Abstract
Anthocyanin biosynthesis in Litchi chinensis is promoted by exogenous abscisic acid (ABA) treatment and inhibited by exogenous N-(2-chloro-pyridin-4-yl)-N′-phenylurea (CPPU) application. However, the mechanisms by which ABA or CPPU regulates anthocyanin biosynthesis are still unclear. To understand the global molecular events of these physiological changes, transcriptome profiling was analyzed in L. chinensis cv. Feizixiao pericarps after 0, 10, and 20 days of exogenous ABA (25 mg/L ABA) and CPPU (4 mg/L) treatment using RNA-seq. Compared with the control, a total of 579 and 827 genes were differently expressed [|log2 fold change| ≥ 1 and P value ≤ 0.005] in ABA- and CPPU-treated pericarp, respectively. Exogenous ABA up-regulated the expressions of genes involved in flavonoid and anthocyanin biosynthesis, including PAL, C4H, CHS, CHI, DFR, LDOX, and GTs. In contrast, exogenous CPPU induced genes related to carbon metabolism, amino acids biosynthesis, and photosynthesis, and down-regulated genes related to anthocyanin biosynthesis. Comparison of transcriptomes in responses to individual treatments with ABA or CPPU revealed that there were cooperative and antagonistic interplay between ABA and cytokinins in litchi fruit ripening. ABA treatment had no significant effect on the genes related to chlorophyll catabolism. On the other hand, CPPU treatment significantly increased the expression of chlorophyll synthesis genes and inhibited the expression of chlorophyll degradation gene (SGR). In addition, ABA and CPPU treatment also affected gene expression in other plant hormone signaling pathways, such as auxin, GA, and ethylene, forming a complex network to regulate anthocyanin biosynthesis. This study provides a valuable overview of global molecular events for studying the mechanisms by which ABA and cytokinins influence anthocyanin biosynthesis in litchi and other fruit trees enriched with anthocyanins.
Similar content being viewed by others
Abbreviations
- 2,4-D:
-
2,4-Dichlorophenoxyacetic acid
- ABA:
-
Abscisic acid
- BA:
-
6-benzylaminopurine
- bHLH:
-
Basic helix-loop-helix
- CTK:
-
Cytokinin
- CPPU:
-
N-(2-chloro-pyridin-4-yl)-N′-phenylurea
- DEGs:
-
Differentially expressed genes
- DFR:
-
Dihydroflavonol-4-reductase
- GAs:
-
Gibberellins
- IAA:
-
Indole-3-acetic acid
- MeJA:
-
Methyl jasmonate
- NAA:
-
Naphthalene acetic acid
- NDGA:
-
Nordihydroguaiaretic acid
- PGRs:
-
Plant growth regulators
- TF:
-
Transcription factor
References
Arnon DI (1949) Copper enzymes in isolated chloroplasts polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15
Bottcher C, Harvey K, Forde CG, Boss PK, Davies C (2011) Auxin treatment of pre-veraison grape (Vitis vinifera L.) berries both delays ripening and increases the synchronicity of sugar accumulation. Aust J Grape Wine Res 17:1–8
Chen J, Mao L, Lu W, Ying T, Luo Z (2016) Transcriptome profiling of postharvest strawberry fruit in response to exogenous auxin and abscisic acid. Planta 243:183–197
Cowan AK, Cairns ALP, Bartels-Rahm B (1999) Regulation of abscisic acid metabolism: towards a metabolic basis for abscisic acid–cytokinin antagonism. J Exp Bot 50:595–603
Das PK, Shin DH, Choi SB, Park YI (2012) Sugar-hormone cross-talk in anthocyanin biosynthesis. Mol Cells 34:501–507
Deikman J, Hammer PE (1995) Induction of anthocyanin accumulation by cytokinins in Arabidopsis thaliana. Plant Physiol 108:47–57
Gan S, Amasino RM (1995) Inhibition of leaf senescence by autoregulated production of cytokinin. Science 270:1986–1988
