Transcriptome de novo assembly and differentially expressed genes related to cytoplasmic male sterility in kenaf (Hibiscus cannabinus L.)

Molecular Breeding

Volumn 34, Issue 4, 2014, Pages 1879-1891

  Chen, Peng ^a   Ran, Shanmin ^a   Li, Ru ^a   Huang, Zhipeng ^a   Qian, Jinghua ^a   Yu, Mingli ^a   Zhou, Ruiyang ^a  

^a GUANGXI UNIVERSITY   (China)

Author keywords

Cytoplasmic male sterility (CMS); Kenaf (Hibiscus cannabinus L.); Solexa sequencing; Transcriptome

Indexed keywords

GENE EXPRESSION; GENE ONTOLOGY; HEMP; PLANTS (BOTANY); SEED;

ANTHER DEVELOPMENT; CYTOPLASMIC MALE STERILITY; DIFFERENTIALLY EXPRESSED GENE; GENE ONTOLOGY TERMS; KENAF (HIBISCUS CANNABINUS L); KENAF (HIBISCUS CANNABINUS L.); MAINTAINER LINES; SOLEXUM SEQUENCING; TRANSCRIPTOMES;

POLYMERASE CHAIN REACTION;

HIBISCUS CANNABINUS;

EID: 84914815856     PISSN: 13803743     EISSN: 15729788     Source Type: Journal    
DOI: 10.1007/s11032-014-0146-8     Document Type: Article

References (72)

