Biological significance of RNA-seq and single-cell genomic research in woody plants

Abstract

RNA-seq and single-cell genomic research emerge as an important research area in the recent years due to its ability to examine genetic information of any number of single cells in all living organisms. The knowledge gained from RNA-seq and single-cell genomic research will have a great impact in many aspects of plant biology. In this review, we summary and discuss the biological significance of RNA-seq and single-cell genomic research in plants including the single-cell DNA-sequencing, RNA-seq and single-cell RNA sequencing in woody plants, methods of RNA-seq and single-cell RNA-sequencing, single-cell RNA-sequencing for studying plant development, and single-cell RNA-sequencing for elucidating cell type composition. We will focus on RNA-seq and single-cell RNA sequencing in woody plants, understanding of plant development through single-cell RNA-sequencing, and elucidation of cell type composition via single-cell RNA-sequencing. Information presented in this review will be helpful to increase our understanding of plant genomic research in a way with the power of plant single-cell RNA-sequencing analysis.

Keywords

Cell type composition / Genomics / Plant development / Single-cell RNA-sequencing methods

References

Bai Y, Dougherty L, Cheng L, Zhong GY, Xu K. Uncovering co-expression gene network modules regulating fruit acidity in diverse apples. BMC Genom, 2015, 16: 612.

Birnbaum K, Shasha DE, Wang JY, Jung JW, Lambert GM, Galbraith DW, Benfey PN. A gene expression map of the Arabidopsis root. Science, 2003, 302: 1956-1960.

Brady SM, Orlando DA, Lee JY, Wang JY, Koch J, Dinneny JR, Mace D, Ohler U, Benfey PN. A high-resolution root spatiotemporal map reveals dominant expression patterns. Science, 2007, 318: 801-806.

Brandt S, Kloska S, Altmann T, Kehr J. Using array hybridization to monitor gene expression at the single cell level. J Exp Bot, 2002, 53: 2315-2323.

Brockmoller T, Ling Z, Li D, Gaquerel E, Baldwin IT, Xu S. Nicotiana attenuata Data Hub (NaDH): an integrative platform for exploring genomic, transcriptomic and metabolomic data in wild tobacco. BMC Genom, 2017, 18: 79.

Carocha V, Soler M, Hefer C, Cassan-Wang H, Fevereiro P, Myburg AA, Paiva JA, Grima-Pettenati J. Genome-wide analysis of the lignin toolbox of Eucalyptus grandis. New Phytol, 2015, 206: 1297-1313.

Cervantes-Perez SA, Espinal-Centeno A, Oropeza-Aburto A, Caballero-Perez J, Falcon F, Aragon-Raygoza A, Sanchez-Segura L, Herrera-Estrella L, Cruz-Hernandez A, Cruz-Ramirez A. Transcriptional profiling of the CAM plant Agave salmiana reveals conservation of a genetic program for regeneration. Dev Biol, 2018, 442: 28-39.

Chang E, Shi S, Liu J, Cheng T, Xue L, Yang X, Yang W, Lan Q, Jiang Z. Selection of reference genes for quantitative gene expression studies in Platycladus orientalis (Cupressaceae) using real-time PCR. PLoS ONE, 2012, 7: e33278.

Chen J, Chen B, Zhang D. Transcript profiling of Populus tomentosa genes in normal, tension, and opposite wood by RNA-seq. BMC Genom, 2015, 16: 164.

Cheng H, Chen X, Zhu J, Huang H. Overexpression of a Hevea brasiliensis ErbB-3 binding protein 1 gene increases drought tolerance and organ size in arabidopsis. Front Plant Sci, 2016, 7: 1703.

Devos N, Szovenyi P, Weston DJ, Rothfels CJ, Johnson MG, Shaw AJ. Analyses of transcriptome sequences reveal multiple ancient large-scale duplication events in the ancestor of Sphagnopsida (Bryophyta). New Phytol, 2016, 211: 300-318.

Dhandapani S, Jin J, Sridhar V, Sarojam R, Chua NH, Jang IC. Integrated metabolome and transcriptome analysis of Magnolia champaca identifies biosynthetic pathways for floral volatile organic compounds. BMC Genom, 2017, 18: 463.

