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Investigating the MicroRNAomes of Two Developmental Phases of Dendrocalamus latiflorus (Poaceae: Bambusoideae) Inflorescences

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Abstract

Plant microRNAs (miRNAs) play important roles in various developmental and physiological processes (e.g. seed germination, vegetative growth, flowering, seed production, and responses to abiotic or biotic stimuli) by targeting mRNAs for cleavage or translational repression at the post-transcriptional level. Bamboo flowering is an unusual physiological phenomenon relative to the typical graminaceous plants. In this study, we focused on the microRNAome of developing Dendrocalamus latiflorus inflorescences. Solexa high-throughput small RNA (sRNA) sequencing technology was used to sequence and quantify the miRNAs expressed during two phases of D. latiflorus flower development. A total of 118 conserved miRNAs and 47 novel miRNAs was identified in the developing flowers. The transcript levels of most of the miRNAs were similar between the two phases. However, five miRNAs showed distinct changes as the flowering developed, with the novel miRNA dla-miR18 in particular showing a large difference in transcript abundance between the two phases. Fifteen of the D. latiflorus miRNAs found in this study appeared likely to be specific to flower development. Moreover, 130 of the floral unigenes of D. latiflorus were determined to be putative targets of the miRNAs, and the miRNA cleavage sites of seven of these putative targets were validated by 5′-RACE. The results of this study provide the first broad survey of the microRNAomes of Bambusoideae and yield valuable insights into the potential roles of microRNAs in bamboo inflorescence development. Our findings represent a starting point for future functional research on the role of miRNA in the flower development in D. latiflorus and related species.

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Abbreviations

AGO:

Argonaute

ath:

Arabidopsis thaliana

bdi:

Brachypodium distachyon

DCL:

Dicer-like

dla:

Dendrocalamus latiflorus

gma:

Glycine max

miRNA:

microRNA

nat-miRNA:

Natural antisense microRNA

NGS:

Next generation sequencing

osa:

Oryza sativa

ptc:

Populus trichocarpa

qRT-PCR:

Quantitative RT-PCR

RACE:

Rapid amplification of complementary DNA ends

sbi:

Sorghum bicolor

siRNA:

Small interfering RNA

sRNA:

Small RNA

tasiRNA:

Transacting siRNA

zma:

Zea mays

References

  • Addo-Quaye C, Eshoo TW, Bartel DP, Axtell MJ (2008) Endogenous siRNA and miRNA targets identified by sequencing of the Arabidopsis degradome. Curr Biol 18(10):758–762. doi:10.1016/j.cub.2008.04.042

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Aliscioni S, Bell HL, Besnard G, Christin PA, Columbus JT, Duvall MR, Edwards EJ, Giussani L, Hasenstab-Lehman K, Hilu KW, Hodkinson TR, Ingram AL, Kellogg EA, Mashayekhi S, Morrone O, Osborne CP, Salamin N, Schaefer H, Spriggs E, Smith SA, Zuloaga F II, GPWG (2012) New grass phylogeny resolves deep evolutionary relationships and discovers C4 origins. New Phytol 193(2):304–312. doi:10.1111/j.1469-8137.2011.03972.x

    Article  CAS  Google Scholar 

  • Ambros V, Bartel B, Bartel DP, Burge CB, Carrington JC, Chen XM, Dreyfuss G, Eddy SR, Griffiths-Jones S, Marshall M, Matzke M, Ruvkun G, Tuschl T (2003) A uniform system for microRNA annotation. RNA 9(3):277–279. doi:10.1261/Rna.2183803

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Aukerman MJ, Sakai H (2003) Regulation of flowering time and floral organ identity by a microRNA and its APETALA2-like target genes. Plant Cell Online 15(11):2730–2741. doi:10.1105/tpc.016238

    Article  CAS  Google Scholar 

  • Axtell MJ, Snyder JA, Bartell DP (2007) Common functions for diverse small RNAs of land plants. Plant Cell 19(6):1750–1769. doi:10.1105/tpc.107.051706

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Axtell MJ, Westholm JO, Lai EC (2011) Vive la difference: biogenesis and evolution of microRNAs in plants and animals. Genome Biol 12 (4). doi:10.1186/Gb-2011-12-4-221

  • Baccarelli A, Bollati V (2009) Epigenetics and environmental chemicals. Curr Opin Pediatr 21(2):243–251. doi:10.1097/MOP.0b013e32832925cc

    Article  PubMed Central  PubMed  Google Scholar 

  • Baker CC, Sieber P, Wellmer F, Meyerowitz EM (2005) The early extra petals1 mutant uncovers a role for microRNA miR164c in regulating petal number in Arabidopsis. Curr Biol 15(4):303–315. doi:10.1016/j.cub.2005.02.017

