Abstract
UV-B radiation is one of the major environmental stresses that triggers a variety of plant responses. However, limited information is available regarding plant biological reactions which help to circumvent the potentially harmful effects of UV-B radiation in lettuce (Lactuca sativa L.). In addition, leaf color is one of the most important economic traits of lettuce. The coloration of lettuce is mainly attributed to anthocyanins. Little is currently known about the correlation between anthocyanin biosynthesis and UV-B radiation in lettuce. Therefore, a comprehensive investigation of plant responses to UV-B radiation is critical for explaining the physiological and morphological alterations and revealing the key roles of UV-B in promoting anthocyanin biosynthesis in lettuce. In this study, RNA-seq was performed using the next-generation Illumina HiSeq™ 2000 sequencing platform and de novo assembly based on eight cDNA libraries of lettuce (Lactuca sativa L. cv. Shenxuan 5, a purple leaf cultivar) under UV-B-free and UV-B-stressed conditions. Over 382 million high-quality reads were assembled into 88,978 unigenes using a combined assembly strategy. Then a total of 69,397 (77.99%) unigenes were annotated based on at least one public database using homology searches. The transcriptome analysis identified a lot of genes differentially expressed in response to UV-B radiation. In particular, several anthocyanin biosynthetic genes were actively regulated by UV-B radiation. The expression patterns of unigenes encoding cinnamate-4-hydroxylase (C4H), 4-coumarate-CoA ligase (4CL), chalcone synthase (CHS), flavonol synthase (FLS), and dihydroflavonol reductase (DFR) differed between samples. This study represents the first investigation of the transcriptome of lettuce under UV-B radiation. The comparative bioinformatics analysis expands our understanding of plant responses to UV-B stress and its role in leaf coloration of lettuce. Our research also provides a bridge to extend studies to other economically important crops.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- PAL:
-
Phenylalanine ammonia-lyase
- C4H:
-
Cinnamate-4-hydroxylase
- 4CL:
-
4-Coumarate-CoA ligase
- CHS:
-
Chalcone synthase
- FLS:
-
Flavonol synthase
- DFR:
-
Dihydroflavonol-4-reductase
- UV-B:
-
Ultraviolet-B
- FDR:
-
False discovery rate
- DEGs:
-
Differentially expressed genes
- KEGG:
-
Kyoto encyclopedia of genes and genomes
- COG:
-
Clusters of orthologous groups of proteins
- GO:
-
Gene ontology
- FPKM:
-
Fragments per kilobase per million fragments
- SSR:
-
Simple sequence repeat
- SNP:
-
Single-nucleotide polymorphism
References
Abdelfatah A, Aranda X, Savé R, de Herralde F, Biel C (2013) Evaluation of the response of maximum daily shrinkage in young cherry trees submitted to water stress cycles in a greenhouse. Agric Water Manage 118:150–158. https://doi.org/10.1016/j.agwat.2012.10.027
Agati G, Brunetti C, Di Ferdinando M, Ferrini F, Pollastri S, Tattini M (2013) Functional roles of flavonoids in photoprotection: new evidence, lessons from the past. Plant Physiol Biochem 72:35–45. https://doi.org/10.1016/j.plaphy.2013.03.014
Alexieva V, Sergiev I, Mapelli S, Karanov E (2001) The effect of drought and ultraviolet radiation on growth and stress markers in pea and wheat Plant. Cell Environ 24:1337–1344. https://doi.org/10.1046/j.1365-3040.2001.00778.x
Ashraf M, Harris PJC (2013) Photosynthesis under stressful environments: an overview. Photosynthetica 51:163–190. https://doi.org/10.1007/s11099-013-0021-6
