The Solanum commersonii genome sequence provides insights into adaptation to stress conditions and genome evolution of wild potato relatives

Plant Cell

Volumn 27, Issue 4, 2015, Pages 954-968

  Aversano, Riccardo ^a   Contaldi, Felice ^a   Ercolano, Maria Raffaella ^a   Grosso, Valentina ^a   Iorizzo, Massimo ^a   Tatino, Filippo ^a   Xumerle, Luciano ^b   Molin, Alessandra Dal ^b   Avanzato, Carla ^b   Ferrarini, Alberto ^b   Delledonne, Massimo ^b   Sanseverino, Walter ^c   Cigliano, Riccardo Aiese ^c   Capella Gutierrez, Salvador ^d,e   Gabaldón, Toni ^d,e,f   Frusciante, Luigi ^a   Bradeen, James M ^g   Carputo, Domenico ^a  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b UNIVERSITY OF VERONA   (Italy)

^c Building M Campus UAB Bellaterra (Cerdanyola del Valles) Department of Biochemistry and Molecular Biology   (Spain)

^d CENTRE FOR GENOMIC REGULATION CRG   (Spain)

^e UNIVERSITAT POMPEU FABRA   (Spain)

^f INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

^g UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SOLANUM COMMERSONII; SOLANUM JAMESII; SOLANUM TUBEROSUM;

ACCLIMATIZATION; CLASSIFICATION; EVOLUTION; GENETICS; PHYLOGENY; PLANT GENOME; POTATO; SOLANUM;

ACCLIMATIZATION; BIOLOGICAL EVOLUTION; GENOME, PLANT; PHYLOGENY; SOLANUM; SOLANUM TUBEROSUM;

EID: 84928947664     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.114.135954     Document Type: Article

References (68)