  • Bedell JA, Budiman MA, Nunberg A, Citek RW, Robbins D, Jones J, Flick E, Rohlfing T, Fries J, Bradford K, McMenamy J, Smith M, Holeman H, Roe BA, Wiley G, Korf IF, Rabinowicz PD, Lakey N, McCombie WR, Jeddeloh JA, Martienssen RA (2005) Sorghum genome sequencing by methylation filtration. Plos Biol 3(1):103–115. doi:10.1371/journal.pbio.0030013

    Article  Google Scholar 

  • Bennetzen JL, Schmutz J, Wang H, Percifield R, Hawkins J, Pontaroli AC, Estep M, Feng L, Vaughn JN, Grimwood J, Jenkins J, Barry K, Lindquist E, Hellsten U, Deshpande S, Wang XW, Wu XM, Mitros T, Triplett J, Yang XH, Ye CY, Mauro-Herrera M, Wang L, Li PH, Sharma M, Sharma R, Ronald PC, Panaud O, Kellogg EA, Brutnell TP, Doust AN, Tuskan GA, Rokhsar D, Devos KM (2012) Reference genome sequence of the model plant Setaria. Nat Biotechnol 30(6):555–561. doi:10.1038/Nbt.2196

    Article  CAS  PubMed  Google Scholar 

  • Bonnet E, Van de Peer Y, Rouze P (2006) The small RNA world of plants. New Phytol 171(3):451–468. doi:10.1111/j.1469-8137.2006.01806.x

    Article  CAS  PubMed  Google Scholar 

  • Borsani O, Zhu JH, Verslues PE, Sunkar R, Zhu JK (2005) Endogenous siRNAs derived from a pair of natural cis-antisense transcripts regulate salt tolerance in Arabidopsis. Cell 123(7):1279–1291. doi:10.1016/j.cell.2005.11.035

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Carrington JC, Ambros V (2003) Role of microRNAs in plant and animal development. Science 301(5631):336–338. doi:10.1126/science.1085242

    Article  CAS  PubMed  Google Scholar 

  • Chen X (2004) A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science 303(5666):2022–2025. doi:10.1126/science.1088060

    Article  CAS  PubMed  Google Scholar 

  • Chen CF, Ridzon DA, Broomer AJ, Zhou ZH, Lee DH, Nguyen JT, Barbisin M, Xu NL, Mahuvakar VR, Andersen MR, Lao KQ, Livak KJ, Guegler KJ (2005) Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Res 33(20):e179. doi:10.1093/nar/gni178

    Article  PubMed Central  PubMed  Google Scholar 

  • Chotard L, Mishra AK, Sylvain MA, Tuck S, Lambright DG, Rocheleau CE (2010) TBC-2 regulates RAB-5/RAB-7-mediated endosomal trafficking in Caenorhabditis elegans. Mol Biol Cell 21(13):2285–2296. doi:10.1091/mbc.E09-11-0947

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Coen ES, Meyerowitz EM (1991) The war of the whorls: genetic interactions controlling flower development. Nature 353(6339):31–37. doi:10.1038/353031a0

    Article  CAS  PubMed  Google Scholar 

  • Cuperus JT, Fahlgren N, Carrington JC (2011) Evolution and functional diversification of MIRNA genes. Plant Cell Online 23(2):431–442. doi:10.1105/tpc.110.082784

    Article  CAS  Google Scholar 

  • Dai XB, Zhao PX (2011) psRNATarget: a plant small RNA target analysis server. Nucleic Acids Res 39:W155–W159. doi:10.1093/Nar/Gkr319

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Dellaporta SL, Calderonurrea A (1994) The sex determination process in maize. Science 266(5190):1501–1505. doi:10.1126/science.7985019

    Article  CAS  PubMed  Google Scholar 

  • Devers EA, Branscheid A, May P, Krajinski F (2011) Stars and symbiosis: microRNA- and microRNA*-mediated transcript cleavage involved in arbuscular mycorrhizal symbiosis. Plant Physiol 156(4):1990–2010. doi:10.1104/pp. 111.172627

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ding Y, Chen Z, Zhu C (2011) Microarray-based analysis of cadmium-responsive microRNAs in rice (Oryza sativa). J Exp Bot 62(10):3563–3573

  • Doench JG, Petersen CP, Sharp PA (2003) siRNAs can function as miRNAs. Gene Dev 17(4):438–442. doi:10.1101/Gad.1064703