DiGuistini S, Wang Y, Liao NY, Taylor G, Tanguay P, Feau N, Henrissat B, Chan SK, Hesse-Orce U, Alamouti SM, Tsui CK, Docking RT, Levasseur A, Haridas S, Robertson G, Birol I, Holt RA, Marra MA, Hamelin RC, Hirst M, Jones SJ, Bohlmann J, Breuil C. Genome and transcriptome analyses of the mountain pine beetle-fungal symbiont Grosmannia clavigera, a lodgepole pine pathogen. Proc Natl Acad Sci USA, 2011, 108: 2504-2509.

Farcuh M, Li B, Rivero RM, Shlizerman L, Sadka A, Blumwald E. Sugar metabolism reprogramming in a non-climacteric bud mutant of a climacteric plum fruit during development on the tree. J Exp Bot, 2017, 68: 5813-5828.

Filichkin SA, Hamilton M, Dharmawardhana PD, Singh SK, Sullivan C, Ben-Hur A, Reddy ASN, Jaiswal P. Abiotic stresses modulate landscape of poplar transcriptome via alternative splicing, differential intron retention, and isoform ratio switching. Front Plant Sci, 2018, 9: 5.

Fox H, Doron-Faigenboim A, Kelly G, Bourstein R, Attia Z, Zhou J, Moshe Y, Moshelion M, David-Schwartz R. Transcriptome analysis of Pinus halepensis under drought stress and during recovery. Tree Physiol, 2018, 38: 423-441.

Fricke W, Pritchard J, Leigh RA, Tomos AD. Cells of the upper and lower epidermis of barley (Hordeum vulgare L.) leaves exhibit distinct patterns of vacuolar solutes. Plant Physiol, 1994, 104: 1201-1208.

Gao F, Wang J, Wei S, Li Z, Wang N, Li H, Feng J, Li H, Zhou Y, Zhang F. Transcriptomic analysis of drought stress responses in Ammopiptanthus mongolicus leaves using the RNA-seq technique. PLoS ONE, 2015, 10: e0124382.

Gao L, Wang Y, Li Z, Zhang H, Ye J, Li G. Gene expression changes during the gummosis development of peach shoots in response to Lasiodiplodia theobromae infection using RNA-seq. Front Physiol, 2016, 7: 170.

Gao L, Lu XP, Zhang L, Qiao Y, Zhao Q, Wang YP, Li MF, Zhang JL. Transcriptomic profiling and physiological analysis of Haloxylon ammodendron in response to osmotic stress. Int J Mol Sci, 2017, 19: 84.

Gecaj RM, Schanzenbach CI, Kirchner B, Pfaffl MW, Riedmaier I, Tweedie-Cullen RY, Berisha B. The dynamics of microRNA transcriptome in bovine corpus luteum during Its formation, function, and regression. Front Genet, 2017, 8: 213.

Grun D, van Oudenaarden A. Design and analysis of single-cell sequencing experiments. Cell, 2015, 163: 799-810.

Grun D, Lyubimova A, Kester L, Wiebrands K, Basak O, Sasaki N, Clevers H, van Oudenaarden A. Single-cell messenger RNA sequencing reveals rare intestinal cell types. Nature, 2015, 525: 251-255.

Hane JK, Anderson JP, Williams AH, Sperschneider J, Singh KB. Genome sequencing and comparative genomics of the broad host-range pathogen Rhizoctonia solani AG8. PLoS Genet, 2014, 10: e1004281.

He B, Dong H, Jiang C, Cao F, Tao S, Xu LA. Analysis of codon usage patterns in Ginkgo biloba reveals codon usage tendency from A/U-ending to G/C-ending. Sci Rep, 2016, 6: 35927.

Hedlund E, Deng Q. Single-cell RNA sequencing: technical advancements and biological applications. Mol Aspects Med, 2018, 59: 36-46.

Hess M, Sczyrba A, Egan R, Kim TW, Chokhawala H, Schroth G, Luo S, Clark DS, Chen F, Zhang T, Mackie RI, Pennacchio LA, Tringe SG, Visel A, Woyke T, Wang Z, Rubin EM. Metagenomic discovery of biomass-degrading genes and genomes from cow rumen. Science, 2011, 331: 463-467.

