Comparison and evolutionary analysis of Brassica nucleotide binding site leucine rich repeat (NLR) genes and importance for disease resistance breeding.
Journal
The plant genome
ISSN: 1940-3372
Titre abrégé: Plant Genome
Pays: United States
ID NLM: 101273919
Informations de publication
Date de publication:
03 2021
03 2021
Historique:
received:
27
01
2020
accepted:
11
08
2020
pubmed:
13
11
2020
medline:
22
4
2021
entrez:
12
11
2020
Statut:
ppublish
Résumé
The Brassica genus contains many agriculturally significant oilseed and vegetable crops, however the crop yield is threatened by a range of fungal and bacterial pathogens. Nucleotide Binding Site Leucine Rich Repeat (NLR) genes play important roles in plant innate immunity. The evolution of NLR genes is influenced by genomic processes and pathogen selection. At the whole genome level, whole genome duplications (WGDs) generate abundant gene copies, most of which are lost during genome fractionation. At sub-genomic levels, some retained copies undergo duplication forming clusters which facilitate rapid evolution through recombination. The number, distribution and genetic variations of the NLR genes vary among Brassica species and within populations suggesting differential selection pressure exerted by pathogen populations throughout the evolutionary history. A study of the evolution of disease resistance genes in agriculturally important plants such as Brassicas helps gain insights into their function and inform the identification of resistance genes for breeding of resistant lines.
Substances chimiques
Nucleotides
0
Leucine
GMW67QNF9C
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
e20060Informations de copyright
© 2020 The Authors. The Plant Genome published by Wiley Periodicals, Inc. on behalf of Crop Science Society of America.
Références
Adams, K. L., & Wendel, J. F. (2005). Polyploidy and genome evolution in plants. Current Opinion in Genetics & Development, 35, 119-125.
Alamery, S., Tirnaz, S., Bayer, P., Tollenaere, R., Chaloub, B., Edwards, D., & Batley, J. (2018). Genome-wide identification and comparative analysis of NBS-LRR resistance genes in Brassica napus. Crop & Pasture Science, 69, 72-93. https://doi.org/10.1071/CP17214
Ameline-Torregrosa, C., Wang, B.-B., O'Bleness, M., Deshpande, S., Zhu, H., Roe, B., … Cannon, S. (2008). Identification and characterization of nucleotide-binding site-leucine-rich repeat genes in the model plant Medicago truncatula. Plant Physiology, 146, 5-21. https://doi.org/10.1104/pp.107.104588
Arora, H., Padmaja, K. L., Paritosh, K., Mukhi, N., Tewari, A. K., Mukhopadhyay, A., … Pental, D. (2019). BjuWRR1, a CC-NB-LRR gene identified in Brassica juncea, confers resistance to white rust caused by Albugo candida. Theoretical and Applied Genetics, 132, 2223-2236. https://doi.org/10.1007/s00122-019-03350-z
Bakker, E. G., Toomajian, C., Kreitman, M., & Bergelson, J. (2006). A genome-wide survey of R gene polymorphisms in Arabidopsis. Plant Cell, 18, 1803-1818. https://doi.org/10.1105/tpc.106.042614
Bayer, P., Edwards, D., & Batley, J. (2018). Bias in resistance gene prediction due to repeat-masking. Nature Plants, 4, 762. https://doi.org/10.1038/s41477-018-0264-0
Bayer, P., Golicz, A. A., Tirnaz, S., Chan, K., Edwards, D., & Batley, J. (2019). Variation in abundance of predicted resistance genes in the Brassica oleracea pangenome. Plant Biotechnology Journal, 17, 789-800. https://doi.org/10.1111/pbi.13015
Bayer, P. E., Hurgobin, B., Golicz, A. A., Chan, C.-K. K., Yuan, Y., Lee, H., … Edwards, D. (2017). Assembly and comparison of two closely related Brassica napus genomes. Plant Biotechnology Journal, 15, 1034-1046. https://doi.org/10.1111/pbi.12742
Chalhoub, B., Denoeud, F., Liu, S., Parkin, I. A. P., Tang, H., Wang, X., … Wincker, P. (2014). Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome. Science, 345, 950-953. https://doi.org/10.1126/science.1253435
Chattopadhyay, C., Kolte, S. J., & Waliyar, F. (2015). Diseases of edible oilseed crops. Boca Raton: CRC Press.