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Exner V, Hirsch-Hoffmann M, Gruissem W, Hennig L (2008) PlantDB—a versatile database for managing plant research. Plant Methods 4. doi:10.1186/1746-4811-4-1

  • German MA, Pillay M, Jeong DH, Hetawal A, Luo SJ, Janardhanan P, Kannan V, Rymarquis LA, Nobuta K, German R, De Paoli E, Lu C, Schroth G, Meyers BC, Green PJ (2008) Global identification of microRNA-target RNA pairs by parallel analysis of RNA ends. Nat Biotechnol 26(8):941–946. doi:10.1038/nbt1417

    Article  CAS  PubMed  Google Scholar 

  • Goff SA, Ricke D, Lan TH, Presting G, Wang RL, Dunn M, Glazebrook J, Sessions A, Oeller P, Varma H, Hadley D, Hutchinson D, Martin C, Katagiri F, Lange BM, Moughamer T, Xia Y, Budworth P, Zhong JP, Miguel T, Paszkowski U, Zhang SP, Colbert M, Sun WL, Chen LL, Cooper B, Park S, Wood TC, Mao L, Quail P, Wing R, Dean R, Yu YS, Zharkikh A, Shen R, Sahasrabudhe S, Thomas A, Cannings R, Gutin A, Pruss D, Reid J, Tavtigian S, Mitchell J, Eldredge G, Scholl T, Miller RM, Bhatnagar S, Adey N, Rubano T, Tusneem N, Robinson R, Feldhaus J, Macalma T, Oliphant A, Briggs S (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296(5565):92–100. doi:10.1126/science.1068275

    Article  CAS  PubMed  Google Scholar 

  • Johnson C, Kasprzewska A, Tennessen K, Fernandes J, Nan GL, Walbot V, Sundaresan V, Vance V, Bowman LH (2009) Clusters and superclusters of phased small RNAs in the developing inflorescence of rice. Genome Res 19(8):1429–1440. doi:10.1101/gr.089854.108

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jones-Rhoades MW, Bartel DP, Bartel B (2006) MicroRNAs and their regulatory roles in plants. Annu Rev Plant Biol 57:19–53. doi:10.1146/annurev.arplant.57.032905.105218

    Article  CAS  PubMed  Google Scholar 

  • Kong Y, Han JH (2005) MicroRNA: biological and computational perspective. Genomics Proteom Bioinforma 3(2):62–72

    CAS  Google Scholar 

  • Kurihara Y, Watanabe Y (2004) Arabidopsis micro-RNA biogenesis through Dicer-like 1 protein functions. Proc Natl Acad Sci USA 101(34):12753–12758. doi:10.1073/pnas.0403115101

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Liang CW, Zhang XW, Zou J, Xu D, Su F, Ye NH (2010) Identification of miRNA from Porphyra yezoensis by high-throughput sequencing and bioinformatics analysis. Plos One 5 (5):-. doi 10.1371/journal.pone.0010698

  • Lin SL, Miller JD, Ying SY (2006) Intronic microRNA (miRNA). J Biomed Biotechnol 2006(4):26818. doi:10.1155/JBB/2006/26818

    PubMed Central  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25(4):402–408

    Article  CAS  PubMed  Google Scholar 

  • Llave C, Kasschau KD, Rector MA, Carrington JC (2002) Endogenous and silencing-associated small RNAs in plants. Plant Cell 14(7):1605–1619. doi:10.1105/Tpc.003210

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lu C, Jeong DH, Kulkarni K, Pillay M, Nobuta K, German R, Thatcher SR, Maher C, Zhang L, Ware D, Liu B, Cao X, Meyers BC, Green PJ (2008) Genome-wide analysis for discovery of rice microRNAs reveals natural antisense microRNAs (nat-miRNAs). Proc Natl Acad Sci USA 105(12):4951–4956. doi:10.1073/pnas.0708743105

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Merchan F, Boualem A, Crespi M, Frugier F (2009) Plant polycistronic precursors containing non-homologous microRNAs target transcripts encoding functionally related proteins. Genome Biol 10(12):R136. doi:10.1186/Gb-2009-10-12-R136

  • Meyers BC, Tej SS, Vu TH, Haudenschild CD, Agrawal V, Edberg SB, Ghazal H, Decola S (2004) The use of MPSS for whole-genome transcriptional analysis in Arabidopsis. Genome Res 14(8):1641–1653. doi:10.1101/Gr.2275604

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Morin RD, Aksay G, Dolgosheina E, Ebhardt HA, Magrini V, Mardis ER, Sahinalp SC, Unrau PJ (2008) Comparative analysis of the small RNA transcriptomes of Pinus contorta and Oryza sativa. Genome Res 18(4):571–584. doi:10.1101/Gr.6897308

