Assembly and analysis of a male sterile rubber tree mitochondrial genome reveals DNA rearrangement events and a novel transcript

BMC Plant Biology

Volumn 14, Issue 1, 2014, Pages

  Shearman, Jeremy R ^a   Sangsrakru, Duangjai ^a   Ruang areerate, Panthita ^a   Sonthirod, Chutima ^a   Uthaipaisanwong, Pichahpuk ^a   Yoocha, Thippawan ^a   Poopear, Supannee ^a   Theerawattanasuk, Kanikar ^b   Tragoonrung, Somvong ^a   Tangphatsornruang, Sithichoke ^a  

^a NATIONAL SCIENCE AND TECHNOLOGY DEVELOPMENT AGENCY   (Thailand)

^b Thailand Ministry of Agriculture and Cooperatives   (Thailand)

Author keywords

Cytoplasmic male sterility; Genome sequencing; Hevea brasiliensis; Mitochondria; Rubber tree

Indexed keywords

ADENOSINE TRIPHOSPHATE; VEGETABLE PROTEIN;

ARTICLE; GENE EXPRESSION REGULATION; GENETICS; HEVEA; METABOLISM; MITOCHONDRIAL GENOME; PHYSIOLOGY;

ADENOSINE TRIPHOSPHATE; GENE EXPRESSION REGULATION, PLANT; GENOME, MITOCHONDRIAL; HEVEA; PLANT PROTEINS;

EID: 84893694361     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/1471-2229-14-45     Document Type: Article

References (69)

