Advertisement

Plant Molecular Biology Reporter

, Volume 36, Issue 3, pp 373–386 | Cite as

Genome-Wide Analysis in Wild and Cultivated Oryza Species Reveals Abundance of NBS Genes in Progenitors of Cultivated Rice

  • Hukam C. Rawal
  • S. V. Amitha Mithra
  • Kirti Arora
  • Vishesh Kumar
  • Neha Goel
  • Dwijesh Chandra Mishra
  • K. K. Chaturvedi
  • Anil Rai
  • S. Vimala Devi
  • T. R. Sharma
  • Amolkumar U. Solanke
Original Paper

Abstract

NBS-encoding genes play a critical role in the plant defense system. Wild relatives of crop plants are rich reservoirs of plant defense genes. Here, we performed a stringent genome-wide identification of NBS-encoding genes in three cultivated and eight wild Oryza species, representing three different genomes (AA, BB, and FF) from four continents. A total of 2688 NBS-encoding genes were identified from 11 Oryza genomes. All the three progenitor species of cultivated rice, namely O. barthii, O. rufipogon, and O. nivara, were the richest reservoir of NBS-encoding genes (214, 313, and 307 respectively). Interestingly, the two Asian cultivated species showed a contrasting pattern in the number of NBS-encoding genes. While indica subspecies maintained nearly equal number of NBS genes as its progenitor (309 and 313), the japonica subspecies had retained only two third in the course of evolution (213 and 307). Other major sources for NBS-encoding genes could be (i) O. longistaminata since it had the highest proportion of NBS-encoding genes and (ii) O. glumaepatula as it clustered distinctly away from the rest of the AA genome species. The present study thus revealed that NBS-encoding genes can be exploited from the primary gene pool for disease resistance breeding in rice.

Keywords

NBS genes NB-ARC domain NBS-LRR Genome-wide analysis Disease resistance Evolution 

Notes

Author Contributions

AS and AM: conceived and designed the experiments; HR and NG: developed the pipelines and analyzed data; KA and VK: PCR validation; HR and AS: finalized tables and figures; DM, KC, and AR: provided the bioinformatic support; VD: supplied plant material; AM, AS, and TS: drafted and finalized the manuscript; and all the authors read and approved the manuscript.

Funding Information

This research received financial support from the Centre for Agricultural Bioinformatics Scheme (CABin) funded by the Indian Council of Agricultural Research (ICAR), New Delhi, India.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Supplementary material

11105_2018_1086_Fig8_ESM.gif (17 kb)
ESM 1

(GIF 16 kb)

11105_2018_1086_MOESM1_ESM.tif (429 kb)
High resolution image (TIF 428 kb)
11105_2018_1086_Fig9_ESM.gif (9 kb)
ESM 2

(GIF 8 kb)

11105_2018_1086_MOESM2_ESM.tif (2 mb)
High resolution image (TIF 2017 kb)
11105_2018_1086_MOESM3_ESM.xlsx (441 kb)
ESM 3 (XLSX 441 kb)
11105_2018_1086_MOESM4_ESM.xlsx (18 kb)
ESM 4 (XLSX 18 kb)
11105_2018_1086_MOESM5_ESM.docx (27 kb)
ESM 5 (DOCX 27 kb)