Guo JC, Hu XW, Duan RJ (2005) Interactive effects of CKs, light and sucrose on the phenotypes and the syntheses of anthocyanins, lignins in cytokinin over-producing transgenic Arabidopsis. J Plant Growth Regul 24:93–101
Hu B, Zhao J, Lai B, Qin Y, Wang H, Hu G (2016) LcGST4 is an anthocyanin-related glutathione S-transferase gene in Litchi chinensis Sonn. Plant Cell Rep 35:831–843
Huang X, Zeng L, Huang HB (2005) Lychee and longan production in China. Acta Hortic 665:27–36
Jeong SW, Das PK, Jeoung SC, Song JY, Lee HK, Kim YK, Kim WJ, Park YI, Yoo SD, Choi SB, Choi G, Park YI (2010) Ethylene suppression of sugar-induced anthocyanin pigmentation in Arabidopsis. Plant Physiol 154:1515–1531
Ji XH, Wang YT, Zhang R, Wu SJ, An MM, Li M, Wang CZ, Chen XL, Zhang YM, Chen XS (2015) Effect of auxin, cytokinin and nitrogen on anthocyanin biosynthesis in callus cultures of red-fleshed apple (Malus sieversii f. niedzwetzkyana). Plant Cell Tissue Organ Cult 120:325–337
Jia HF, Chai YM, Li CL, Lu D, Luo JJ, Qin L, Shen YY (2011) Abscisic acid plays an important role in the regulation of strawberry fruit ripening. Plant Physiol 157:188–199
Jiang YM, Joyce DC (2003) ABA effects on ethylene production, PAL activity, anthocyanin and phenolic contents of strawberry fruit. Plant Growth Regul 39:171–174
Jiang JP, Su MX, Lee PM (1986) The production and physiological effects of ethylene during ontogeny and after harvest of litchi fruits. Acta Phytophysiol Sin 12:95–103
Kim JS, Lee BH, Kim SH, Oh KH, Yun Cho K (2006) Response to environmental and chemical signals for anthocyanin biosynthesis in nonchlorophyllous corn (Zea mays L.) leaf. J Plant Biol 49:16–25
Kumar R, Khurana A, Sharma AK (2014) Role of plant hormones and their interplay in development and ripening of fleshy fruits. J Exp Bot 65:4561–4575
Lai B, Li XJ, Hu B, Qin YH, Huang XM, Wang HC, Hu GB (2014) LcMYB1 is a key determinant of differential anthocyanin accumulation among genotypes, tissues, developmental phases and ABA and light stimuli in Litchi chinensis. PLoS ONE 9(1):e86293
Lai B, Hu B, Qin YH, Zhao JT, Wang HC, Hu GB (2015) Transcriptomic analysis of Litchi chinensis pericarp during maturation with a focus on chlorophyll degradation and flavonoid biosynthesis. BMC Genomics 16:225
Lee HS, Wicker L (1991) Anthocyanin pigments in the skin of lychee fruit. J Food Sci 56:466–468
Leng P, Yuan B, Guo Y (2014) The role of abscisic acid in fruit ripening and responses to abiotic stress. J Exp Bot 65(16):4577–4588
Li XJ, Lai B, Zhao JT, Qin YH, He JM, Huang XM, Wang HC, Hu GB (2016a) Sequence differences in LcFGRT4 alleles are responsible for the diverse anthocyanin composition in the pericarp of Litchi chinensis. Mol Breed 36:93
Li S, Wang W, Gao J, Yin K, Wang R, Wang C, Petersen M, Mundy J, Qiu JL (2016b) MYB75 phosphorylation by MPK4 is required for light-induced anthocyanin accumulation in Arabidopsis. Plant Cell 28(11):2866
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
Lloyd A, Brockman A, Aguirre L, Campbell A, Bean A, Cantero A, Gonzalez A (2017) Advances in the MYB-bHLH-WD repeat (MBW) pigment regulatory model: addition of a WRKY factor and co-option of an anthocyanin MYB for betalain regulation. Plant Cell Physiol 58:1431–1441
Loreti E, Povero G, Novi G, Solfanelli C, Alpi A, Perata P (2008) Gibberellins, jasmonate and abscisic acid modulate the sucrose-induced expression of anthocyanin biosynthetic genes in Arabidopsis. New Phytol 179:1004–1016
McAtee P, Karim S, Schaffer R, David K (2013) A dynamic interplay between phytohormones is required for fruit development, maturation, and ripening. Front Plant Sci 4:79