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Moxon S, Jing RC, Szittya G, Schwach F, Pilcher RLR, Moulton V, Dalmay T (2008) Deep sequencing of tomato short RNAs identifies microRNAs targeting genes involved in fruit ripening. Genome Res 18(10):1602–1609. doi:10.1101/gr.080127.108

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nelson DC, Lasswell J, Rogg LE, Cohen MA, Bartel B (2000) FKF1, a clock-controlled gene that regulates the transition to flowering in Arabidopsis. Cell 101(3):331–340. doi:10.1016/S0092-8674(00)80842-9

    Article  CAS  PubMed  Google Scholar 

  • Pant BD, Musialak-Lange M, Nuc P, May P, Buhtz A, Kehr J, Walther D, Scheible WR (2009) Identification of nutrient-responsive Arabidopsis and rapeseed microRNAs by comprehensive real-time polymerase chain reaction profiling and small RNA sequencing. Plant Physiol 150(3):1541–1555. doi:10.1104/pp. 109.139139

    Article  PubMed Central  PubMed  Google Scholar 

  • Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, Haberer G, Hellsten U, Mitros T, Poliakov A, Schmutz J, Spannagl M, Tang HB, Wang XY, Wicker T, Bharti AK, Chapman J, Feltus FA, Gowik U, Grigoriev IV, Lyons E, Maher CA, Martis M, Narechania A, Otillar RP, Penning BW, Salamov AA, Wang Y, Zhang LF, Carpita NC, Freeling M, Gingle AR, Hash CT, Keller B, Klein P, Kresovich S, McCann MC, Ming R, Peterson DG, Mehboob-ur-Rahman, Ware D, Westhoff P, Mayer KFX, Messing J, Rokhsar DS (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457(7229):551–556. doi:10.1038/Nature07723

    Article  CAS  PubMed  Google Scholar 

  • Peng ZH, Lu TT, Li LB, Liu XH, Gao ZM, Hu T, Yang XW, Feng Q, Guan JP, Weng QJ, Fan DL, Zhu CR, Lu Y, Han B, Jiang ZH (2010) Genome-wide characterization of the biggest grass, bamboo, based on 10,608 putative full-length cDNA sequences. BMC Plant Biol 10. doi:10.1186/1471-2229-10-116

  • Peng Z, Lu Y, Li L, Zhao Q, Feng Q, Gao Z, Lu H, Hu T, Yao N, Liu K (2013) The draft genome of the fast-growing non-timber forest species moso bamboo (Phyllostachys heterocycla). Nat Genet. doi:10.1038/ng.2569

    Google Scholar 

  • Pennell RI, Lamb C (1997a) Programmed cell death in plants. Plant Cell 9(7):1157–1168. doi:10.1105/tpc.9.7.1157

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Poethig RS (2009) Small RNAs and developmental timing in plants. Curr Opin Genet Dev 19(4):374–378. doi:10.1016/j.gde.2009.06.001

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Purugganan MD, Rounsley SD, Schmidt RJ, Yanofsky MF (1995) Molecular evolution of flower development: diversification of the plant MADS-box regulatory gene family. Genetics 140(1):345–356

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rajagopalan R, Vaucheret H, Trejo J, Bartel DP (2006) A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana. Genes Dev 20(24):3407–3425. doi:10.1101/Gad.1476406

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Reinhart BJ, Weinstein EG, Rhoades MW, Bartel B, Bartel DP (2002) MicroRNAs in plants. Genes Dev 16(13):1616–1626. doi:10.1101/gad.1004402

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rhoades MW, Reinhart BJ, Lim LP, Burge CB, Bartel B, Bartel DP (2002) Prediction of plant microRNA targets. Cell 110(4):513–520. doi:10.1016/S0092-8674(02)00863-2

    Article  CAS  PubMed  Google Scholar 

  • Schmid M, Uhlenhaut NH, Godard F, Demar M, Bressan R, Weigel D, Lohmann JU (2003) Dissection of floral induction pathways using global expression analysis. Development 130(24):6001–6012. doi:10.1242/dev.00842

