Transcriptome Sequencing and De Novo Analysis of a Cytoplasmic Male Sterile Line and Its Near-Isogenic Restorer Line in Chili Pepper (Capsicum annuum L.)

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Liu, Chen ^a   Ma, Ning ^a   Wang, Ping Yong ^a   Fu, Nan ^a   Shen, Huo Lin ^a  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTOME;

ARTICLE; CAPSICUM ANNUUM; CELL INTERACTION; CELL NUCLEUS; CYTOPLASMIC MALE STERILITY; GENE EXPRESSION; GENETIC ANALYSIS; HYBRID SEED PRODUCTION; MITOCHONDRION; NEAR ISOGENIC LINE; NONHUMAN; NUCLEOTIDE SEQUENCE; PLANT GENE; POLLEN; PROTEIN DATABASE; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY;

CAPSICUM; CYTOPLASM; FLOWERS; GENE EXPRESSION PROFILING; GENE ONTOLOGY; GENOMICS; HYBRIDIZATION, GENETIC; MOLECULAR SEQUENCE ANNOTATION; PLANT INFERTILITY; SEQUENCE ANALYSIS, RNA;

CAPSICUM ANNUUM; CAPSICUM FRUTESCENS;

EID: 84878639748     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0065209     Document Type: Article

References (92)

1. Bosland PW, (1992) Chiles: a diverse crop. HortTechnology 2: 6-10.
2. Bosland PW, Votava EJ (2012) Peppers: vegetable and spice capsicums, 2nd Edition
3. De AK (2003) Capsicum: the genus Capsicum.
4. Hong S-T, Chung J-E, An G, Kim S-R, (1998) Analysis of 176 expressed sequence tags generated from cDNA clones of hot pepper by single-pass sequencing. Journal of Plant Biology 41: 116-124.
5. Chen CM, Hao XF, Chen GJ, Cao BH, Chen QH, et al. (2011) Characterization of a new male sterility-related gene Camf1 in Capsicum annum L. Molecular Biology Reports. 39: 737-744.
6. Zhang BX, Huang SW, Yang GM, Guo JZ, (2000) Two RAPD markers linked to a major fertility restorer gene in pepper. Euphytica 113: 155-161.
7. Guo JZ, Guan JX, Ma JH, (1981) A preliminary studyon the genetic performance of main agronomic traits in F1 of pepper (Capsicum annuum L.). China Vegetables 1: 9-12.
8. Guo JZ, Ma JH, (1984) Determination of the combining ability of several quantitative traits constituting yield. China Vegetables 3: 1-4.
9. Zheng BB, Wu XM, Ge XX, Deng XX, Grosser JW, et al. (2012) Comparative Transcript Profiling of a Male Sterile Cybrid Pummelo and Its Fertile Type Revealed Altered Gene Expression Related to Flower Development. PLoS ONE 7: e43758.
10. Chase CD, (2007) Cytoplasmic male sterility: a window to the world of plant mitochondrial-nuclear interactions. Trends in Genetics 23: 81-90.
11. Linke B, Borner T, (2005) Mitochondrial effects on flower and pollen development. Mitochondrion 5: 389-402.
12. Bentolila S, Stefanov S, (2012) A reevaluation of rice mitochondrial evolution based on the complete sequence of male-fertile and male-sterile mitochondrialgenomes. Plant Physiology 158: 996-1017.
13. Peterson PA, (1958) Cytoplasmically inherited male sterility in Capsicum. American Naturalist 92: 111-119.
14. Kim DH, Kim BD, (2006) The organization of mitochondrial atp6 gene region in male fertile and CMS lines of pepper (Capsicum annuum L.). Current Genetics 49: 59-67.
15. Kim DH, Kang JG, Kim B-D, (2007) Isolation and characterization of the cytoplasmic male sterility-associated orf456 gene of chili pepper (Capsicum annuum L.). Plant Molecular Biology 63: 519-532.
16. Kim DH, Kim BD, (2005) Development of SCAR markets for early identification of cytoplasmic male sterility genotype in chili pepper (Capsicum annuum L.). Molecules and Cells 20: 416-422.
