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

Volumn 15, Issue 1, 2015, Pages

  Tan, Feng Quan ^a   Tu, Hong ^a   Liang, Wu Jun ^a   Long, Jian Mei ^a   Wu, Xiao Meng ^a   Zhang, Hong Yan ^a   Guo, Wen Wu ^a  

^a HUAZHONG AGRICULTURAL UNIVERSITY   (China)

Author keywords

Citrus; Doubled diploid; Primary and secondary metabolism; Stress tolerance; Transcriptome

Indexed keywords

CITRUS; CITRUS JUNOS;

TRANSCRIPTOME;

CITRUS; COMPARATIVE STUDY; CROSS BREEDING; DIPLOIDY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE ONTOLOGY; GENETIC TRANSCRIPTION; GENETICS; LIQUID CHROMATOGRAPHY; MASS FRAGMENTOGRAPHY; METABOLISM; METABOLOME; METABOLOMICS; PHYSIOLOGICAL STRESS; PLANT LEAF; PRINCIPAL COMPONENT ANALYSIS; SECONDARY METABOLISM; TETRAPLOIDY; UPREGULATION;

CHROMATOGRAPHY, LIQUID; CITRUS; CROSSES, GENETIC; DIPLOIDY; GAS CHROMATOGRAPHY-MASS SPECTROMETRY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENE ONTOLOGY; METABOLOME; METABOLOMICS; PLANT LEAVES; PRINCIPAL COMPONENT ANALYSIS; SECONDARY METABOLISM; STRESS, PHYSIOLOGICAL; TETRAPLOIDY; TRANSCRIPTION, GENETIC; TRANSCRIPTOME; UP-REGULATION;

EID: 84925456130     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/s12870-015-0450-4     Document Type: Article

References (84)

