Sex specific expression and distribution of small RNAs in papaya

BMC Genomics

Volumn 15, Issue 1, 2014, Pages

  Aryal, Rishi ^a   Jagadeeswaran, Guru ^b   Zheng, Yun ^c   Yu, Qingyi ^d,e   Sunkar, Ramanjulu ^b   Ming, Ray ^a,e  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b OKLAHOMA STATE UNIVERSITY   (United States)

^c KUNMING UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^d TEXAS A AND M UNIVERSITY   (United States)

^e FUJIAN AGRICULTURE AND FORESTRY UNIVERSITY   (China)

Author keywords

Carica papaya; Centromere; miRNA; Sex chromosome; Sex determination; siRNA

Indexed keywords

BASE SEQUENCE; CARICA; CENTROMERE; CHROMOSOMES, PLANT; GENE EXPRESSION REGULATION, PLANT; GENE LIBRARY; GENES, PLANT; MICRORNAS; RNA, SMALL UNTRANSLATED; SEQUENCE ANALYSIS, RNA; SEX CHROMOSOMES;

EID: 84892381849     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-15-20     Document Type: Article

References (60)

1. Axtell MJ, Snyder JA, Bartel DP. Common functions for diverse small RNAs of land plants. Plant Cell 2007, 19(6):1750-1769. 10.1105/tpc.107.051706, 1955733, 17601824.
2. Bartel B, Bartel DP. MicroRNAs: at the root of plant development?. Plant Physiol 2003, 132(2):709-717. 10.1104/pp.103.023630, 523861, 12805599.
3. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004, 116:281-297. 10.1016/S0092-8674(04)00045-5, 14744438.
4. Reinhart BJ, Weinstein EG, Rhoades MW, Bartel B, Bartel DP. MicroRNAs in plants. Genes Dev 2002, 16(13):1616-1626. 10.1101/gad.1004402, 186362, 12101121.
5. Rhoades MW, Reinhart BJ, Lim LP, Burge CB, Bartel B, Bartel DP. Prediction of plant microRNA targets. Cell 2002, 110:513-520. 10.1016/S0092-8674(02)00863-2, 12202040.
6. Bernstein E, Allis CD. RNA meets chromatin. Genes Dev 2005, 19(14):1635-1655. 10.1101/gad.1324305, 16024654.
7. Cantu D, Vanzetti LS, Sumner A, Dubcovsky M, Matvienko M, Distelfeld A, Michelmore RW, Dubcovsky J. Small RNAs, DNA methylation and transposable elements in wheat. BMC Genomics 2010, 11:408. 10.1186/1471-2164-11-408, 2996936, 20584339.
8. Axtell MJ. Classification and comparison of small RNAs from plants. Annu Rev Plant Biol 2013, 64:137-159. 10.1146/annurev-arplant-050312-120043, 23330790.
9. Sunkar R, Chinnusamy V, Zhu J, Zhu JK. Small RNAs as big players in plant abiotic stress responses and nutrient deprivation. Trends Plant Sci 2007, 12(7):301-309. 10.1016/j.tplants.2007.05.001, 17573231.
10. Grant-Downton R, Hafidh S, Twell D, Dickinson HG. Small RNA pathways are present and functional in the angiosperm male gametophyte. Mol Plant 2009, 2(3):500-512. 10.1093/mp/ssp003, 19825633.
11. Olmedo-Monfil V, Duran-Figueroa N, Arteaga-Vazquez M, Demesa-Arevalo E, Autran D, Grimanelli D, Slotkin RK, Martienssen RA, Vielle-Calzada J-P. Control of female gamete formation by a small RNA pathway in Arabidopsis. Nature 2010, 464(11):628-634.
12. Wu G, Park MY, Conway SR, Wang JW, Weigel D, Poethig RS. The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell 2009, 138(4):750-759. 10.1016/j.cell.2009.06.031, 2732587, 19703400.
13. Kim JJ, Lee JH, Kim W, Jung HS, Huijser P, Ahn JH. The microRNA156-SQUAMOSA PROMOTER BINDING PROTEIN-LIKE3 module regulates ambient temperature-responsive flowering via FLOWERING LOCUS T in Arabidopsis. Plant Physiol 2012, 159(1):461-478. 10.1104/pp.111.192369, 3375978, 22427344.