1. McBride HM, Neuspiel M, Wasiak S. Mitochondria: more than just a powerhouse. Curr Biol 2006, 16:R551-R560. 10.1016/j.cub.2006.06.054, 16860735.
2. Unseld M, Marienfeld JR, Brandt P, Brennicke A. The mitochondrial genome of Arabidopsis thaliana contains 57 genes in 366,924 nucleotides. Nat Genet 1997, 15:57-61. 10.1038/ng0197-57, 8988169.
3. Palmer JD, Herbon LA. Unicircular structure of the Brassica hirta mitochondrial genome. Curr Genet 1987, 11:565-570. 10.1007/BF00384620, 2836082.
4. Rodríguez-Moreno L, González VM, Benjak A, Martí MC, Puigdomènech P, Aranda MA, Garcia-Mas J. Determination of the melon chloroplast and mitochondrial genome sequences reveals that the largest reported mitochondrial genome in plants contains a significant amount of DNA having a nuclear origin. BMC Genomics 2011, 12:424. 10.1186/1471-2164-12-424, 3175227, 21854637.
5. Turmel M, Otis C, Lemieux C. The mitochondrial genome of Chara vulgaris: insights into the mitochondrial DNA architecture of the last common ancestor of green algae and land plants. Plant Cell 2003, 15:1888-1903. 10.1105/tpc.013169, 167177, 12897260.
6. Bullerwell CE, Gray MW. Evolution of the mitochondrial genome: protist connections to animals, fungi and plants. Curr Opin Microbiol 2004, 7:528-534. 10.1016/j.mib.2004.08.008, 15451509.
7. Chang S, Yang T, Du T, Huang Y, Chen J, Yan J, He J, Guan R. Mitochondrial genome sequencing helps show the evolutionary mechanism of mitochondrial genome formation in Brassica. BMC Genomics 2011, 12:497. 10.1186/1471-2164-12-497, 3204307, 21988783.
8. Allen JO, Fauron CM, Minx P, Roark L, Oddiraju S, Lin GN, Meyer L, Sun H, Kim K, Wang C, Du F, Xu D, Gibson M, Cifrese J, Clifton SW, Newton KJ. Comparisons among two fertile and three male-sterile mitochondrial genomes of maize. Genetics 2007, 177:1173-1192. 10.1534/genetics.107.073312, 2034622, 17660568.
9. Dewey RE, Levings CS, Timothy DH. Novel recombinations in the maize mitochondrial genome produce a unique transcriptional unit in the Texas male-sterile cytoplasm. Cell 1986, 44:439-449. 10.1016/0092-8674(86)90465-4, 2417728.
10. Young EG, Hanson MR. A fused mitochondrial gene associated with cytoplasmic male sterility is developmentally regulated. Cell 1987, 50:41-49. 10.1016/0092-8674(87)90660-X, 2885095.
11. Wang Z, Zou Y, Li X, Zhang Q, Chen L, Wu H, Su D, Chen Y, Guo J, Luo D, Long Y, Zhong Y, Liu Y-G. 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 Online 2006, 18:676-687.
12. Laver HK, Reynolds SJ, Moneger F, Leaver CJ. Mitochondrial genome organization and expression associated with cytoplasmic male sterility in sunflower (Helianthus annuus). Plant J Cell Mol Biol 1991, 1:185-193.
13. Landgren M, Zetterstrand M, Sundberg E, Glimelius K. Alloplasmic male-sterile Brassica lines containing B. tournefortii mitochondria express an ORF 3' of the atp6 gene and a 32 kDa protein. off. Plant Mol Biol 1996, 32:879-890. 10.1007/BF00020485, 8980539.
14. Gallagher LJ, Betz SK, Chase CD. Mitochondrial RNA editing truncates a chimeric open reading frame associated with S male-sterility in maize. Curr Genet 2002, 42:179-184. 10.1007/s00294-002-0344-5, 12491012.
15. Dill CL, Wise RP, Schnable PS. Rf8 and Rf* mediate unique T-urf13-transcript accumulation, revealing a conserved motif associated with RNA processing and restoration of pollen fertility in T-cytoplasm maize. Genetics 1997, 147:1367-1379. 1208258, 9383077.
16. Rivarola M, Foster JT, Chan AP, Williams AL, Rice DW, Liu X, Melake-Berhan A, Huot Creasy H, Puiu D, Rosovitz MJ, Khouri HM, Beckstrom-Sternberg SM, Allan GJ, Keim P, Ravel J, Rabinowicz PD. Castor bean organelle genome sequencing and worldwide genetic diversity analysis. PLoS One 2011, 6:e21743. 10.1371/journal.pone.0021743, 3131294, 21750729.
17. Iorizzo M, Senalik D, Szklarczyk M, Grzebelus D, Spooner D, Simon P. De novo assembly of the carrot mitochondrial genome using next generation sequencing of whole genomic DNA provides first evidence of DNA transfer into an angiosperm plastid genome. BMC Plant Biol 2012, 12:61. 10.1186/1471-2229-12-61, 3413510, 22548759.