1. Otto SP, Whitton J. Polyploid incidence and evolution. Annu Rev Genet. 2000;34:401-37.
2. Comai L. The advantages and disadvantages of being polyploid. Nat Rev Genet. 2005;6:836-46.
3. Doyle JJ, Flagel LE, Paterson AH, Rapp RA, Soltis DE, Soltis PS, et al. Evolutionary genetics of genome merger and doubling in plants. Annu Rev Genet. 2008;42:443-61.
4. Wendel JF. Genome evolution in polyploids. Plant Molecular Evolution. 2000;42:225-49.
5. Adams KL, Wendel JF. Polyploidy and genome evolution in plants. Curr Opin Plant Biol. 2005;8:135-41.
6. Chen ZJ. Genetic and epigenetic mechanisms for gene expression and phenotypic variation in plant polyploids. Annu Rev Plant Biol. 2007;58:377.
7. Doyle JJ, Egan AN. Dating the origins of polyploidy events. New Phytol. 2010;186:73-85.
8. Abel S, Becker H. The effect of autopolyploidy on biomass production in homozygous lines of Brassica rapa and Brassica oleracea. Plant Breed. 2007;126:642-3.
9. Li X, Yu E, Fan C, Zhang C, Fu T, Zhou Y. Developmental, cytological and transcriptional analysis of autotetraploid Arabidopsis. Planta. 2012;236:579-96.
10. Yao H, Kato A, Mooney B, Birchler JA. Phenotypic and gene expression analyses of a ploidy series of maize inbred Oh43. Plant Mol Biol. 2011;75:237-51.
11. Martin SL, Husband BC. Whole genome duplication affects evolvability of flowering time in an autotetraploid plant. PLoS One. 2012;7:e44784.
12. Cohen H, Tel-Zur N. Morphological changes and self-incompatibility breakdown associated with autopolyploidization in Hylocereus species (Cactaceae). Euphytica. 2012;184:345-54.
13. Chao DY, Dilkes B, Luo H, Douglas A, Yakubova E, Lahner B, et al. Polyploids exhibit higher potassium uptake and salinity tolerance in Arabidopsis. Science. 2013;341:658-9.
14. del Pozo JC, Ramirez-Parra E. Deciphering the molecular bases for drought tolerance in Arabidopsis autotetraploids. Plant Cell Environ. 2014. doi:10.1111/pce.12344.
15. Lavania U, Srivastava S. Enhanced productivity of tropane alkaloids and fertility in artificial autotetraploids of Hyoscyamus niger L. Euphytica. 1991;52:73-7.
16. De Jesus-Gonzalez L, Weathers P. Tetraploid Artemisia annua hairy roots produce more artemisinin than diploids. Plant Cell Rep. 2003;21:809-13.
17. Lavania UC, Srivastava S, Lavania S, Basu S, Misra NK, Mukai Y. Autopolyploidy differentially influences body size in plants, but facilitates enhanced accumulation of secondary metabolites, causing increased cytosine methylation. Plant J. 2012;71:539-49.
18. Caruso I, Lepore L, De Tommasi N, Dal Piaz F, Frusciante L, Aversano R, et al. Secondary metabolite profile in induced tetraploids of wild Solanum commersonii Dun. Chem Biodivers. 2011;8:2226-37.
19. Wang J, Tian L, Lee HS, Wei NE, Jiang H, Watson B, et al. Genomewide nonadditive gene regulation in Arabidopsis allotetraploids. Genetics. 2006;172:507-17.
20. Ni Z, Kim ED, Ha M, Lackey E, Liu J, Zhang Y, et al. Altered circadian rhythms regulate growth vigour in hybrids and allopolyploids. Nature. 2008;457:327-31.
21. Bassene J, Froelicher Y, Dubois C, Ferrer R, Navarro L, Ollitrault P, et al. Non-additive gene regulation in a citrus allotetraploid somatic hybrid between C. reticulata Blanco and C. limon (L.) Burm. Heredity. 2009;105:299-308.
22. Riddle NC, Jiang H, An L, Doerge R, Birchler JA. Gene expression analysis at the intersection of ploidy and hybridity in maize. Theor Appl Genet. 2010;120:341-53.
23. Bombarely A, Edwards KD, Sanchez-Tamburrino J, Mueller LA. Deciphering the complex leaf transcriptome of the allotetraploid species Nicotiana tabacum: a phylogenomic perspective. BMC Genomics. 2012;13:406.
24. Stupar RM, Bhaskar PB, Yandell BS, Rensink WA, Hart AL, Ouyang S, et al. Phenotypic and transcriptomic changes associated with potato autopolyploidization. Genetics. 2007;176:2055-67.
