Abstract
As a specialized seed appendage, the aril is a noteworthy and taxonomically important feature of Celastrus orbiculatus; the aril also has important ornamental value and biological functions. To better understand the mechanism of aril development, paraffin sections were used to examine its morphogenesis, and RNA-sequencing (RNA-seq) technology was employed for transcriptional profiling of the developing aril. Our results revealed that the aril of C. orbiculatus was formed by the cells of the exostomal region of the outer integument. By analyzing global changes in the transcriptome, 41,560,806, 42,789,340, and 44,496,748 clean reads from three cDNA libraries were generated and assembled into 87,600 unigenes with N50 of 1328 bp, in which 31,971 (36.49%) were annotated to Nr database. Furthermore, a total of 25,914 (29.79%), 14,394 (16.4%) and 11,957 (13.65%) genes were successfully annotated with hierarchical 48 GO terms, 26 KOGs and 32 KEGG pathways. Totally, 104, 1887 and 1967 differently expressed genes were identified in CO-F2 versus CO-F3, CO-F2 versus CO-YF1 and CO-F3 versus CO-YF1, respectively. GO and KEGG pathway analyses of DEGs involved in cell–cell communication and plant hormone signal transduction contributed to aril development were identified. Furthermore, we found putative key target genes of WRKY, Aux/IAA, ARF and MADS-box family’s transcription factors related to aril development. Real-time qPCR was performed on eight genes randomly selected from important transcription factors to validate the expression profiles obtained by RNA-seq. This work provides a platform for future genetic and functional genomics research on the molecular mechanisms of aril structure, and expands our understanding of the molecular mechanism and evolutionary analysis of aril development in other members of the Celastraceae.
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References
Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11:1–12
Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J, Wittwer CT (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55(4):611–622
Corner EJH (1954) The durian theory extended-II. The arillate fruit and the compound leaf. Phytomorphology 4:152–165
Corner EJH (1976) The seeds of dicotyledons. Cambridge University Press, Cambridge, pp 23–24
Cucinotta M, Colombo L, Roig VI (2014) Ovule development, a new model for lateral organ formation. Front Plant Sci 117:1–12
Daniel HH, Xie C (2014) A poor man’s BLASTX—high-throughput metagenomic protein database search using PAUDAB. Bioinformatics 30:38–39
Davies KJ, Delsignore ME, Lin SW (1987) Protein damage and degradation by oxygen radicals I. J Biol Chem 262:895–901
Dubois A, Remay A, Raymond O, Balzergue S, Chauvet A, Maene M, Pecrix Y, Yang SH, Jeauffre J et al (2011) Genomic approach to study floral development genes in Rosa sp. PLoS ONE 6:e28455
Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 95:14863–14868
Endress PK (1973) Arils and aril-like structures in woody Ranales. New Phytol 72:1159–1171
Endress PK (2011) Angiosperm ovules: diversity, development, evolution. Ann Bot 107:1465–1489
Éric C, Audrey LH, Erin LZ, Matton DP (2011) Cell-cell communication and signalling pathways within the ovule: from its inception to fertilization. New Phytol 192:13–28
Favaro R, Pinyopich A, Battaglia R, Kooiker M, Borghi L, Ditta G, Yanofsky MF, Kater MM, Colombo L (2003) MADS-box protein complexes control carpel and ovule development in Arabidopsis. Plant Cell 15:2603–2611
Gan DF, Zhuang D, Ding F, Yu ZZ, Zhao Y (2013) Identification and expression analysis of primary auxin-responsive Aux/IAA gene family in cucumber (Cucumis sativus). J Genet 92:513–521
Götz S, García-Gómez JM, Terol J, Williams TD, Nagaraj SH, Nueda MJ, Robles M, Talon M, Dopazo J, Conesa A (2008) High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res 36:3420–3435
Grabherr MG, Haas BJ, Yassour M, Levin JZ, Nusbaum C, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R et al (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652
Grear JW, Dengler NG (1976) The seed appendage of Eriosema (Fabaceae). Brittonia 28:281–288
Hou D (1955) A revision of the genus Celastrus. Ann Mo Bot Gard 42:215–302
Howe EA, Sinha R, Schlauch D, Quackenbush J (2011) RNA-Seq analysis in MeV. Bioinformatics 27:3209–3210
Huang X, Bao YN, Wang B, Liu LJ, Chen J, Daim LJ, Peng DX (2016) Identification and expression of Aux/IAA, ARF, and LBD family transcription factors in Boehmeria nivea. Biol Plantarum 60:1–7
