Extensive transcriptome changes underlying the fruit skin colour intensity variation in purple eggplant

  • Xiaohui ZHOU Institute of Vegetable Crops, Jiangsu Academy of Agricultural Sciences, Jiangsu Key Laboratory for Horticultural Crop Genetic Improvement, Nanjing 210095 (CN)
  • Songyu LIU Institute of Vegetable Crops, Jiangsu Academy of Agricultural Sciences, Jiangsu Key Laboratory for Horticultural Crop Genetic Improvement, Nanjing 210095 (CN)
  • Yaping LIU Institute of Vegetable Crops, Jiangsu Academy of Agricultural Sciences, Jiangsu Key Laboratory for Horticultural Crop Genetic Improvement, Nanjing 210095 (CN)
  • Jun LIU Institute of Vegetable Crops, Jiangsu Academy of Agricultural Sciences, Jiangsu Key Laboratory for Horticultural Crop Genetic Improvement, Nanjing 210095 (CN)
  • Yan YANG Institute of Vegetable Crops, Jiangsu Academy of Agricultural Sciences, Jiangsu Key Laboratory for Horticultural Crop Genetic Improvement, Nanjing 210095 (CN)
  • Dan WANG Institute of Vegetable Crops, Jiangsu Academy of Agricultural Sciences, Jiangsu Key Laboratory for Horticultural Crop Genetic Improvement, Nanjing 210095 (CN)
  • Yong ZHUANG Institute of Vegetable Crops, Jiangsu Academy of Agricultural Sciences, Jiangsu Key Laboratory for Horticultural Crop Genetic Improvement, Nanjing 210095 (CN)
Keywords: anthocyanin, colour intensity, eggplant, flavonoid biosynthesis, transcriptome

Abstract

Fruit skin colour intensity is one of the most important economic traits of purple eggplant. A wide diversity for fruit skin colour intensity exists in purple eggplant and the accumulation of anthocyanins and chlorophylls of fruit skin mainly affected colour intensity. However, limited information is available contributing to the molecular mechanisms underlying fruit skin colour intensity variation in purple eggplant. In the present study, variation of two purple eggplant advanced lines EP26 and EP28, with different fruit skin colour intensity was investigated. Higher anthocyanin contents and lower chlorophyll contents were observed in EP26 with deeper fruit skin colour intensity at two developmental stages. Comparative transcriptome analysis of EP26 and EP28 identified a total of 2218 differential expressed genes (DEGs) at two developmental stages. Kyoto Encyclopaedia of Genes and Genomes (KEGG) pathway enrichment analysis showed that these DEGs were mainly involved in flavonoid biosynthesis and photosynthesis. In addition, a total of 131 transcription factors including MYB, bHLH, WRKY, and NAC exhibited dynamic changes, which might be responsible for the variation of fruit pigments accumulation between EP26 and EP28. Taken together, these results expand our knowledge of molecular mechanisms underlying fruit skin colour intensity variation in eggplant, which allowing for improvement of fruit coloration in eggplant breeding.

Metrics

Metrics Loading ...

References

Azuma K, Ohyama A, Ippoushi K, Ichiyanagi T, Takeuchi A, Saito T, Fukuoka H (2008). Structures and antioxidant activity of anthocyanins in many accessions of eggplant and its related species. Journal of Agricultural and Food Chemistry 56:10154-10159. http://doi.org/10.1021/jf801322m

Beale SL (2005). Green genes gleaned. Trends in Plant Science 10:309-312. http://doi.org/10.1016/j.tplants.2005.05.005

Boss PK, Davies C, Robinson SP (1996). Analysis of the expression of anthocyanin pathway genes in developing Vitis vinifera L. cv Shiraz grape berries and the implications for pathway regulation. Plant Physiology 111(4):1059-1066. http://doi.org/10.1104/pp.111.4.1059

Cericola F, Portis E, Lanteri S, Toppino L, Barchi L, Acciarri N, Pulcini L, Sala T, Rotino GL (2014). Linkage disequilibrium and genome-wide association analysis for anthocyanin pigmentation and fruit color in eggplant. BMC Genomics 15:896. http://doi.org/10.1186/1471-2164-15-896