Hodzic E. Single-cell analysis: advances and future perspectives. Bosn J Basic Med Sci, 2016, 16: 313-314.

Honaas LA, Wafula EK, Wickett NJ, Der JP, Zhang Y, Edger PP, Altman NS, Pires JC, Leebens-Mack JH, dePamphilis CW. Selecting superior De Novo transcriptome assemblies: lessons learned by leveraging the best plant genome. PLoS ONE, 2016, 11: e0146062.

Hou X, Guo Q, Wei W, Guo L, Guo D, Zhang L. Screening of genes related to early and late flowering in tree peony based on bulked segregant RNA sequencing and verification by quantitative real-time PCR. Molecules, 2018 23 3 689

Hu Z, Zhang T, Gao XX, Wang Y, Zhang Q, Zhou HJ, Zhao GF, Wang ML, Woeste KE, Zhao P. De novo assembly and characterization of the leaf, bud, and fruit transcriptome from the vulnerable tree Juglans mandshurica for the development of 20 new microsatellite markers using illumina sequencing. Mol Genet Genom: MGG, 2016, 291: 849-862.

Huang X, Li K, Xu X, Yao Z, Jin C, Zhang S. Genome-wide analysis of WRKY transcription factors in white pear (Pyrus bretschneideri) reveals evolution and patterns under drought stress. BMC Genom, 2015, 16: 1104.

Hussey SG, Saidi MN, Hefer CA, Myburg AA, Grima-Pettenati J. Structural, evolutionary and functional analysis of the NAC domain protein family in Eucalyptus. New Phytol, 2015, 206: 1337-1350.

Iaria DL, Chiappetta A, Muzzalupo I. A de novo transcriptomic approach to identify flavonoids and anthocyanins “switch-off” in olive (Olea europaea L.) drupes at different stages of maturation. Front Plant Sci, 2015 6 392 1246

Jia T, Wei D, Meng S, Allan AC, Zeng L. Identification of regulatory genes implicated in continuous flowering of longan (Dimocarpus longan L.). PLoS ONE, 2014, 9: e114568.

Jo Y, Lian S, Cho JK, Choi H, Chu H, Cho WK. De novo transcriptome assembly of two different apricot cultivars. Genom Data, 2015, 6: 275-276.

Jo Y, Lian S, Cho JK, Choi H, Chu H, Cho WK. De novo transcriptome assembly of two different Prunus mume cultivars. Genom Data, 2015, 6: 273-274.

Jo Y, Choi H, Kim SM, Kim SL, Lee BC, Cho WK. Integrated analyses using RNA-seq data reveal viral genomes, single nucleotide variations, the phylogenetic relationship, and recombination for Apple stem grooving virus. BMC Genom, 2016, 17: 579.

Jouraku A, Yamamoto K, Kuwazaki S, Urio M, Suetsugu Y, Narukawa J, Miyamoto K, Kurita K, Kanamori H, Katayose Y, Matsumoto T, Noda H. KONAGAbase: a genomic and transcriptomic database for the diamondback moth, Plutella xylostella. BMC Genom, 2013, 14: 464.

Jue D, Sang X, Liu L, Shu B, Wang Y, Xie J, Liu C, Shi S. The ubiquitin-conjugating enzyme gene family in Longan (Dimocarpus longan Lour.): genome-wide identification and gene xxpression during flower induction and abiotic stress responses. Molecules, 2018 23 3 662

Junker JP, van Oudenaarden A. Single-cell transcriptomics enters the age of mass production. Mol Cell, 2015, 58: 563-564.

Kang YJ, Kim SK, Kim MY, Lestari P, Kim KH, Ha BK, Jun TH, Hwang WJ, Lee T, Lee J, Shim S, Yoon MY, Jang YE, Han KS, Taeprayoon P, Yoon N, Somta P, Tanya P, Kim KS, Gwag JG, Moon JK, Lee YH, Park BS, Bombarely A, Doyle JJ, Jackson SA, Schafleitner R, Srinives P, Varshney RK, Lee SH. Genome sequence of mungbean and insights into evolution within Vigna species. Nat Commun, 2014, 5: 5443.