Jack T, Brockman LL, Meyerowitz EM (1992) The homeotic gene APETALA3 of Arabidopsis thaliana encodes a MADS box and is expressed in petals and stamens. Cell 68:683–697
Jain M (2011) A next-generation approach to the characterization of a non-model plant transcriptome. Curr Sci 101:1435–1439
Jofuku KD, den Boer BG, Montagu MV, Okamuro JK (1994) Control of Arabidopsis flower and seed development by the homeotic gene APETALA2. Plant Cell 6:1211–1225
Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, Katayama T, Kawashima S, Okuda S, Tokimatsu T, Yamanishi Y (2008) KEGG for linking genomes to life and the environment. Nucleic Acids Res 36:480–484
Kapil RN, Bor J, Bouman F (1980) Seed appendages in angiosperms. Bot Jahrb Syst 101:555–573
Kloos A, Bouman F (1980) Case studies in aril development Passiflora suberosa L. and Turnera ulmifolia L. Beitr Biol Pflanzen 55: 49–66
Lai B, Hu B, Qin YH, Zhao JT, Wang CH, Hu GB (2015) Transcriptomic analysis of Litchi chinensis pericarp during maturation with a focus on chlorophyll degradation and flavonoid biosynthesis. BMC Genom 16:225–229
Li J, Dai X, Zhao Y (2006) A role for auxin response factor 19 in auxin and ethylene signaling in Arabidopsis. Plant Physiol 140:899–908
Li SB, Xie ZZ, Hu CG, Zhang JZ (2016) A review of auxin response factors (ARFs) in plants. Front Plant Sci 7:1–7
Lisci M, Bianchini M, Pacini E (1996) Structure and function of the elaiosome in some angiosperm species. Flora 191:131–141
Liscum E, Reed JW (2002) Genetics of Aux/IAA and ARF action in plant growth and development. Plant Mol Biol 49:387–400
Liu Q, Zhang G, Chen S (2001) Structure and regulatory function of plant transcription factors. Chin Sci Bull 46: 271–278
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 25:402–408
Losa A, Colombo M, Brambilla V, Colombo L (2010) Genetic interaction between AINTEGUMENTA (ANT) and the ovule identity genes SEEDSTICK (STK), SHATTERPROOF1 (SHP1) and SHATTERPROOF2 (SHP2). Plant Reprod 23:115–121
Mao XZ, Cai T, Olyarchuk JG, Wei LP (2005) Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary. Bioinformatics 21:3787–3793
Marshall E, Costa LM, Gutierrezmarcos J (2011) Cysteine-rich peptides (CRPs) mediate diverse aspects of cell-cell communication in plant reproduction and development. J Exp Bot 62:1677–1686
Miers JIV (1856) On several instances of the anomalous development of the raphe in seeds, and the probable causes of such deviations from the usual course of structure, especially in reference to Stemonurus (Urandra of Thwaites), with some prefatory remarks on that genus. Trans Linn Soc London 22:97–112
Mu XY, Zhao LC, Zhang ZX (2012) Phylogeny of Celastrus L. (Celastraceae) inferred from two nuclear and three plastid markers. J Plant Res 125:619–630
Nesi N, Debeaujon I, Jond C, Stewart AJ, Jenkins GI, Caboche M, Lepiniec L (2002) The TRANSPARENT TESTA16 locus encodes the ARABIDOPSIS BSISTER MADS domain protein and is required for proper development and pigmentation of the seed coat. Plant Cell 14:63–79
Oikawa A, Otsuka T, Nakabayashi R, Jikumaru Y, Isuzugawa K, Murayama H (2015) Metabolic profiling of developing pear fruits reveals dynamic variation in primary and secondary metabolites, including plant hormones. PLoS ONE 10:e0131408
Pagnussat GC, Alandete SM, Bowman JL, Sundaresan V (2009) Auxin-dependent patterning and gamete specification in the Arabidopsis female gametophyte. Science 324:1684–1689
Par̆enicová L, de Folter S, Kieffer M, Horner DS, Favalli C, Busscher J (2003) Molecular and phylogenetic analyses of the complete MADS-box transcription factor family in Arabidopsis new openings to the MADS world. Plant Cell 15:1538–1551
Pfeiffer A (1891) Die arillargebilde der pflanzensamen. Bot Jg 13:492–540
Reed JW (2001) Roles and activities of Aux/IAA proteins in Arabidopsis. Trends Plant Sci 6:420–425
Rijpkema AS, Vandenbussche M, Koes R, Heijmans K, Gerats T (2010) Variations on a theme: changes in the floral ABCs in angiosperms. Cell Dev Biol 21:100–107
Roberta ANM, Mariana MP (2014) Expression of paralogous SEP-, FUL-, AG-and STK-like MADS-box genes in wild-type and peloric Phalaenopsis flowers. Front Plant Sci 5:1–17
Saldanha AJ (2004) Java Treeview-extensible visualization of microarray data. Bioinformatics 20:3246–3248