17. Wang S-B, Liu J-B, Pan B-G, (2007) Inheritance and distribution of fertility restoring gene of cytoplasmic male sterile pepper. Acta Agriculturae Boreali-Sinica 22: 86-89.
18. Wang LH, Zhang BX, Lefebvre V, Huang SW, Daubeze AM, et al. (2004) QTL analysis of fertility restoration in cytoplasmic male sterile pepper. Theoretical and Applied Genetics 109: 1058-1063.
19. Kim DS, Kim DH, Yoo JH, Kim BD, (2006) Cleaved amplified polymorphic sequence and amplified fragment length polymorphism markers linked to the fertility restorer gene in chili pepper (Capsicum annuum L.). Molecules and Cells 21: 135-140.
20. Lee J, Yoon JB, Park HG, (2008) Linkage analysis between the partial restoration (pr) and the restorer-of-fertility (Rf) loci in pepper cytoplasmic male sterility. Theoretical and Applied Genetics 117: 383-389.
21. Jo YD, Kim YM, Park MN, Yoo JH, Park M, et al. (2010) Development and evaluation of broadly applicable markers for Restorer-of-fertility in pepper. Molecular Breeding 25: 187-201.
22. Gulyas G, Pakozdi K, Lee JS, Hirata Y, (2006) Analysis of fertility restoration by using cytoplasmic male-sterile red pepper (Capsicum annuum L.) lines. Breeding Science 56: 331-334.
23. Min WK, Lim H, Lee YP, Sung SK, Kim BD, et al. (2008) Identification of a third haplotype of the sequence linked to the Restorer-of-fertility (Rf) gene and its implications for male-sterility phenotypes in peppers (Capsicum annuum L.). Molecules and Cells 25: 20-29.
24. Lee J, Yoon JB, Park HG, (2008) A CAPS marker associated with the partial restoration of cytoplasmic male sterility in chili pepper (Capsicum annuum L.). Molecular Breeding 21: 95-104.
25. Young ND, Zamir D, Ganal MW, Tanksley SD, (1988) Use of isogenic lines and simultaneous probing to identify dna markers tightly linked to the Tm-2-Alpha gene in tomato. Genetics 120: 579-585.
26. Muehlbauer GJ, Specht JE, Thomascompton MA, Staswick PE, Bernard RL, (1988) NEar-isogenic lines- a potential resource in the integration of conventional and molecular marker linkage maps. Crop Science 28: 729-735.
27. Zhou RH, Zhu ZD, Kong XY, Huo NX, Tian QZ, et al. (2005) Development of wheat near-isogenic lines for powdery mildew resistance. Theoretical and Applied Genetics 110: 640-648.
28. Guo S, Ma N, Yang WC, Sun YJ, Shen HL, (2011) Expression Analysis of Restorer Alleles-Induced Genes in Pepper. Agricultural Sciences in China 10: 1010-1015.
29. Guo S, Shen HL, Yang WC, Yang J, Wang W, (2009) Isolation of fertility restoration-related ESTs in pepper cytoplasmic male sterility lines using SSH. Acta Horticulturae Sinica 36: 1443-1449.
30. Wang W, Liu C, Shen HL, (2011) Construction of SSH-cDNA library for cytoplasm male sterility lines and maintainer lines in pepper. China Cucurbits and Vegetables 24: 1-5.
31. Schuster SC, (2008) Next-generation sequencing transforms today's biology. Nature Methods 5: 16-18.
32. Ansorge WJ, (2009) Next-generation DNA sequencing techniques. New Biotechnology 25: 195-203.
33. Kim KH, Kang YJ, Kim DH, Yoon MY, Moon J-K, et al. (2011) RNA-Seq Analysis of a Soybean Near-Isogenic Line Carrying Bacterial Leaf Pustule-Resistant and-Susceptible Alleles. DNA Research 18: 483-497.
34. Bennett MD, Leitch IJ, (2005) Nuclear DNA amounts in angiosperms: Progress, problems and prospects. Annals of Botany 95: 45-90.
35. Nicolai M, Pisani C, Bouchet JP, Vuylsteke M, Palloix A, (2012) Discovery of a large set of SNP and SSR genetic markers by high-throughput sequencing of pepper (Capsicum annuum). Genetics and Molecular Research 11: 43-47.