Kang Z, Zhang X, Ding S, Tang C, Wang Y, Jong H, Cameron SL, Wang M, Yang D. Transcriptomes of three species of Tipuloidea (Diptera, Tipulomorpha) and implications for phylogeny of Tipulomorpha. PLoS ONE, 2017, 12: e0173207.

Kavas M, Baloglu MC, Atabay ES, Ziplar UT, Dasgan HY, Unver T. Genome-wide characterization and expression analysis of common bean bHLH transcription factors in response to excess salt concentration. Mol Genet Genom: MGG, 2016, 291: 129-143.

Kitajima S, Aoki W, Shibata D, Nakajima D, Sakurai N, Yazaki K, Munakata R, Taira T, Kobayashi M, Aburaya S, Savadogo EH, Hibino S, Yano H. Comparative multi-omics analysis reveals diverse latex-based defense strategies against pests among latex-producing organs of the fig tree (Ficus carica). Planta, 2018, 247: 1423-1438.

Kullan AR, van Dyk MM, Hefer CA, Jones N, Kanzler A, Myburg AA. Genetic dissection of growth, wood basic density and gene expression in interspecific backcrosses of Eucalyptus grandis and E. urophylla. BMC Genet, 2012, 13: 60.

Landis JB, Soltis DE, Soltis PS. Comparative transcriptomic analysis of the evolution and development of flower size in Saltugilia (Polemoniaceae). BMC Genom, 2017, 18: 475.

Le Provost G, Lesur I, Lalanne C, Da Silva C, Labadie K, Aury JM, Leple JC, Plomion C. Implication of the suberin pathway in adaptation to waterlogging and hypertrophied lenticels formation in pedunculate oak (Quercus robur L.). Tree Physiol, 2016, 36: 1330-1342.

Leyva-Perez MO, Jimenez-Ruiz J, Gomez-Lama Cabanas C, Valverde-Corredor A, Barroso JB, Luque F, Mercado-Blanco J. Tolerance of olive (Olea europaea) cv Frantoio to verticillium dahliae relies on both basal and pathogen-induced differential transcriptomic responses. New Phytol, 2018, 217: 671-686.

Libault M, Farmer A, Brechenmacher L, Drnevich J, Langley RJ, Bilgin DD, Radwan O, Neece DJ, Clough SJ, May GD, Stacey G. Complete transcriptome of the soybean root hair cell, a single-cell model, and its alteration in response to Bradyrhizobium japonicum infection. Plant Physiol, 2010, 152: 541-552.

Liu L, Missirian V, Zinkgraf M, Groover A, Filkov V. Evaluation of experimental design and computational parameter choices affecting analyses of ChIP-seq and RNA-seq data in undomesticated poplar trees. BMC Genom, 2014 15 Suppl 5 S3

Liu JJ, Williams H, Li XR, Schoettle AW, Sniezko RA, Murray M, Zamany A, Roke G, Chen H. Profiling methyl jasmonate-responsive transcriptome for understanding induced systemic resistance in whitebark pine (Pinus albicaulis). Plant Mol Biol, 2017, 95: 359-374.

Liu XY, Li J, Liu MM, Yao Q, Chen JZ. Transcriptome profiling to understand the effect of citrus rootstocks on the growth of ‘Shatangju’ Mandarin. PLoS ONE, 2017, 12: e0169897.

Liu J, Wu X, Yao X, Yu R, Larkin PJ, Liu CM. Mutations in the DNA demethylase OsROS1 result in a thickened aleurone and improved nutritional value in rice grains. Proc Natl Acad Sci USA, 2018, 115: 11327-11332.

Long Y, Zhang J, Tian X, Wu S, Zhang Q, Zhang J, Dang Z, Pei XW. De novo assembly of the desert tree Haloxylon ammodendron (C. A. Mey.) based on RNA-seq data provides insight into drought response, gene discovery and marker identification. BMC Genom, 2014, 15: 1111.

Lu X, Li J, Chen H, Hu J, Liu P, Zhou B. RNA-seq analysis of apical meristem reveals integrative regulatory network of ROS and chilling potentially related to flowering in Litchi chinensis. Sci Rep, 2017, 7: 10183.

