Transcriptome and metabolome of synthetic Solanum autotetraploids reveal key genomic stress events following polyploidization

New Phytologist

Volumn 210, Issue 4, 2016, Pages 1382-1394

  Fasano, Carlo ^a   Diretto, Gianfranco ^b   Aversano, Riccardo ^a   D'Agostino, Nunzio ^c   Di Matteo, Antonio ^a   Frusciante, Luigi ^a   Giuliano, Giovanni ^b   Carputo, Domenico ^a  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b ENEA C R CASACCIA   (Italy)

^c Centro di Ricerca per l'Orticoltura   (Italy)

Author keywords

Autopolyploid; Metabolome; Nucleotide pool imbalance; Potato; Transcriptome; Wild Solanum

Indexed keywords

AMINO ACID; GENE EXPRESSION; GENETIC ANALYSIS; GENOMICS; GENOTYPE; HYBRIDIZATION; METABOLISM; POLYPLOIDY; POTATO; WILD POPULATION;

SOLANUM; SOLANUM BULBOCASTANUM; SOLANUM COMMERSONII; SOLANUM TUBEROSUM;

TRANSCRIPTOME;

BIOLOGICAL MODEL; DIPLOIDY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETICS; GENOTYPE; HYBRIDIZATION; METABOLISM; METABOLOME; METABOLOMICS; PLANT CHROMOSOME; PLANT LEAF; POLYPLOIDY; SOLANUM; SPECIES DIFFERENCE;

CHROMOSOMES, PLANT; DIPLOIDY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENE REGULATORY NETWORKS; GENOTYPE; HYBRIDIZATION, GENETIC; METABOLOME; METABOLOMICS; MODELS, BIOLOGICAL; PLANT LEAVES; POLYPLOIDY; SOLANUM; SPECIES SPECIFICITY; TRANSCRIPTOME;

EID: 84959386575     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.13878     Document Type: Article

References (94)