    Article  CAS  PubMed  Google Scholar 

  • Schnable PS, Ware D, Fulton RS, Stein JC, Wei FS, Pasternak S, Liang CZ, Zhang JW, Fulton L, Graves TA, Minx P, Reily AD, Courtney L, Kruchowski SS, Tomlinson C, Strong C, Delehaunty K, Fronick C, Courtney B, Rock SM, Belter E, Du FY, Kim K, Abbott RM, Cotton M, Levy A, Marchetto P, Ochoa K, Jackson SM, Gillam B, Chen WZ, Yan L, Higginbotham J, Cardenas M, Waligorski J, Applebaum E, Phelps L, Falcone J, Kanchi K, Thane T, Scimone A, Thane N, Henke J, Wang T, Ruppert J, Shah N, Rotter K, Hodges J, Ingenthron E, Cordes M, Kohlberg S, Sgro J, Delgado B, Mead K, Chinwalla A, Leonard S, Crouse K, Collura K, Kudrna D, Currie J, He RF, Angelova A, Rajasekar S, Mueller T, Lomeli R, Scara G, Ko A, Delaney K, Wissotski M, Lopez G, Campos D, Braidotti M, Ashley E, Golser W, Kim H, Lee S, Lin JK, Dujmic Z, Kim W, Talag J, Zuccolo A, Fan C, Sebastian A, Kramer M, Spiegel L, Nascimento L, Zutavern T, Miller B, Ambroise C, Muller S, Spooner W, Narechania A, Ren LY, Wei S, Kumari S, Faga B, Levy MJ, McMahan L, Van Buren P, Vaughn MW, Ying K, Yeh CT, Emrich SJ, Jia Y, Kalyanaraman A, Hsia AP, Barbazuk WB, Baucom RS, Brutnell TP, Carpita NC, Chaparro C, Chia JM, Deragon JM, Estill JC, Fu Y, Jeddeloh JA, Han YJ, Lee H, Li PH, Lisch DR, Liu SZ, Liu ZJ, Nagel DH, McCann MC, SanMiguel P, Myers AM, Nettleton D, Nguyen J, Penning BW, Ponnala L, Schneider KL, Schwartz DC, Sharma A, Soderlund C, Springer NM, Sun Q, Wang H, Waterman M, Westerman R, Wolfgruber TK, Yang LX, Yu Y, Zhang LF, Zhou SG, Zhu Q, Bennetzen JL, Dawe RK, Jiang JM, Jiang N, Presting GG, Wessler SR, Aluru S, Martienssen RA, Clifton SW, McCombie WR, Wing RA, Wilson RK (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326(5956):1112–1115. doi:10.1126/science.1178534

    Article  CAS  PubMed  Google Scholar 

  • Schreiber AW, Shi BJ, Huang CY, Langridge P, Baumann U (2011) Discovery of barley miRNAs through deep sequencing of short reads. BMC Genomics 12. doi:10.1186/1471-2164-12-129

  • Seggerson K, Tang LJ, Moss EG (2002) Two genetic circuits repress the Caenorhabditis elegans heterochronic gene lin-28 after translation initiation. Dev Biol 243(2):215–225. doi:10.1006/dbio.2001.0563

    Article  CAS  PubMed  Google Scholar 

  • Sikand K, Slaibi JE, Singh R, Slane SD, Shukla GC (2011) miR 488(star) inhibits androgen receptor expression in prostate carcinoma cells. Int J Cancer 129(4):810–819. doi:10.1002/Ijc.25753

    Article  CAS  PubMed  Google Scholar 

  • Sun L-M, Ai X-Y, Li W-Y, Guo W-W, Deng X-X, Hu C-G, Zhang J-Z (2012) Identification and comparative profiling of miRNAs in an early flowering mutant of trifoliate orange and its wild type by genome-wide deep sequencing. PLoS ONE 7(8):e43760. doi:10.1371/journal.pone.0043760

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sunkar R, Girke T, Jain PK, Zhu J-K (2005) Cloning and characterization of microRNAs from rice. Plant Cell Online 17(5):1397–1411. doi:10.1105/tpc.105.031682

    Article  CAS  Google Scholar 

  • Szittya G, Moxon S, Santos DM, Jing R, Fevereiro MPS, Moulton V, Dalmay T (2008) High-throughput sequencing of Medicago truncatula short RNAs identifies eight new miRNA families. BMC Genomics 9. doi:10.1186/1471-2164-9-593

  • Tsuji H, Aya K, Ueguchi–Tanaka M, Shimada Y, Nakazono M, Watanabe R, Nishizawa NK, Gomi K, Shimada A, Kitano H (2006) GAMYB controls different sets of genes and is differentially regulated by microRNA in aleurone cells and anthers. Plant J 47(3):427–444. doi:10.1111/j.1365-313X.2006.02795.x

    Article  CAS  PubMed  Google Scholar 

  • Unver T, Budak H (2009) Conserved microRNAs and their targets in model grass species Brachypodium distachyon. Planta 230(4):659–669. doi:10.1007/s00425-009-0974-7