Audic S, Claverie J-M (1997) The significance of digital gene expression profiles. Genome Res 7:986–995. https://doi.org/10.1101/gr.7.10.986
Bairoch A, Boeckmann B (1991) The SWISS-PROT protein sequence data bank. Nucleic Acids Res 19:2247–2249
Barling A et al (2013) A detailed gene expression study of the Miscanthus genus reveals changes in the transcriptome associated with the rejuvenation of spring rhizomes. BMC Genomics 14:864. https://doi.org/10.1186/1471-2164-14-864
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B (Methodol) 57:289–300
Boyer JS (1976) Photosynthesis at low water potentials. Philos Trans R Soc Lond B Biol Sci 273:501–512
Bradshaw HD Jr, Schemske DW (2003) Allele substitution at a flower colour locus produces a pollinator shift in monkeyflowers. Nature 426:176. https://doi.org/10.1038/nature02106
Broun P (2005) Transcriptional control of flavonoid biosynthesis: a complex network of conserved regulators involved in multiple aspects of differentiation in Arabidopsis. Curr Opin Plant Biol 8:272–279. https://doi.org/10.1016/j.pbi.2005.03.006
Caldwell CR, Britz SJ (2006) Effect of supplemental ultraviolet radiation on the carotenoid and chlorophyll composition of green house-grown leaf lettuce (Lactuca sativa L.) cultivars. J Food Compos Anal 19:637–644. https://doi.org/10.1016/j.jfca.2005.12.016
Camire ME, Chaovanalikit A, Dougherty MP, Briggs J (2002) Blueberry and grape anthocyanins as breakfast cereal colorants. J Food Sci 67:438–441. https://doi.org/10.1111/j.1365-2621.2002.tb11425.x
Canli T et al (2016) Differential transcriptome expression in human nucleus accumbens as a function of loneliness. Mol Psychiatry 22:1069. https://doi.org/10.1038/mp.2016.186
Chalker-Scott L (1999) Environmental significance of anthocyanins in plant stress responses. Photochem Photobiol 70:1–9. https://doi.org/10.1111/j.1751-1097.1999.tb01944.x
Chen S et al (2013) Transcriptome analysis in sheepgrass (Leymus chinensis): a dominant perennial grass of the eurasian steppe. PLoS One 8:e67974. https://doi.org/10.1371/journal.pone.0067974
Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676. https://doi.org/10.1093/bioinformatics/bti610
Consortium GO (2004) The gene ontology (GO) database and informatics resource. Nucleic Acids Res 32:D258–D261. https://doi.org/10.1093/nar/gkh036
Crifò T, Puglisi I, Petrone G, Recupero GR, Lo Piero AR (2011) Expression analysis in response to low temperature stress in blood oranges: implication of the flavonoid biosynthetic pathway. Gene 476:1–9. https://doi.org/10.1016/j.gene.2011.02.005
DuPont MS, Mondin Z, Williamson G, Price KR (2000) Effect of variety, processing, and storage on the flavonoid glycoside content and composition of lettuce and endive. J Agric Food Chem 48:3957–3964. https://doi.org/10.1021/jf0002387
Eissa P, Babaeian M, Tavassoli A, Esmaeilian Y (2011) Effects of UV irradiation on plants. Afr J Microbiol Res 5:1710–1716. https://doi.org/10.5897/ajmr11.263
Escobar-Bravo R, Klinkhamer PGL, Leiss KA (2017) Interactive effects of UV-B light with abiotic factors on plant growth and chemistry, and their consequences for defense against arthropod herbivores. Front Plant Sci 8:278. https://doi.org/10.3389/fpls.2017.00278
Esringu A, Aksakal O, Tabay D, Kara AA (2016) Effects of sodium nitroprusside (SNP) pretreatment on UV-B stress tolerance in lettuce (Lactuca sativa L.) seedlings. Environ Sci Pollut Res 23:589–597. https://doi.org/10.1007/s11356-015-5301-1
Gazula A, Kleinhenz MD, Scheerens JC, Ling PP (2007) Anthocyanin levels in nine lettuce (Lactuca sativa) cultivars: influence of planting date and relations among analytic, Instrumented, and visual assessments of color. HortScience 42:232–238