1. Ainouche ML, Fortune PM, Salmon A, Parisod C, Grandbastien MA, Fukunaga K, Ricou M, Misset MT. 2009. Hybridization, polyploidy and invasion: lessons from Spartina (poaceae). Biological Invasions 11: 1159-1173.
2. Allario T, Brumos J, Colmenero-Flores JM, Tadeo F, Froelicher Y, Talon M, Navarro L, Ollitrault P, Morillon R. 2011. Large changes in anatomy and physiology between diploid rangpur lime (Citrus limonia) and its autotetraploid are not associated with large changes in leaf gene expression. Journal of Experimental Botany 62: 2507-2519.
3. Anderson JF, Siller E, Barral JM. 2011. The neurodegenerative-disease-related protein sacsin is a molecular chaperone. Journal of Molecular Biology 411: 870-880.
4. Aversano R, Caruso I, Aronne G, De Micco V, Scognamiglio N, Carputo D. 2013. Stochastic changes affect Solanum wild species following autopolyploidization. Journal of Experimental Botany 64: 625-635.
5. Aversano R, Contaldi F, Ercolano MR, Grosso V, Iorizzo M, Tatino F, Xumerle L, Dal Molin A, Avanzato C, Ferrarini A et al. 2015a. The Solanum commersonii genome sequence provides insights into adaptation to stress conditions and genome evolution of wild potato relatives. Plant Cell 27: 954-968.
6. Aversano R, Ercolano MR, Caruso I, Fasano C, Rosellini D, Carputo D. 2012. Molecular tools for exploring polyploid genomes in plants. International Journal of Molecular Sciences 13: 10316-10335.
7. Aversano R, Scarano MT, Aronne G, Caruso I, D'Amelia V, De Micco V, Fasano C, Termolino P, Carputo D. 2015b. Genotype-specific changes associated to early synthesis of autotetraploids in wild potato species. Euphytica 202: 307-316.
8. Banyai W, Sangthong R, Karaket N, Inthima P, Mii M, Supaibulwatana K. 2010. Overproduction of artemisinin in tetraploid Artemisia annua L. Plant Biotechnology 27: 427-433.
9. Banzai T, Hanagata N, Dubinsky Z, Karube I. 2003. Fructose-2, 6-bisphosphate contents were increased in response to salt, water and osmotic stress in leaves of Bruguiera gymnorrhiza by differential changes in the activity of the bifunctional enzyme 6-phosphofructo-2-kinase/fructose-2, 6-bisphosphate 2-phosphatase. Plant Molecular Biology 53: 51-59.
10. Bombarely A, Edwards KD, Sanchez-Tamburrino J, Mueller LA. 2012. Deciphering the complex leaf transcriptome of the allotetraploid species Nicotiana tabacum: a phylogenomic perspective. BMC Genomics 13: 406.
11. Caruso I, Lepore L, De Tommasi N, Dal Piaz F, Frusciante L, Aversano R, Garramone R, Carputo D. 2011. Secondary metabolite profile in induced tetraploids of wild Solanum commersonii dun. Chemistry & Biodiversity 8: 2226-2237.
12. Castillo RO, Spooner DM. 1997. Phylogenetic relationships of wild potatoes, Solanum series Conicibaccata (sect. Petota). Systematic Botany 22: 45-83.
13. Chen ZJ. 2013. Genomic and epigenetic insights into the molecular bases of heterosis. Nature Reviews Genetics 14: 471-482.
14. Cle C, Hill LM, Niggeweg R, Martin CR, Guisez Y, Prinsen E, Jansen MA. 2008. Modulation of chlorogenic acid biosynthesis in Solanum lycopersicum; consequences for phenolic accumulation and UV-tolerance. Phytochemistry 69: 2149-2156.
15. Cohen H, Fait A, Tel-Zur N. 2013. Morphological, cytological and metabolic consequences of autopolyploidization in Hylocereus (Cactaceae) species. BMC Plant Biology 13: 173.
16. Combes MC, Dereeper A, Severac D, Bertrand B, Lashermes P. 2013. Contribution of subgenomes to the transcriptome and their intertwined regulation in the allopolyploid Coffea arabica grown at contrasted temperatures. New Phytologist 200: 251-260.
17. Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M. 2005. Blast2go: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21: 3674-3676.