    Article  CAS  PubMed  Google Scholar 

  • 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(1):129–136. doi:10.1016/j.molcel.2006.03.011

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Vogel JP, Garvin DF, Mockler TC, Schmutz J, Rokhsar D, Bevan MW, Barry K, Lucas S, Harmon-Smith M, Lail K, Tice H, Grimwood J, McKenzie N, Huo NX, Gu YQ, Lazo GR, Anderson OD, You FM, Luo MC, Dvorak J, Wright J, Febrer M, Idziak D, Hasterok R, Lindquist E, Wang M, Fox SE, Priest HD, Filichkin SA, Givan SA, Bryant DW, Chang JH, Wu HY, Wu W, Hsia AP, Schnable PS, Kalyanaraman A, Barbazuk B, Michael TP, Hazen SP, Bragg JN, Laudencia-Chingcuanco D, Weng YQ, Haberer G, Spannagl M, Mayer K, Rattei T, Mitros T, Lee SJ, Rose JKC, Mueller LA, York TL, Wicker T, Buchmann JP, Tanskanen J, Schulman AH, Gundlach H, de Oliveira AC, Maia LD, Belknap W, Jiang N, Lai JS, Zhu LC, Ma JX, Sun C, Pritham E, Salse J, Murat F, Abrouk M, Bruggmann R, Messing J, Fahlgren N, Sullivan CM, Carrington JC, Chapman EJ, May GD, Zhai JX, Ganssmann M, Gurazada SGR, German M, Meyers BC, Green PJ, Tyler L, Wu JJ, Thomson J, Chen S, Scheller HV, Harholt J, Ulvskov P, Kimbrel JA, Bartley LE, Cao PJ, Jung KH, Sharma MK, Vega-Sanchez M, Ronald P, Dardick CD, De Bodt S, Verelst W, Inze D, Heese M, Schnittger A, Yang XH, Kalluri UC, Tuskan GA, Hua ZH, Vierstra RD, Cui Y, Ouyang SH, Sun QX, Liu ZY, Yilmaz A, Grotewold E, Sibout R, Hematy K, Mouille G, Hofte H, Pelloux J, O'Connor D, Schnable J, Rowe S, Harmon F, Cass CL, Sedbrook JC, Byrne ME, Walsh S, Higgins J, Li PH, Brutnell T, Unver T, Budak H, Belcram H, Charles M, Chalhoub B, Baxter I, Initiative IB (2010) Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature 463(7282):763–768. doi:10.1038/Nature08747

    Article  CAS  Google Scholar 

  • Voinnet O (2009) Origin, biogenesis, and activity of plant microRNAs. Cell 136(4):669–687. doi:10.1016/j.cell.2009.01.046

    Article  CAS  PubMed  Google Scholar 

  • Wang J-W, Czech B, Weigel D (2009) miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138(4):738–749. doi:10.1016/j.cell.2009.06.014

    Article  CAS  PubMed  Google Scholar 

  • 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. doi:10.1186/1471-2164-12-367

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wang ZJ, Huang JQ, Huang YJ, Li Z, Zheng BS (2012) Discovery and profiling of novel and conserved microRNAs during flower development in Carya cathayensis via deep sequencing. Planta 236(2):613–621. doi:10.1007/s00425-012-1634-x

    Article  CAS  PubMed  Google Scholar 

  • Wei B, Cai T, Zhang RZ, Li AL, Huo NX, Li S, Gu YQ, Vogel J, Jia JZ, Qi YJ, Mao L (2009a) Novel microRNAs uncovered by deep sequencing of small RNA transcriptomes in bread wheat (Triticum aestivum L.) and Brachypodium distachyon (L.) Beauv. Funct Integr Genom 9(4):499–511. doi:10.1007/s10142-009-0128-9

    Article  CAS  Google Scholar 

  • Wei YY, Chen S, Yang PC, Ma ZY, Kang L (2009b) Characterization and comparative profiling of the small RNA transcriptomes in two phases of locust. Genome Biol 10 (1). doi:10.1186/Gb-2009-10-1-R6

  • 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 (6). doi:10.1186/Gb-2011-12-6-R53

  • Wheeler BM, Heimberg AM, Moy VN, Sperling EA, Holstein TW, Heber S, Peterson KJ (2009) The deep evolution of metazoan microRNAs. Evol Dev 11(1):50–68. doi:10.1111/j.1525-142X.2008.00302.x

    Article  CAS  PubMed  Google Scholar 

  • Wollmann H, Weigel D (2010) Small RNAs in flower development. Eur J Cell Biol 89(2):250–257. doi:10.1016/j.ejcb.2009.11.004