18. Fang Y, Wu H, Zhang T, Yang M, Yin Y, Pan L, Yu X, Zhang X, Hu S, Al-Mssallem IS, Yu J. A complete sequence and transcriptomic analyses of date palm (Phoenix dactylifera L.) mitochondrial genome. PLoS One 2012, 7:e37164. 10.1371/journal.pone.0037164, 3360038, 22655034.
19. Rahman AYA, Usharraj AO, Misra BB, Thottathil GP, Jayasekaran K, Feng Y, Hou S, Ong SY, Ng FL, Lee LS, Tan HS, Sakaff MKLM, Teh BS, Khoo BF, Badai SS, Aziz NA, Yuryev A, Knudsen B, Dionne-Laporte A, Mchunu NP, Yu Q, Langston BJ, Freitas TAK, Young AG, Chen R, Wang L, Najimudin N, Saito JA, Alam M. Draft genome sequence of the rubber tree Hevea brasiliensis. BMC Genomics 2013, 14:75. 10.1186/1471-2164-14-75, 3575267, 23375136.
20. Tangphatsornruang S, Uthaipaisanwong P, Sangsrakru D, Chanprasert J, Yoocha T, Jomchai N, Tragoonrung S. Characterization of the complete chloroplast genome of Hevea brasiliensis reveals genome rearrangement, RNA editing sites and phylogenetic relationships. Gene 2011, 475:104-112. 10.1016/j.gene.2011.01.002, 21241787.
21. Priyadarshan PM, Clément-Demange A. Breeding Hevea rubber: formal and molecular genetics. Adv Genet 2004, 52:51-115.
22. Triwitayakorn K, Chatkulkawin P, Kanjanawattanawong S, Sraphet S, Yoocha T, Sangsrakru D, Chanprasert J, Ngamphiw C, Jomchai N, Therawattanasuk K, Tangphatsornruang S. Transcriptome sequencing of Hevea brasiliensis for development of microsatellite markers and construction of a genetic linkage map. DNA Res Int J Rapid Publ Rep Genes Genomes 2011, 18:471-482.
23. Boetzer M, Henkel CV, Jansen HJ, Butler D, Pirovano W. Scaffolding pre-assembled contigs using SSPACE. Bioinforma Oxf Engl 2011, 27:578-579.
24. Darling ACE, Mau B, Blattner FR, Perna NT. Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res 2004, 14:1394-1403. 10.1101/gr.2289704, 442156, 15231754.
25. Lohse M, Bolger AM, Nagel A, Fernie AR, Lunn JE, Stitt M, Usadel B. RobiNA: a user-friendly, integrated software solution for RNA-Seq-based transcriptomics. Nucleic Acids Res 2012, 40(Web Server issue):W622-W627. 3394330, 22684630.
26. 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. 10.1186/gb-2013-14-4-r36, 23618408.
27. Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 2009, 10:R25. 10.1186/gb-2009-10-3-r25, 2690996, 19261174.
28. Schattner P, Brooks AN, Lowe TM. The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucleic Acids Res 2005, 33(Web Server issue):W686-W689. 1160127, 15980563.
29. Alverson AJ, Wei X, Rice DW, Stern DB, Barry K, Palmer JD. Insights into the evolution of mitochondrial genome size from complete sequences of Citrullus lanatus and Cucurbita pepo (Cucurbitaceae). Mol Biol Evol 2010, 27:1436-1448. 10.1093/molbev/msq029, 2877997, 20118192.
30. Koboldt DC, Chen K, Wylie T, Larson DE, McLellan MD, Mardis ER, Weinstock GM, Wilson RK, Ding L. VarScan: variant detection in massively parallel sequencing of individual and pooled samples. Bioinforma Oxf Engl 2009, 25:2283-2285.
31. Mower JP. The PREP suite: predictive RNA editors for plant mitochondrial genes, chloroplast genes and user-defined alignments. Nucleic Acids Res 2009, 37(Web Server issue):W253-W259. 2703948, 19433507.
32. Krogh A, Larsson B, von Heijne G, Sonnhammer EL. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 2001, 305:567-580. 10.1006/jmbi.2000.4315, 11152613.
33. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011, 28:2731-2739. 10.1093/molbev/msr121, 3203626, 21546353.
34. Mackenzie MI. Higher plant mitochondria. Plant Cell 1999, 11:571-586. 144202, 10213779.
35. Manchekar M, Scissum-Gunn K, Song D, Khazi F, McLean SL, Nielsen BL. DNA recombination activity in soybean mitochondria. J Mol Biol 2006, 356:288-299. 10.1016/j.jmb.2005.11.070, 16376379.
36. Alverson AJ, Rice DW, Dickinson S, Barry K, Palmer JD. Origins and recombination of the bacterial-sized multichromosomal mitochondrial genome of cucumber. Plant Cell 2011, 23:2499-2513. 10.1105/tpc.111.087189, 3226218, 21742987.