References

  1. Altschul S, Gish W, Miller W, Myers E, Lipman D (1990) Basic local alignment search tool. J Mol Biol 215(3):403–410CrossRefPubMedGoogle Scholar
  2. Ameline-Torregrosa C, Wang BB, O’Bleness MS et al (2008) Identification and characterization of NBS–LRR genes in the model plant Medicago truncatula. Plant Physiol 146:5–21CrossRefPubMedPubMedCentralGoogle Scholar
  3. Andolfo G, Jupe F, Witek K, Etherington GJ, Ercolano MR, Jones JD (2014) Defining the full tomato NB-LRR resistance gene repertoire using genomic and cDNA RenSeq. BMC Plant Biol 14:120.  https://doi.org/10.1186/1471-2229-14-120 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL (2009) BLAST+: architecture and applications. BMC Bioinf 10:421CrossRefGoogle Scholar
  5. Cheng X, Jiang H, Zhao Y, Qian Y, Zhu S, Cheng B (2009) A genomic analysis of disease-resistance genes encoding nucleotide binding sites in Sorghum bicolor. Genet Mol Biol 33(2):292–297.  https://doi.org/10.1590/S1415-47572010005000036 CrossRefGoogle Scholar
  6. Das A, Soubam D, Singh PK, Thakur S, Singh NK, Sharma TR (2012) A novel blast resistance gene, Pi54rh cloned from wild species of rice, Oryza rhizomatis confers broad spectrum resistance to Magnaporthe oryzae. Funct Integr Genomics 12:215–228.  https://doi.org/10.1007/s10142-012-0284-1 CrossRefPubMedGoogle Scholar
  7. Devanna NB, Vijayan J, Sharma TR (2014) The Blast resistance gene Pi54of cloned from Oryza officinalis interacts with Avr-Pi54 through its novel non-LRR domains. PLoS One 9(8):e104840.  https://doi.org/10.1371/journal.pone.0104840 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Guo YL, 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 Physiol 157:757–769.  https://doi.org/10.1104/pp.111.181990 CrossRefPubMedPubMedCentralGoogle Scholar
  9. He Z, Zhai W, Wen H, Tang T, Wang Y, Lu X, Greenberg AJ, Hudson RR, Wu CI, Shi S (2011) Two evolutionary histories in the genome of rice: the roles of domestication genes. PLoS Genet 7:e1002100.  https://doi.org/10.1371/journal.pgen.1002100 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Heidel AJ, Lawal HM, Felder M et al (2011) Phylogeny-wide analysis of social amoeba genomes highlights ancient origins for complex intercellular communication. Genome Res 21:1882–1891.  https://doi.org/10.1101/gr.121137.111 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Holub EB (2001) The arms race is ancient history in Arabidopsis, the wildflower. Nat Rev Genet 2:516–527CrossRefPubMedGoogle Scholar
  12. Hulsen T, Huynen MA, J-de V, Groenen PMA (2006) Benchmarking ortholog identification methods using functional genomics data. Genome Biol 7:R31.  https://doi.org/10.1186/gb-2006-7-4-r31 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Jaillon O, Aury JM, Noel B et al (2001) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463–467Google Scholar
  14. Jones P, Binns D, Chang HY, Fraser M, Li W, McAnulla C, McWilliam H, Maslen J, Mitchell A, Nuka G, Pesseat S, Quinn AF, Sangrador-Vegas A, Scheremetjew M, Yong SY, Lopez R, Hunter S (2014) InterProScan 5: genome-scale protein function classification. Bioinformatics 30(9):1236–1240.  https://doi.org/10.1093/bioinformatics/btu031 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Joshi RK, Nayak S (2013) Perspectives of genomic diversification and molecular recombination towards R-gene evolution in plants. Physiol Mol Biol Plants 19:1–9CrossRefPubMedGoogle Scholar
  16. Khush GS (1997) Origin, dispersal, cultivation and variation of rice. Plant Mol Biol 35:24–34CrossRefGoogle Scholar
  17. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) ClustalW and ClustalX version 2.0. Bioinformatics 23:2947–2948.  https://doi.org/10.1093/bioinformatics/btm404. CrossRefPubMedGoogle Scholar
  18. Li J, Ding J, Zhang W, Zhang Y, Tang P, Chen JQ, Tian D, Yang S (2010) Unique evolutionary pattern of numbers of gramineous NBS-LRR genes. Mol Gen Genomics 283:427–438.  https://doi.org/10.1007/s00438-010-0527-6 CrossRefGoogle Scholar
  19. Liu W, Liu J, Triplett L, Leach JE, Wang GL (2014) Novel insights into rice innate immunity against bacterial and fungal pathogens. Annu Rev Phytopathol 52:213–241.  https://doi.org/10.1146/annurev-phyto-102313-045926 CrossRefPubMedGoogle Scholar