Götz S et al (2008) High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res 36:3420–3435. https://doi.org/10.1093/nar/gkn176
Gowik U, Bräutigam A, Weber KL, Weber APM, Westhoff P (2011) Evolution of C4 photosynthesis in the genus flaveria: how many and which genes does it take to make C4? Plant Cell 23:2087–2105. https://doi.org/10.1105/tpc.111.086264
Grabherr MG et al (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652. https://doi.org/10.1038/nbt.1883
Guillaumie S et al (2011) Transcriptional analysis of late ripening stages of grapevine berry. BMC Plant Biol 11:165. https://doi.org/10.1186/1471-2229-11-165
Guo S et al (2010) Transcriptome sequencing and comparative analysis of cucumber flowers with different sex types. BMC Genomics 11:384. https://doi.org/10.1186/1471-2164-11-384
Holton TA, Cornish EC (1995) Genetics and biochemistry of anthocyanin biosynthesis. Plant Cell 7:1071–1083
Iseli C, Jongeneel C, Bucher P (1999) ESTScan: a program for detecting, evaluating, and reconstructing potential coding regions in EST sequences. Proc Int Conf Intell Syst Mol Biol 138–148
Jansen MAK, Martret BL, Koornneef M (2010) Variations in constitutive and inducible UV-B tolerance; dissecting photosystem II protection in Arabidopsis thaliana accessions. Physiol Plant 138:22–34. https://doi.org/10.1111/j.1399-3054.2009.01293.x
Jayaprakasam B, Vareed SK, Olson LK, Nair MG (2005) Insulin secretion by bioactive anthocyanins and anthocyanidins present in fruits. J Agric Food Chem 53:28–31. https://doi.org/10.1021/jf049018+
Jayaprakasam B, Olson LK, Schutzki RE, Tai M-H, Nair MG (2006) Amelioration of Obesity and glucose intolerance in high-fat-fed C57BL/6 mice by anthocyanins and ursolic acid in cornelian cherry (Cornus mas). J Agric Food Chem 54:243–248. https://doi.org/10.1021/jf0520342
Kanehisa M, Goto S (2000) KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28:27–30. https://doi.org/10.1093/nar/28.1.27
Kanehisa M et al (2006) From genomics to chemical genomics: new developments in KEGG. Nucleic Acids Res 34:D354–D357. https://doi.org/10.1093/nar/gkj102
Kanehisa M et al (2008) KEGG for linking genomes to life and the environment. Nucleic Acids Res 36:D480–D484. https://doi.org/10.1093/nar/gkm882
Kawanabe T, Fujimoto R, Sasaki T, Taylor JM, Dennis ES (2012) A comparison of transcriptome and epigenetic status between closely related species in the genus Arabidopsis. Gene 506:301–309. https://doi.org/10.1016/j.gene.2012.07.003
Khoo H-E, Prasad KN, Kong K-W, Jiang Y, Ismail A (2011) Carotenoids and their isomers: color pigments in fruits and vegetables. Molecules 16:1710
Kleinhenz MD, Gazula A, Scheerens JC, French DG (2003) Variety, shading, and growth stage effects on pigment concentrations in lettuce grown under contrasting temperature regimens. Horttechnology 13:677–683
Lagorce A, Fourçans A, Dutertre M, Bouyssiere B, Zivanovic Y, Confalonieri F (2012) Genome-wide transcriptional response of the archaeon Thermococcus gammatolerans to cadmium. PLoS One 7:e41935. https://doi.org/10.1371/journal.pone.0041935
Lei Z et al (2008) Antioxidant stress is promoted by nano-anatase in spinach chloroplasts under UV-B radiation. Biol Trace Elem Res 121:69–79. https://doi.org/10.1007/s12011-007-8028-0
Lepiniec L, Debeaujon I, Routaboul J-M, Baudry A, Pourcel L, Nesi N, Caboche M (2006) Genetics and biochemistry of seed flavonoids. Annu Rev Plant Biol 57:405–430. https://doi.org/10.1146/annurev.arplant.57.032905.105252
