High-Throughput Sequencing of Small RNAs from Pollen and Silk and Characterization of miRNAs as Candidate Factors Involved in Pollen-Silk Interactions in Maize

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Li, Xiao Ming ^a   Sang, Ya Lin ^a   Zhao, Xiang Yu ^a   Zhang, Xian Sheng ^a  

^a SHANDONG AGRICULTURAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AUXIN; MICRORNA; UNCLASSIFIED DRUG; ZMA MICRORNA 156K; ZMA MICRORNA 159H; ZMA MICRORNA 159I; ZMA MICRORNA 160A; ZMA MICRORNA 160B; ZMA MICRORNA 160C; ZMA MICRORNA 160D; ZMA MICRORNA 160E; ZMA MICRORNA 160G; ZMA MICRORNA 162; ZMA MICRORNA 164A; ZMA MICRORNA 164B; ZMA MICRORNA 164C; ZMA MICRORNA 164D; ZMA MICRORNA 164F; ZMA MICRORNA 166G; ZMA MICRORNA 166H; ZMA MICRORNA 166M; ZMA MICRORNA 167A; ZMA MICRORNA 167B; ZMA MICRORNA 167C; ZMA MICRORNA 167D; ZMA MICRORNA 167E; ZMA MICRORNA 390A; ZMA MICRORNA 390B; ZMA MICRORNA 399B; PLANT RNA;

ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE TARGETING; GENETIC ANALYSIS; GENETIC TRANSCRIPTION; HIGH THROUGHPUT SEQUENCING; MAIZE; NONHUMAN; PLANT REPRODUCTION; POLLEN GERMINATION; POLLEN SILK INTERACTION; POLLEN TUBE GROWTH; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SEQUENCE; SIGNAL TRANSDUCTION; GENETICS; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; POLLEN; VALIDATION STUDY;

BASE SEQUENCE; BLOTTING, NORTHERN; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; MICRORNAS; POLLEN; REAL-TIME POLYMERASE CHAIN REACTION; RNA, PLANT; ZEA MAYS; FRAGARIA; FRUIT; GENE EXPRESSION REGULATION, PLANT; GENE LIBRARY; GENOME, PLANT; SIGNAL TRANSDUCTION; TEMPERATURE; TIME FACTORS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84882644109     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0072852     Document Type: Article

References (72)

1. Cheung AY, (1995) Pollen-pistil interactions in compatible pollination. Proc Natl Acad Sci U S A 92: 3077-3080.
2. Hiscock SJ, Allen AM, (2008) Diverse cell signalling pathways regulate pollen-stigma interactions: the search for consensus. New Phytol 179: 286-317.
3. Takayama S, Isogai A, (2005) Self-incompatibility in plants. Annu Rev Plant Biol 56: 467-489.
4. Edlund AF, Swanson R, Preuss D, (2004) Pollen and stigma structure and function: the role of diversity in pollination. Plant Cell 16Suppl: S84-97.
5. Sanchez AM, Bosch M, Bots M, Nieuwland J, Feron R, et al. (2004) Pistil factors controlling pollination. Plant Cell 16Suppl: S98-106.
6. Xu XH, Chen H, Sang YL, Wang F, Ma JP, et al. (2012) Identification of genes specifically or preferentially expressed in maize silk reveals similarity and diversity in transcript abundance of different dry stigmas. BMC Genomics 13: 294.
7. Sang YL, Xu M, Ma FF, Chen H, Xu XH, et al. (2012) Comparative proteomic analysis reveals similar and distinct features of proteins in dry and wet stigmas. Proteomics 12: 1983-1998.
8. Qin Y, Leydon AR, Manziello A, Pandey R, Mount D, et al. (2009) Penetration of the stigma and style elicits a novel transcriptome in pollen tubes, pointing to genes critical for growth in a pistil. PLoS Genet 5: e1000621.
9. Bushati N, Cohen SM, (2007) microRNA functions. Annu Rev Cell Dev Biol 23: 175-205.
10. Voinnet O, (2009) Origin, biogenesis, and activity of plant microRNAs. Cell 136: 669-687.
11. Jones-Rhoades MW, Bartel DP, Bartel B, (2006) MicroRNAS and their regulatory roles in plants. Annu Rev Plant Biol 57: 19-53.