Medina-Puche L, Cumplido-Laso G, Amil-Ruiz F, Hoffmann T, Ring L, Rodríguez-Franco A, Caballero JL, Schwab W, Muñoz-Blanco J, Blanco-Portales R (2014) MYB10 plays a major role in the regulation of flavonoid/phenylpropanoid metabolism during ripening of Fragaria × ananassa fruits. J Exp Bot 65:401–417
Minana FMH, Primomillo E, Primomillo J (1989) Isolation and identification of cytokinins from developing citrus-fruits. Citriculture 1–4:367–379
Rodyoung A, Masuda Y, Tomiyama H, Saito T, Okawa K, Ohara H, Kondo S (2016) Effects of light emitting diode irradiation at night on abscisic acid metabolism and anthocyanin synthesis in grapes in different growing seasons. Plant Growth Regul 79:39–46
Shen XJ, Zhao K, Liu LL, Zhang KC, Huazhao Yuan HZ, Liao X, Wang Q, Xinwei Guo XW, Li F, Li TH (2014) A role for PacMYBA in ABA-regulated anthocyanin biosynthesis in red-colored sweet cherry cv. Hong Deng (Prunus avium L.). Plant Cell Physiol 55(5):862–880
Singh SP, Saini MK, Singh J, Pongener A, Sidhu GS (2014) Preharvest application of abscisic acid promotes anthocyanins accumulation in pericarp of litchi fruit without adversely affecting postharvest quality. Postharvest Biol Technol 96:14–22
Sun T, Gubler F (2004) Molecular mechanism of gibberellin signaling in plants. Annu Rev Plant Biol 55(1):197–223
Teng S, Keurentjes J, Bentsink L, Koornneef M, Smeekens S (2005) Sucrose-specific induction of anthocyanin biosynthesis in Arabidopsis requires the MYB75/PAP1 gene. Plant Physiol 139:1840–1852
Thiruvengadam M, Baskar V, Kim SH, Chung IM (2016) Effects of abscisic acid, jasmonic acid and salicylic acid on the content of phytochemicals and their gene expression profiles and biological activity in turnip (Brassica rapa ssp. rapa). Plant Growth Regul 80:377–390
Wang H, Huang H, Huang X (2007) Differential effects of abscisic acid and ethylene on the fruit maturation of Litchi chinensis Sonn. Plant Growth Regul 52:189–198
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 Litchi chinensis Sonn. PLoS ONE 6:e19455
Wheeler S, Loveys B, Ford C, Davies C (2009) The relationship between the expression of abscisic acid biosynthesis genes, accumulation of abscisic acid and the promotion of Vitis vinifera L. berry ripening by abscisic acid. Aust J Grape Wine Res 15:195e204
Wrolstad RE, Culbertson JD, Cornwell CJ, Mattick LR (1982) Detection of adulteration in blackberry juice concentrates and wines. J Assoc Off Anal Chem 65:1417–1423
Xu W, Dubos C, Lepiniec L (2015) Transcriptional control of flavonoid biosynthesis by MYB-bHLH-WDR complexes. Trends Plant Sci 20:176–185
Zhang HN, Li WC, Wang HC, Shi SY, Shu B, Liu LQ, Wei YZ, Xie JH (2016) Transcriptome profiling of light-regulated anthocyanin biosynthesis in the pericarp of litchi. Front Plant Sci 7:963
Acknowledgements
The paper was supported by the Pearl River S&T Nova Program of Guangzhou (No. 201610010147), China Litchi and Longan Industry Technology Research System (Project No. CARS-32-05), and YangFan Innovative & Entrepreneurial Research Team Project (No. 2014YT02H013).
Availability of supporting data
All of the raw reads are available in the NCBI Sequence Read Archive database (Accession Number PRJNA415698).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Hu, B., Li, J., Wang, D. et al. Transcriptome profiling of Litchi chinensis pericarp in response to exogenous cytokinins and abscisic acid. Plant Growth Regul 84, 437–450 (2018). https://doi.org/10.1007/s10725-017-0351-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10725-017-0351-7