Florea L, Salzberg SL (2013). Thousands of exon skipping events differentiate among splicing patterns in sixteen human tissues. F1000Res. 2:188. http://doi.org/10.12688/f1000research.2-188.v1

Gao L, Yang H, Liu H, Yang J, Hu Y (2016). Extensive transcriptome changes underlying the flower color intensity variation in Paeonia ostii. Frontiers in Plant Science 6:1205. http://doi.org/10.3389/fpls.2015.01205

He YJ, Chen H, Zhou L, Liu Y, Chen HY (2019). Comparative transcription analysis of photosensitive and non-photosensitive eggplants to identify genes involved in dark regulated anthocyanin synthesis. BMC Genomics 20:678. https://doi.org/10.1186/s12864-019-6023-4

Hu DG, Sun CH, Ma QJ, You CX, Cheng L, Hao YJ (2016). MdMYB1 regulates anthocyanin and malate accumulation by directly facilitating their transport into vacuoles in apples. Plant Physiology 170(3):1315-30. http://doi.org/10.1104/pp.15.01333

Huang J, Xing M, Li Y, Cheng F, Gu H, Yue C, Zhang Y (2019). Comparative transcriptome analysis of the skin-specific accumulation of anthocyanins in black peanut (Arachis hypogaea L.). Journal of Agricultural and Food Chemistry 67:1312-1324. http://doi.org/10.1021/acs.jafc.8b05915

Jiang MM, Liu Y, Ren L, Lian HL, Chen HY (2016a). Molecular cloning and characterization of anthocyanin biosynthesis genes in eggplant (Solanum melongena L.). Acta Physiologia Plantarum 38(7):163. http://doi.org/10.1007/s11738-016-2172-0

Jiang MM, Ren L, Lian HL, Liu Y, Chen HY (2016b). Novel insight into the mechanism underlying light-controlled anthocyanin accumulation in eggplant (Solanum melongena L.). Plant Science 249:46-58. http://doi.org/10.1016/j.plantsci.2016.04.001

Jin S, Rahim MA, Afrin KS, Park J, Kang J, Nou I (2018). Transcriptome profiling of two contrasting ornamental cabbage (Brassica oleracea var. acephala) lines provides insights into purple and white inner leaf pigmentation. BMC Genomics 19:797. http://doi.org/10.1186/s12864-018-5199-3

Kim SH, Lee JR, Hong ST, Yoo YK, An G, Kim SR (2003). Molecular cloning and analysis of anthocyanin biosynthesis genes preferentially expressed in apple skin. Plant Science 165:403-413. http://doi.org/10.1016/S0168-9452(03)00201-2

Kumar AM, Söll D (2000). Antisense HEMA1 RNA expression inhibits heme and chlorophyll biosynthesis in Arabidopsis. Plant Physiology 122 (1):49-56. http://doi.org/10.1104/pp.122.1.49

Lee J, He K, Stolc V, Lee H, Figueroa P, Gao Y, Tongprasit W, Zhao H, Lee I, Denga XW (2007). Analysis of transcription factor HY5 genomic binding sites revealed its hierarchical role in light regulation of development. Plant Cell 19:731-749. http://doi.org/10.1105/tpc.106.047688

Li J, He YJ, Zhou L, Liu Y, Jiang MM, Ren L, Chen HY (2018). Transcriptome profiling of genes related to light-induced anthocyanin biosynthesis in eggplant (Solanum melongena L.) before purple color becomes evident. BMC Genomics 19: 201. https://doi.org/10.1186/s12864-018-4587-z

Li J, Ren L, Gao Z, Jiang MM, Liu Y, Zhou L, He YJ, Chen HY (2017). Combined transcriptomic and proteomic analysis constructs a new model for light-induced anthocyanin biosynthesis in eggplant (Solanum melongena L.). Plant Cell and Environment 40:3069-3087. https://doi.org/10.1111/pce.13074