14. Nodine MD, Bartel DP. MicroRNAs prevent precocious gene expression and enable pattern formation during plant embryogenesis. Genes Dev 2010, 24(23):2678-2692. 10.1101/gad.1986710, 2994041, 21123653.
15. Juarez MT, Kui JS, Thomas J, Heller BA, Timmermans MCP. microRNA-mediated repression of rolled leaf1 specifies maize leaf polarity. Nature 2004, 428:84-88. 10.1038/nature02363, 14999285.
16. Achard P, Herr A, Baulcombe DC, Harberd NP. Modulation of floral development by a gibberellin-regulated microRNA. Development 2004, 131(14):3357-3365. 10.1242/dev.01206, 15226253.
17. Aukerman MJ, Sakai H. Regulation of flowering time and floral organ identity by microRNA and its Apatala2-like target gene. Plant Cell 2003, 15(11):2730-2741. 10.1105/tpc.016238, 280575, 14555699.
18. Cartolano M, Castillo R, Efremova N, Kuckenberg M, Zethof J, Gerats T, Schwarz-Sommer Z, Vandenbussche M. A conserved microRNA module exerts homeotic control over Petunia hybrida and Antirrhinum majus floral organ identity. Nat Genet 2007, 39(7):901-905. 10.1038/ng2056, 17589508.
19. Chen X. A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science 2004, 303(5666):2022-2025. 10.1126/science.1088060, 12893888.
20. Yamaguchi A, Wu MF, Yang L, Wu G, Poethig RS, Wagner D. The microRNA-regulated SBP-Box transcription factor SPL3 is a direct upstream activator of LEAFY, FRUITFULL, and APETALA1. Dev Cell 2009, 17(2):268-278. 10.1016/j.devcel.2009.06.007, 2908246, 19686687.
21. Zhao L, Kim Y, Dinh TT, Chen X. miR172 regulates stem cell fate and defines the inner boundary of APETALA3 and PISTILLATA expression domain in Arabidopsis floral meristems. Plant J 2007, 51(5):840-849. 10.1111/j.1365-313X.2007.03181.x, 2629596, 17573799.
22. Banks JA. MicroRNA, sex determination and floral meristem determinacy in maize. Genome Biol 2008, 9(1):204. 10.1186/gb-2008-9-1-204, 2395233, 18254926.
23. Chuck G, Meeley R, Irish E, Sakai H, Hake S. The maize tasselseed4 microRNA controls sex determination and meristem cell fate by targeting Tasselseed6/indeterminate spikelet1. Nat Genet 2007, 39(12):1517-1521. 10.1038/ng.2007.20, 18026103.
24. She X, Xu X, Fedotov A, Kelly WG, Maine EM. Regulation of heterochromatin assembly on unpaired chromosomes during Caenorhabditis elegans meiosis by components of a small RNA-mediated pathway. PLoS Genet 2009, 5(8):e1000624. 10.1371/journal.pgen.1000624, 2726613, 19714217.
25. Carvalho FA, Renner SS. A dated phylogeny of the papaya family (Caricaceae) reveals the crop's closest relatives and the family's biogeographic history. Mol Phylogen Evol 2012, 65(1):46-53.
26. Storey WB. Genetics of the papaya. J Hered 1953, 44:70-78.
27. Ming R, Yu Q, Moore PH. Sex determination in papaya. Semin Cell Dev Biol 2007, 18(3):401-408. 10.1016/j.semcdb.2006.11.013, 17353137.
28. Yu Q, Navajas-Pérez R, Tong E, Robertson J, Moore PH, Paterson AH, Ming R. Recent origin of dioecious and gynodioecious Y chromosomes in papaya. Tropical Plant Biology 2008, 1(1):49-57.
29. Zhang W, Wang X, Yu Q, Ming R, Jiang J. DNA methylation and heterochromatinization in the male-specific region of the primitive Y chromosome of papaya. Genome Res 2008, 18(12):1938-1943. 10.1101/gr.078808.108, 2593574, 18593814.
30. Wang J, Na J-K, Yu Q, Gschwend AR, Han J, Zeng F, Aryal R, VanBuren R, Murray JE, Zhang W, et al. Sequencing papaya X and Yh chromosomes revealed molecular basis of incipient sex chromosome evolution. Proc Natl Acad Sci USA 2012, 109(34):13710-13715. 10.1073/pnas.1207833109, 3427123, 22869747.