25. Yu Z, Haberer G, Matthes M, Rattei T, Mayer KF, Gierl A, et al. Impact of natural genetic variation on the transcriptome of autotetraploid Arabidopsis thaliana. Proc Natl Acad Sci U S A. 2010;107:17809-14.
26. Allario T, Brumos J, Colmenero-Flores JM, Tadeo F, Froelicher Y, Talon M, et al. 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. J Exp Bot. 2011;62:2507-19.
27. Gong XQ, Liu JH. Genetic transformation and genes for resistance to abiotic and biotic stresses in Citrus and its related genera. Plant Cell Tissue Organ Cult. 2013;113:137-47.
28. Liu JJ, Chen KL, Hu Q, Yang M, Zhou QM, Li HW, et al. Preliminary study on Ziyang xiangcheng (Citrus junos Sieb ex Tanaka), a special local citrus germplasm. Southwest China J Agric Sci. 2008;21:1658-60 (in Chinese with English abstract).
29. Zhou GF, Peng SA, Liu YZ, Wei QJ, Han J, Islam MZ. The physiological and nutritional responses of seven different citrus rootstock seedlings to boron deficiency. Trees. 2014;28:295-307.
30. Aleza P, Froelicher Y, Schwarz S, Agustí M, Hernández M, Juárez J, et al. Tetraploidization events by chromosome doubling of nucellar cells are frequent in apomictic citrus and are dependent on genotype and environment. Ann Bot. 2011;108:37-50.
31. Rao MN, Soneji JR, Chen C, Huang S, Gmitter Jr FG. Characterization of zygotic and nucellar seedlings from sour orange-like citrus rootstock candidates using RAPD and EST-SSR markers. Tree Genet Genom. 2008;4:113-24.
32. Ruiz C, Breto MP, Asins M. A quick methodology to identify sexual seedlings in citrus breeding programs using SSR markers. Euphytica. 2000;112:89-94.
33. Saleh B, Allario T, Dambier D, Ollitrault P, Morillon R. Tetraploid citrus rootstocks are more tolerant to salt stress than diploid. C R Biol. 2008;331:703-10.
34. Mouhaya W, Allario T, Brumos J, Andrés F, Froelicher Y, Luro F, et al. Sensitivity to high salinity in tetraploid citrus seedlings increases with water availability and correlates with expression of candidate genes. Funct Plant Biol. 2010;37:674-85.
35. Liang WJ, Xie KD, Guo DY, Xie ZZ, Yi HL, Guo WW. Spontaneous generation and SSR molecular characterization of autotetraploids in ten citrus rootstocks. J Fruit Sci. 2014;31:1-6 (in Chinese with English abstract).
36. Liang WJ, Xie KD, Guo DY, Xie ZZ, Xu Q, Yi HL, et al. Spontaneous generation and SSR characterization of polyploids from ten citrus cultivars. Acta Hort Sin. 2014;41:409-16 (in Chinese with English abstract).
37. Yun Z, Gao H, Liu P, Liu S, Luo T, Jin S, et al. Comparative proteomic and metabolomic profiling of citrus fruit with enhancement of disease resistance by postharvest heat treatment. BMC Plant Biol. 2013;13:44.
38. Maere S, Heymans K, Kuiper M. BiNGO: a Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics. 2005;21:3448-9.
39. Zhang X, Ju HW, Chung MS, Huang P, Ahn SJ, Kim CS. The RR-type MYB-like transcription factor, AtMYBL, is involved in promoting leaf senescence and modulates an abiotic stress response in Arabidopsis. Plant Cell Physiol. 2011;52:138-48.
40. Vincent D, Lapierre C, Pollet B, Cornic G, Negroni L, Zivy M. Water deficits affect caffeate O-methyltransferase, lignification, and related enzymes in maize leaves. A proteomic investigation. Plant Physiol. 2005;137:949-60.
41. 2A-adrenoreceptor agonists differentially alter citrus leaf and fruit abscission by affecting expression of ACC synthase and ACC oxidase. J Exp Bot. 2005;56:1867-75.
42. Liu YC, Wu YR, Huang XH, Sun J, Xie Q. AtPUB19, a U-box E3 ubiquitin ligase, negatively regulates abscisic acid and drought responses in Arabidopsis thaliana. Mol Plant. 2011;4:938-46.
43. Ding Y, Liu N, Virlouvet L, Riethoven JJ, Fromm M, Avramova Z. Four distinct types of dehydration stress memory genes in Arabidopsis thaliana. BMC Plant Biol. 2013;13:229.
44. Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K. AP2/ERF family transcription factors in plant abiotic stress responses. Biochim Biophys Acta. 1819;2012:86-96.
45. Neilson EH, Goodger JQ, Woodrow IE, Moller BL. Plant chemical defense: at what cost? Trends Plant Sci. 2013;18:250-8.
46. Couee I, Sulmon C, Gouesbet G, El Amrani A. Involvement of soluble sugars in reactive oxygen species balance and responses to oxidative stress in plants. J Exp Bot. 2006;57:449-59.
47. Patterson JH, Newbigin E, Tester M, Bacic A, Roessner U. Metabolic responses to salt stress of barley (Hordeum vulgare L.) cultivars, Sahara and Clipper, which differ in salinity tolerance. J Exp Bot. 2009;60:4089-103.
48. Vinocur B, Altman A. Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Curr Opin Biotechnol. 2005;16:123-32.
49. Seki M, Umezawa T, Urano K, Shinozaki K. Regulatory metabolic networks in drought stress responses. Curr Opin Plant Biol. 2007;10:296-302.
50. Ghasempour H, Gaff D, Williams R, Gianello R. Contents of sugars in leaves of drying desiccation tolerant flowering plants, particularly grasses. Plant Growth Regul. 1998;24:185-91.
51. Farrant JM, Lehner A, Cooper K, Wiswedel S. Desiccation tolerance in the vegetative tissues of the fern Mohria caffrorum is seasonally regulated. Plant J. 2009;57:65-79.
52. Krasensky J, Jonak C. Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. J Exp Bot. 2012;63:1593-608.
53. Vendruscolo ECG, Schuster I, Pileggi M, Scapim CA, Molinari HBC, Marur CJ, et al. Stress-induced synthesis of proline confers tolerance to water deficit in transgenic wheat. J Plant Physiol. 2007;164:1367-76.
54. Verbruggen N, Hermans C. Proline accumulation in plants: a review. Amino Acids. 2008;35:753-9.
55. Yobi A, Wone BW, Xu W, Alexander DC, Guo L, Ryals JA, et al. Comparative metabolic profiling between desiccation-sensitive and desiccation-tolerant species of Selaginella reveals insights into the resurrection trait. Plant J. 2012;72:983-99.
56. Grosser JW, Gmitter Jr FG. Protoplast fusion for production of tetraploids and triploids: applications for scion and rootstock breeding in citrus. Plant Cell Tiss Org Cult. 2011;104:343-57.
57. Martelotto LG, Ortiz JPA, Stein J, Espinoza F, Quarin CL, Pessino SC. A comprehensive analysis of gene expression alterations in a newly synthesized Paspalum notatum autotetraploid. Plant Sci. 2005;169:211-20.
58. Lu B, Pan X, Zhang L, Huang B, Sun L, Li B, et al. A genome-wide comparison of genes responsive to autopolyploidy in Isatis indigotica using Arabidopsis thaliana Affymetrix genechips. Plant Mol Biol Rep. 2006;24:197-204.
59. Auger DL, Gray AD, Ream TS, Kato A, Coe EH, Birchler JA. Nonadditive gene expression in diploid and triploid hybrids of maize. Genetics. 2005;169:389-97.
60. Zhu JK. Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol. 2003;6:441-5.
61. Rizhsky L, Liang H, Shuman J, Shulaev V, Davletova S, Mittler R. When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiol. 2004;134:1683-96.
62. Schafleitner R, Gutierrez Rosales RO, Gaudin A, Alvarado Aliaga CA, Martinez GN, Tincopa Marca LR, et al. Capturing candidate drought tolerance traits in two native Andean potato clones by transcription profiling of field grown plants under water stress. Plant Physiol Biochem. 2007;45:673-90.
63. Tu Y, Rochfort S, Liu Z, Ran Y, Griffith M, Badenhorst P, et al. Functional analyses of caffeic acid O-methyltransferase and cinnamoyl-CoA-reductase genes from perennial ryegrass (Lolium perenne). Plant Cell. 2010;22:3357-73.
64. Barry CS, Blume B, Bouzayen M, Cooper W, Hamilton AJ, Grierson D. Differential expression of the 1-aminocyclopropane-1-carboxylate oxidase gene family of tomato. Plant J. 1996;9:525-35.