18. D'Agostino N, Traini A, Frusciante L, Chiusano M. 2009. Solest database: a "one-stop shop" approach to the study of Solanaceae transcriptomes. BMC Plant Biology 9: 142.
19. Dalmay T, Horsefield R, Braunstein TH, Baulcombe DC. 2001. SDE3 encodes an rna helicase required for post-transcriptional gene silencing in Arabidopsis. EMBO Journal 20: 2069-2078.
20. Di Matteo A, Sacco A, Anacleria M, Pezzotti M, Delledonne M, Ferrarini A, Frusciante L, Barone A. 2010. The ascorbic acid content of tomato fruits is associated with the expression of genes involved in pectin degradation. BMC Plant Biology 10: 163.
21. Diretto G, Al-Babili S, Tavazza R, Scossa F, Papacchioli V, Migliore M, Beyer P, Giuliano G. 2010. Transcriptional-metabolic networks in β-carotene-enriched potato tubers: the long and winding road to the golden phenotype. Plant Physiology 154: 899-912.
22. Fawcett JA, Maere S, Van de Peer Y. 2009. Plants with double genomes might have had a better chance to survive the Cretaceous-Tertiary extinction event. Proceedings of the National Academy of Sciences, USA 106: 5737-5742.
23. Ferguson KM, Lemmon MA, Schlessinger J, Sigler PB. 1995. Structure of the high affinity complex of inositol trisphosphate with a phospholipase c pleckstrin homology domain. Cell 83: 1037-1046.
24. Fernie AR, Carrari F, Sweetlove LJ. 2004. Respiratory metabolism: glycolysis, the TCA cycle and mitochondrial electron transport. Current Opinion in Plant Biology 7: 254-261.
25. Flynn RL, Zou L. 2010. Oligonucleotide/oligosaccharide-binding fold proteins: a growing family of genome guardians. Critical Reviews in Biochemistry and Molecular Biology 45: 266-275.
26. Forde BG, Lea PJ. 2007. Glutamate in plants: metabolism, regulation, and signalling. Journal of Experimental Botany 58: 2339-2358.
27. Galitski T, Saldanha AJ, Styles CA, Lander ES, Fink GR. 1999. Ploidy regulation of gene expression. Science 285: 251-254.
28. Gremme G, Brendel V, Sparks ME, Kurtz S. 2005. Engineering a software tool for gene structure prediction in higher organisms. Information and Software Technology 47: 965-978.
29. Guo M, Davis D, Birchler JA. 1996. Dosage effects on gene expression in a maize ploidy series. Genetics 142: 1349-1355.
30. Gust AA, Willmann R, Desaki Y, Grabherr HM, Nurnberger T. 2012. Plant LysM proteins: modules mediating symbiosis and immunity. Trends in Plant Science 17: 495-502.
31. Hammer Ø, Harper DAT, Ryan PD. 2001. PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4: 1-9.
32. Hegarty MJ, Barker GL, Wilson ID, Abbott RJ, Edwards KJ, Hiscock SJ. 2006. Transcriptome shock after interspecific hybridization in Senecio is ameliorated by genome duplication. Current Biology 16: 1652-1659.
33. Higgins J, Magusin A, Trick M, Fraser F, Bancroft I. 2012. Use of mRNA-seq to discriminate contributions to the transcriptome from the constituent genomes of the polyploid crop species Brassica napus. BMC Genomics 13: 247.
34. Jackson S, Chen ZJ. 2010. Genomic and expression plasticity of polyploidy. Current Opinion in Plant Biology 13: 153-159.
35. Jaillon O, Aury JM, Noel B, Policriti A, Clepet C, Casagrande A, Choisne N, Aubourg S, Vitulo N, Jubin C et al. 2007. The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449: 463-467.
36. Jiang J, Wang Y, Zhu B, Fang T, Fang Y, Wang Y. 2015. Digital gene expression analysis of gene expression differences within Brassica diploids and allopolyploids. BMC Plant Biology 15: 22.
37. Jiao Y, Wickett NJ, Ayyampalayam S, Chanderbali AS, Landherr L, Ralph PE, Tomsho LP, Hu Y, Liang H, Soltis PS et al. 2011. Ancestral polyploidy in seed plants and angiosperms. Nature 473: 97-100.