Li R, Li Y, Fang X, Yang H, Wang J, Kristiansen K, Wang J (2009a) SNP detection for massively parallel whole-genome resequencing. Genome Res 19:1124–1132. https://doi.org/10.1101/gr.088013.108
Li R, Yu C, Li Y, Lam T-W, Yiu S-M, Kristiansen K, Wang J (2009b) SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 25:1966–1967. https://doi.org/10.1093/bioinformatics/btp336
Lin Z, Li S, Chang D, Guizhu L, Yuebiao L, Shuxian L, Mianda C (1988) The changes of pigments, phenolics contents and activities of polyphenol oxidase and phenylalanine ammonia-lyse in pericarp of postharvest litchi fruit. Acta Bot Sin 30:40–45
Mancinelli AL (1985) Light-dependent anthocyanin synthesis: a model system for the study of plant photomorphogenesis. Bot Rev 51:107–157. https://doi.org/10.1007/bf02861059
Mazza CA, Zavala J, Scopel AL, Ballaré CL (1999) Perception of solar UVB radiation by phytophagous insects: behavioral responses and ecosystem implications. Proc Natl Acad Sci 96:980–985
Mazza CA, Boccalandro HE, Giordano CV, Battista D, Scopel AL, Ballaré CL (2000) Functional significance and induction by solar radiation of ultraviolet-absorbing sunscreens in field-grown soybean crops. Plant Physiol 122:117–126. https://doi.org/10.1104/pp.122.1.117
Meng X-l, Liu P, Jia F-l, Li J, Gao B-Q (2015) De novo transcriptome analysis of Portunus trituberculatus ovary and testis by RNA-Seq: identification of genes involved in gonadal development. PLoS One 10:e0128659. https://doi.org/10.1371/journal.pone.0128659
Mondello L, Cotroneo A, Errante G, Dugo G, Dugo P (2000) Determination of anthocyanins in blood orange juices by HPLC analysis. J Pharm Biomed Anal 23:191–195. https://doi.org/10.1016/S0731-7085(00)00269-7
Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5:621. https://doi.org/10.1038/nmeth.1226
Mulabagal V, Van Nocker S, Dewitt DL, Nair MG (2007) Cultivars of apple fruits that are not marketed with potential for anthocyanin production. J Agric Food Chem 55:8165–8169. https://doi.org/10.1021/jf0718300
Nicolle C et al (2004a) Health effect of vegetable-based diet: lettuce consumption improves cholesterol metabolism and antioxidant status in the rat. Clin Nutr 23:605–614. https://doi.org/10.1016/j.clnu.2003.10.009
Nicolle C et al (2004b) Characterisation and variation of antioxidant micronutrients in lettuce (Lactuca sativa folium). J Sci Food Agric 84:2061–2069. https://doi.org/10.1002/jsfa.1916
Oh M-M, Carey EE, Rajashekar CB (2009) Environmental stresses induce health-promoting phytochemicals in lettuce. Plant Physiol Biochem 47:578–583. https://doi.org/10.1016/j.plaphy.2009.02.008
Oh M-M, Carey EE, Rajashekar CB (2010) Regulated Water Deficits Improve Phytochemical Concentration in Lettuce. J Am Soc Hort Sci 135:223–229
Orshinsky AM, Hu J, Opiyo SO, Reddyvari-Channarayappa V, Mitchell TK, Boehm MJ (2012) RNA-Seq analysis of the Sclerotinia homoeocarpa—creeping bentgrass pathosystem. PLoS One 7:e41150. https://doi.org/10.1371/journal.pone.0041150
Park J-S et al (2007) Genes up-regulated during red coloration in UV-B irradiated lettuce leaves. Plant Cell Rep 26:507–516. https://doi.org/10.1007/s00299-006-0255-x
Park J-S, Kim J-B, Cho K-J, Cheon C-I, Sung M-K, Choung M-G, Roh K-H (2008) Arabidopsis R2R3-MYB transcription factor AtMYB60 functions as a transcriptional repressor of anthocyanin biosynthesis in lettuce (Lactuca sativa). Plant Cell Rep 27:985–994. https://doi.org/10.1007/s00299-008-0521-1
Patel RK, Jain M (2012) NGS QC toolkit: a toolkit for quality control of next generation sequencing data. PLoS One 7:e30619. https://doi.org/10.1371/journal.pone.0030619