Lyu MJ, Gowik U, Kelly S, Covshoff S, Mallmann J, Westhoff P, Hibberd JM, Stata M, Sage RF, Lu H, Wei X, Wong GK, Zhu XG. RNA-seq based phylogeny recapitulates previous phylogeny of the genus Flaveria (Asteraceae) with some modifications. BMC Evol Biol, 2015, 15: 116.

Makita Y, Kawashima M, Lau NS, Othman AS, Matsui M. Construction of Para rubber tree genome and multi-transcriptome database accelerates rubber researches. BMC Genom, 2018, 19: 922.

Meyer FE, Shuey LS, Naidoo S, Mamni T, Berger DK, Myburg AA, van den Berg N, Naidoo S. Dual RNA-equencing of Eucalyptus nitens during Phytophthora cinnamomi challenge reveals pathogen and host factors influencing compatibility. Front Plant Sci, 2016, 7: 191.

Miguel A, de Vega-Bartol J, Marum L, Chaves I, Santo T, Leitao J, Varela MC, Miguel CM. Characterization of the cork oak transcriptome dynamics during acorn development. BMC Plant Biol, 2015, 15: 158.

Moazzam Jazi M, Rajaei S, Seyedi SM. Isolation of high quality RNA from pistachio (Pistacia vera L.) and other woody plants high in secondary metabolites. Physiol Mol Biol Plants, 2015, 21: 597-603.

Nadeau JA, Petereit J, Tillett RL, Jung K, Fotoohi M, MacLean M, Young S, Schlauch K, Blomquist GJ, Tittiger C. Comparative transcriptomics of mountain pine beetle pheromone-biosynthetic tissues and functional analysis of CYP6DE3. BMC Genom, 2017, 18: 311.

Offermann S, Friso G, Doroshenk KA, Sun Q, Sharpe RM, Okita TW, Wimmer D, Edwards GE, van Wijk KJ. Developmental and subcellular organization of single-cell C(4) photosynthesis in Bienertia sinuspersici determined by large-scale proteomics and cDNA assembly from 454 DNA sequencing. J Proteome Res, 2015, 14: 2090-2108.

Oikawa T, Wauthier E, Dinh TA, Selitsky SR, Reyna-Neyra A, Carpino G, Levine R, Cardinale V, Klimstra D, Gaudio E, Alvaro D, Carrasco N, Sethupathy P, Reid LM. Model of fibrolamellar hepatocellular carcinomas reveals striking enrichment in cancer stem cells. Nat Commun, 2015, 6: 8070.

Okada K, Wada M, Moriya S, Katayose Y, Fujisawa H, Wu J, Kanamori H, Kurita K, Sasaki H, Fujii H, Terakami S, Iwanami H, Yamamoto T, Abe K. Expression of a putative dioxygenase gene adjacent to an insertion mutation is involved in the short internodes of columnar apples (Malus x domestica). J Plant Res, 2016, 129: 1109-1126.

Ostria-Gallardo E, Ranjan A, Chitwood DH, Kumar R, Townsley BT, Ichihashi Y, Corcuera LJ, Sinha NR. Transcriptomic analysis suggests a key role for SQUAMOSA PROMOTER BINDING PROTEIN LIKE, NAC and YUCCA genes in the heteroblastic development of the temperate rainforest tree Gevuina avellana (Proteaceae). New Phytol, 2016, 210: 694-708.

Ouyang K, Li J, Zhao X, Que Q, Li P, Huang H, Deng X, Singh SK, Wu AM, Chen X. Transcriptomic analysis of multipurpose timber yielding tree Neolamarckia cadamba during xylogenesis using RNA-seq. PLoS ONE, 2016, 11: e0159407.

Pang M, Woodward AW, Agarwal V, Guan X, Ha M, Ramachandran V, Chen X, Triplett BA, Stelly DM, Chen ZJ. Genome-wide analysis reveals rapid and dynamic changes in miRNA and siRNA sequence and expression during ovule and fiber development in allotetraploid cotton (Gossypium hirsutum L.). Genome Biol, 2009, 10: 122.

Parveen I, Wang M, Zhao J, Chittiboyina AG, Tabanca N, Ali A, Baerson SR, Techen N, Chappell J, Khan IA, Pan Z. Investigating sesquiterpene biosynthesis in Ginkgo biloba: molecular cloning and functional characterization of (E, E)-farnesol and alpha-bisabolene synthases. Plant Mol Biol, 2015, 89: 451-462.