  20. Lozano R, Hamblin MT, Prochnik S, Jannink JL (2015) Identification and distribution of the NBS-LRR gene family in the Cassava genome. BMC Genomics 16:360.  https://doi.org/10.1186/s12864-015-1554-9 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Lukasik E, Takken FL (2009) STANDing strong, resistance proteins instigators of plant defence. Curr Opin Plant Biol 12:427–436.  https://doi.org/10.1016/j.pbi.2009.03.001 CrossRefPubMedGoogle Scholar
  22. Marchler-Bauer A, Lu S, Anderson JB, Chitsaz F, Derbyshire MK, DeWeese-Scott C, Fong JH, Geer LY, Geer RC, Gonzales NR, Gwadz M, Hurwitz DI, Jackson JD, Ke Z, Lanczycki CJ, Lu F, Marchler GH, Mullokandov M, Omelchenko MV, Robertson CL, Song JS, Thanki N, Yamashita RA, Zhang D, Zhang N, Zheng C, Bryant SH (2011) CDD: a conserved domain database for the functional annotation of proteins. Nucleic Acids Res 39(Database issue):D225–D229CrossRefPubMedGoogle Scholar
  23. Meyers BC, Kozik A, Griego A, Kuang H, Michelmore RW (2003) Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell 15:809–834.  https://doi.org/10.1105/tpc.009308 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Molina J, Sikora M, Garud N, Flowers JM, Rubinstein S, Reynolds A, Huang P, Jackson S, Schaal BA, Bustamante CD, Boyko AR, Purugganan MD (2011) Molecular evidence for a single evolutionary origin of domesticated rice. Proc Natl Acad Sci 108:8351–8356CrossRefPubMedGoogle Scholar
  25. Nandety RS, Caplan JL, Cavanaugh K, Perroud B, Wroblewski T, Michelmore RW, Meyers BC (2013) The role of TIR-NBS and TIR-X proteins in plant basal defence responses. Plant Physiol 162:1459–1472.  https://doi.org/10.1104/pp.113.219162 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Nguyen BD, Brar DS, Bui BC, Nguyen TV, Pham LN, Nguyen HT (2013) Identification and mapping of the QTL for aluminum tolerance introgressed from new source, Oryza rufipogon Griff. into indica rice, (Oryza sativa L.). Theor Appl Genet 106:583–593CrossRefGoogle Scholar
  27. Park KC, Kim NH, Cho YS, Kang KH, Lee JK, Kim NS (2003) Genetic variations of AA genome Oryza species measured by MITE-AFLP. Theor Appl Genet 107:203–209CrossRefPubMedGoogle Scholar
  28. Porter BW, Paidi M, Ming R, Alam M, Nishijima WT, Zhu YJ (2009) Genome-wide analysis of Carica papaya reveals a small NBS resistance gene family. Mol Gen Genomics 281:609–626.  https://doi.org/10.1007/s00438-009-0434-x CrossRefGoogle Scholar
  29. Rahman ML, Jiang W, Chu SH, Qiao Y, Ham TH, Woo MO, Lee J, Khanam MS, Chin JH, Jeung JU, Brar DS, Jena KK, Koh HJ (2009) High-resolution mapping of two rice brown plant hopper resistance genes, Bph20(t) and Bph21(t), originating from Oryza minuta. Theor Appl Genet 119:1237–1246CrossRefPubMedGoogle Scholar
  30. Ram T, Majumder ND, Krishnaveni D, Ansari MM (2007) Rice variety Dhanarasi, an example of improving yield potential and disease resistance by introgressing gene(s) from wild species (O. rufipogon). Curr Sci 92:987–992Google Scholar
  31. Rawal HC, Singh NK, Sharma TR (2013) Conservation, divergence and genome wide distribution of PAL and POX A gene families in plants. Int J Genomics 13:1–10.  https://doi.org/10.1155/2013/678969 CrossRefGoogle Scholar
  32. Sanchez PL, Wing RA, Brar DS. 2014 The wild relative of Rice: genomes and genomics, in Genetics and genomics of rice, ed. Zhang Q. and Wing R.A. (Plant genetics and genomics: crops and models 5, Springer), 9–25. DOI  https://doi.org/10.1007/978-1-4614-7903-1_2
  33. Second G (1982) Origin of the genetic diversity of cultivated rice (Oryza spp.): study of the polymorphism scored at 40 isozyme loci. Jpn J Genet 57:25–57CrossRefGoogle Scholar
  34. Seo E, Kim S, Yeom SI, Choi D (2016) Genome-wide comparative analyses reveal the dynamic evolution of nucleotide-binding leucine-rich repeat gene family among Solanaceae plants. Front Plant Sci 7:1205.  https://doi.org/10.3389/fpls.2016.01205 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Sharma T, Rai A, Gupta S, Vijayan J, Devanna B, Ray S (2012) Rice blast management through host-plant resistance: retrospect and prospects. Agric Res 1(1):37–52.  https://doi.org/10.1007/s40003-011-0003-5 CrossRefGoogle Scholar
  36. Singh S, Chand S, Singh NK, Sharma TR (2015) Genome-wide distribution, organisation and functional characterization of disease resistance and defence response genes across rice species. PLoS One 10(4):e0125964.  https://doi.org/10.1371/journal.pone.0125964 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Tanweer FA, Rafii MY, Sijam K, Rahim HA, Ahmed F, Latif MA (2015) Current advance methods for the identification of blast resistance genes in rice. C R Biol 338:321–334.  https://doi.org/10.1016/j.crvi.2015.03.001 CrossRefPubMedGoogle Scholar
