254. DOI: 10.1111/j.1365-313X.1991.00245.x
-
Simonetti, E., Alba, E., Montes, M.J., Delibes, Á. & López-Braña, I. (2010). Analysis of ascorbate peroxidase genes expressed in resistant and susceptible wheat lines infected by the cereal cyst nematode, Heterodera avenae. Plant Cell Reports 29, 1169-1178. DOI: 10.1007/s00299-010-0903-z
-
Szakasits, D., Heinen, P., Wieczorek, K., Hofmann, J., Wagner, F., Kreil, D.P., Sykacek, P., Grundler, F.M.W. & Bohlmann, H. (2009). The transcriptome of syncytia induced by the cyst nematode Heterodera schachtii in Arabidopsis roots. Plant Journal 57, 771-784. DOI: 10.1111/j.1365-313X.2008.03727.x
-
Tegeder, M. (2012). Transporters for amino acids in plant cells: some functions and many unknowns. Current Opinion in Plant Biology 15, 315-321. DOI: 10.1016/j.pbi.2012.02.001
-
Tegeder, M. & Rentsch, D. (2010). Uptake and partitioning of amino acids and peptides. Molecular Plant 3, 997-1011. DOI: 10.1093/mp/ssq047
-
Tulpan, D., Leger, S., Tchagang, A. & Pan, Y. (2015). Enrichment of Triticum aestivum gene annotations using orthologue cliques and gene ontologies in other plants. BMC Genomics 16, 1-20. DOI: 10.1186/s12864-015-1496-2
-
Wipf, D., Ludewig, U., Tegeder, M., Rentsch, D., Koch, W. & Frommer, W.B. (2002). Conservation of amino acid transporters in fungi, plants and animals. Trends in Biochemical Science 27, 139-147. DOI: 10.1016/S0968-0004(01)02054-0
-
Zhao, H., Ma, H., Yu, L., Wang, X. & Zhao, J. (2012). Genome-wide survey and expression analysis of amino acid transporter gene family in rice (Oryza sativa L.). PloS ONE 7, e49210. DOI: 10.1371/journal.pone.0049210
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Amino acid permease 6 modulates host response to cyst nematodes in wheat and Arabidopsis
In: NematologySearch for other papers by Shree R. Pariyar in
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Summary
Cyst nematodes are plant parasites that cause significant crop loss in wheat and other crops. Infective juveniles invade roots and induce syncytial feeding structures as the only source of nutrients throughout their life. A previous genome-wide association study in wheat identified amino acid permease 6 (TaAAP6) to be linked to susceptibility to the cereal cyst nematode Heterodera filipjevi. To characterise the role of AAP6 during nematode parasitism, we analysed the expression of TaAAP6 and the Arabidopsis orthologue AtAAP6. TaAAP6 was found to be highly expressed in nematode-infected roots of susceptible wheat, whereas it was not upregulated in nematode-infected roots of resistant accessions. AtAAP6 was also found to be highly upregulated in nematode-induced syncytia compared with non-infected roots. Infection assays with an AtAAP6 knock-out mutant revealed reduction in developing females, female size, and size of female-associated syncytia, thus indicating the importance of AAP6 in cyst nematode parasitism.
| All Time | Past 365 days | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 1090 | 339 | 84 |
| Full Text Views | 209 | 5 | 3 |
| PDF Views & Downloads | 65 | 13 | 6 |