36. Gongora-Castillo E, Fajardo-Jaime R, Fernandez-Cortes A, Jofre-Garfias AE, Lozoya-Gloria E, et al. (2012) The capsicum transcriptome DB: a "hot" tool for genomic research. Bioinformation 8: 43-47.
37. Lu FH, Yoon MY, Cho YI, Chung JW, Kim KT, et al. (2011) Transcriptome analysis and SNP/SSR marker information of red pepper variety YCM334 and Taean. Scientia Horticulturae 129: 38-45.
38. Lu FH, Cho MC, Park YJ, (2012) Transcriptome profiling and molecular marker discovery in red pepper, Capsicum annuum L. TF68. Molecular Biology Reports 39: 3327-3335.
39. Chen C, Liu S, Hao X, Chen G, Cao B, et al. (2012) Characterization of a Pectin Methylesterase Gene Homolog, CaPME1, Expressed in Anther Tissues of Capsicum annuum L. Plant Molecular Biology Reporter. 30: 403-412.
40. Liu S, Chen C, Chen G, Cao B, Chen Q, et al. (2012) RNA-sequencing tag profiling of the placenta and pericarp of pungent pepper provides robust candidates contributing to capsaicinoid biosynthesis. Plant Cell Tissue and Organ Culture 110: 111-121.
41. Qiu WM, Zhu AD, Wang Y, Chai LJ, Ge XX, et al. (2012) Comparative transcript profiling of gene expression between seedless Ponkan mandarin and its seedy wild type during floral organ development by suppression subtractive hybridization and cDNA microarray. BMC Genomics 13: 397.
42. Scott RJ, Spielman M, Dickinson HG, (2004) Stamen structure and function. Plant Cell 16(Suppl): S46-S60.
43. Ness RW, Siol M, Barrett SCH, (2011) De novo sequence assembly and characterization of the floral transcriptome in cross- and self-fertilizing plants. BMC Genomics 12: 298.
44. Wang XW, Luan JB, Li JM, Bao YY, Zhang CX, et al. (2010) De novo characterization of a whitefly transcriptome and analysis of its gene expression during development. BMC Genomics 11: 400.
45. Blanca J, Canizares J, Roig C, Ziarsolo P, Nuez F, et al. (2011) Transcriptome characterization and high throughput SSRs and SNPs discovery in Cucurbita pepo (Cucurbitaceae). BMC Genomics 12: 104.
46. Parchman TL, Geist KS, Grahnen JA, Benkman CW, Buerkle CA, (2010) Transcriptome sequencing in an ecologically important tree species: assembly, annotation, and marker discovery. BMC Genomics 11: 180.
47. Zhang XM, Zhao L, Larson-Rabin Z, Li DZ, Guo ZH, (2012) De Novo Sequencing and Characterization of the Floral Transcriptome of Dendrocalamus latiflorus (Poaceae: Bambusoideae). PloS One 7: e42082.
48. Wei W, Qi X, Wang L, Zhang Y, Hua W, et al. (2011) Characterization of the sesame (Sesamum indicum L.) global transcriptome using Illumina paired-end sequencing and development of EST-SSR markers. BMC Genomics 12: 451.
49. Tan MH, Au KF, Yablonovitch AL, Wills AE, Chuang J, et al. (2013) RNA sequencing reveals a diverse and dynamic repertoire of the Xenopus tropicalis transcriptome over development. Genome Research 23: 201-216.
50. Ekman DR, Lorenz WW, Przybyla AE, Wolfe NL, Dean JFD, (2003) SAGE analysis of transcriptome responses in Arabidopsis roots exposed to 2,4,6-trinitrotoluene. Plant Physiology 133: 1397-1406.
51. Wang G, Zhu Q, Meng Q, Wu C, (2012) Transcript profiling during salt stress of young cotton (Gossypium hirsutum) seedlings via Solexa sequencing. Acta Physiologiae Plantarum 34: 107-115.
52. Kim BS, Ahn JH, Lee JM, Park DG, Kim HY, (2012) Restorer Genotype for Male Sterile Cytoplasm of Genetic Resources Moderately Resistant to Phytophthora capsici in Capsicum Pepper. Korean journal of horticultural science & technology 30: 73-78.