38. Kaeppler SM, Phillips RL, Olhoft P. 1998. Molecular basis of heritable tissue culture-induced variation in plants. In: Jain SM, Brar DS, Ahloowalia BS, eds. Somaclonal variation and induced mutations in crop improvement. Dordrecht, the Netherlands: Kluwer Academic Publishers, 465-484.
39. Kaur H, Heinzel N, Schottner M, Baldwin IT, Galis I. 2010. R2R3-NaMYB8 regulates the accumulation of phenylpropanoid-polyamine conjugates, which are essential for local and systemic defense against insect herbivores in Nicotiana attenuata. Plant Physiology 152: 1731-1747.
40. Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA. 2009. Circos: an information aesthetic for comparative genomics. Genome Research 19: 1639-1645.
41. Lavania U. 2005. Genomic and ploidy manipulation for enhanced production of phyto-pharmaceuticals. Plant Genetic Resources: Characterization and Utilization 3: 170-177.
42. Levy AA, Feldman M. 2004. Genetic and epigenetic reprogramming of the wheat genome upon allopolyploidization. Biological Journal of the Linnean Society 82: 607-613.
43. Liepman AH, Olsen LJ. 2003. Alanine aminotransferase homologs catalyze the glutamate: glyoxylate aminotransferase reaction in peroxisomes of arabidopsis. Plant Physiology 131: 215-227.
44. -ΔΔCt method. Methods 25: 402-408.
45. Lopez-Bucio J, Nieto-Jacobo MF, Ramirez-Rodriguez VV, Herrera-Estrella L. 2000. Organic acid metabolism in plants: from adaptive physiology to transgenic varieties for cultivation in extreme soils. Plant Science 160: 1-13.
46. Lorenc-Kukula K, Jafra S, Oszmianski J, Szopa J. 2005. Ectopic expression of anthocyanin 5-O-glucosyltransferase in potato tuber causes increased resistance to bacteria. Journal of Agriculture and Food Chemistry 53: 272-281.
47. Lou Y, Baldwin IT. 2003. Manduca sexta recognition and resistance among allopolyploid Nicotiana host plants. Proceedings of the National Academy of Sciences, USA 100(Suppl 2): 14581-14586.
48. Lu BB, Pan XZ, Zhang L, Huang BB, Sun L, Bin L, Yi B, Zheng SQ, Yu XJ, Ding RX et al. 2006. A genome-wide comparison of genes responsive to autopolyploidy in Isatis indigotica using Arabidopsis thaliana Affymetrix genechips. Plant Molecular Biology Reporter 24: 197-204.
49. Mathews CK. 2006. DNA precursor metabolism and genomic stability. FASEB Journal 20: 1300-1314.
50. Maury S, Geoffroy P, Legrand M. 1999. Tobacco O-methyltransferases involved in phenylpropanoid metabolism. The different caffeoyl-coenzyme A/5-hydroxyferuloyl-coenzyme a 3/5-O-methyltransferase and caffeic acid/5-hydroxyferulic acid 3/5-O-methyltransferase classes have distinct substrate specificities and expression patterns. Plant Physiology 121: 215-223.
51. Medina-Bolivar F, Flores HE. 1995. Selection for hyoscyamine and cinnamoyl putrescine overproduction in cell and root cultures of Hyoscyamus muticus. Plant Physiology 108: 1553-1560.
52. Mentzen WI, Peng J, Ransom N, Nikolau BJ, Wurtele ES. 2008. Articulation of three core metabolic processes in Arabidopsis: fatty acid biosynthesis, leucine catabolism and starch metabolism. BMC Plant Biology 8: 76.
53. Mishra BK, Pathak S, Sharma A, Trivedi PK, Shukla S. 2010. Modulated gene expression in newly synthesized auto-tetraploid of Papaver somniferum L. South African Journal of Botany 76: 447-452.
54. Murashige T, Skoog F. 1962. A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiologia Plantarum 15: 473-497.
55. Niggeweg R, Michael AJ, Martin C. 2004. Engineering plants with increased levels of the antioxidant chlorogenic acid. Nature Biotechnology 22: 746-754.
56. Parisod C, Holderegger R, Brochmann C. 2010. Evolutionary consequences of autopolyploidy. New Phytologist 186: 5-17.
57. Pearse IS, Krugel T, Baldwin IT. 2006. Innovation in anti-herbivore defense systems during neopolypoloidy - the functional consequences of instantaneous speciation. Plant Journal 47: 196-210.