1. Andolfo, G., Sanseverino, W., Aversano, R., Frusciante, L., and Ercolano, M.R. (2014a). Genome-wide identification and analysis of candidate genes for disease resistance in tomato. Mol. Breed. 33: 227–233.
2. Andolfo, G., Jupe, F., Witek, K., Etherington, G.J., Ercolano, M.R., and Jones, J.D.G. (2014b). Defining the full tomato NB-LRR resistance gene repertoire using genomic and cDNA RenSeq. BMC Plant Biol. 14: 120.
3. Ballvora, A., Ercolano, M.R., Weiss, J., Meksem, K., Bormann, C.A., Oberhagemann, P., Salamini, F., and Gebhardt, C. (2002). The R1 gene for potato resistance to late blight (Phytophthora in-festans) belongs to the leucine zipper/NBS/LRR class of plant resistance genes. Plant J. 30: 361–371.
4. Ballvora, A., Jöcker, A., Viehöver, P., Ishihara, H., Paal, J., Meksem, K., Bruggmann, R., Schoof, H., Weisshaar, B., and Gebhardt, C. (2007). Comparative sequence analysis of Solanum and Arabidopsis in a hot spot for pathogen resistance on potato chromosome V reveals a patchwork of conserved and rapidly evolving genome segments. BMC Genomics 8: 112.
5. Bamberg, J.B., Martin, M.W., and Schartner, J.J. (1994). Elite Selections of Tuber-Bearing Solanum Species Germplasm: Inter-Regional Potato Introduction Station, NRSP-6. (Madison, WI: University of Wisconsin Press).
6. Bennetzen, J.L. (2007). Patterns in grass genome evolution. Curr. Opin. Plant Biol. 10: 176–181.
7. Boerner, S., and McGinnis, K.M. (2012). Computational identification and functional predictions of long noncoding RNA in Zea mays. PLoS ONE 7: e43047.
8. Bradeen, J.M., and Haynes, K.G. (2011). Introduction to potato. In Genetics, Genomics and Breeding of Potato, J.M. Bradeen and C. Kole, eds (Enfield, NH: CRC Press/Science Publishers), pp. 1–19.
9. Bradshaw, J.E., and Ramsay, G. (2005). Utilisation of the commonwealth potato collection in potato breeding. Euphytica 146: 9–19.
10. Camadro, E.L., Erazzú, L.E., Maune, J.F., and Bedogni, M.C. (2012). A genetic approach to the species problem in wild potato. Plant Biol. (Stuttg.) 14: 543–554.
11. Cantarel, B.L., Korf, I., Robb, S.M.C., Parra, G., Ross, E., Moore, B., Holt, C., Sánchez Alvarado, A., and Yandell, M. (2008). MAKER: an easy-to-use annotation pipeline designed for emerging model organism genomes. Genome Res. 18: 188–196.
12. Cardi, T., D’Ambrosio, E., Consoli, D., Puite, K.J., and Ramulu, K.S. (1993). Production of somatic hybrids between frost-tolerant Sola-num commersonii and S. tuberosum: characterization of hybrid plants. Theor. Appl. Genet. 87: 193–200.
13. Carputo, D., Alioto, D., Aversano, R., Garramone, R., Miraglia, V., Villano, C., and Frusciante, L. (2013). Genetic diversity among potato species as revealed by phenotypic resistances and SSR markers. Plant Genet. Resour. C. 11: 131–139.
14. Carputo, D., Aversano, R., Barone, A., Di Matteo, A., Iorizzo, M., Sigillo, L., Zoina, A., and Frusciante, L. (2009). Resistance to Ralstonia solanacearum of sexual hybrids between Solanum com-mersonii and S. tuberosum. Am. J. Potato Res. 86: 196–202.
15. Carputo, D., Barone, A., Cardi, T., Sebastiano, A., Frusciante, L., and Peloquin, S.J. (1997). Endosperm balance number manipulation for direct in vivo germplasm introgression to potato from a sexually isolated relative (Solanum commersonii Dun.). Proc. Natl. Acad. Sci. USA 94: 12013–12017.
16. Carputo, D., Castaldi, L., Caruso, I., Aversano, R., Monti, L., and Frusciante, L. (2007). Resistance to frost and tuber soft rot in near-pentaploid Solanum tuberosum-S.commersonii hybrids. Breed. Sci. 57: 145–151.
17. Carvallo, M.A., Pino, M.-T., Jeknic, Z., Zou, C., Doherty, C.J., Shiu, S.-H., Chen, T.H.H., and Thomashow, M.F. (2011). A comparison of the low temperature transcriptomes and CBF regulons of three plant species that differ in freezing tolerance: Solanum commer-sonii, Solanum tuberosum, and Arabidopsis thaliana. J. Exp. Bot. 62: 3807–3819.
18. Chipman, A.D., et al. (2014). The first myriapod genome sequence reveals conservative arthropod gene content and genome organisation in the centipede Strigamia maritima. PLoS Biol. 12: e1002005.
19. Dohm, J.C., et al. (2014). The genome of the recently domesticated crop plant sugar beet (Beta vulgaris). Nature 505: 546–549.
20. Edgar, R.C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32: 1792–1797.
21. Gabaldón, T. (2008). Large-scale assignment of orthology: back to phylogenetics? Genome Biol. 9: 235.
22. Garcia-Mas, J., et al. (2012). The genome of melon (Cucumis melo L.). Proc. Natl. Acad. Sci. USA 109: 11872–11877.
23. Hanneman, R.E., and Bamberg, J.B. (1986). Inventory of Tuber-Bearing Solanum Species. (Sturgeon Bay, WI: Potato Introduction Station).