Schneitz K, Baker SC, Gasser CS, Redweijk A (1998) Pattern formation and growth during floral organogenesis: HUELLENLOS and AINTEGUMENTA are required for the formation of the proximal region of the ovule primordium in Arabidopsis thaliana. Development 125:2555–2563
Sheldon CC, Finnegan EJ, Dennis ES, Peacock WJ (2006) Quantitative effect of vernalization on FLC and SOC1 expression. Plant J 45:871–883
Shiv BT, Gretchen H, Tom G (2003) The roles of auxin response factor domains in auxin-responsive transcription. Plant Cell 15:533–543
Sun X, Gong SY, Nie XY, Li Y, Li W, Huang GQ, Li XB (2015) A R2R3-MYB transcription factor that is specifically expressed in cotton (Gossypium hirsutum) fibers affects secondary cell wall biosynthesis and deposition in transgenic Arabidopsis. Physiol Plant 154:420–432
Tanabe M, Kanehisa M (2012) Using the KEGG database resource. Curr Protoc Bioinform 43:1–12
Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, Koonin EV (2003) The COG database: an updated version includes eukaryotes. BMC Bioinform 4:41
Tiano L, Serrato VG, Corallo A (1998) The aril of Chamaecytisus proliferus (L.fil.) Link (Leguminosae): its structure, histochemistry and role in the dispersal and in water-seed interaction. Acta Bot Neerl 47:299–312
Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, Van Baren MJ, Salzberg SL, Wold BJ, Pachter L (2010) Transcript assembly and quantification by RNA-seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotech 28:511–515
Unamba CIN, Akshay N, Sharma RK (2015) Next generation sequencing technologies:the doorway to the unexplored genomics of non-model plants. Front Plant Sci 6:1–16
Wang L, Feng Z, Wang X, Zhang X (2010) DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26:136–138
Wang Y, Huang H, Ma Y, Fu J, Wang L, Dai S (2014) Construction and de novo characterization of a transcriptome of Chrysanthemum lavandulifolium: analysis of gene expression patterns in floral bud emergence. Plant Cell 116:297–309
Wang L, Yin X, Cheng C, Wang H, Guo R, Xu X, Zhao J, Zheng Y, Wang X (2015) Evolutionary and expression analysis of a MADS-box gene superfamily involved in ovule development of seeded and seedless grapevines. Mol Genet Genom 290:825–846
Werker E (1997) Seed anatomy. Encyclopaedia of plant anatomy. Gebrüder Borntraeger, Berlin, pp 286–299
Wheeler MJ, de Graaf BHJ, Hadjiosif N, Perry RM, Poulter NS, Osman K, Vatovec S, Harper A, Franklin FCH, Tong VEF (2009) Identification of the pollen self-incompatibility determinant in Papaver rhoeas. Nature 459:992–995
Yanagisawa S, Yoo SD, Sheen J (2003) Differential regulation of EIN3 stability by glucose and ethylene signaling in plants. Nature 425:521–525
Young MD, Wakefield MJ, Smyth GK, Oshlack A (2010) Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol 2:11–14
Zhang X, Zhang ZX, Thomas S (2012) Aril development in Celastraceae. Feddes Repert 123:1–11
Zou Z, Yang L, Wang D, Huang Q, Mo Y, Xie G (2016) Gene structures, evolution and transcriptional profiling of the WRKY gene family in castor bean (Ricinus communis L.). PLoS ONE 11:e0148243
Acknowledgements
This work was supported by funding from the National Natural Science Foundation of China (31370213) and Beijing Natural Science Foundation (5133036). The authors thank Wenkai Hui for technical assistance, as well as Ruohan Wang and Jun Niu for critical reading of the manuscript.
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Conceived and designed the experiments: KZ, SD, ZZ, LZ. Performed the experiments: KZ, JL, YZ, SX. Analyzed the data: KZ, SD, LZ. Contributed reagents/materials/analysis tools: KZ, SD, YZ. Wrote the paper: KZ, LZ.
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Kuiling Zu declares that he/she has no conflict of interest. Jianxia Li declares that he/she has no conflict of interest. Shubin Dong declares that he/she has no conflict of interest. Yunyu Zhao declares that he/she has no conflict of interest. Shenjian Xu declares that he/she has no conflict of interest. Zhixiang Zhang declares that he/she has no conflict of interest. Liangcheng Zhao declares that he/she has no conflict of interest.
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Zu, K., Li, J., Dong, S. et al. Morphogenesis and global analysis of transcriptional profiles of Celastrus orbiculatus aril: unravelling potential genes related to aril development. Genes Genom 39, 623–635 (2017). https://doi.org/10.1007/s13258-017-0528-5
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DOI: https://doi.org/10.1007/s13258-017-0528-5