65. Ouvrard O, Cellier F, Ferrare K, Tousch D, Lamaze T, Dupuis JM, et al. Identification and expression of water stress-and abscisic acid-regulated genes in a drought-tolerant sunflower genotype. Plant Mol Biol. 1996;31:819-29.
66. Seo YJ, Park JB, Cho YJ, Jung C, Seo HS, Park SK, et al. Overexpression of the ethylene-responsive factor gene BrERF4 from Brassica rapa increases tolerance to salt and drought in Arabidopsis plants. Mol Cells. 2010;30:271-7.
67. Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R. Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ. 2010;33:453-67.
68. Ballester A-R, Teresa Lafuente M, González-Candelas L. Citrus phenylpropanoids and defence against pathogens. Part II: Gene expression and metabolite accumulation in the response of fruits to Penicillium digitatum infection. Food Chem. 2013;136:285-91.
69. Fontaine J-X, Tercé-Laforgue T, Armengaud P, Clément G, Renou J-P, Pelletier S, et al. Characterization of a NADH-dependent glutamate dehydrogenase mutant of Arabidopsis demonstrates the key role of this enzyme in root carbon and nitrogen metabolism. Plant Cell. 2012;24:4044-65.
70. Fernie AR, Stitt M. On the discordance of metabolomics with proteomics and transcriptomics: coping with increasing complexity in logic, chemistry, and network interactions scientific correspondence. Plant Physiol. 2012;158:1139-45.
71. Ha M, Lu J, Tian L, Ramachandran V, Kasschau KD, Chapman EJ, et al. Small RNAs serve as a genetic buffer against genomic shock in Arabidopsis interspecific hybrids and allopolyploids. Proc Natl Acad Sci U S A. 2009;106:17835-40.
72. Parisod C, Alix K, Just J, Petit M, Sarilar V, Mhiri C, et al. Impact of transposable elements on the organization and function of allopolyploid genomes. New Phytol. 2010;186:37-45.
73. Ng DW, Zhang C, Miller M, Shen Z, Briggs S, Chen Z. Proteomic divergence in Arabidopsis autopolyploids and allopolyploids and their progenitors. Heredity. 2011;108:419-30.
74. Marmagne A, Brabant P, Thiellement H, Alix K. Analysis of gene expression in resynthesized Brassica napus allotetraploids: transcriptional changes do not explain differential protein regulation. New Phytol. 2010;186:216-27.
75. Froelicher Y, Dambier D, Bassene J, Costantino G, Lotfy S, Didout C, et al. Characterization of microsatellite markers in mandarin orange (Citrus reticulata Blanco). Mol Ecol Resour. 2008;8:119-22.
76. Cristofani-Yaly M, Novelli VM, Bastianel M, Machado MA. Transferability and level of heterozygosity of microsatellite markers in Citrus species. Plant Mol Biol Rep. 2011;29:418-23.
77. Yi B, Zeng F, Lei S, Chen Y, Yao X, Zhu Y, et al. Two duplicate CYP704B1-homologous genes BnMs1 and BnMs2 are required for pollen exine formation and tapetal development in Brassica napus. Plant J. 2010;63:925-38.
78. Hu Z, Zhang M, Wen Q, Wei J, Yi H, Deng X, et al. Abnormal microspore development leads to pollen abortion in a seedless mutant of 'Ougan'mandarin (Citrus suavissima Hort. ex Tanaka). J Am Soc Hortic Sci. 2007;132:777-82.
79. Zheng BB, Wu XM, Ge XX, Deng XX, Grosser JW, Guo WW. Comparative transcript profiling of a male sterile cybrid pummelo and its fertile type revealed altered gene expression related to flower development. PLoS One. 2012;7:e43758.
80. Xu Q, Chen LL, Ruan X, Chen D, Zhu A, Chen C, et al. The draft genome of sweet orange (Citrus sinensis). Nat Genet. 2013;45:59-66.
81. Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 2013;14:R36.
82. Anders S, Huber W. Differential expression analysis for sequence count data. Genome Biol. 2010;11:R106.
83. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Series B Stat Methodol. 1995;57:289-300.
84. Xie C, Mao X, Huang J, Ding Y, Wu J, Dong S, et al. KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases. Nucleic Acids Res. 2011;39 Suppl 2:316-22.