    Article  CAS  PubMed  Google Scholar 

  • Wu G, Park MY, Conway SR, Wang J-W, Weigel D, Poethig RS (2009a) The sequential action of miR156 and miR172 regulates developmental timing in  Arabidopsis. Cell 138(4):750–759. doi:10.1016/j.cell.2009.06.031

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wu L, Zhang QQ, Zhou HY, Ni FR, Wu XY, Qi YJ (2009b) Rice MicroRNA effector complexes and targets. Plant Cell 21(11):3421–3435. doi:10.1105/tpc.109.070938

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Xie K, Shen J, Hou X, Yao J, Li X, Xiao J, Xiong L (2012) Gradual increase of miR156 regulates temporal expression changes of numerous genes during leaf development in rice. Plant Physiol 158(3):1382–1394. doi:10.1104/pp. 111.190488

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yao Y, Guo G, Ni Z, Sunkar R, Du J, Zhu JK, Sun Q (2007) Cloning and characterization of microRNAs from wheat (Triticum aestivum L.). Genome Biol 8(6):R96

    Article  PubMed Central  PubMed  Google Scholar 

  • Yeung EC, Meinke DW (1993) Embryogenesis in angiosperms—development of the suspensor. Plant Cell 5(10):1371–1381

    Article  PubMed Central  PubMed  Google Scholar 

  • Yu J, Hu SN, Wang J, Wong GKS, Li SG, Liu B, Deng YJ, Dai L, Zhou Y, Zhang XQ, Cao ML, Liu J, Sun JD, Tang JB, Chen YJ, Huang XB, Lin W, Ye C, Tong W, Cong LJ, Geng JN, Han YJ, Li L, Li W, Hu GQ, Huang XG, Li WJ, Li J, Liu ZW, Li L, Liu JP, Qi QH, Liu JS, Li L, Li T, Wang XG, Lu H, Wu TT, Zhu M, Ni PX, Han H, Dong W, Ren XY, Feng XL, Cui P, Li XR, Wang H, Xu X, Zhai WX, Xu Z, Zhang JS, He SJ, Zhang JG, Xu JC, Zhang KL, Zheng XW, Dong JH, Zeng WY, Tao L, Ye J, Tan J, Ren XD, Chen XW, He J, Liu DF, Tian W, Tian CG, Xia HG, Bao QY, Li G, Gao H, Cao T, Wang J, Zhao WM, Li P, Chen W, Wang XD, Zhang Y, Hu JF, Wang J, Liu S, Yang J, Zhang GY, Xiong YQ, Li ZJ, Mao L, Zhou CS, Zhu Z, Chen RS, Hao BL, Zheng WM, Chen SY, Guo W, Li GJ, Liu SQ, Tao M, Wang J, Zhu LH, Yuan LP, Yang HM (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science 296(5565):79–92. doi:10.1126/science.1068037

    Article  CAS  PubMed  Google Scholar 

  • Yu N, Cai W-J, Wang S, Shan C-M, Wang L-J, Chen X-Y (2010a) Temporal control of trichome distribution by microRNA156-targeted SPL genes in Arabidopsis thaliana. Plant Cell Online 22(7):2322–2335. doi:10.1105/tpc.109.072579

    Article  CAS  Google Scholar 

  • Yu N, Cai WJ, Wang SC, Shan CM, Wang LJ, Chen XY (2010b) Temporal control of trichome distribution by MicroRNA156-targeted SPL genes in Arabidopsis thaliana. Plant Cell 22(7):2322–2335. doi:10.1105/tpc.109.072579

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zeng Y, Yi R, Cullen BR (2003) MicroRNAs and small interfering RNAs can inhibit mRNA expression by similar mechanisms. Proc Natl Acad Sci USA 100(17):9779–9784. doi:10.1073/pnas.1630797100

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang BH, Wang QL, Wang KB, Pan XP, Liu F, Guo TL, Cobb GP, Anderson TA (2007) Identification of cotton microRNAs and their targets. Gene 397(1–2):26–37. doi:10.1016/j.gene.2007.03.020

    Article  CAS  PubMed  Google Scholar 

  • Zhang LF, Chia JM, Kumari S, Stein JC, Liu ZJ, Narechania A, Maher CA, Guill K, McMullen MD, Ware D (2009) A genome-wide characterization of microRNA genes in maize. Plos Genet 5 (11):e1000716. doi:10.1371/journal.pgen.1000716