37. Chen J, Guan R, Chang S, Du T, Zhang H, Xing H. Substoichiometrically different mitotypes coexist in mitochondrial genomes of Brassica napus L. PLoS One 2011, 6:e17662. 10.1371/journal.pone.0017662, 3053379, 21423700.
38. Kazakoff SH, Imelfort M, Edwards D, Koehorst J, Biswas B, Batley J, Scott PT, Gresshoff PM. Capturing the biofuel wellhead and powerhouse: the chloroplast and mitochondrial genomes of the leguminous feedstock tree Pongamia pinnata. PLoS One 2012, 7:e51687. 10.1371/journal.pone.0051687, 3522722, 23272141.
39. Mower JP, Case AL, Floro ER, Willis JH. Evidence against equimolarity of large repeat arrangements and a predominant master circle structure of the mitochondrial genome from a monkeyflower (Mimulus guttatus) lineage with cryptic CMS. Genome Biol Evol 2012, 4:670-686. 10.1093/gbe/evs042, 3381676, 22534162.
40. Sloan DB, Alverson AJ, Chuckalovcak JP, Wu M, McCauley DE, Palmer JD, Taylor DR. Rapid evolution of enormous, multichromosomal genomes in flowering plant mitochondria with exceptionally high mutation rates. PLoS Biol 2012, 10:e1001241. 10.1371/journal.pbio.1001241, 3260318, 22272183.
41. Tanaka Y, Tsuda M, Yasumoto K, Yamagishi H, Terachi T. A complete mitochondrial genome sequence of Ogura-type male-sterile cytoplasm and its comparative analysis with that of normal cytoplasm in radish (Raphanus sativus L.). BMC Genomics 2012, 13:352. 10.1186/1471-2164-13-352, 3473294, 22846596.
42. Zhang T, Hu S, Zhang G, Pan L, Zhang X, Al-Mssallem IS, Yu J. The organelle genomes of Hassawi rice (Oryza sativa L.) and its hybrid in saudi arabia: genome variation, rearrangement, and origins. PLoS One 2012, 7:e42041. 10.1371/journal.pone.0042041, 3409126, 22870184.
43. McKinney EA, Oliveira MT. Replicating animal mitochondrial DNA. Genet Mol Biol 2013, 36:308-315. 10.1590/S1415-47572013000300002, 3795181, 24130435.
44. Woloszynska M. Heteroplasmy and stoichiometric complexity of plant mitochondrial genomes-though this be madness, yet there's method in't. J Exp Bot 2010, 61:657-671. 10.1093/jxb/erp361, 19995826.
45. Bonen L. Cis- and trans-splicing of group II introns in plant mitochondria. Mitochondrion 2008, 8:26-34. 10.1016/j.mito.2007.09.005, 18006386.
46. Wang D, Wu Y-W, Shih AC-C, Wu C-S, Wang Y-N, Chaw S-M. Transfer of chloroplast genomic DNA to mitochondrial genome occurred at least 300 MYA. Mol Biol Evol 2007, 24:2040-2048. 10.1093/molbev/msm133, 17609537.
47. Adams KL, Palmer JD. Evolution of mitochondrial gene content: gene loss and transfer to the nucleus. Mol Phylogenet Evol 2003, 29:380-395. 10.1016/S1055-7903(03)00194-5, 14615181.
48. Chang S, Wang Y, Lu J, Gai J, Li J, Chu P, Guan R, Zhao T. The mitochondrial genome of soybean reveals complex genome structures and gene evolution at intercellular and phylogenetic levels. PLoS One 2013, 8:e56502. 10.1371/journal.pone.0056502, 3576410, 23431381.
49. Keren I, Bezawork-Geleta A, Kolton M, Maayan I, Belausov E, Levy M, Mett A, Gidoni D, Shaya F, Ostersetzer-Biran O. AtnMat2, a nuclear-encoded maturase required for splicing of group-II introns in Arabidopsis mitochondria. RNA N Y N 2009, 15:2299-2311.
50. Keren I, Tal L, des Francs-Small CC, Araújo WL, Shevtsov S, Shaya F, Fernie AR, Small I, Ostersetzer-Biran O. nMAT1, a nuclear-encoded maturase involved in the trans-splicing of nad1 intron 1, is essential for mitochondrial complex I assembly and function. Plant J Cell Mol Biol 2012, 71:413-426.
51. Kiang AS, Kavanagh TA. Cytoplasmic male sterility (CMS) in Lolium perenne L. 2. The mitochondrial genome of a CMS line is rearranged and contains a chimaeric atp 9 gene. TAG Theor Appl Genet Theor Angew Genet 1996, 92:308-315.
52. Folkerts O, Hanson MR. The male sterility-associated pcf gene and the normal atp9-1 gene in Petunia are located on different mitochondrial DNA molecules. Genetics 1991, 129:885-895. 1204755, 1836443.
53. Carlsson J, Leino M, Sohlberg J, Sundström JF, Glimelius K. Mitochondrial regulation of flower development. Mitochondrion 2008, 8:74-86. 10.1016/j.mito.2007.09.006, 18054525.