53. Teixeira RT, Knorpp C, Glimelius K, (2005) Modified sucrose, starch, and ATP levels in two alloplasmic male-sterile lines of B-napus. Journal of Experimental Botany 56: 1245-1253.
54. Wang XZ, Teng XY, Yen LF, Zhou RG, (1986) The relationgship between the ATP content in anthers of maize and sorghum and cytoplasmic male-sterility. Acta Agronomica Sinca 12: 177-182.
55. Hanson MR, Bentolila S, (2004) Interactions of mitochondrial and nuclear genes that affect male gametophyte development. Plant Cell 16: S154-S169.
56. Singh M, Brown GG, (1991) Suppression of cytoplasmic male-sterility by nuclear genes alters expression of a novel mitochondrial gene region. Plant Cell 3: 1349-1362.
57. Moneger F, Smart CJ, Leaver CJ, (1994) Nuclear restoration of cytoplasmic male-sterility in sunflower is associated with the tissue-specific regulation of a novel mitochondrial gene. Embo Journa l 13: 8-17.
58. Budar F, Pelletier G, (2001) Male sterility in plants: occurrence, determinism, significance and use. Comptes Rendus De L Academie Des Sciences Serie Iii-Sciences De La Vie-Life Sciences 324: 543-550.
59. Young EG, Hanson MR, (1987) A fused mitochondrial gene associated with cytoplasmic male-sterility is developmentally regulated. Cell 50: 41-49.
60. Huang J, Yang P, Li B, Huang JL, Yang P, et al. (2004) Study on the activity of several enzymes of cytoplasmic male-sterile cotton line Jin A. Cotton Science. 16: 229-232.
61. Liu Y, Wang X, Wang Y, Zhuo D, (1988) Structural variance analysis of mitochondria coI and coII genes from normal and cytoplasmic male-sterile varieties of rice oryza-sativa. Acta Genetica Sinica 15: 348-354.
62. Ricard B, Lejeune B, Araya A, (1986) Studies on wheat mitochondrial-DNA organization- comparison of mitochondrial-DNA from normal and cytoplasmic male sterile varieties of wheat. Plant Science 43: 141-149.
63. Small ID, Peeters N, (2000) The PPR motif- a TPR-related motif prevalent in plant organellar proteins. Trends in Biochemical Sciences 25: 46-47.
64. Brown GG, Formanova N, Jin H, Wargachuk R, Dendy C, et al. (2003) The radish Rfo restorer gene of Ogura cytoplasmic male sterility encodes a protein with multiple pentatricopeptide repeats. Plant Journal 35: 262-272.
65. Akagi H, Nakamura A, Yokozeki-Misono Y, Inagaki A, Takahashi H, et al. (2004) Positional cloning of the rice Rf-1 gene, a restorer of BT-type cytoplasmic male sterility that encodes a mitochondria-targeting PPR protein. Theoretical and Applied Genetics 108: 1449-1457.
66. Alfonso AA, Bentolila S, Hanson MR, (2003) Evaluation of the fertility restoring ability of Rf-PPR592 in petunia. Philippine Agricultural Scientist 86: 303-315.
67. Zhang M, Liang C, Duan J, Huang Y, Liou H, et al. (1997) Lipid peroxidation difference in leaves, panicles and anthers of CMS rice and its maintainer. Acta Agronomica Sinica 23: 603-606.
68. Chen XF, Liang CY, (1992) Energy and activated oxygen metabolisms in anthers of Hubei photoperiod-sensitive genic male-sterile rice. Acta Botanica Sinica 34: 416-425.
69. Zhang J, Zong X, Wang J, Gao D, Yu G, et al. (2001) Changes in activity of protective enzymes in the anther of thermo-photosensitive genic male sterile wheat. Journal of Triticeae Crops 21: 26-30.
70. Duan J, Liang C, Zhang M, Duan J, Liang CY, et al. (1996) The relationship between membrane lipid peroxidation and cytoplasmic male sterility in maize. Plant Physiology Communications 32: 331-334.
71. Li SQ, Wan CX, Kong J, Zhang ZJ, Li YS, et al. (2004) Programmed cell death during microgenesis in a Honglian CMS line of rice is correlated with oxidative stress in mitochondria. Functional Plant Biology 31: 369-376.