58. Pignatta D, Dilkes BP, Yoo SY, Henry IM, Madlung A, Doerge RW, Jeffrey Chen Z, Comai L. 2010. Differential sensitivity of the Arabidopsis thaliana transcriptome and enhancers to the effects of genome doubling. New Phytologist 186: 194-206.
59. Poole R, Barker G, Wilson ID, Coghill JA, Edwards KJ. 2007. Measuring global gene expression in polyploidy; a cautionary note from allohexaploid wheat. Functional & Integrative Genomics 7: 207-219.
60. Potato Genome Sequencing Consortium. 2011. Genome sequence and analysis of the tuber crop potato. Nature 475: 189-195.
61. del Pozo JC, Ramirez-Parra E. 2014. Deciphering the molecular bases for drought tolerance in Arabidopsis autotetraploids. Plant, Cell & Environment 37: 2722-2737.
62. Pruzinska A, Tanner G, Anders I, Roca M, Hortensteiner S. 2003. Chlorophyll breakdown: pheophorbide a oxygenase is a rieske-type iron-sulfur protein, encoded by the accelerated cell death 1 gene. Proceedings of the National Academy of Sciences, USA 100: 15259-15264.
63. Quevillon E, Silventoinen V, Pillai S, Harte N, Mulder N, Apweiler R, Lopez R. 2005. InterProScan: protein domains identifier. Nucleic Acids Research 33: W116-W120.
64. Ralevic V, Burnstock G. 1998. Receptors for purines and pyrimidines. Pharmacological Reviews 50: 413-492.
65. Rambani A, Page JT, Udall JA. 2014. Polyploidy and the petal transcriptome of Gossypium. BMC Plant Biology 14: 3.
66. Ramsak Z, Baebler S, Rotter A, Korbar M, Mozetic I, Usadel B, Gruden K. 2014. GoMapMan: integration, consolidation and visualization of plant gene annotations within the MapMan ontology. Nucleic Acids Research 42: D1167-D1175.
67. Ramsey J, Schemske DW. 2002. Neopolyploidy in flowering plants. Annual Review of Ecology and Systematics 33: 589-639.
68. van der Rest B, Danoun S, Boudet AM, Rochange SF. 2006. Down-regulation of cinnamoyl-CoA reductase in tomato (Solanum lycopersicum L.) induces dramatic changes in soluble phenolic pools. Journal of Experimental Botany 57: 1399-1411.
69. Riddle NC, Jiang H, An L, Doerge RW, Birchler JA. 2010. Gene expression analysis at the intersection of ploidy and hybridity in maize. TAG. Theoretical and Applied Genetics. 120: 341-353.
70. Rietz S, Holk A, Scherer GF. 2004. Expression of the patatin-related phospholipase A gene AtPLA IIA in Arabidopsis thaliana is up-regulated by salicylic acid, wounding, ethylene, and iron and phosphate deficiency. Planta 219: 743-753.
71. Rouillard JM, Zuker M, Gulari E. 2003. OligoArray 2.0: design of oligonucleotide probes for DNA microarrays using a thermodynamic approach. Nucleic Acids Research 31: 3057-3062.
72. Saeed AI, Sharov V, White J, Li J, Liang W, Bhagabati N, Braisted J, Klapa M, Currier T, Thiagarajan M et al. 2003. TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34: 374-378.
73. Sang Y, Cui D, Wang X. 2001. Phospholipase D and phosphatidic acid-mediated generation of superoxide in Arabidopsis. Plant Physiology 126: 1449-1458.
74. Seabra AR, Silva LS, Carvalho HG. 2013. Novel aspects of glutamine synthetase (GS) regulation revealed by a detailed expression analysis of the entire GS gene family of Medicago truncatula under different physiological conditions. BMC Plant Biology 13: 137.
75. Sharma SK, Bolser D, de Boer J, Sonderkaer M, Amoros W, Carboni MF, D'Ambrosio JM, de la Cruz G, Di Genova A, Douches DS et al. 2013. Construction of reference chromosome-scale pseudomolecules for potato: integrating the potato genome with genetic and physical maps. G3 (Bethesda, Md.) 3: 2031-2047.
76. Soltis DE, Buggs RJA, Doyle JJ, Soltis PS. 2010. What we still don't know about polyploidy. Taxon 59: 1387-1403.