1. Alexopoulou E, Christou M, Mardikis M, Chatziathanassiou A (2000) Growth and yields of kenaf varieties in central Greece. Ind Crop Prod 11:163–172
2. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl Acids Res 25:3389–3402
3. Ambrose BA, Lerner DR, Ciceri P, Padilla CM, Yanofsky MF, Schmidt RJ (2000) Molecular and genetic analyses of the silky1 gene reveal conservation in floral organ specification between eudicots and monocots. Mol Cell 5:569–579
4. Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11:R106
5. Bairoch A, Apweiler R (1997) The SWISS-PROT protein sequence data bank and its supplement TrEMBL. Nucl Acids Res 25:31–36
6. Bañuelos GS, Bryla DR, Cook CG (2002) Vegetative production of kenaf and canola under irrigation in central California. Ind Crop Prod 15:237–245
7. Becker A, Theißen G (2003) The major clades of MADS-box genes and their role in the development and evolution of flowering plants. Mol Phylogenet Evol 29:464–489
8. Bemer M, Heijmans K, Airoldi C, Davies B, Angenent GC (2010) An atlas of type I MADS box gene expression during female gametophyte and seed development in Arabidopsis. Plant Physiol 154:287–300
9. Cloonan N, Forrest AR, Kolle G, Gardiner BB, Faulkner GJ, Brown MK, Taylor DF, Steptoe AL, Wani S, Bethel G (2008) Stem cell transcriptome profiling via massive-scale mRNA sequencing. Nat Methods 5:613–619
10. Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676
11. Cushing DA, Forsthoefel NR, Gestaut DR, Vernon DM (2005) Arabidopsis emb175 and other ppr knockout mutants reveal essential roles for pentatricopeptide repeat (PPR) proteins in plant embryogenesis. Planta 221:424–436
12. Delannoy E, Stanley W, Bond C, Small I (2007) Pentatricopeptide repeat (PPR) proteins as sequence-specificity factors in post-transcriptional processes in organelles. Biochem Soc Trans 35:1643–1647
13. Dubos C, Stracke R, Grotewold E, Weisshaar B, Martin C, Lepiniec L (2010) MYB transcription factors in Arabidopsis. Trends Plant Sci 15(10):573–581
14. Filichkin SA, Priest HD, Givan SA, Shen R, Bryant DW, Fox SE, Wong WK, Mockler TC (2010) Genome-wide mapping of alternative splicing in Arabidopsis thaliana. Genome Res 20:45–58
15. Fujii S, Yamada M, Fujita M, Itabashi E, Hamada K, Yano K, Kurata N, Toriyama K (2010) Cytoplasmic–nuclear genomic barriers in rice pollen development revealed by comparison of global gene expression profiles among five independent cytoplasmic male sterile lines. Plant Cell Physiol 51:610–620
16. Gagliardi D, Leaver CJ (1999) Polyadenylation accelerates the degradation of the mitochondrial mRNA associated with cytoplasmic male sterility in sunflower. EMBO J 18:3757–3766
17. Gonzalez A, Zhao M, Leavitt JM, Lloyd AM (2008) Regulation of the anthocyanin biosynthetic pathway by the TTG1/bHLH/Myb transcriptional complex in Arabidopsis seedlings. Plant J 53:814–827
18. Gramzow L, Ritz MS, Theißen G (2010) On the origin of MADS-domain transcription factors. Trends Genet 26:149–153
19. Hama E, Takumi S, Ogihara Y, Murai K (2004) Pistillody is caused by alterations to the class-B MADS-box gene expression pattern in alloplasmic wheats. Planta 218:712–720
20. Hanson MR, Bentolila S (2004) Interactions of mitochondrial and nuclear genes that affect male gametophyte development. Plant Cell 16(suppl 1):S154–S169
21. Higginson T, Li SF, Parish RW (2003) AtMYB103 regulates tapetum and trichome development in Arabidopsis thaliana. Plant J 35:177–192
22. Hu J, Wang K, Huang W, Liu G, Gao Y, Wang J, Huang Q, Ji Y, Qin X, Wan L (2012) The rice pentatricopeptide repeat protein RF5 restores fertility in Hong-Lian cytoplasmic male-sterile lines via a complex with the glycine-rich protein GRP162. Plant Cell 24:109–122
23. Kanehisa M, Goto S, Kawashima S, Okuno Y, Hattori M (2004) The KEGG resource for deciphering the genome. Nucl Acids Res 32(suppl 1):D277–D280
24. Kang YH, Kirik V, Hulskamp M, Nam KH, Hagely K, Lee MM, Schiefelbein J (2009) The MYB23 gene provides a positive feedback loop for cell fate specification in the Arabidopsis root epidermis. Plant Cell 21:1080–1094
25. Kelley DR, Schatz MC, Salzberg SL (2010) Quake: quality-aware detection and correction of sequencing errors. Genome Biol 11:R116
26. Kemble L, Krishnan P, Henning K, Tilmon H (2002) PM—power and machinery: development and evaluation of kenaf harvesting technology. Biosyst Eng 81:49–56