72. Wan C, Li S, Wen L, Kong J, Wang K, et al. (2007) Damage of oxidative stress on mitochondria during microspores development in Honglian CMS line of rice. Plant Cell Reports 26: 373-382.
73. Deng MH, Wen JF, Huo JL, Zhu HS, Dai XZ, et al. (2012) Relationship of metabolism of reactive oxygen species with cytoplasmic male sterility in pepper (Capsicum annuum L.). Scientia Horticulturae 134: 232-236.
74. Zhang Z, Hou X, Zhang ZX, Hou XL, (2005) Relation between cytoplasmic male sterility and reactive oxygen species metabolism in pepper. Acta Botanica Boreali-Occidentalia Sinica 25: 799-802.
75. Li YY, Wei YY, Zhang RH, Lu J, (2006) Studies on the Metabolism of Male Sterile Pepper in the Development of Microspore. Acta Agriculturae Boreali-Occidentalis Sinica 15: 134-137.
76. Wang YF, Hu CQ, Lin ZG, Li FY, Jin JK, (1984) A Comparative Analysis on the Amphi-line of the Male Sterility in Brassica pekinensis, Rupr. Acta Horticulturae Sinica 11: 182-186.
77. Liu ZS, Guan CY, (1990) Studies on male sterility in oilseed rape. I. A comparison of the biochemical characteristics between a Polima cytoplasmic male-sterile line of rape (Brassica napus L.) and its maintainer line. Oil Crops of China 3: 1-4.
78. Iwabuchi M, Kyozuka J, Shimamoto K, (1993) Processing followed by complete editing of an altered mitochondrial atp6 RNA restores fertility of cytoplasmic male sterile rice. Embo Journal 12: 1437-1446.
79. Begu D, Graves PV, Domec C, Arselin G, Litvak S, et al. (1990) RNA editing of wheat mitochondrial ATP synthase subunit-9- direct protein and cDNA sequencing. Plant Cell 2: 1283-1290.
80. Trevaskis B, Hemming MN, Dennis ES, Peacock WJ, (2007) The molecular basis of vernalization-induced flowering in cereals. Trends in Plant Science 12: 352-357.
81. Imaizumi T, Kay SA, (2006) Photoperiodic control of flowering: not only by coincidence. Trends in Plant Science 11: 567-567.
82. Li L, Xia K, Fu Y, Tian Y, Li L, et al. (2010) Plant F-box protein and its biological function. Agricultural Science & Technology- Hunan 11: 9-12.
83. Shen HL, Jiang JZ, Wang ZY, Geng SS, (1994) Studies on the breeding and inheritance of male-sterile lines of pepper (Capsicum annuum L.). Acta Agriculturae Universitatis Pekinensis 20: 25-30.
84. Zhang J, Gong Z, Liu K, Huang W, Li D, et al. (2007) Interrelation of cytological development period of pepper's microspore and the morphology of flower organ. Journal of Northwest A & F University- Natural Science Edition 35: 153-158.
85. Liu M, Qiao G, Jiang J, Yang H, Xie L, et al. (2012) Transcriptome Sequencing and De Novo Analysis for Ma Bamboo (Dendrocalamus latiflorus Munro) Using the Illumina Platform. PloS One 7: e46766.
86. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, et al. (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotechnology 29: 644-U130.
87. Rice P, Longden I, Bleasby A, (2000) EMBOSS: The European molecular biology open software suite. Trends in Genetics 16: 276-277.
88. Chen ZZ, Xue CH, Zhu S, Zhou FF, Ling XFB, et al. (2005) GoPipe: Streamlined Gene Ontology annotation for batch anonymous sequences with statistics. Progress in Biochemistry and Biophysics 32: 187-190.
89. Kanehisa M, Goto S, Furumichi M, Tanabe M, Hirakawa M, (2010) KEGG for representation and analysis of molecular networks involving diseases and drugs. Nucleic Acids Research 38: D355-D360.
90. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B, (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nature Methods 5: 621-628.
91. Wang L, Feng Z, Wang X, Wang X, Zhang X, (2010) DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26: 136-138.
92. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-Delta Delta C) method. Methods 25: 402-408.