Chen, Q., Han, Z., Jiang, H., Tian, D., & Yang, S. (2010). Strong positive selection drives rapid diversification of R-genes in Arabidopsis relatives. Journal of Molecular Evolution, 70, 137-148. https://doi.org/10.1007/s00239-009-9316-4
Cheng, F., Wu, J., & Wang, X. (2014). Genome triplication drove the diversification of Brassica plants. Hortic Research, 1, 14024. https://doi.org/10.1038/hortres.2014.24
Cheung, F., Trick, M., Drou, N., Lim, Y. P., Park, J.-Y., Kwon, S.-J., … Bancroft, I. (2009). Comparative analysis between homoeologous genome segments of Brassica napus and its progenitor species reveals extensive sequence-level divergence. Plant Cell, 21, 1912-1928. https://doi.org/10.1105/tpc.108.060376
De Araujo, A. C., Fonesca, F. C. D. A., Cotta, M. G., Alves, G. S. C., & MillerR, R. N. G. (2019). Plant NLR receptor proteins and their potential in the development of durable genetic resistance to biotic stresses. Biotechnology Research and Innovation, 3, 80-94.
Diederichsen, E., Frauen, M., Linders, E. G. A., Hatakeyama, K., & Hirai, M. (2009). Status and perspectives of clubroot resistance breeding in crucifer crops. Journal of Plant Growth Regulation, 28, 265-281. https://doi.org/10.1007/s00344-009-9100-0
Dolatabadian, A., Bayer, P., Tirnaz, S., Hurgobin, B., Edwards, D., & Batley, J. (2020). Characterization of disease resistance genes in the Brassica napus pangenome reveals significant structural variation. Plant Biotechnology Journal, 18, 969-982. https://doi.org/10.1111/pbi.13262
Edwards, D., Batley, J., Parkin, I., & Kole, C. (2011). Genetics, genomics and breeding of oilseed Brassicas. In Genetics, genomics and breeding of oilseed Brassicas. Boca Raton: CRC Press.
Florence, E., Saskia, E., & Takaki, E. (2013). Evolution and conservation of plant NLR functions. Frontiers in Immunology, 4, 297.
Fu, Y., Zhang, Y., Mason, A. S., Lin, B., Zhang, D., Yu, H., & Fu, D. (2019). NBS-Encoding Genes in Brassica napus Evolved Rapidly After Allopolyploidization and Co-localize With Known Disease Resistance Loci. Frontiers in Plant Science, 10, 26. https://doi.org/10.3389/fpls.2019.00026
Golicz, A. A., Bayer, P. E., Barker, G. C., Edger, P. P., Kim, H., Martinez, P. A., … Edwards, D. (2016). The pangenome of an agronomically important crop plant Brassica oleracea. Nature Communications, 7, 13390. https://doi.org/10.1038/ncomms13390
Guo, Y.-L., Fitz, J., Schneeberger, K., Ossowski, S., Cao, J., & Weigel, D. (2011). Genome-wide comparison of nucleotide-binding site-leucine-rich repeat-encoding genes in Arabidopsis. Plant Physiology, 157, 757-769. https://doi.org/10.1104/pp.111.181990
Gupta, V., Sharma, S., Padmaja, K. L., Bisht Naveen, C., Jagannath, A., Panjabi, P., … Pental, D. (2008). Comparative mapping of Brassica juncea and Arabidopsis thaliana using Intron Polymorphism (IP) markers: Homoeologous relationships, diversification and evolution of the A, B and C Brassica genomes. BMC Genomics, 9, 113-131.