27. Kotak S, Larkindale J, Lee U, von Koskull-Döring P, Vierling E, Scharf K-D (2007) Complexity of the heat stress response in plants. Curr Opin Plant Biol 10(3):310–316
28. Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359
29. Li R, Zhu H, Ruan J, Qian W, Fang X, Shi Z, Li Y, Li S, Shan G, Kristiansen K (2010) De novo assembly of human genomes with massively parallel short read sequencing. Genome Res 20:265–272
30. Li YJ, Fu YR, Huang JG, Wu CA, Zheng CC (2011) Transcript profiling during the early development of the maize brace root via Solexa sequencing. FEBS J 278:156–166
31. Li Y, Jiang J, Du ML, Li L, Wang XL, Li XB (2013) A cotton gene encoding MYB-like transcription factor is specifically expressed in pollen and is involved in regulation of late anther/pollen development. Plant Cell Physiol 54:893–906
32. Linke B, Nothnagel T, Börner T (2003) Flower development in carrot CMS plants: mitochondria affect the expression of MADS box genes homologous to GLOBOSA and DEFICIENS. Plant J 34:27–37
33. Lister R, O’Malley RC, Tonti-Filippini J, Gregory BD, Berry CC, Millar AH, Ecker JR (2008) Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell 133:523–536
34. Liu C, Ma N, Wang P-Y, Fu N, Shen H-L (2013a) 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 8:e65209
35. Liu T, Zhu S, Tang Q, Chen P, Yu Y, Tang S (2013b) De novo assembly and characterization of transcriptome using Illumina paired-end sequencing and identification of CesA gene in ramie (Boehmeria nivea L.). BMC Genom 14:125
36. Liu Y-J, Xiu Z-H, Meeley R, Tan B-C (2013c) Empty pericarp5 encodes a pentatricopeptide repeat protein that is required for mitochondrial RNA editing and seed development in maize. Plant Cell 25:868–883
37. Lurin C, Andrés C, Aubourg S, Bellaoui M, Bitton F, Bruyère C, Caboche M, Debast C, Gualberto J, Hoffmann B (2004) Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell 16:2089–2103
38. Mandaokar A, Thines B, Shin B, Markus Lange B, Choi G, Koo YJ, Yoo YJ, Choi YD, Choi G (2006) Transcriptional regulators of stamen development in Arabidopsis identified by transcriptional profiling. Plant J 46:984–1008
39. Mardis ER (2008) Next-generation DNA sequencing methods. Annu Rev Genomics Hum Genet 9:387–402
40. Mascarenhas JP (1989) The male gametophyte of flowering plants. Plant Cell 1:657
41. Masiero S, Colombo L, Grini PE, Schnittger A, Kater MM (2011) The emerging importance of type I MADS box transcription factors for plant reproduction. Plant Cell 23:865–872
42. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5:621–628
43. Münster T, Pahnke J, Di Rosa A, Kim JT, Martin W, Saedler H, Theissen G (1997) Floral homeotic genes were recruited from homologous MADS-box genes preexisting in the common ancestor of ferns and seed plants. Proc Natl Acad Sci USA 94:2415–2420
44. Nagalakshmi U, Wang Z, Waern K, Shou C, Raha D, Gerstein M, Snyder M (2008) The transcriptional landscape of the yeast genome defined by RNA sequencing. Science 320:1344–1349
45. Nagasawa N, Miyoshi M, Sano Y, Satoh H, Hirano H, Sakai H, Nagato Y (2003) SUPERWOMAN1 and DROOPING LEAF genes control floral organ identity in rice. Development 130:705–718
46. Nakamura T, Meierhoff K, Westhoff P, Schuster G (2003) RNA-binding properties of HCF152, an Arabidopsis PPR protein involved in the processing of chloroplast RNA. Eur J Biochem 270:4070–4081
47. Okuda K, Nakamura T, Sugita M, Shimizu T, Shikanai T (2006) A pentatricopeptide repeat protein is a site recognition factor in chloroplast RNA editing. J Biol Chem 28:37661–37667
48. Parchman T, Geist K, Grahnen J, Benkman C, Buerkle CA (2010) Transcriptome sequencing in an ecologically important tree species: assembly, annotation, and marker discovery. BMC Genom 11:180
49. Sabar M, Gagliardi D, Balk J, Leaver CJ (2003) ORFB is a subunit of F1FO-ATP synthase: insight into the basis of cytoplasmic male sterility in sunflower. EMBO Rep 4:381–386
50. Schmitz-Linneweber C, Williams-Carrier R, Barkan A (2005) RNA immunoprecipitation and microarray analysis show a chloroplast pentatricopeptide repeat protein to be associated with the 5′ region of mRNAs whose translation it activates. Plant Cell 17:2791–2804
51. Schwarz-Sommer Z, Davies B, Hudson A (2003) An everlasting pioneer: the story of Antirrhinum research. Nat Rev Genet 4:655–664