  • Zhang XM, Zhao L, Larson-Rabin Z, Li DZ, Guo ZH (2012a) De novo sequencing and characterization of the floral transcriptome of Dendrocalamus latiflorus (Poaceae: Bambusoideae). Plos One 7 (8). doi:e42082. doi:10.1371/journal.pone.0042082

  • Zhang GY, Liu X, Quan ZW, Cheng SF, Xu X, Pan SK, Xie M, Zeng P, Yue Z, Wang WL, Tao Y, Bian C, Han CL, Xia QJ, Peng XH, Cao R, Yang XH, Zhan DL, Hu JC, Zhang YX, Li HN, Li H, Li N, Wang JY, Wang CC, Wang RY, Guo T, Cai YJ, Liu CZ, Xiang HT, Shi QX, Huang P, Chen QC, Li YR, Wang J, Zhao ZH, Wang J (2012b) Genome sequence of foxtail millet (Setaria italica) provides insights into grass evolution and biofuel potential. Nat Biotechnol 30(6):549–555. doi:10.1038/Nbt.2195

    Article  CAS  PubMed  Google Scholar 

  • Zhao CZ, Xia H, Frazier TP, Yao YY, Bi YP, Li AQ, Li MJ, Li CS, Zhang BH, Wang XJ (2010) Deep sequencing identifies novel and conserved microRNAs in peanuts (Arachis hypogaea L.). BMC Plant Biol 10. doi:10.1186/1471-2229-10-3

  • Zhao H, Chen D, Peng Z, Wang L, Gao Z (2013) Identification and characterization of microRNAs in the leaf of Ma bamboo (Dendrocalamus latiflorus) by deep sequencing. PLoS ONE 8(10):e78755. doi:10.1371/journal.pone.0078755

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhu Q-H, Helliwell CA (2011) Regulation of flowering time and floral patterning by miR172. J Exp Bot 62(2):487–495

    Article  CAS  PubMed  Google Scholar 

  • Zhu Q-H, Upadhyaya NM, Gubler F, Helliwell CA (2009) Over-expression of miR172 causes loss of spikelet determinacy and floral organ abnormalities in rice (Oryza sativa). BMC Plant Biol 9(1):149. doi:10.1186/1471-2229-9-149

    Article  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

This work was supported by the National Natural Science Foundation of China (Grant No. U1136603,31470322,30990244) and the Western Light Talent Culture Project of the Chinese Academy of Sciences (No. 2010312D11035). We thank Ms. Xian-Lun Yin of Kunming Institute of Botany, Chinese Academy of Science for her help with the biological experiments; Xing-Jun Wang from High-Tech Research Center, Shandong Academy of Agricultural Sciences and Dr. Andreas Schreiber from Australian Centre for Plant Functional Genomics, University of Adelaide for technical advice and Dr. Larson-Rabin Zachary visiting scientist to Kunming Institute of Botany from the University of Wisconsin for revision of the manuscript.

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Correspondence to De-Zhu Li or Zhen-Hua Guo.

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Xu-Yao Zhao and Xiao-Yan Wang contributed equally to this work.

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Additional file 1

Primers used in this study (DOCX 21 kb)

Additional file 2

miRNAs suspected of being technical variants: those miRNAs with an abundance of less than 0.12% of the most abundant possible parent sequence, and their possible parent sequence will always be highly conserved members of the same miRNA families (DOCX 17 kb)

Additional file 3

All identified known miRNAs in D. latiflorus. Abbreviations: dla, Dendrocalamus latiflorus; ath, Arabidopsis thaliana; bdi, Brachypodium distachyon; osa, Oryza sativa; zma, Zea mays (DOCX 30 kb)

Additional file 4

Known monocot-specific miRNAs (DOCX 16 kb)

Additional file 5

New members of MIRfam2275 (DOCX 17 kb)

Additional file 6

Evolutionary tree built from conserved miRNA genes (DOCX 21 kb)

Additional file 7

All predicted novel miRNAs in D. latiflorus (DOCX 27 kb)

Additional file 8

Dissolution curves of U6 SnRNA and 17 miRNAs (GIF 23 kb)

High resolution (TIFF 2007 kb)

Additional file 9

Targets of all known miRNAs and novel miRNAs (XLSX 24 kb)

Additional file 10

Conserved miRNA expression difference between two phases (DOCX 16 kb)

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Zhao, XY., Wang, XY., Zhao, L. et al. Investigating the MicroRNAomes of Two Developmental Phases of Dendrocalamus latiflorus (Poaceae: Bambusoideae) Inflorescences. Plant Mol Biol Rep 33, 1141–1155 (2015). https://doi.org/10.1007/s11105-014-0808-z

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