Hatakeyama, K., Niwa, T., Kato, T., Ohara, T., Kakizaki, T., & Matsumoto, S. (2017). The tandem repeated organization of NB-LRR genes in the clubroot-resistant CRb locus in Brassica rapa L. Molecular Genetics and Genomics, 292, 397-405. https://doi.org/10.1007/s00438-016-1281-1
Hofberger, J., Zhou, B., Tang, H., Jones, J., & Schranz, M. (2014). A novel approach for multi-domain and multi-gene family identification provides insights into evolutionary dynamics of disease resistance genes in core eudicot plants. BMC Genomics, 15, 966.
Hulbert, S. H., Webb, C. A., Smith, S. M., & Sun, Q. (2001). Resistance gene complexes: Evolution and utilization. Annual Review of Phytopathology, 39, 285-312. https://doi.org/10.1146/annurev.phyto.39.1.285
Hurgobin, B., Golicz, A. A., Bayer, P. E., Chan, C. K., Tirnaz, S., Dolatabadian, A., … Edwards, D. (2017). Homoeologous exchange is a major cause of gene presence/absence variation in the amphidiploid Brassica napus. Plant Biotechnology Journal, 16, 1265-1274. https://doi.org/10.1111/pbi.12867
Inturrisi, F., Bayer, P., Yang, H., Tirnaz, S., Edwards, D., & Batley, J. (2020). Genome wide identification and comparative analysis of NBS-LRR resistance genes in Brassica juncea. Molecular Breeding, 40, 78. https://doi.org/10.1007/s11032-020-01159-z
Jin, M., Lee, S.-S., Ke, L., Kim, J. S., Seo, M.-S., Sohn, S.-H., … Bonnema, G. (2014). Identification and mapping of a novel dominant resistance gene, TuRB07 to Turnip mosaic virus in Brassica rapa. Theoretical and Applied Genetics, 127, 509-519. https://doi.org/10.1007/s00122-013-2237-z
Joshi, R., & Nayak, S. (2013). Perspectives of genomic diversification and molecular recombination towards R -gene evolution in plants. Physiology and Molecular Biology of Plants, 19, 1-9. https://doi.org/10.1007/s12298-012-0138-2
Jupe, F., Pritchard, L., Etherington, G. J., MacKenzie, K., Cock, P. J. A., Wright, F., … Hein, I. (2012). Identification and localisation of the NB-LRR gene family within the potato genome. BMC Genomics, 13, 75.
Kato, T., Hatakeyama, K., Fukino, N., & Matsumoto, S. (2013). Fine mapping of the clubroot resistance gene CRb and development of a useful selectable marker in Brassica rapa. Breeding Science, 63, 116-124. https://doi.org/10.1270/jsbbs.63.116
Kourelis, J., & van Der Hoorn, R. A. L. (2018). Defended to the nines: 25 years of resistance gene cloning identifies nine mechanisms for R protein function. Plant Cell, 30, 285-299. https://doi.org/10.1105/tpc.17.00579
Kuang, H., Woo, S.-S., Meyers, B. C., Nevo, E., & Michelmore, R. W. (2004). Multiple genetic processes result in heterogeneous rates of evolution within the major cluster disease resistance genes in lettuce. Plant Cell, 16, 2870-2894. https://doi.org/10.1105/tpc.104.025502
Kushalappa, A. C., Yogendra, K. N., & Karre, S. (2016). Plant innate immune response: Qualitative and quantitative resistance. Crc Critical Reviews in Plant Science, 35, 38-55. https://doi.org/10.1080/07352689.2016.1148980
Leister, D. (2004). Tandem and segmental gene duplication and recombination in the evolution of plant disease resistance genes. Trends in Genetics, 20, 116-122. https://doi.org/10.1016/j.tig.2004.01.007
Li, P., Quan, X., Jia, G., Xiao, J., Cloutier, S., & You, F. M. (2016a). RGAugury: A pipeline for genome-wide prediction of resistance gene analogs (RGAs) in plants. BMC Genomics, 17, 852.
Li, Q., Li, J., Sun, J.-L., Ma, X.-F., Wang, T.-T., Berkey, R., … Wang, W.-M. (2016b). Multiple evolutionary events involved in maintaining homologs of resistance to powdery mildew 8 in Brassica napus. Frontiers in Plant Science, 7, 1065.