12. Peng T, Sun H, Du Y, Zhang J, Li J, et al. (2013) Characterization and Expression Patterns of microRNAs Involved in Rice Grain Filling. PLoS One 8: e54148.
13. Wei LQ, Yan LF, Wang T, (2011) Deep sequencing on genome-wide scale reveals the unique composition and expression patterns of microRNAs in developing pollen of Oryza sativa. Genome Biol 12: R53.
14. Kang M, Zhao Q, Zhu D, Yu J, (2012) Characterization of microRNAs expression during maize seed development. BMC Genomics 13: 360.
15. Yang J, Liu X, Xu B, Zhao N, Yang X, et al. (2013) Identification of miRNAs and their targets using high-throughput sequencing and degradome analysis in cytoplasmic male-sterile and its maintainer fertile lines of brassica juncea. BMC Genomics 14: 9.
16. Dresselhaus T, Lausser A, Marton ML, (2011) Using maize as a model to study pollen tube growth and guidance, cross-incompatibility and sperm delivery in grasses. Ann Bot 108: 727-737.
17. Zhao M, Tai H, Sun S, Zhang F, Xu Y, et al. (2012) Cloning and characterization of maize miRNAs involved in responses to nitrogen deficiency. PLoS One 7: e29669.
18. Xing S, Salinas M, Hohmann S, Berndtgen R, Huijser P, (2010) miR156-targeted and nontargeted SBP-box transcription factors act in concert to secure male fertility in Arabidopsis. Plant Cell 22: 3935-3950.
19. Wang JW, Czech B, Weigel D, (2009) miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138: 738-749.
20. Yu S, Galvao VC, Zhang YC, Horrer D, Zhang TQ, et al. (2012) Gibberellin regulates the Arabidopsis floral transition through miR156-targeted SQUAMOSA promoter binding-like transcription factors. Plant Cell 24: 3320-3332.
21. Xie K, Wu C, Xiong L, (2006) Genomic organization, differential expression, and interaction of SQUAMOSA promoter-binding-like transcription factors and microRNA156 in rice. Plant Physiol 142: 280-293.
22. Vaucheret H, Vazquez F, Crete P, Bartel DP, (2004) The action of ARGONAUTE1 in the miRNA pathway and its regulation by the miRNA pathway are crucial for plant development. Genes Dev 18: 1187-1197.
23. Vaucheret H, Mallory AC, Bartel DP, (2006) AGO1 homeostasis entails coexpression of MIR168 and AGO1 and preferential stabilization of miR168 by AGO1. Mol Cell 22: 129-136.
24. Schwab R, Palatnik JF, Riester M, Schommer C, Schmid M, et al. (2005) Specific effects of microRNAs on the plant transcriptome. Dev Cell 8: 517-527.
25. Meyers BC, Axtell MJ, Bartel B, Bartel DP, Baulcombe D, et al. (2008) Criteria for annotation of plant MicroRNAs. Plant Cell 20: 3186-3190.
26. Rice P, Longden I, Bleasby A, (2000) EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet 16: 276-277.
27. Jones-Rhoades MW, Bartel DP, (2004) Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell 14: 787-799.
28. Gruber AR, Lorenz R, Bernhart SH, Neubock R, Hofacker IL, (2008) The Vienna RNA websuite. Nucleic Acids Res 36: W70-74.
29. Zhang BH, Pan XP, Cox SB, Cobb GP, Anderson TA, (2006) Evidence that miRNAs are different from other RNAs. Cell Mol Life Sci 63: 246-254.
30. Liu P, Yan K, Lei YX, Xu R, Zhang YM, et al. (2012) Transcript profiling of microRNAs during the early development of the maize brace root via Solexa sequencing. Genomics 101: 149-156.
31. Okamura K, Phillips MD, Tyler DM, Duan H, Chou YT, et al. (2008) The regulatory activity of microRNA* species has substantial influence on microRNA and 3′ UTR evolution. Nat Struct Mol Biol 15: 354-363.
32. Rajagopalan R, Vaucheret H, Trejo J, Bartel DP, (2006) A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana. Genes Dev 20: 3407-3425.
33. Yang JS, Phillips MD, Betel D, Mu P, Ventura A, et al. (2011) Widespread regulatory activity of vertebrate microRNA* species. RNA 17: 312-326.
