Abstract
The para rubber tree is the most widely cultivated tree species for producing natural rubber (NR) latex. Unfortunately, rubber tree characteristics such as a long life cycle, heterozygous genetic backgrounds, and poorly understood genetic profiles are the obstacles to breeding new rubber tree varieties, such as those with improved NR yields. Recent evidence has revealed the potential importance of controlling microRNA (miRNA) decay in some aspects of NR regulation. To gain a better understanding of miRNAs and their relationship with rubber tree gene regulation networks, large genomic DNA insert-containing libraries were generated to complement the incomplete draft genome sequence and applied as a new powerful tool to predict a function of interested genes. Bacterial artificial chromosome and fosmid libraries, containing a total of 120,576 clones with an average insert size of 43.35 kb, provided approximately 2.42 haploid genome equivalents of coverage based on the estimated 2.15 gb rubber tree genome. Based on these library sequences, the precursors of 1 member of rubber tree-specific miRNAs and 12 members of conserved miRNAs were successfully identified. A panel of miRNAs was characterized for phytohormone response by precisely identifying phytohormone-responsive motifs in their promoter sequences. Furthermore, the quantitative real-time PCR on ethylene stimulation of rubber trees was performed to demonstrate that the miR2118, miR159, miR164 and miR166 are responsive to ethylene, thus confirmed the prediction by genomic DNA analysis. The cis-regulatory elements identified in the promoter regions of these miRNA genes help augment our understanding of miRNA gene regulation and provide a foundation for further investigation of the regulation of rubber tree miRNAs.
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References
Achard P, Herr A, Baulcombe DC, Harberd NP (2004) Modulation of floral development by a gibberellin-regulated microRNA. Development 131:3357–3365
Association of Natural Rubber Producing Countries (ANRPC) (2010) Average annual yield in member countries in a monthly bulletin of market trends and statistics. Nat Rubber Trends Stat 2:11
Barvkar VT, Pardeshi VC, Kale SM, Qiu S, Rollins M, Datla R, Gupta VS, Kadoo NY (2013) Genome-wide identification and characterization of microRNA genes and their targets in flax (Linum usitatissimum). Planta 237:1149–1161
Cacao SMB, Silva NV, Domingues DS, Vieira LGE, Diniz LEC, Vinecky F, Alves GSC et al (2013) Construction and characterization of a BAC library from the Coffea arabica genotype Timor hybrid CIFC 832/2. Genetica 141:217–226
Chen L, Wang T, Zhao M, Zhang W (2012) Ethylene-responsive miRNAs in roots of Medicago truncatula identified by high-throughput sequencing at whole genome level. Plant Sci 184:14–19
Cui X, Xu SM, Mu DS, Yang ZM (2009) Genomic analysis of rice microRNA promoters and clusters. Gene 431:61–66
Duan C, Argout X, Gébelin V, Summo M, Dufayard JF, Leclercq J, Kuswanhadi PP et al (2013) Identification of the Hevea brasiliensis AP2/ERF superfamily by RNA sequencing. BMC Genomics 14:30
Dusotoit-Coucaud A, Kongsawadworakul P, Maurousset L, Viboonjun U, Brunel N, Pujade-Renaud V, Chrestin H, Sakr S (2010) Ethylene stimulation of latex yield depends on the expression of a sucrose transporter (HbSUT1B) in rubber tree (Hevea brasiliensis). Tree Physiol 30:1586–1598
Epicentre® (2002) CopyControl™ BAC cloning kit. Product manual. http://genomeprojectsolutions.com/pdfs/pcc1BAC.pdf. Accessed 1 May 2011
Figueira TRS, Okura V, Silva FR, Silva MJ, Kudrna D, Ammiraju JSS, Talag J, Wing R, Arruda P (2012) A BAC library of the SP80-3280 sugarcane variety (Saccharum sp.) and its inferred microsynteny with the sorghum genome. BMC Res Notes 5:185
Gébelin V, Argout X, Engchuan W, Pitollat B, Duan C, Montoro P, Leclercq J (2012) Identification of novel microRNAs in Hevea brasiliensis and computational prediction of their targets. BMC Plant Biol 12:18
Gébelin V, Leclercq J, Argout X, Chaidamsari T, Hu S, Tang C, Sarah G, Yang M, Montoro P (2013a) The small RNA profile in latex from Hevea brasiliensis trees is affected by tapping panel dryness. Tree Physiol 31:1084–1098
Gébelin V, Leclercq J, Chaorong T, Songnian H, Tang C, Montoro P (2013b) Regulation of MIR genes in response to abiotic stress in Hevea brasiliensis. Int J Mol Sci 14:19587–19604