Liu, J., Liu, X., Dai, L., & Wang, G. (2007). Recent progress in elucidating the structure, function and evolution of disease resistance genes in plants. Journal of Genetics and Genomics, 34, 765-776. https://doi.org/10.1016/S1673-8527(07)60087-3
Liu, S., Liu, Y., Yang, X., Tong, C., Edwards, D., Parkin, I. A., … Paterson, A. H. (2014). The Brassica oleracea genome reveals the asymmetrical evolution of polyploid genomes. Nature Communications, 5, 3930. https://doi.org/10.1038/ncomms4930
Luo, S., Zhang, Y., Hu, Q., Chen, J., Li, K., Lu, C., … Kuang, H. (2012). Dynamic nucleotide-binding site and leucine-rich repeat-encoding genes in the grass family. Plant Physiology, 159, 197-210. https://doi.org/10.1104/pp.111.192062
Lv, H., Fang, Z., Yang, L., Zhang, Y., & Wang, Y. (2020). An update on the arsenal: Mining resistance genes for disease management of Brassica crops in the genomic era. Horticulture Research, 7, 1-18 https://doi.org/10.1038/s41438-020-0257-9
Lysak, M. A., Koch, M. A., Pecinka, A., & Schubert, I. (2005). Chromosome triplication found across the tribe Brassiceae. Genome Research, 15, 516-525. https://doi.org/10.1101/gr.3531105
Marone, D., Russo, M., Laidò, G., Leonardis, A., & Mastrangelo, A. (2013). Plant nucleotide binding site-leucine-rich repeat (NBS-LRR) genes: Active guardians in host defense responses. International Journal of Molecular Sciences, 14, 7302-7326. https://doi.org/10.3390/ijms14047302
Melamed-Bessudo, C., Shilo, S., & Levy, A. A. (2016). Meiotic recombination and genome evolution in plants. Current Opinion in Plant Biology, 30, 82-87. https://doi.org/10.1016/j.pbi.2016.02.003
Meyers, B. C., Kozik, A., Griego, A., Kuang, H., & Michelmore, R. W. (2003). Genome-wide analysis of NBS-LRR-Encoding genes in Arabidopsis. Plant Cell, 15, 809-834. https://doi.org/10.1105/tpc.009308
Meyers, B. C., Morgante, M., & Michelmore, R. W. (2002). TIR-X and TIR-NBS proteins: Two new families related to disease resistance TIR-NBS-LRR proteins encoded in Arabidopsis and other plant genomes. Plant Journal, 32, 77-92. https://doi.org/10.1046/j.1365-313X.2002.01404.x
Michelmore, R. W., Christopoulou, M., & Caldwell, K. S. (2013). Impacts of resistance gene genetics, function, and evolution on a durable future. Annual Review of Phytopathology, 51, 291-319. https://doi.org/10.1146/annurev-phyto-082712-102334
Mondragón-Palomino, M., Meyers, B. C., Michelmore, R. W., & Gaut, B. S. (2002). Patterns of positive selection in the complete NBS-LRR gene family of Arabidopsis thaliana. Genome Research, 12, 1305-1315. https://doi.org/10.1101/gr.159402
Mun, J.-H., Kwon, S.-J., Yang, T.-J., Seol, Y.-J., Jin, M., Kim, J.-A., … Park, B.-S. (2009a). Genome-wide comparative analysis of the Brassica rapa gene space reveals genome shrinkage and differential loss of duplicated genes after whole genome triplication. Genome Biology, 10, R111.1-R111.18. https://doi.org/10.1186/gb-2009-10-10-r111
Mun, J.-H., Yu, H.-J., Park, S., & Park, B.-S. (2009b). Genome-wide identification of NBS-encoding resistance genes in Brassica rapa. Molecular Genetics and Genomics, 282, 617-631. https://doi.org/10.1007/s00438-009-0492-0
Paritosh, K., Gupta, V., Yadava, S. K., Singh, P., Pradhan, A. K., & Pental, D. (2014). RNA-seq based SNPs for mapping in Brassica juncea (AABB): Synteny analysis between the two constituent genomes A (from B. rapa) and B (from B. nigra) shows highly divergent gene block arrangement and unique block fragmentation patterns. BMC Genomics, 15, 396.