31. Gschwend AR, Yu Q, Tong EJ, Zeng F, Han J, VanBuren R, Aryal R, Charlesworth D, Moore PH, Paterson AH, et al. Rapid divergence and expansion of the X chromosome in papaya. Proc Natl Acad Sci USA 2012, 109(34):13716-13721. 10.1073/pnas.1121096109, 3427119, 22869742.
32. Aryal R, Yang X, Yu Q, Sunkar R, Li L, Ming R. Asymmetric purine-pyrimidine distribution in cellular small RNA population of papaya. BMC Genomics 2012, 13:682. 10.1186/1471-2164-13-682, 3582581, 23216749.
33. Aryal R, Ming R. Sex determination in flowering plants: papaya as a model system. Plant Sci 2013, http://dx.doi.org/10.1016/j.plantsci.2013.10.018.
34. Meyers BC, Axtell MJ, Bartel B, Bartel DP, Baulcombe D, Bowman JL, Cao X, Carrington JC, Chen X, Green PJ, et al. Criteria for annotation of plant MicroRNAs. Plant Cell 2008, 20(12):3186-3190. 10.1105/tpc.108.064311, 2630443, 19074682.
35. Porter BW, Aizawa KS, Zhu YJ, Christopher DA. Differentially expressed and new non-protein-coding genes from a Carica papaya root transcriptome survey. Plant Sci 2008, 174(1):38-50.
36. Chen ZH, Bao ML, Sun YZ, Yang YJ, Xu XH, Wang JH, Han N, Bian HW, Zhu MY. Regulation of auxin response by miR393-targeted transport inhibitor response protein 1 is involved in normal development in Arabidopsis. Plant Mol Biol 2011, 77(6):619-629. 10.1007/s11103-011-9838-1, 22042293.
37. Mallory AC, Bartel DP, Bartel B. MicroRNA-directed regulation of Arabidopsis AUXIN RESPONSE FACTOR17 is essential for proper development and modulates expression of early auxin response genes. Plant Cell 2005, 17(5):1360-1375. 10.1105/tpc.105.031716, 1091760, 15829600.
38. Liu Q, Zhang YC, Wang CY, Luo YC, Huang QJ, Chen SY, Zhou H, Qu LH, Chen YQ. Expression analysis of phytohormone-regulated microRNAs in rice, implying their regulation roles in plant hormone signaling. FEBS Lett 2009, 583(4):723-728. 10.1016/j.febslet.2009.01.020, 19167382.
39. Na JK, Wang J, Murray JE, Gschwend AR, Zhang W, Yu Q, Navajas-Perez R, Feltus FA, Chen C, Kubat Z, et al. Construction of physical maps for the sex-specific regions of papaya sex chromosomes. BMC Genomics 2012, 13(1):176. 10.1186/1471-2164-13-176, 3430574, 22568889.
40. Reinhart BJ, Bartel DP. Small RNAs correspond to centromere heterochromatic repeats. Science 2002, 297(5588):1831. 10.1126/science.1077183, 12193644.
41. Yu Q, Hou S, Hobza R, Feltus FA, Wang X, Jin W, Skelton RL, Blas A, Lemke C, Saw JH, et al. Chromosomal location and gene paucity of the male specific region on papaya Y chromosome. Mol Genet Genomics 2007, 278(2):177-185. 10.1007/s00438-007-0243-z, 17520292.
42. Ma H, Moore PH, Liu Z, Kim MS, Yu Q, Fitch MMM, Sekioka T, Paterson AH, Ming R. High-density linkage mapping revealed suppression of recombination at the sex determination locus in papaya. Genetics 2004, 166:419-436. 10.1534/genetics.166.1.419, 1470706, 15020433.
43. Liu Z, Moore PH, Ma H, Ackerman CM, Ragiba M, Yu Q, Pearl HM, Kim MS, Charlton JW, Stiles JI, et al. A primitive Y chromosome in papaya marks incipient sex chromosome evolution. Nature 2004, 427:348-352. 10.1038/nature02228, 14737167.
44. The International Brachypodium Initiative Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature 2010, 463(7282):763-768. 10.1038/nature08747, 20148030, The International Brachypodium Initiative.