  38. Tuskan GA, DiFazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A, Schein J, Sterck L, Aerts A, Bhalerao RR, Bhalerao RP, Blaudez D, Boerjan W, Brun A, Brunner A, Busov V, Campbell M, Carlson J, Chalot M, Chapman J, Chen GL, Cooper D, Coutinho PM, Couturier J, Covert S, Cronk Q, Cunningham R, Davis J, Degroeve S, Dejardin A, dePamphilis C, Detter J, Dirks B, Dubchak I, Duplessis S, Ehlting J, Ellis B, Gendler K, Goodstein D, Gribskov M, Grimwood J, Groover A, Gunter L, Hamberger B, Heinze B, Helariutta Y, Henrissat B, Holligan D, Holt R, Huang W, Islam-Faridi N, Jones S, Jones-Rhoades M, Jorgensen R, Joshi C, Kangasjarvi J, Karlsson J, Kelleher C, Kirkpatrick R, Kirst M, Kohler A, Kalluri U, Larimer F, Leebens-Mack J, Leple JC, Locascio P, Lou Y, Lucas S, Martin F, Montanini B, Napoli C, Nelson DR, Nelson C, Nieminen K, Nilsson O, Pereda V, Peter G, Philippe R, Pilate G, Poliakov A, Razumovskaya J, Richardson P, Rinaldi C, Ritland K, Rouze P, Ryaboy D, Schmutz J, Schrader J, Segerman B, Shin H, Siddiqui A, Sterky F, Terry A, Tsai CJ, Uberbacher E, Unneberg P, Vahala J, Wall K, Wessler S, Yang G, Yin T, Douglas C, Marra M, Sandberg G, van de Peer Y, Rokhsar D (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604CrossRefPubMedGoogle Scholar
  39. Van der Biezen EA, Jones JD (1998) The NB-ARC domain: a novel signalling motif shared by plant resistance gene products and regulators of cell death in animals. Curr Biol 8(7):R226–R227CrossRefPubMedGoogle Scholar
  40. Van Zee JP, Schlueter JA, Schlueter S, Dixon P, Sierra CA, Hill CA (2016) Paralog analyses reveal gene duplication events and genes under positive selection in Ixodes scapularis and other ixodid ticks. BMC Genomics 17:241.  https://doi.org/10.1186/s12864-015-2350-2 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Vaughan DA (1994) The wild relatives of rice: a genetic resources handbook. International Rice Research Institute, Manila, p 137Google Scholar
  42. Vaughan DA, Lu BR, Tomooka N (2008) The evolving story of rice evolution. Plant Sci 174:394–408CrossRefGoogle Scholar
  43. Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78.  https://doi.org/10.1093/jhered/93.1.77 CrossRefPubMedGoogle Scholar
  44. Wambugu PW, Brozynska M, Furtado A, Waters DL, Henry RJ (2015) Relationships of wild and domesticated rices (Oryza AA genome species) based upon whole chloroplast genome sequences. Sci Rep 5:13957.  https://doi.org/10.1038/srep13957 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Waters DL, Nock CJ, Ishikawa R, Rice N, Henry RJ (2012) Chloroplast genome sequence confirms distinctness of Australian and Asian wild rice. Ecol Evol 2:211–217.  https://doi.org/10.1002/ece3.66 CrossRefPubMedPubMedCentralGoogle Scholar
  46. Yang S, Zhang X, Yue JX, Tian D, Chen JQ (2008) Recent duplications dominate NBS-encoding gene expansion in two woody species. Mol Gen Genomics 280:187–198.  https://doi.org/10.1007/s00438-008-0355-0 CrossRefGoogle Scholar
  47. Yue JX, Meyers BC, Chen JQ, Tian DC, Yang SH (2012) Tracing the origin and evolutionary history of plant nucleotide-binding site-leucine-rich repeat (NBS-LRR) genes. New Phytol 193:1049–1063.  https://doi.org/10.1111/j.1469-8137.2011.04006.x CrossRefPubMedGoogle Scholar
  48. Zhang QJ, Zhu T, Xia EH, Shi C, Liu YL, Zhang Y, Liu Y, Jiang WK, Zhao YJ, Mao SY, Zhang LP, Huang H, Jiao JY, Xu PZ, Yao QY, Zeng FC, Yang LL, Gao J, Tao DY, Wang YJ, Bennetzen JL, Gao LZ (2014) Rapid diversification of five Oryza AA genomes associated with rice adaptation. Proc Natl Acad Sci USA 111:E4954–E4962.  https://doi.org/10.1073/pnas.1418307111 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Hukam C. Rawal
    • 1
  • S. V. Amitha Mithra
    • 1
  • Kirti Arora
    • 1
  • Vishesh Kumar
    • 1
  • Neha Goel
    • 1
  • Dwijesh Chandra Mishra
    • 2
  • K. K. Chaturvedi
    • 2
  • Anil Rai
    • 2
  • S. Vimala Devi
    • 3
  • T. R. Sharma
    • 1
    • 4
  • Amolkumar U. Solanke
    • 1
  1. 1.ICAR-National Research Centre on Plant BiotechnologyNew DelhiIndia
  2. 2.ICAR-Indian Agricultural Statistics Research InstituteNew DelhiIndia
  3. 3.ICAR-National Bureau of Plant Genetic ResourcesNew DelhiIndia
  4. 4.National Agri-Food Biotechnology InstituteMohaliIndia

Personalised recommendations