54. Yoshimi M, Kitamura Y, Isshiki S, Saito T, Yasumoto K, Terachi T, Yamagishi H. Variations in the structure and transcription of the mitochondrial atp and cox genes in wild Solanum species that induce male sterility in eggplant (S. melongena). TAG Theor Appl Genet Theor Angew Genet 2013, 126:1851-1859.
55. Wang J, Wang X, Xu H, Tang H, Zhang G, Liu Y-G. Structural and expressional variation analyses of mitochondrial genomes reveal candidate transcripts for the S(V) cytoplasmic male sterility in wheat (Triticum aestivum L.). J Genet Genomics Yi Chuan Xue Bao 2013, 40:437-439.
56. Kim DH, Kang JG, Kim B-D. Isolation and characterization of the cytoplasmic male sterility-associated orf456 gene of chili pepper (Capsicum annuum L.). Plant Mol Biol 2007, 63:519-532. 10.1007/s11103-006-9106-y, 17238047.
57. Sabar M, Gagliardi D, Balk J, Leaver CJ. ORFB is a subunit of F1F(O)-ATP synthase: insight into the basis of cytoplasmic male sterility in sunflower. EMBO Rep 2003, 4:381-386. 10.1038/sj.embor.embor800, 1319156, 12671689.
58. Dieterich J-H, Braun H-P, Schmitz UK. Alloplasmic male sterility in Brassica napus (CMS " Tournefortii-Stiewe" ) is associated with a special gene arrangement around a novel atp9 gene. Mol Genet Genomics MGG 2003, 269:723-731.
59. Tang HV, Pring DR, Shaw LC, Salazar RA, Muza FR, Yan B, Schertz KF. Transcript processing internal to a mitochondrial open reading frame is correlated with fertility restoration in male-sterile sorghum. Plant J Cell Mol Biol 1996, 10:123-133.
60. Li J, Pandeya D, Jo YD, Liu WY, Kang B-C. Reduced activity of ATP synthase in mitochondria causes cytoplasmic male sterility in chili pepper. Planta 2013, 237:1097-1109. 10.1007/s00425-012-1824-6, 23274393.
61. Igarashi K, Kazama T, Motomura K, Toriyama K. Whole genomic sequencing of RT98 mitochondria derived from Oryza rufipogon and northern blot analysis to uncover a cytoplasmic male sterility-associated gene. Plant Cell Physiol 2013, 54:237-243. 10.1093/pcp/pcs177, 23248202.
62. Geisler DA, Päpke C, Obata T, Nunes-Nesi A, Matthes A, Schneitz K, Maximova E, Araújo WL, Fernie AR, Persson S. Downregulation of the δ-subunit reduces mitochondrial ATP synthase levels, alters respiration, and restricts growth and gametophyte development in Arabidopsis. Plant Cell 2012, 24:2792-2811. 10.1105/tpc.112.099424, 3426115, 22805435.
63. Xu P, Yang Y, Zhang Z, Chen W, Zhang C, Zhang L, Zou S, Ma Z. Expression of the nuclear gene TaF(A)d is under mitochondrial retrograde regulation in anthers of male sterile wheat plants with timopheevii cytoplasm. J Exp Bot 2008, 59:1375-1381. 10.1093/jxb/ern068, 18390847.
64. Wen L, Ruesch KL, Ortega VM, Kamps TL, Gabay-Laughnan S, Chase CD. A nuclear restorer-of-fertility mutation disrupts accumulation of mitochondrial ATP synthase subunit alpha in developing pollen of S male-sterile maize. Genetics 2003, 165:771-779. 1462797, 14573487.
65. Bergman P, Edqvist J, Farbos I, Glimelius K. Male-sterile tobacco displays abnormal mitochondrial atp1 transcript accumulation and reduced floral ATP/ADP ratio. Plant Mol Biol 2000, 42:531-544. 10.1023/A:1006388814458, 10798621.
66. Rezvani Z, Didari E, Arastehkani A, Ghodsinejad V, Aryani O, Kamalidehghan B, Houshmand M. Fifteen novel mutations in the mitochondrial NADH dehydrogenase subunit 1, 2, 3, 4, 4L, 5 and 6 genes from Iranian patients with Leber's hereditary optic neuropathy (LHON). Mol Biol Rep 2013, 40:6837-6841. 10.1007/s11033-013-2801-2, 24158608.
67. Lee S-LJ, Warmke H. Organelle size and number in fertile and T-cytoplasmic male-sterile corn. Am J Bot 1979, 66:141-148.
68. Balk J, Leaver CJ. The PET1-CMS mitochondrial mutation in sunflower is associated with premature programmed cell death and cytochrome c release. Plant Cell 2001, 13:1803-1818. 139137, 11487694.
69. Reape TJ, McCabe PF. Apoptotic-like programmed cell death in plants. New Phytol 2008, 180:13-26. 10.1111/j.1469-8137.2008.02549.x, 18631291.