52. Siedow JN, Umbach AL (1995) Plant mitochondrial electron transfer and molecular biology. Plant Cell 7:821
53. Song S, Qi T, Huang H, Ren Q, Wu D, Chang C, Peng W, Liu Y, Peng J, Xie D (2011) The jasmonate-ZIM domain proteins interact with the R2R3-MYB transcription factors MYB21 and MYB24 to affect jasmonate-regulated stamen development in Arabidopsis. Plant Cell 23:1000–1013
54. Stracke R, Ishihara H, Huep G, Barsch A, Mehrtens F, Niehaus K, Weisshaar B (2007) Differential regulation of closely related R2R3-MYB transcription factors controls flavonol accumulation in different parts of the Arabidopsis thaliana seedling. Plant J 50:660–677
55. Tatusov RL, Koonin EV, Lipman DJ (1997) A genomic perspective on protein families. Science 278:631–637
56. Tatusov RL, Galperin MY, Natale DA, Koonin EV (2000) The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res 28:33–36
57. Twell D (2011) Male gametogenesis and germline specification in flowering plants. Sex Plant Reprod 24:149–160
58. Wang Z, Zou Y, Li X, Zhang Q, Chen L, Wu H, Su D, Chen Y, Guo J, Luo D (2006) Cytoplasmic male sterility of rice with boro II cytoplasm is caused by a cytotoxic peptide and is restored by two related PPR motif genes via distinct modes of mRNA silencing. Plant Cell 18:676–687
59. Wang ET, Sandberg R, Luo S, Khrebtukova I, Zhang L, Mayr C, Kingsmore SF, Schroth GP, Burge CB (2008) Alternative isoform regulation in human tissue transcriptomes. Nature 456:470–476
60. Wang QQ, Liu F, Chen XS, Ma XJ, Zeng HQ, Yang ZM (2010a) Transcriptome profiling of early developing cotton fiber by deep-sequencing reveals significantly differential expression of genes in a fuzzless/lintless mutant. Genomics 96:369–376
61. Wang Z, Fang B, Chen J, Zhang X, Luo Z, Huang L, Chen X, Li Y (2010b) De novo assembly and characterization of root transcriptome using Illumina paired-end sequencing and development of cSSR markers in sweetpotato (Ipomoea batatas). BMC Genom 11:726
62. Xie C, Mao X, Huang J, Ding Y, Wu J, Dong S, Kong L, Gao G, Li C-Y, Wei L (2011) KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases. Nucl Acids Res 39(suppl 2):W316–W322
63. Yang C, Xu Z, Song J, Conner K, Barrena GV, Wilson ZA (2007) Arabidopsis MYB26/MALE STERILE35 regulates secondary thickening in the endothecium and is essential for anther dehiscence. Plant Cell 19:534–548
64. Yang JH, Huai Y, Zhang MF (2009) Mitochondrial atpA gene is altered in a new orf220-type cytoplasmic male-sterile line of stem mustard (Brassica juncea). Mol Biol Rep 36:273–280
65. Yanofsky MF, Ma H, Bowman JL, Drews GN, Feldmann KA, Meyerowitz EM (1990) The protein encoded by the Arabidopsis homeotic gene agamous resembles transcription factors. Nature 346:35–39
66. Ye J, Fang L, Zheng H, Zhang Y, Chen J, Zhang Z, Wang J, Li S, Li R, Bolund L (2006) WEGO: a web tool for plotting GO annotations. Nucl Acids Res 34(suppl 2):W293–W297
67. Young EG, Hanson MR (1987) A fused mitochondrial gene associated with cytoplasmic male sterility is developmentally regulated. Cell 50:41–49
68. Zhang ZB, Zhu J, Gao JF, Wang C, Li H, Li H, Zhang HQ, Zhang S, Wang DM, Wang QX (2007) Transcription factor AtMYB103 is required for anther development by regulating tapetum development, callose dissolution and exine formation in Arabidopsis. Plant J 52:528–538
69. Zhao Y, Chen P, Liao X, Zhou B, Liao J, Huang Z, Kong X, Zhou R (2013) A comparative study of the atp9 gene between a cytoplasmic male sterile line and its maintainer line and further development of a molecular marker specific for male sterile cytoplasm in kenaf (Hibiscus cannabinus L.). Mol Breed 32(4):969–976
70. Zhou RY, Zhang X, Zhang JQ, Gan ZX, Wei H (2008) A breakthrough in kenaf cytoplasmic male sterile linesbreeding and heterosis utilization (in Chinese). Sci Agric Sin 41:314
71. Zhu LM, Ai S, Zhou RY (2007) A cytological study on microsporogenesis of cytoplasmic male sterile lines in kenaf (Hibiscus cannabinus L.) (in Chinese). Acta Agron Sin 31:999–1003
72. Zubko MK, Zubko EI, Ruban AV, Adler K, Mock HP, Misera S, Gleba YY, Grimm B (2001) Extensive developmental and metabolic alterations in cybrids Nicotiana tabacum (Hyoscyamus niger) are caused by complex nucleo-cytoplasmic incompatibility. Plant J 25:627–639