Parkin, I. A. P., Koh, C. S., Tang, H., Robinson, S. J., Kagale, S., Clarke, W. E., … Sharpe, A. G. (2014). Transcriptome and methylome profiling reveals relics of genome dominance in the mesopolyploid Brassica oleracea. Genome Biology, 15, R77. https://doi.org/10.1186/gb-2014-15-6-r77
Peele, H. M., Guan, N., Fogelqvist, J., & Dixelius, C. (2014). Loss and retention of resistance genes in five species of the Brassicaceae family. BMC Plant Biology, 14, 1-11. https://doi.org/10.1186/s12870-014-0298-z
Raman, R., Taylor, B., Marcroft, S., Stiller, J., Eckermann, P., Coombes, N., … Raman, H. (2012). Molecular mapping of qualitative and quantitative loci for resistance to Leptosphaeria maculans causing blackleg disease in canola (Brassica napus L.). Theoretical and Applied Genetics, 125, 405-418. https://doi.org/10.1007/s00122-012-1842-6
Ratnaparkhe, M. B., Wang, X., Li, J., Compton, R. O., Rainville, L. K., Lemke, C., … Paterson, A. H. (2011). Comparative analysis of peanut NBS-LRR gene clusters suggests evolutionary innovation among duplicated domains and erosion of gene microsynteny. New Phytologist, 192, 164-178. https://doi.org/10.1111/j.1469-8137.2011.03800.x
Sekhwal, M. K., Li, P., Lam, I., Wang, X., Cloutier, S., & You, F. M. (2015). Disease resistance gene analogs (RGAs) in plants. International Journal of Molecular Sciences, 16, 19248-19290. https://doi.org/10.3390/ijms160819248
Shao, Z. Q., Xue, J. Y., Wang, Q., Wang, B., & Chen, J. Q. (2019). Revisiting the origin of plant NBS-LRR genes. Trends in Plant Science, 24, 9-12. https://doi.org/10.1016/j.tplants.2018.10.015
Shao, Z.-Q., Xue, J.-Y., Wu, P., Zhang, Y.-M., Wu, Y., Hang, Y.-Y., … Chen, J.-Q. (2016). Large-scale analyses of angiosperm nucleotide-binding site-leucine-rich repeat genes reveal three anciently diverged classes with distinct evolutionary patterns. Plant Physiology, 170, 2095-2109. https://doi.org/10.1104/pp.15.01487
Sun, X., Zhang, Y., Yang, S., Chen, J.-Q., Hohn, B., & Tian, D. (2008). Insertion DNA promotes ectopic recombination during meiosis in Arabidopsis. Molecular Biology and Evolution, 25, 2079-2083. https://doi.org/10.1093/molbev/msn158
Tang, H., Woodhouse, M. R., Feng, C., Schnable, J. C., Pedersen, B. S., Conant, G., … Pires, J. C. (2012). Altered patterns of fractionation and exon deletions in Brassica rapa support a two-step model of paleohexaploidy. Genetics, 190, 1563-1574. https://doi.org/10.1534/genetics.111.137349
Tirnaz, S., Bayer, P., Inturrisi, F., Zhang, F., Yang, H., Dolatabadian, A., … Batley, J. (2020). Resistance gene analogs in the Brassicaceae: Identification, characterization, distribution and evolution, a resource for plant breeding. Plant Physiology. https://doi.org/10.1104/pp.20.00835
Town, C. D., Cheung, F., Maiti, R., Crabtree, J., Haas, B. J., Wortman, J. R., … Bancroft, I. (2006). Comparative genomics of Brassica oleracea and Arabidopsis thaliana reveal gene loss, fragmentation, and dispersal after polyploidy. Plant Cell, 18, 1348-1359. https://doi.org/10.1105/tpc.106.041665
U, N. (1935). Genome analysis in Brassica with special reference to the experimental formation of B. napus and peculiar mode of fertilization. Japanese Journal of Botany, 7, 389-452.