Paul A, Jha A, Bhardwaj S, Singh S, Shankar R, Kumar S. RNA-seq-mediated transcriptome analysis of actively growing and winter dormant shoots identifies non-deciduous habit of evergreen tree tea during winters. Sci Rep, 2014, 4: 5932.

Peng XJ, Wang YC, He RP, Zhao ML, Shen SH. Global transcriptomics identification and analysis of transcriptional factors in different tissues of the paper mulberry. BMC Plant Biol, 2014, 14: 194.

Picelli S. Single-cell RNA-sequencing: the future of genome biology is now. RNA Biol, 2017, 14: 637-650.

Qiu Z, Wan L, Chen T, Wan Y, He X, Lu S, Wang Y, Lin J. The regulation of cambial activity in Chinese fir (Cunninghamia lanceolata) involves extensive transcriptome remodeling. New Phytol, 2013, 199: 708-719.

Qu CP, Xu ZR, Hu YB, Lu Y, Yang CJ, Sun GY, Liu GJ. RNA-seq reveals transcriptional level changes of poplar roots in different forms of nitrogen treatments. Front Plant Sci, 2016, 7: 51.

Rains MK, Gardiyehewa de Silva ND, Molina I. Reconstructing the suberin pathway in poplar by chemical and transcriptomic analysis of bark tissues. Tree Physiol, 2018, 38: 340-361.

Rao G, Sui J, Zeng Y, He C, Duan A, Zhang J. De novo transcriptome and small RNA analysis of two Chinese willow cultivars reveals stress response genes in Salix matsudana. PLoS ONE, 2014, 9: e109122.

Ren Y, Zhu Y, Wang Q, Xiang H, Wang B. Transcriptome of Pterospermum kingtungense provides implications on the mechanism underlying its rapid vegetative growth and limestone adaption. Sci Rep, 2017, 7: 3198.

Rinerson CI, Scully ED, Palmer NA, Donze-Reiner T, Rabara RC, Tripathi P, Shen QJ, Sattler SE, Rohila JS, Sarath G, Rushton PJ. The WRKY transcription factor family and senescence in switchgrass. BMC Genom, 2015, 16: 912.

Robert JA, Pitt C, Bonnett TR, Yuen MM, Keeling CI, Bohlmann J, Huber DP. Disentangling detoxification: gene expression analysis of feeding mountain pine beetle illuminates molecular-level host chemical defense detoxification mechanisms. PLoS ONE, 2013, 8: e77777.

Rocheta M, Sobral R, Magalhaes J, Amorim MI, Ribeiro T, Pinheiro M, Egas C, Morais-Cecilio L, Costa MM. Comparative transcriptomic analysis of male and female flowers of monoecious Quercus suber. Front Plant Sci, 2014, 5: 599.

Shearman JR, Sangsrakru D, Ruang-Areerate P, Sonthirod C, Uthaipaisanwong P, Yoocha T, Poopear S, Theerawattanasuk K, Tragoonrung S, Tangphatsornruang S. Assembly and analysis of a male sterile rubber tree mitochondrial genome reveals DNA rearrangement events and a novel transcript. BMC Plant Biol, 2014, 14: 45.

Shi Y, Sha G, Sun X. Genome-wide study of NAGNAG alternative splicing in Arabidopsis. Planta, 2014, 239: 127-138.

Shi Q, Zhou L, Wang Y, Li K, Zheng B, Miao K. Transcriptomic analysis of Paeonia delavayi wild population flowers to identify differentially expressed genes involved in purple-red and yellow petal pigmentation. PLoS ONE, 2015, 10: e0135038.

Shu B, Li W, Liu L, Wei Y, Shi S. Transcriptomes of Arbuscular Mycorrhizal fungi and litchi host interaction after tree girdling. Front Microbiol, 2016, 7: 408.

Sui JL, Xiao XH, Qi JY, Fang YJ, Tang CR. The SWEET gene family in Hevea brasiliensis - its evolution and expression compared with four other plant species. FEBS Open Bio, 2017, 7: 1943-1959.