34. Griffiths-Jones S, Hui JH, Marco A, Ronshaugen M, (2011) MicroRNA evolution by arm switching. EMBO Rep 12: 172-177.
35. Zheng B, Chen X, McCormick S, (2011) The anaphase-promoting complex is a dual integrator that regulates both MicroRNA-mediated transcriptional regulation of cyclin B1 and degradation of Cyclin B1 during Arabidopsis male gametophyte development. Plant Cell 23: 1033-1046.
36. Allen RS, Li J, Alonso-Peral MM, White RG, Gubler F, et al. (2010) MicroR159 regulation of most conserved targets in Arabidopsis has negligible phenotypic effects. Silence 1: 18.
37. Yoon EK, Yang JH, Lim J, Kim SH, Kim SK, et al. (2010) Auxin regulation of the microRNA390-dependent transacting small interfering RNA pathway in Arabidopsis lateral root development. Nucleic Acids Res 38: 1382-1391.
38. Wu JZ, Lin Y, Zhang XL, Pang DW, Zhao J, (2008) IAA stimulates pollen tube growth and mediates the modification of its wall composition and structure in Torenia fournieri. J Exp Bot 59: 2529-2543.
39. Kato N, He H, Steger AP, (2010) A systems model of vesicle trafficking in Arabidopsis pollen tubes. Plant Physiol 152: 590-601.
40. Guo F, McCubbin AG, (2012) The pollen-specific R-SNARE/longin PiVAMP726 mediates fusion of endo- and exocytic compartments in pollen tube tip growth. J Exp Bot 63: 3083-3095.
41. Wu MF, Tian Q, Reed JW, (2006) Arabidopsis microRNA167 controls patterns of ARF6 and ARF8 expression, and regulates both female and male reproduction. Development 133: 4211-4218.
42. Ru P, Xu L, Ma H, Huang H, (2006) Plant fertility defects induced by the enhanced expression of microRNA167. Cell Res 16: 457-465.
43. Nogueira FT, Madi S, Chitwood DH, Juarez MT, Timmermans MC, (2007) Two small regulatory RNAs establish opposing fates of a developmental axis. Genes Dev 21: 750-755.
44. Jung JH, Park CM, (2007) MIR166/165 genes exhibit dynamic expression patterns in regulating shoot apical meristem and floral development in Arabidopsis. Planta 225: 1327-1338.
45. Zhu H, Hu F, Wang R, Zhou X, Sze SH, et al. (2011) Arabidopsis Argonaute10 specifically sequesters miR166/165 to regulate shoot apical meristem development. Cell 145: 242-256.
46. Wang L, Gu X, Xu D, Wang W, Wang H, et al. (2011) miR396-targeted AtGRF transcription factors are required for coordination of cell division and differentiation during leaf development in Arabidopsis. J Exp Bot 62: 761-773.
47. Zhao B, Ge L, Liang R, Li W, Ruan K, et al. (2009) Members of miR-169 family are induced by high salinity and transiently inhibit the NF-YA transcription factor. BMC Mol Biol 10: 29.
48. Li WX, Oono Y, Zhu J, He XJ, Wu JM, et al. (2008) The Arabidopsis NFYA5 transcription factor is regulated transcriptionally and posttranscriptionally to promote drought resistance. Plant Cell 20: 2238-2251.
49. Hwang EW, Shin SJ, Yu BK, Byun MO, Kwon HB, (2011) miR171 Family Members are Involved in Drought Response in Solanum tuberosum. J Plant Biol 54: 43-48.
50. Kantar M, Lucas SJ, Budak H, (2011) miRNA expression patterns of Triticum dicoccoides in response to shock drought stress. Planta 233: 471-484.
51. Xia K, Wang R, Ou X, Fang Z, Tian C, et al. (2012) OsTIR1 and OsAFB2 downregulation via OsmiR393 overexpression leads to more tillers, early flowering and less tolerance to salt and drought in rice. PLoS One 7: e30039.
52. Frazier TP, Sun G, Burklew CE, Zhang B, (2011) Salt and drought stresses induce the aberrant expression of microRNA genes in tobacco. Mol Biotechnol 49: 159-165.