Peng T et al (2013) Screening of UV-B-induced genes from apple peels by SSH: possible involvement of MdCOP1-mediated signaling cascade genes in anthocyanin accumulation. Physiol Plant 148:432–444. https://doi.org/10.1111/ppl.12002
Pertea G et al (2003) TIGR gene indices clustering tools (TGICL): a software system for fast clustering of large EST datasets. Bioinformatics 19:651–652. https://doi.org/10.1093/bioinformatics/btg034
Pruitt KD, Tatusova T, Maglott DR (2007) NCBI reference sequences (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res 35:D61–D65. https://doi.org/10.1093/nar/gkl842
Ramos SJ, Rutzke MA, Hayes RJ, Faquin V, Guilherme LRG, Li L (2011) Selenium accumulation in lettuce germplasm. Planta 233:649–660. https://doi.org/10.1007/s00425-010-1323-6
Rodriguez-Amaya DB (2010) Quantitative analysis, in vitro assessment of bioavailability and antioxidant activity of food carotenoids—a review. J Food Compos Anal 23:726–740. https://doi.org/10.1016/j.jfca.2010.03.008
Rozema J et al (2002) The role of UV-B radiation in aquatic and terrestrial ecosystems—an experimental and functional analysis of the evolution of UV-absorbing compounds. J Photochem Photobiol B Biol 66:2–12. https://doi.org/10.1016/S1011-1344(01)00269-X
Schaefer HM, Schaefer V, Levey DJ (2004) How plant–animal interactions signal new insights in communication. Trends Ecol Evol 19:577–584. https://doi.org/10.1016/j.tree.2004.08.003
Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3:1101. https://doi.org/10.1038/nprot.2008.73
Seeram NP, Cichewicz RH, Chandra A, Nair MG (2003) Cyclooxygenase inhibitory and antioxidant compounds from crabapple fruits. J Agric Food Chem 51:1948–1951. https://doi.org/10.1021/jf025993u
Steyn WJ, Wand SJE, Holcroft DM, Jacobs G (2002) Anthocyanins in vegetative tissues: a proposed unified function in photoprotection. New Phytol 155:349–361. https://doi.org/10.1046/j.1469-8137.2002.00482.x
Stracke R et al (2010) The Arabidopsis bZIP transcription factor HY5 regulates expression of the PFG1/MYB12 gene in response to light and ultraviolet-B radiation plant. Cell Environ 33:88–103. https://doi.org/10.1111/j.1365-3040.2009.02061.x
Sun Y et al (2013) Transcriptome exploration in Leymus chinensis under saline-alkaline treatment using 454 pyrosequencing. PLoS One 8:e53632. https://doi.org/10.1371/journal.pone.0053632
Surget-Groba Y, Montoya-Burgos JI (2010) Optimization of de novo transcriptome assembly from next-generation sequencing data. Genome Res 20:1432–1440. https://doi.org/10.1101/gr.103846.109
Takahama U (2004) Oxidation of vacuolar and apoplastic phenolic substrates by peroxidase: physiological significance of the oxidation reactions. Phytochem Rev 3:207–219. https://doi.org/10.1023/B:PHYT.0000047805.08470.e3
Tall JM, Seeram NP, Zhao C, Nair MG, Meyer RA, Raja SN (2004) Tart cherry anthocyanins suppress inflammation-induced pain behavior in rat. Behav Brain Res 153:181–188. https://doi.org/10.1016/j.bbr.2003.11.011
Tatusov RL, Koonin EV, Lipman DJ (1997) A genomic perspective on protein families. Science 278:631–637. https://doi.org/10.1126/science.278.5338.631
Tatusov RL et al (2003) The COG database: an updated version includes eukaryotes. BMC Bioinform 4:41. https://doi.org/10.1186/1471-2105-4-41
Teramura AH (1983) Effects of ultraviolet-B radiation on the growth and yield of crop plants. Physiol Plant 58:415–427
Toledo-Silva G, Cardoso-Silva CB, Jank L, Souza AP (2013) De Novo transcriptome assembly for the tropical grass panicum maximum Jacq. PLoS One 8:e70781. https://doi.org/10.1371/journal.pone.0070781