Sun AJ, Gao HB, Liu G, Ge HF, Ke ZP, Li S. Identification of MSX1 and DCLK1 as mRNA biomarkers for colorectal cancer detection through DNA methylation information. J Cell Physiol, 2017, 232: 1879-1884.

Sundell D, Mannapperuma C, Netotea S, Delhomme N, Lin YC, Sjodin A, Van de Peer Y, Jansson S, Hvidsten TR, Street NR. The plant genome integrative explorer resource: plantGenIE.org. New Phytol, 2015, 208: 1149-1156.

Thavamanikumar S, Southerton S, Thumma B. RNA-seq using two populations reveals genes and alleles controlling wood traits and growth in Eucalyptus nitens. PLoS ONE, 2014, 9: e101104.

Torales SL, Rivarola M, Pomponio MF, Fernandez P, Acuna CV, Marchelli P, Gonzalez S, Azpilicueta MM, Hopp HE, Gallo LA, Paniego NB, Poltri SN. Transcriptome survey of Patagonian southern beech Nothofagus nervosa (= N. Alpina): assembly, annotation and molecular marker discovery. BMC Genom, 2012, 13: 291.

Torales SL, Rivarola M, Pomponio MF, Gonzalez S, Acuna CV, Fernandez P, Lauenstein DL, Verga AR, Hopp HE, Paniego NB, Poltri SN. De novo assembly and characterization of leaf transcriptome for the development of functional molecular markers of the extremophile multipurpose tree species Prosopis alba. BMC Genom, 2013, 14: 705.

Unruh SA, McKain MR, Lee YI, Yukawa T, McCormick MK, Shefferson RP, Smithson A, Leebens-Mack JH, Pires JC. Phylotranscriptomic analysis and genome evolution of the Cypripedioideae (Orchidaceae). Am J Bot, 2018, 105(4): 631-640.

Utturkar SM, Cude WN, Robeson MS Jr, Yang ZK, Klingeman DM, Land ML, Allman SL, Lu TY, Brown SD, Schadt CW, Podar M, Doktycz MJ, Pelletier DA. Enrichment of root endophytic bacteria from Populus deltoides and single-cell-genomics snalysis. Appl Environ Microbiol, 2016, 82: 5698-5708.

Wang Y, Lim L, Madilao L, Lah L, Bohlmann J, Breuil C. Gene discovery for enzymes involved in limonene modification or utilization by the mountain pine beetle-associated pathogen Grosmannia clavigera. Appl Environ Microbiol, 2014, 80: 4566-4576.

Wang P, Ma Y, Ma L, Li Y, Wang S, Li L, Yang R, Wang Q. Development and characterization of EST-SSR markers for Catalpa bungei (Bignoniaceae). Appl Plant Sci, 2016 4 4 1500117

Wang C, Lu P, Zhong S, Chen H, Zhou B. LcMCII-1 is involved in the ROS-dependent senescence of the rudimentary leaves of Litchi chinensis. Plant Cell Rep, 2017, 36: 89-102.

Wilks C, Gaddipati P, Nellore A, Langmead B. Snaptron: querying splicing patterns across tens of thousands of RNA-seq samples. Bioinformatics, 2018, 34: 114-116.

Wu CC, Kruse F, Vasudevarao MD, Junker JP, Zebrowski DC, Fischer K, Noel ES, Grun D, Berezikov E, Engel FB, van Oudenaarden A, Weidinger G, Bakkers J. Spatially resolved genome-wide transcriptional profiling identifies BMP signaling as essential regulator of Zebrafish Cardiomyocyte regeneration. Dev Cell, 2016, 36: 36-49.

Wuest SE, Schmid MW, Grossniklaus U. Cell-specific expression profiling of rare cell types as exemplified by its impact on our understanding of female gametophyte development. Curr Opin Plant Biol, 2013, 16: 41-49.

Xiao X, Hong Y, Xia W, Feng S, Zhou X, Fu X, Zang J, Xiao Y, Niu X, Li C, Chen Y. Transcriptome analysis of Ceriops tagal in saline environments using RNA-sequencing. PLoS ONE, 2016, 11: e0167551.