Li LZ, He YJ, Ge HY, Liu Y, Chen HY (2021). Functional characterization of SmMYB86, a negative regulator of anthocyanin biosynthesis in eggplant (Solanum melongena L.). Plant Science 302:110696. http://doi.org/10.1016/j.plantsci.2020.110696

Li W, Yang S, Lu Z, He Z, Ye Y, Zhao B, Wang L, Jin B (2018). Cytological, physiological, and transcriptomic analyses of golden leaf coloration in Ginkgo biloba L. Horticulture Research 5:12. http://doi.org/10.1038/s41438-018-0015-4

Li YY, Mao K, Zhao C, Zhao XY, Zhang HL, Shu HR, Hao YJ (2012). MdCOP1 ubiquitin E3 ligases interact with MdMYB1 to regulate light-induced anthocyanin biosynthesis and red fruit coloration in apple. Plant Physiology 160:1011-1022. https://doi.org/10.1104/pp.112.199703

Liu Y, Tikunov Y, Schouten RE, Marcelis LFM, Visser RGF, Bovy A (2018). Anthocyanin biosynthesis and degradation mechanisms in Solanaceous vegetables: a review. Frontiers in Chemistry 6:52. http://doi.org/10.3389/fchem.2018.00052

Livak KJ, Schmittgen TD (2001). Analysis of relative gene expression data using real-time quantitative PCR and 2(-Delta Delta C(T)) method. Methods 25:402-408. https://doi.org/10.1006/meth.2001.1262

Love MI, Huber W, Anders S (2014). Moderated estimation of fold change and dispersion for RNA-Seq data with DESeq2. Genome Biology 15: 550. http://doi.org/10.1186/s13059-014-0550-8

McCormac AC, Terry MJ (2002). Light-signalling pathways leading to the co-ordinated expression of HEMA1 and Lhcb during chloroplast development in Arabidopsis thaliana. The Plant Journal 32:549-559. http://doi.org/10.1046/j.1365-313X.2002.01443.x

Nothmann J, Rylski I, Spigelman M (1976). Color and variations in color intensity of fruit of eggplant cultivars. Scientia Horticulture 4:191-197. http://doi.org/10.1016/S0304-4238(76)80012-X

Ohmiya A, Sasaki K, Nashima K, Oda-Yamamizo C, Hirashima M, Sumitomo K (2017). Transcriptome analysis in petals and leaves of chrysanthemums with different chlorophyll levels. BMC Plant Biology 17:202. http://doi.org/10.1186/s12870-017-1156-6

Qi TC, Song SS, Xie DX (2011). The jasmonate-ZIM-Domain proteins interact with the WD-Repeat/bHLH/MYB complexes to regulate jasmonate-mediated anthocyanin accumulation and trichome initiation in Arabidopsis thaliana. Plant Cell 5:1795-1814. http://doi.org/10.1105/tpc.111.083261

Reinbothe C, Bakkouri ME, Buhr F, Muraki N, Nomata J, Kurisu G, Fujita Y, Reinbothe S (2010). Chlorophyll biosynthesis: spotlight on protochlorophyllide reduction. Trends in plant science 15(11):614-24. http://doi.org/10.1016/j.tplants.2010.07.002

Sadilova E, Stintzing FC, Carle R (2006). Anthocyanins, colour and antioxidant properties of eggplant (Solanum melongena L.) and violet pepper (Capsicum annuum L.) peel extracts. Zeitschrift für Naturforschung 61c:527-535. http://doi.org/10.1515/znc-2006-7-810

Stommel JR, Dumm JM (2015). Coordinated regulation of biosynthetic and regulatory genes coincides with anthocyanin accumulation in developing eggplant fruit. Journal of American Society for Horticultural Science 140(2):129-135. https://doi.org/10.21273/JASHS.140.2.129

Toppino L, Barchi L, Mercati F, Acciarri N, Perrone D, Martina M, … Rotino GL (2020). A new intra-specific and high-resolution genetic map of eggplant based on a RIL population, and location of QTLs related to plant anthocyanin pigmentation and seed vigour. Genes 11:745. https://doi.org/10.3390/genes11070745