24. Hawkes, J.G. (1990). The Potato: Evolution, Biodiversity and Genetic Resources. (Washington, D.C.: John Wiley & Sons).
25. Hirsch, C.N., Hirsch, C.D., Felcher, K., Coombs, J., Zarka, D., Van Deynze, A., De Jong, W., Veilleux, R.E., Jansky, S.H., Bethke, P., Douches, D.S., and Buell, C.R. (2013). Retrospective view of North American potato (Solanum tuberosum L.) breeding in the 20th and 21st centuries. G3 (Bethesda) 3: 1003–1013.
26. Huamán, Z., Hoekstra, R., and Bamberg, J.B. (2000). The Inter-genebank potato database and the dimensions of available wild potato germplasm. Am. J. Potato Res. 77: 353–362.
27. Huerta-Cepas, J., Marcet-Houben, M., Pignatelli, M., Moya, A., and Gabaldón, T. (2010). The pea aphid phylome: a complete catalogue of evolutionary histories and arthropod orthology and paralogy relationships for Acyrthosiphon pisum genes. Insect Mol. Biol. 19 (suppl. 2): 13–21.
28. Huerta-Cepas, J., and Gabaldón, T. (2011). Assigning duplication events to relative temporal scales in genome-wide studies. Bio-informatics 27: 38–45.
29. Huerta-Cepas, J., Capella-Gutiérrez, S., Pryszcz, L.P., Marcet-Houben, M., and Gabaldón, T. (2014). PhylomeDB v4: zooming into the plurality of evolutionary histories of a genome. Nucleic Acids Res. 42: D897–D902.
30. Jaglo, K.R., Kleff, S., Amundsen, K.L., Zhang, X., Haake, V., Zhang, J.Z., Deits, T., and Thomashow, M.F. (2001). Components of the Arabidopsis C-repeat/dehydration-responsive element binding factor cold-response pathway are conserved in Brassica napus and other plant species. Plant Physiol. 127: 910–917.
31. Johnston, S.A., den Nijs, T.P., Peloquin, S.J., and Hanneman, R.E.,. (1980). The significance of genic balance to endosperm development in interspecific crosses. Theor. Appl. Genet. 57: 5–9.
32. Lanfermeijer, F.C., Dijkhuis, J., Sturre, M.J.G., de Haan, P., and Hille, J. (2003). Cloning and characterization of the durable tomato mosaic virus resistance gene Tm-2(2) from Lycopersicon escu-lentum. Plant Mol. Biol. 52: 1037–1049.
33. Lee, B.-H., Henderson, D.A., and Zhu, J.-K. (2005). The Arabidopsis cold-responsive transcriptome and its regulation by ICE1. Plant Cell 17: 3155–3175.
34. Li, L., Stoeckert, C.J., and Roos, D.S. (2003). OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 13: 2178–2189.
35. Liu, B., Shi, Y., Yuan, Y., Hu, X., Zhang, H., Li, N., Li, Z., Chen, Y., Mu, D., and Fan, W. (2012). Estimation of genomic characteristics by analyzing k-mer frequency in de novo genome projects, http://arxiv.org/abs/1308.2012.
36. Lukashin, A.V., and Borodovsky, M. (1998). GeneMark.hmm: new solutions for gene finding. Nucleic Acids Res. 26: 1107–1115.
37. Luo, R., et al. (2012). SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. Gigascience 1: 18.
38. Lynch, M., and Force, A. (2000). The probability of duplicate gene preservation by subfunctionalization. Genetics 154: 459–473.
39. Matsui, A., Nguyen, A.H., Nakaminami, K., and Seki, M. (2013). Arabidopsis non-coding RNA regulation in abiotic stress responses. Int. J. Mol. Sci. 14: 22642–22654.
40. Mboup, M., Fischer, I., Lainer, H., and Stephan, W. (2012). Trans-species polymorphism and allele-specific expression in the CBF gene family of wild tomatoes. Mol. Biol. Evol. 29: 3641–3652.
41. Michael, T.P., and Jackson, S. (2013). The first 50 plant genomes. The Plant Genome 6: 1–7.
42. Micheletto, S., Boland, R., and Huarte, M. (2000). Argentinian wild diploid Solanum species as sources of quantitative late blight resistance. Theor. Appl. Genet. 101: 902–906.
43. Novák, P., Neumann, P., Pech, J., Steinhaisl, J., and Macas, J. (2013). RepeatExplorer: a Galaxy-based web server for genome-wide characterization of eukaryotic repetitive elements from next-generation sequence reads. Bioinformatics 29: 792–793.
44. Palta, J.P., and Simon, G. (1993). Breeding potential for improvement of freezing stress resistance: genetic separation of freezing tolerance, freezing avoidance, and capacity to cold acclimate. In Advances in Plant Cold Hardiness, P.H. Li, ed (Boca Raton, FL: CRC Press), pp. 299–310.
45. Peele, H.M., Guan, N., Fogelqvist, J., and Dixelius, C. (2014). Loss and retention of resistance genes in five species of the Brassicaceae family. BMC Plant Biol. 14: 298.
46. Pennycooke, J.C., Cheng, H., Roberts, S.M., Yang, Q., Rhee, S.Y., and Stockinger, E.J. (2008). The low temperature-responsive, Solanum CBF1 genes maintain high identity in their upstream regions in a genomic environment undergoing gene duplications, deletions, and rearrangements. Plant Mol. Biol. 67: 483–497.