Trapnell C et al (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28:511. https://doi.org/10.1038/nbt.1621
Tsormpatsidis E, Henbest RGC, Battey NH, Hadley P (2010) The influence of ultraviolet radiation on growth, photosynthesis and phenolic levels of green and red lettuce: potential for exploiting effects of ultraviolet radiation in a production system. Ann Appl Biol 156:357–366. https://doi.org/10.1111/j.1744-7348.2010.00393.x
Ubi BE, Honda C, Bessho H, Kondo S, Wada M, Kobayashi S, Moriguchi T (2006) Expression analysis of anthocyanin biosynthetic genes in apple skin: effect of UV-B and temperature. Plant Sci 170:571–578. https://doi.org/10.1016/j.plantsci.2005.10.009
Varshney RK, Graner A, Sorrells ME (2005) Genic microsatellite markers in plants: features and applications. Trends Biotechnol 23:48–55. https://doi.org/10.1016/j.tibtech.2004.11.005
Wang H, Nair MG, Strasburg GM, Chang Y-C, Booren AM, Gray JI, DeWitt DL (1999) Antioxidant and antiinflammatory activities of anthocyanins and their aglycon, cyanidin, from tart cherries. J Nat Prod 62:294–296. https://doi.org/10.1021/np980501m
Wang Z, Gerstein M, Snyder M (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10:57. https://doi.org/10.1038/nrg2484
Wilhelm BT et al (2008) Dynamic repertoire of a eukaryotic transcriptome surveyed at single-nucleotide resolution. Nature 453:1239. https://doi.org/10.1038/nature07002
Winkel-Shirley B (2001) Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiol 126:485–493. https://doi.org/10.1104/pp.126.2.485
Wolf JBW (2013) Principles of transcriptome analysis and gene expression quantification: an RNA-seq tutorial. Mol Ecol Resour 13:559–572. https://doi.org/10.1111/1755-0998.12109
Xu H, Gao Y, Wang J (2012) Transcriptomic analysis of rice (Oryza sativa) developing embryos using the RNA-Seq technique. PLoS One 7:e30646. https://doi.org/10.1371/journal.pone.0030646
Yamasaki H, Sakihama Y, Ikehara N (1997) Flavonoid-peroxidase reaction as a detoxification mechanism of plant cells against H2O2. Plant Physiol 115:1405–1412. https://doi.org/10.1104/pp.115.4.1405
Zhang L, Wang Y, Sun M, Wang J, Kawabata S, Li Y (2014) BrMYB4, a suppressor of genes for phenylpropanoid and anthocyanin biosynthesis, is down-regulated by UV-B but not by pigment-inducing sunlight in turnip cv. Tsuda. Plant Cell Physiol 55:2092–2101. https://doi.org/10.1093/pcp/pcu137
Zhou ZS, Yang SN, Li H, Zhu CC, Liu ZP, Yang ZM (2013) Molecular dissection of mercury-responsive transcriptome and sense/antisense genes in Medicago truncatula. J Hazard Mater 252–253:123–131. https://doi.org/10.1016/j.jhazmat.2013.02.011
Zlatev ZS, Lidon FJC, Kaimakanova M (2012) Plant physiological responses to UV-B radiation Emirates. J Food Agric 24:481–501. https://doi.org/10.9755/ejfa.v24i6.14669
Acknowledgements
The work was supported by the National Natural Science Foundation of China (NSFC Grant number: 31501762); Scientific Research Project of Shanghai Science and Technology Commission (Grant number: 153919N1600). The funding body has not participated in or interfered with the research.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by M. Stobiecki.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Zhang, L., Gong, F., Song, Y. et al. De novo transcriptome analysis of lettuce (Lactuca sativa L.) and the identification of structural genes involved in anthocyanin biosynthesis in response to UV-B radiation. Acta Physiol Plant 41, 148 (2019). https://doi.org/10.1007/s11738-019-2941-7
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11738-019-2941-7