Ueno, H., Matsumoto, E., Aruga, D., Kitagawa, S., Matsumura, H., & Hayashida, N. (2012). Molecular characterization of the CRa gene conferring clubroot resistance in Brassica rapa. Plant Molecular Biology, 80, 621-629. https://doi.org/10.1007/s11103-012-9971-5
Van de Wouw, A. P., & Howlett, B. J. (2019). Advances in understanding the Leptosphaeria maculans-Brassica pathosystem and their impact on disease management. Canadian Journal of Plant Pathology, 42, 1-15.
Wang, X., Wang, H., Wang, J., Sun, R., Wu, J., Liu, S., … Li, Y. (2011). The genome of the mesopolyploid crop species Brassica rapa. Nature Genetics, 43, 1035-1040. https://doi.org/10.1038/ng.919
Wu, P., Shao, Z.-Q., Wu, X.-Z., Wang, Q., Wang, B., Chen, J.-Q., … Xue, J.-Y. (2014). Loss retention and evolution of NBS-encoding genes upon whole genome triplication of Brassica rapa. Gene, 540, 54-61. https://doi.org/10.1016/j.gene.2014.01.082
Yang, J., Liu, D., Wang, X., Ji, C., Cheng, F., Liu, B., … Zhang, M. (2016). The genome sequence of allopolyploid Brassica juncea and analysis of differential homoeolog gene expression influencing selection. Nature Genetics, 48, 1225-1232B. https://doi.org/10.1038/ng.3657
Yang, S., Zhang, X., Yue, J.-X., Tian, D., & Chen, J.-Q. (2008). Recent duplications dominate NBS-encoding gene expansion in two woody species. Molecular Genetics and Genomics, 280, 187-198. https://doi.org/10.1007/s00438-008-0355-0
Yu, J., Tehrim, S., Zhang, F., Tong, C., Huang, J., Cheng, X., … Liu, S. (2014). Genome-wide comparative analysis of NBS-encoding genes between Brassica species and Arabidopsis thaliana. BMC Genomics, 15, 3.
Zhang, R., Murat, F., Pont, C., Langin, T., & Salse, J. (2014). Paleo-evolutionary plasticity of plant disease resistance genes. BMC Genomics, 15, 187.
Zhang, X., Feng, Y., Cheng, H., Tian, D., Yang, S., & Chen, J.-Q. (2011). Relative evolutionary rates of NBS-encoding genes revealed by soybean segmental duplication. Molecular Genetics and Genomics, 285, 79-90. https://doi.org/10.1007/s00438-010-0587-7
Zhang, Y. M., Shao, Z. Q., Wang, Q., Hang, Y. Y., Xue, J. Y., Wang, B., & Chen, J. Q. (2016). Uncovering the dynamic evolution of nucleotide-binding site-leucine-rich repeat (NBS-LRR) genes in Brassicaceae. Journal of Integrative Plant Biology, 58, 165-177. https://doi.org/10.1111/jipb.12365
Zheng, F., Wu, H., Zhang, R., Li, S., He, W., Wong, F.-L., … Lam, H.-M. (2016). Molecular phylogeny and dynamic evolution of disease resistance genes in the legume family. BMC Genomics, 17, 402.
Zhou, T., Wang, Y., Chen, J. Q., Araki, H., Jing, Z., Jiang, K., … Tian, D. (2004). Genome-wide identification of NBS genes in japonica rice reveals significant expansion of divergent non-TIR NBS-LRR genes. Molecular Genetics and Genomics, 271, 402-415. https://doi.org/10.1007/s00438-004-0990-z
Zou, J., Hu, D., Liu, P., Raman, H., Liu, Z., Liu, X., … Meng, J. (2016). Co-linearity and divergence of the A subgenome of Brassica juncea compared with other Brassica species carrying different A subgenomes. BMC Genomics, 17, 18.