53. Ferreira TH, Gentile A, Vilela RD, Costa GG, Dias LI, et al. (2012) microRNAs associated with drought response in the bioenergy crop sugarcane (Saccharum spp.). PLoS One 7: e46703.
54. Zhang X, Zou Z, Gong P, Zhang J, Ziaf K, et al. (2011) Over-expression of microRNA169 confers enhanced drought tolerance to tomato. Biotechnol Lett 33: 403-409.
55. Gupta OP, Permar V, Koundal V, Singh UD, Praveen S, (2012) MicroRNA regulated defense responses in Triticum aestivum L. during Puccinia graminis f.sp. tritici infection. Mol Biol Rep 39: 817-824.
56. Zhao JP, Jiang XL, Zhang BY, Su XH, (2012) Involvement of microRNA-mediated gene expression regulation in the pathological development of stem canker disease in Populus trichocarpa. PLoS One 7: e44968.
57. Yin X, Wang J, Cheng H, Wang X, Yu D (2012) Detection and evolutionary analysis of soybean miRNAs responsive to soybean mosaic virus. Planta.
58. Kasschau KD, Xie Z, Allen E, Llave C, Chapman EJ, et al. (2003) P1/HC-Pro, a viral suppressor of RNA silencing, interferes with Arabidopsis development and miRNA unction. Dev Cell 4: 205-217.
59. Lan L, Li M, Lai Y, Xu W, Kong Z, et al. (2005) Microarray analysis reveals similarities and variations in genetic programs controlling pollination/fertilization and stress responses in rice (Oryza sativa L.). Plant Mol Biol 59: 151-164.
60. Quiapim AC, Brito MS, Bernardes LA, Dasilva I, Malavazi I, et al. (2009) Analysis of the Nicotiana tabacum stigma/style transcriptome reveals gene expression differences between wet and dry stigma species. Plant Physiol 149: 1211-1230.
61. Kessler SA, Shimosato-Asano H, Keinath NF, Wuest SE, Ingram G, et al. (2010) Conserved molecular components for pollen tube reception and fungal invasion. Science 330: 968-971.
62. Dawkins MD, Owens JN, (1993) In Vitro and in Vivo Pollen Hydration, Germination, and Pollen-Tube Growth in White Spruce, Picea Glauca (Moench) Voss. Int J Plant Sci 154: 506-521.
63. Du Z, Zhou X, Ling Y, Zhang Z, Su Z, (2010) agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res 38: W64-70.
64. Liu X, Huang J, Wang Y, Khanna K, Xie Z, et al. (2010) The role of floral organs in carpels, an Arabidopsis loss-of-function mutation in MicroRNA160a, in organogenesis and the mechanism regulating its expression. Plant J 62: 416-428.
65. Si-Ammour A, Windels D, Arn-Bouldoires E, Kutter C, Ailhas J, et al. (2011) miR393 and secondary siRNAs regulate expression of the TIR1/AFB2 auxin receptor clade and auxin-related development of Arabidopsis leaves. Plant Physiol 157: 683-691.
66. Windels D, Vazquez F, (2011) miR393: integrator of environmental cues in auxin signaling? Plant Signal Behav 6: 1672-1675.
67. Schreiber DN, Bantin J, Dresselhaus T, (2004) The MADS box transcription factor ZmMADS2 is required for anther and pollen maturation in maize and accumulates in apoptotic bodies during anther dehiscence. Plant Physiol 134: 1069-1079.
68. Liu S, Li D, Li Q, Zhao P, Xiang Z, et al. (2010) MicroRNAs of Bombyx mori identified by Solexa sequencing. BMC Genomics 11: 148.
69. Gardner PP, Daub J, Tate JG, Nawrocki EP, Kolbe DL, et al. (2009) Rfam: updates to the RNA families database. Nucleic Acids Res 37: D136-D140.
70. Wang T, Chen L, Zhao M, Tian Q, Zhang WH, (2011) Identification of drought-responsive microRNAs in Medicago truncatula by genome-wide high-throughput sequencing. BMC Genomics 12: 367.
71. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-ΔΔC(T)) Method. Methods 25: 402-408.
72. Romualdi C, Bortoluzzi S, D′Alessi F, Danieli GA, (2003) IDEG6: a web tool for detection of differentially expressed genes in multiple tag sampling experiments. Physiol Genomics. 12: 159-62.