47. Potato Genome Sequencing Consortium; Xu, X., et al. (2011). Genome sequence and analysis of the tuber crop potato. Nature 475: 189–195.
48. Ramsay, N.A., and Glover, B.J. (2005). MYB-bHLH-WD40 protein complex and the evolution of cellular diversity. Trends Plant Sci. 10: 63–70.
49. Rhoades, M.W., Reinhart, B.J., Lim, L.P., Burge, C.B., Bartel, B., and Bartel, D.P. (2002). Prediction of plant microRNA targets. Cell 110: 513–520.
50. Rodríguez, F., and Spooner, D.M. (2009). Nitrate reductase phylog-eny of potato (Solanum sect. Petota) genomes with emphasis on the origins of the polyploid species. Syst. Bot. 34: 207–219.
51. Rymarquis, L.A., Kastenmayer, J.P., Hüttenhofer, A.G., and Green, P.J. (2008). Diamonds in the rough: mRNA-like non-coding RNAs. Trends Plant Sci. 13: 329–334.
52. Sakamoto, H., Maruyama, K., Sakuma, Y., Meshi, T., Iwabuchi, M., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2004). Arabidopsis Cys2/His2-type zinc-finger proteins function as transcription re-pressors under drought, cold, and high-salinity stress conditions. Plant Physiol. 136: 2734–2746.
53. Seibt, K.M., Wenke, T., Wollrab, C., Junghans, H., Muders, K., Dehmer, K.J., Diekmann, K., and Schmidt, T. (2012). Development and application of SINE-based markers for genotyping of potato varieties. Theor. Appl. Genet. 125: 185–196.
54. Stanke, M., and Waack, S. (2003). Gene prediction with a hidden Markov model and a new intron submodel. Bioinformatics 19 (suppl. 2): 2215–2225.
55. Stevenson, W.R., Loria, R., Franc, G.D., and Weingartner, D.P. (2001). Compendium of Potato Diseases, 2nd ed. (St. Paul, MN: American Phytopathological Society Press).
56. Stockinger, E.J., Mao, Y., Regier, M.K., Triezenberg, S.J., and Thomashow, M.F. (2001). Transcriptional adaptor and histone acetyltransferase proteins in Arabidopsis and their interactions with CBF1, a transcriptional activator involved in cold-regulated gene expression. Nucleic Acids Res. 29: 1524–1533.
57. Stone, J.M., Palta, J.P., Bamberg, J.B., Weiss, L.S., and Harbage, J.F. (1993). Inheritance of freezing resistance in tuber-bearing So-lanum species: evidence for independent genetic control of non-acclimated freezing tolerance and cold acclimation capacity. Proc. Natl. Acad. Sci. USA 90: 7869–7873.
58. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28: 2731–2739.
59. Tomato Genome Consortium (2012). The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485: 635–641.
60. van der Vossen, E.A.G., Gros, J., Sikkema, A., Muskens, M., Wouters, D., Wolters, P., Pereira, A., and Allefs, S. (2005). The Rpi-blb2 gene from Solanum bulbocastanum is an Mi-1 gene ho-molog conferring broad-spectrum late blight resistance in potato. Plant J. 44: 208–222.
61. Varshney, R.K., et al. (2012). Draft genome sequence of pigeonpea (Cajanus cajan), an orphan legume crop of resource-poor farmers. Nat. Biotechnol. 30: 83–89.
62. Vitte, C., and Bennetzen, J.L. (2006). Analysis of retrotransposon structural diversity uncovers properties and propensities in angio-sperm genome evolution. Proc. Natl. Acad. Sci. USA 103: 17638–17643.
63. Wang, Z., Zhu, Y., Wang, L., Liu, X., Liu, Y., Phillips, J., and Deng, X. (2009). A WRKY transcription factor participates in dehydration tolerance in Boea hygrometrica by binding to the W-box elements of the galactinol synthase (BhGolS1) promoter. Planta 230: 1155–1166.
64. Wang-Pruski, G., and Schofield, A. (2012). Potato: improving crop productivity and abiotic stress tolerance. In Improving Crop Resistance to Abiotic Stress, N. Tuteja, S.S. Gill, F.A. Tiburcio, and R. Tuteja, eds (Weinheim, Germany: Wiley-VCH Verlag), pp. 1121–1153.
65. Wenke, T., Döbel, T., Sörensen, T.R., Junghans, H., Weisshaar, B., and Schmidt, T. (2011). Targeted identification of short interspersed nuclear element families shows their widespread existence and extreme heterogeneity in plant genomes. Plant Cell 23: 3117–3128.
66. Zhang, R., Murat, F., Pont, C., Langin, T., and Salse, J. (2014). Paleo-evolutionary plasticity of plant disease resistance genes. BMC Genomics 15: 187.
67. Zheng, L.-Y., Guo, X.-S., He, B., Sun, L.-J., Peng, Y., Dong, S.-S., Liu, T.-F., Jiang, S., Ramachandran, S., Liu, C.-M., and Jing, H.-C. (2011). Genome-wide patterns of genetic variation in sweet and grain sorghum (Sorghum bicolor). Genome Biol. 12: R114.
68. Zhuo, C., Wang, T., Lu, S., Zhao, Y., Li, X., and Guo, Z. (2013). A cold responsive galactinol synthase gene from Medicago falcata (MfGolS1) is induced by myo-inositol and confers multiple tolerances to abiotic stresses. Physiol. Plant. 149: 67–78.