Xie Y, Wang X. Comparative transcriptomic analysis identifies genes responsible for fruit count and oil yield in the oil tea plant Camellia chekiangoleosa. Sci Rep, 2018, 8: 6637.

Yadav RK, Girke T, Pasala S, Xie M, Reddy GV. Gene expression map of the Arabidopsis shoot apical meristem stem cell niche. Proc Natl Acad Sci USA, 2009, 106: 4941-4946.

Yakovlev IA, Carneros E, Lee Y, Olsen JE, Fossdal CG. Transcriptional profiling of epigenetic regulators in somatic embryos during temperature induced formation of an epigenetic memory in Norway spruce. Planta, 2016, 243: 1237-1249.

Yang X, Cheng YF, Deng C, Ma Y, Wang ZW, Chen XH, Xue LB. Comparative transcriptome analysis of eggplant (Solanum melongena L.) and turkey berry (Solanum torvum Sw.): phylogenomics and disease resistance analysis. BMC Genom, 2014, 15: 412.

Ye X, Zhong Z, Liu H, Lin L, Guo M, Guo W, Wang Z, Zhang Q, Feng L, Lu G, Zhang F, Chen Q. Whole genome and transcriptome analysis reveal adaptive strategies and pathogenesis of Calonectria pseudoreteaudii to Eucalyptus. BMC Genom, 2018, 19: 358.

Yuan Y, Lee H, Hu H, Scheben A, Edwards D. Single-cell genomic analysis in plants. Genes, 2018, 9: 50.

Zhang C, Wang Y, Fu J, Dong L, Gao S, Du D. Transcriptomic analysis of cut tree peony with glucose supply using the RNA-seq technique. Plant Cell Rep, 2014, 33: 111-129.

Zhang X, Berkowitz O, Teixeira da Silva JA, Zhang M, Ma G, Whelan J, Duan J. RNA-seq analysis identifies key genes associated with haustorial development in the root hemiparasite Santalum album. Front Plant Sci, 2015, 6: 661.

Zhang Y, Barthe G, Grosser JW, Wang N. Transcriptome analysis of root response to citrus blight based on the newly assembled Swingle citrumelo draft genome. BMC Genom, 2016, 17: 485.

Zhang H, Shen J, Wei Y, Chen H. Transcriptome profiling of litchi leaves in response to low temperature reveals candidate regulatory genes and key metabolic events during floral induction. BMC Genom, 2017, 18: 363.

Zhang TJ, Zheng J, Yu ZC, Huang XD, Zhang QL, Tian XS, Peng CL. Functional characteristics of phenolic compounds accumulated in young leaves of two subtropical forest tree species of different successional stages. Tree Physiol, 2018, 38(10): 1486-1501.

Zhao X, Ouyang K, Gan S, Zeng W, Song L, Zhao S, Li J, Doblin MS, Bacic A, Chen XY, Marchant A, Deng X, Wu AM. Biochemical and molecular changes associated with heteroxylan biosynthesis in Neolamarckia cadamba (Rubiaceae) during xylogenesis. Front Plant Sci, 2014, 5: 602.

Zheng L, Meng Y, Ma J, Zhao X, Cheng T, Ji J, Chang E, Meng C, Deng N, Chen L, Shi S, Jiang Z. Transcriptomic analysis reveals importance of ROS and phytohormones in response to short-term salinity stress in Populus tomentosa. Front Plant Sci, 2015, 6: 678.

Zheng D, Ye W, Song Q, Han F, Zhang T, Chen ZJ. Histone modifications define expression bias of homoeologous genomes in allotetraploid cotton. Plant Physiol, 2016, 172: 1760-1771.

Zhou Q, Zheng Y. Comparative De Novo Transcriptome analysis of fertilized ovules in Xanthoceras sorbifolium uncovered a pool of genes expressed specifically or preferentially in the selfed ovule that are potentially involved in late-acting self-incompatibility. PLoS ONE, 2015, 10: e0140507.

Ziegenhain C, Vieth B, Parekh S, Reinius B, Guillaumet-Adkins A, Smets M, Leonhardt H, Heyn H, Hellmann I, Enard W. Comparative analysis of single-cell RNA sequencing methods. Mol Cell, 2017 65 631–643 e634