Gonthier L, Bellec A, Blassiau C, Prat E, Helmstetter N, Rambaud C, Huss B, Hendriks T, Berges H, Quillet MC (2010) Construction and characterization of two BAC libraries representing a deep coverage of the genome of chicory (Cichorium intybus L., Asteraceae). BMC Res 3:225
Gray WM (2004) Hormonal regulation of plant growth and development. PLoS Biol 2:1270–1273
Gschwend AR, Yu Q, Moore P, Saski C, Chen C, Wang J, Na JK, Ming R (2011) Construction of papaya male and female BAC libraries and application in physical mapping of the sex chromosomes. J Biomed Biotechnol. doi:10.1155/2011/929472
Hansen KF, Sakamoto K, Obrietan K (2011) MicroRNAs: a potential interface between the circadian clock and human health. Genome Med 3:10
Hazen SP, Naef F, Quisel T, Gendron JM, Chen H, Ecker JR, Borevitz JO, Kay SA (2009) Exploring the transcriptional landscape of plant circadian rhythms using genome tiling arrays. Genome Biol 10:17
Heikkinen L, Asikainen S, Wong G (2008) Identification of phylogenetically conserved sequence motifs in microRNA 5′ flanking sites from C. elegans and C. briggsae. BMC Mol Biol 9:105
Jeukens J, Boyle B, Kukavica-Ibrulj I, St-Cyr J, Le Vesque RC, Bernatchez L (2011) BAC library construction, screening and clone sequencing of lake whitefish (Coregonus clupeaformis, Salmonidae) towards the elucidation of adaptive species divergence. Mol Ecol Resour 11:541–549
Kamimura M, Tateishi K, Tanaka-Okuyama M, Okabe T, Shibata F, Sahara K, Yasukochi Y (2012) EST sequencing and fosmid library construction in a non-model moth, Mamestra brassicae, for comparative mapping. Genome 55(11):775–781
Kim CG, Fujiyam A, Saitou N (2003) Construction of a gorilla fosmid library and its PCR screening system. Genomics 82:571–574
Lertpanyasampatha M, Gao L, Kongsawadworakul P, Viboonjun U, Chrestin H, Liu R, Chen X, Narangajavana J (2012) Genome-wide analysis of microRNAs in rubber tree (Hevea brasiliensis L.) using high-throughput sequencing. Planta 236(2):437–445
Lertpanyasampatha M, Pramoolkit P, Kongsawadworakul P, Viboonjun U, Chrestin H, Narangajavana J (2013) Conserved microRNAs and their targets in rubber tree and the related Euphorbiaceous species. J Plant Biochem Biot 22(1):52–61
Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, VandePeer Y, Rouzé P, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30(1):325–327
Liu Q, Zhang YC, Wang CY, Luo YC, Huang QJ, Chen SY, Zhou H, Qu LH, Chen YQ (2009) Expression analysis of phytohormone-regulated microRNAs in rice, implying their regulation roles in plant hormone signaling. FEBS Lett 583:723–728
Liu SY, Yu K, Huffner M, Park SJ, Banik M, Pauls KP, Crosby W (2010) Construction of a BAC library and a physical map of a major QTL for CBB resistance of common bean (Phaseolus vulgaris L.). Genetica 138(7):709–716
Luo M, Wing RA (2003) An improved method for plant BAC library construction. Methods Mol Biol 236:3–20
Markham NR, Zuker M (2008) UNAFold: software for nucleic acid folding and hybridization. Methods Mol Biol 453:3–31
Megraw M, Baev V, Rusinov V, Jensen ST, Kalantidis K, Hatzigeorgiou AG (2006) MicroRNA promoter element discovery in Arabidopsis. RNA 12:1612–1619
Osoegawa K, Vessere GM, Shu CL, Hoskins RA, Abad JP, Pablos B, Villasante A, Jong PJ (2007) BAC clones generated from sheared DNA. Genomics 89(2):291–299
Ozsolak F, Poling LL, Wang Z, Liu H, Liu XS, Roeder RG, Zhang X, Song JS, Fisher DE (2008) Chromatin structure analyses identify miRNA promoters. Genes Dev 22:3172–3183
Patanun O, Lertpanyasampatha M, Sojikul P, Viboonjun U, Narangajavana J (2012) Computational identification of microRNAs and their targets in cassava (Manihot esculenta Crantz.). Mol Biotechnol 53:257–269
Pei H, Ma N, Tian J, Luo J, Chen J, Li J, Zheng Y, Chen X, Fei Z, Gao J (2013a) An NAC transcription factor controls ethylene-regulated cell expansion in flower petals. Plant Physiol 163:775–791
Pei H, Ma N, Chen J, Zheng Y, Tian J, Jing L, Zhang S, Fei Z, Gao J (2013b) Integrative analysis of miRNA and MRNA profiles in response to ethylene in rose petals during flower opening. PLoS One 8:5
Peterson D, Tomkins J, Frisch D, Wing R, Paterson A (2002) Construction of plant bacterial artificial chromosome (BAC) libraries: an illustrated guide. J Agric Genomics 5:1–100