77. Sondheimer E, Covitz F, Marquisee MJ. 1961. Association of naturally occurring compounds, the chlorogenic acid-caffeine complex. Archives of Biochemistry and Biophysics 93: 63-71.
78. Spooner DM, Ghislain M, Simon R, Jansky SH, Gavrilenko T. 2014. Systematics, diversity, genetics, and evolution of wild and cultivated potatoes. Botanical Review 80: 283-383.
79. Stupar RM, Bhaskar PB, Yandell BS, Rensink WA, Hart AL, Ouyang S, Veilleux RE, Busse JS, Erhardt RJ, Buell CR et al. 2007. Phenotypic and transcriptomic changes associated with potato autopolyploidization. Genetics 176: 2055-2067.
80. Tan FQ, Tu H, Liang WJ, Long JM, Wu XM, Zhang HY, Guo WW. 2015. Comparative metabolic and transcriptional analysis of a doubled diploid and its diploid citrus rootstock (C. junos cv. Ziyang xiangcheng) suggests its potential value for stress resistance improvement. BMC Plant Biology 15: 89.
81. Tayale A, Parisod C. 2013. Natural pathways to polyploidy in plants and consequences for genome reorganization. Cytogenetic and Genome Research 140: 79-96.
82. Thimm O, Blasing O, Gibon Y, Nagel A, Meyer S, Kruger P, Selbig J, Muller LA, Rhee SY, Stitt M. 2004. MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant Journal 37: 914-939.
83. Tomato Genome Sequencing Consortium. 2012. The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485: 635-641.
84. Toujani W, Munoz-Bertomeu J, Flores-Tornero M, Rosa-Tellez S, Anoman AD, Alseekh S, Fernie AR, Ros R. 2013. Functional characterization of the plastidial 3-phosphoglycerate dehydrogenase family in Arabidopsis. Plant Physiology 163: 1164-1178.
85. Traini A, Iorizzo M, Mann H, Bradeen JM, Carputo D, Frusciante L, Chiusano ML. 2013. Genome microscale heterogeneity among wild potatoes revealed by diversity arrays technology marker sequences. International Journal of Genomics 2013: 257218.
86. Traut TW. 1994. Physiological concentrations of purines and pyrimidines. Molecular and Cellular Biochemistry 140: 1-22.
87. Wang J, Tian L, Lee HS, Wei NE, Jiang H, Watson B, Madlung A, Osborn TC, Doerge RW, Comai L et al. 2006. Genomewide nonadditive gene regulation in Arabidopsis allotetraploids. Genetics 172: 507-517.
88. Wood TE, Takebayashi N, Barker MS, Mayrose I, Greenspoon PB, Rieseberg LH. 2009. The frequency of polyploid speciation in vascular plants. Proceedings of the National Academy of Sciences, USA 106: 13875-13879.
89. Xing SH, Guo XB, Wang Q, Pan QF, Tian YS, Liu P, Zhao JY, Wang GF, Sun XF, Tang KX. 2011. Induction and flow cytometry identification of tetraploids from seed-derived explants through colchicine treatments in Catharanthus roseus (L.) G. Don. Journal of Biomedicine & Biotechnology 2011: 793198.
90. Yao H, Kato A, Mooney B, Birchler JA. 2011. Phenotypic and gene expression analyses of a ploidy series of maize inbred Oh43. Plant Molecular Biology 75: 237-251.
91. Yu H, Zhang F, Wang G, Liu Y, Liu D. 2013. Partial deficiency of isoleucine impairs root development and alters transcript levels of the genes involved in branched-chain amino acid and glucosinolate metabolism in Arabidopsis. Journal of Experimental Botany 64: 599-612.
92. Yu Z, Haberer G, Matthes M, Rattei T, Mayer KF, Gierl A, Torres-Ruiz RA. 2010. Impact of natural genetic variation on the transcriptome of autotetraploid Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA 107: 17809-17814.
93. Zhang X, Deng M, Fan G. 2014. Differential transcriptome analysis between Paulownia fortunei and its synthesized autopolyploid. International Journal of Molecular Sciences 15: 5079-5093.
94. Zrenner R, Stitt M, Sonnewald U, Boldt R. 2006. Pyrimidine and purine biosynthesis and degradation in plants. Annual Review of Plant Biology 57: 805-836.