Toppino L, Barchi L, Scalzo RL, Palazzolo E, Francese G, Fibiani M, … Rotino G (2016). Mapping quantitative trait loci affecting biochemical and morphological fruit properties in eggplant (Solanum melongena L.). Frontiers in Plant Science 7:256. http://doi.org/10.3389/fpls.2016.00256

Wang N, Liu W, Zhang T, Jiang S, Xu H, Wang Y, … Chen X (2018). Transcriptomic analysis of red-fleshed apples reveals the novel role of MdWRKY11 in flavonoid and anthocyanin biosynthesis. Journal of Agricultural and Food Chemistry 66:7076-7086. http://doiorg/10.1021/acs.jafc.8b01273

Waters MT, Wang P, Korkaric M, Capper RG, Saunders NJ, Langdale JA (2009). GLK transcription factors coordinate expression of the photosynthetic apparatus in Arabidopsis. Plant Cell 21:1109-28. http://doi.org/10.1105/tpc.108.065250

Wei YZ, Hu FC, Hu GB, Li XJ, Huang XM, Wang HC (2011). Differential expression of anthocyanin biosynthetic genes in relation to anthocyanin accumulation in the pericarp of Lithi chinensis Sonn. PLoS One 6(4):e19455. http://doi.org/10.1371/journal.pone.0019455

Xie C, Mao X, Huang J, Ding Y, Wu J, Dong S, Kong L, Gao G, Li C, Wei L (2011). KOBAS 2.0: A web server for annotation and identification of enriched pathways and diseases. Nucleic Acids Research 39:316-322. http://doi.org/10.1093/nar/gkr483

Xie XB, Li S, Zhang RF, Zhao J, Chen YC, Zhao Q, … Hao YJ (2012). The bHLH transcription factor MdbHLH3 promotes anthocyanin accumulation and fruit colouration in response to low temperature in apples. Plant Cell and Environment 35:1884-1897. http://doi.org/10.1111/j.1365-3040.2012.02523.x

Zhang L, Xu B, Wu T, Yang Y, Fan L, Wen M, Sui J (2017). Transcriptomic profiling of two pak choi varieties with contrasting anthocyanin contents provides an insight into structural and regulatory genes in anthocyanin biosynthetic pathway. BMC Genomics 18:288. http://doi.org/10.1186/s12864-017-3677-7

Zhang SM, Zhang AD, Wu XX, Zhu ZW, Yang ZF, Zhu YL, Zha DS (2019). Transcriptome analysis revealed expression of genes related to anthocyanin biosynthesis in eggplant (Solanum melongena L.) under high-temperature stress. BMC Plant Biology 19:387. https://doi.org/10.1186/s12870-019-1960-2

Zhang Y, Butelli E, Martin C (2014). Engineering anthocyanin biosynthesis in plants. Current Opinion in Plant Biology 19:81-90. http://doi.org/10.1016/j.pbi.2014.05.011

Zhang Y, Hu Z, Chu G, Huang C, Tian S, Zhao Z, Chen G (2014). Anthocyanin accumulation and molecular analysis of anthocyanin biosynthesis-associated genes in eggplant (Solanum melongena L.). Journal of agricultural and food chemistry 62:2906-2912. http://doi.org/10.1021/jf404574c

Zhou H, Kui L, Wang H, Gu C, Dare AP, Espley R, He H, Allan AC, Han Y (2015). Molecular genetics of blood-fleshed peach reveals activation of anthocyanin biosynthesis by NAC transcription factors. The Plant Journal 82(1):105-121. http://doi.org/10.1111/tpj.12792

Published
2021-09-24
How to Cite
ZHOU, X., LIU, S., LIU, Y., LIU, J., YANG, Y., WANG, D., & ZHUANG, Y. (2021). Extensive transcriptome changes underlying the fruit skin colour intensity variation in purple eggplant. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 49(3), 12434. https://doi.org/10.15835/nbha49312434
Section
Research Articles
CITATION
DOI: 10.15835/nbha49312434