Rahman AYA, Usharraj AO, Misra BB, Thottathil GP, Jayasekaran K, Feng Y, Hou S et al (2013) Draft genome sequence of the rubber tree Hevea brasiliensis. BMC Genomics 14:75
Roche D, Conner JA, Budiman MA, Frisch D, Wing R, Hanna WW, Ozias-Akins P (2002) Construction of BAC libraries from two apomictic grasses to study the microcolinearity of their apospory-specific genomic regions. Theor Appl Genet 104:804–812
Sambrook J, Fritsch EF, Maniatis T (2001) Molecular cloning: a laboratory manual, 3rd edn. CSH Laboratory Press, New York
Schulte D, Ariyadasa R, Shi B, Fleury D, Saski C, Atkins M, Jong P, Wu CC, Graner A, Langridge P, Stein N (2011) BAC library resources for map-based cloning and physical map construction in barley (Hordeum vulgare L.). BMC Genomics 12:247
Sehgal SK, Li W, Rabinowicz PD, Chan A, Simkova H, Dolezel J, Gill BS (2012) Chromosome arm-specific BAC end sequences permit comparative analysis of homoeologous chromosomes and genomes of polyploid wheat. BMC Plant Biol 12:64
Solonenko SA, Ignacio-Espinoza JC, Alberti A, Cruaud C, Hallam S, Konstantinidis K, Tyson G, Wincker P, Sullivan MB (2013) Sequencing platform and library preparation choices impact viral metagenomes. BMC Genomics 14:320
Triwitayakorn K, Chatkulkawin P, Kanjanawattanawong S, Sraphet S, Yoocha T, Sangsrakru D, Chanprasert J et al (2011) Transcriptome sequencing of Hevea brasiliensis for development of microsatellite markers and construction of a genetic linkage map. DNA Res 18:471–482
Vinod KK, Suryakumar M, Chandrasekhar TR, Nazeer MA (2010) Temporal stability of growth and yield among Hevea genotypes introduced to a non-traditional rubber growing region of peninsular India. Ann For Res 53(2):107–115
Vrba L, Munoz-Rodrıguez JL, Stampfer MR, Futscher B (2013) MiRNA gene promoters are frequent targets of aberrant DNA methylation in human breast cancer. PLoS one 8:1
Wang J, Sun Z, Zhou Y, Wang Q, Ye J, Chen Z, Liu J (2012) Screening of a xylanase clone from a fosmid library of rumen microbiota in Hu sheep. Anim Biotechnol 23(3):156–173
Zhang HB (2000) Construction and manipulation of large-insert bacterial clone libraries. In: Manual. Department of Soil and Crop Sciences and Crop Biotechnology Center, Texas A&M University
Zhang HB, Zhao X, Ding X, Paterson AH, Wing RA (1995) Preparation of megabase-size DNA from plant nuclei. Plant J 7(1):175–184
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
Zhang L, Bao Z, Cheng J, Li H, Huang X, Wang S, Zhang C, Hu J (2007) Fosmid library construction and initial analysis of end sequences in Zhikong Scallop (Chlamys farreri). Mar Biotechnol 9:606–612
Zhang M, Zhang Y, Scheuring CF, Wu CC, Dong JJ, Zhang HB (2012) Preparation of megabase-sized DNA from a variety of organisms using the nuclei method for advanced genomics research. Nat Protoc 7:467–478
Zhao X, Li L (2013) Comparative analysis of microRNA promoters in Arabidopsis and rice. Genomics Proteomics Bioinform 11:56–60
Zhao JP, Jiang XL, Zhang BY, Su XH (2012) Involvement of microRNA-mediated gene expression regulation in the pathological development of stemcanker disease in Populus trichocarpa. PLoS One 7(9):e44968
Zhao X, Zhang H, Li L (2013) Identification and analysis of the proximal promoters of microRNA genes in Arabidopsis. Genomics 101:187–194
Zhou X, Ruan J, Zhang W, Wang G (2007) Characterization and identification of microRNA core promoters in four model species. PLoS Comput Biol 3:3
Acknowledgments
The plant materials used in BAC and fosmid library construction were provided by Ms. Kanikar Teerawatanasuk, CRRC-Rubber Research Institute of Thailand (CRRC-RRIT), Department of Agriculture. We would like to express special gratitude to Ms. Samaporn Teeravechyan, National Center for Genetic Engineering and Biotechnology (BIOTEC) (Thailand) for her help in English editing. This work was supported by BIOTEC, RRIT, and Mahidol University.
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Communicated by S. Hohmann.
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Kanjanawattanawong, S., Tangphatsornruang, S., Triwitayakorn, K. et al. Characterization of rubber tree microRNA in phytohormone response using large genomic DNA libraries, promoter sequence and gene expression analysis. Mol Genet Genomics 289, 921–933 (2014). https://doi.org/10.1007/s00438-014-0862-0
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DOI: https://doi.org/10.1007/s00438-014-0862-0