45. Lu C, Tej SS, Luo S, Haudenschild CD, Meyers BC, Green PJ. Elucidation of the small RNA component of the transcriptome. Science 2005, 309(5740):1567-1569. 10.1126/science.1114112, 16141074.
46. Lu C, Kulkarni K, Souret FF, MuthuValliappan R, Tej SS, Poethig RS, Henderson IR, Jacobsen SE, Wang W, Green PJ, et al. MicroRNAs and other small RNAs enriched in the Arabidopsis RNA-dependent RNA polymerase-2 mutant. Genome Res 2006, 16(10):1276-1288. 10.1101/gr.5530106, 1581437, 16954541.
47. Hayden KE, Willard HF. Composition and organization of active centromere sequences in complex genomes. BMC Genomics 2012, 13:324. 10.1186/1471-2164-13-324, 3422206, 22817545.
48. Nagaki K, Cheng Z, Ouyang S, Talbert PB, Kim M, Jones KM, Henikoff S, Buell CR, Jiang J. Sequencing of a rice centromere uncovers active genes. Nat Genet 2004, 36(2):138-145. 10.1038/ng1289, 14716315.
49. Kumar LSS, Abraham A, Srinivasan VK. The cytology of Carica papaya Linn. Indian J Agr SCi 1945, 15:242-253.
50. Liu Q, Chen YQ. Insights into the mechanism of plant development: interactions of miRNAs pathway with phytohormone response. Biochem Biophys Res Commun 2009, 384(1):1-5. 10.1016/j.bbrc.2009.04.028, 19366618.
51. Larsson E, Franks RG, Sundberg E. Auxin and the Arabidopsis thaliana gynoecium. J Exp Bot 2013, 64(9):2619-2627. 10.1093/jxb/ert099, 23585670.
52. Geuten K, Irish V. Hidden variability of floral homeotic B genes in Solanaceae provides a molecular basis for the evolution of novel functions. Plant Cell 2010, 22(8):2562-2578. 10.1105/tpc.110.076026, 2947177, 20807882.
53. Mallory AC, Dugas DV, Bartel DP, Bartel B. MicroRNA regulation of NAC-domain targets is required for proper formation and separation of adjacent embryonic, vegetative, and floral organs. Curr Biol 2004, 14(12):1035-1046. 10.1016/j.cub.2004.06.022, 15202996.
54. Jung JH, Park CM. MIR166/165 genes exhibit dynamic expression patterns in regulating shoot apical meristem and floral development in Arabidopsis. Planta 2007, 225(6):1327-1338. 10.1007/s00425-006-0439-1, 17109148.
55. Knauer S, Holt AL, Rubio-Somoza I, Tucker EJ, Hinze A, Pisch M, Javelle M, Timmermans MC, Tucker MR, Laux T. A protodermal miR394 signal defines a region of stem cell competence in the Arabidopsis shoot meristem. Dev Cell 2013, 24(2):125-132. 10.1016/j.devcel.2012.12.009, 23333352.
56. Sunkar R, Zhou X, Zheng Y, Zhang W, Zhu JK. Identification of novel and candidate miRNAs in rice by high throughput sequencing. BMC Plant Biol 2008, 8:25. 10.1186/1471-2229-8-25, 2292181, 18312648.
57. Jagadeeswaran G, Nimmakayala P, Zheng Y, Gowdu K, Reddy UK, Sunkar R. Characterization of the small RNA component of leaves and fruits from four different cucurbit species. BMC Genomics 2012, 13:329. 10.1186/1471-2164-13-329, 3431224, 22823569.
58. Jagadeeswaran G, Zheng Y, Sumathipala N, Jiang H, Arrese EL, Soulages JL, Zhang W, Sunkar R. Deep sequencing of small RNA libraries reveals dynamic regulation of conserved and novel microRNAs and microRNA-stars during silkworm development. BMC Genomics 2010, 11:52. 10.1186/1471-2164-11-52, 2824724, 20089182.
59. Hofacker IL. Vienna RNA secondary structure server. Nucleic Acids Res 2003, 31(13):3429-3431. 10.1093/nar/gkg599, 169005, 12824340.
60. Jones-Rhoades MW, Bartel DP. Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell 2004, 14(6):787-799. 10.1016/j.molcel.2004.05.027, 15200956.