Abstract
The functions of l-isoleucine (Ile) in anthocyanin biosynthesis were investigated in apple fruit. Whole trees (Malus × domestica Bokh.) were treated with Ile or n-propyl dihydrojasmonate (PDJ), which is a jasmonic acid (JA) analog, 20 and 30 days before harvest. Both Ile and PDJ treatments stimulated anthocyanin formation at 30 and 35 days after treatment (DAT). The expressions of MdUF3GT and MdMYB1 genes under the Ile and PDJ treatments were higher than those in the untreated control at 19 and 30 DAT. Endogenous JA and jasmonoyl-l-isoleucine (JA-Ile) concentrations in Ile- and PDJ- treated fruit were increased at 19 and 30 DAT. At 30 DAT, the Ile and PDJ treatments stimulated the expressions of MdJAR1, which is related to the conjugation of JA to Ile, and MdMYC2, which is a transcription factor in the JA response. Our study suggests that Ile can induce anthocyanin formation depending on the increase of JA-Ile production and the up-regulation of MdJAR1 and MdMYC2 in apples.
Similar content being viewed by others
Abbreviations
- PDJ:
-
n-Propyl dihydrojasmonate
- l-Ile:
-
Isoleucine
- JA:
-
Jasmonic acid
- 2,4-DP:
-
2, 4-Dichlorophenoxylpropionic acid
- JA-Ile:
-
Jasmonoyl-l-isoleucine
- ACC:
-
1-Aminocyclopropane-1-carboxylic acid
- ACS:
-
ACC synthase
- ACO:
-
ACC oxidase
- UFGT:
-
UDP-glucose-flavonoid 3-O-glucosyltransferase
References
An JP, Li HH, Song LQ, Su L, Liu X, You CX, Wang XF, Hao YJ (2016) The molecular cloning and functional characterization of MdMYC2, abHLH transcription factor in apple. Plant Physiol Biochem 108:24–31
An XH, Tian Y, Chen KQ, Liu D, Xie XB, Cheng CG, Cong PH, Hao YJ (2015) MdMYB9 and MdMYB11 are involved in the regulation of the JA-induced biosynthesis of anthocyanin and proanthocyanidin in apples. Plant Cell Physiol 56:650–662
Chen KE, Zhao XY, An XH, Liu DD, You CX, Hao YJ (2017) MdHIR proteins repress anthocyanin accumulation by interacting with the MdJAZ2 protein to inhibit its degradation in apples. Sci Rep 7:1–7
Correia S, Aires A, Queiros F, Carvalho R, Schouten R, Silva AP, Goncalves B (2020) Climate conditions and spray treatments induce shifts in health promoting compounds in cherry (Prunus avium L.) fruits. Sci Hot. https://doi.org/10.1016/j.scientia2019109147
Fang H, Dong Y, Yue X, Chen X, He N, Hu J, Jiang S, Xu H, Wang Y, Su M, Zhang J, Zhang Z, Wang N, Chen X (2019) MdCOL4 interaction mediates crosstalk between UV-B and high temperature to control fruit coloration in apple. Plant Cell Physiol 60:1055–1066
Garrido-Bigotes A, Figueroa NE, Figueroa PM, Figueroa CR (2018) Jasmonate signaling pathway in strawberry: Genome-wide identification, molecular characterization and expression of JAZs and MYCs during fruit development and ripening. PLoS ONE 13:e0197118
Hataitip N, Shishido M, Okawa K, Ohara H, Ban Y, Kita M, Moriguchi T, Ikeura H, Hayata Y, Kondo S (2011) Effect of jasmonates on ethylene biosynthesis and aroma volatile emission in Japanese apricot infected by a pathogen (Colletotrichum gloeosporioides). J Agri Food Chem 59:6423–6429
Kondo S, Fiebig A, Okawa K, Ohara H, Kowitcharoen L, Nimitkeatkai H, Kittikorn M, Kim M (2011) Jasmonic acid, polyamine, and antioxidant levels in apple seedlings as affected by Ultraviolet-C irradiation. Plant Growth Regul 64:83–89
Kondo S, Jitratham A, Kittikorn M, Kanlayanarat S (2004) Relationships between jasmonates and chilling injury in mangosteens are affected by spermine. HortScience 39:1346–1348
Kondo S, Katayama R, Uchino K (2005a) Antioxidant activity in meiwa kumquat as affected by environmental and growing factors. Environ Exp Bot 54:60–68
Kondo S, Kittikorn M, Kanlayanarat S (2005b) Preharvest antioxidant activities of tropical fruit and the effect of low temperature storage on antioxidants and jasmonates. Postharvest Biol Technol 36:309–318
Kondo S, Maeda M, Kobayashi S, Honda C (2002) Expression of anthocyanin biosynthetic genes in Malus sylvestris L. ‘Mutsu’ non-red apples. J Hort Sci Biotech 77:718–723
Kondo S, Meemak S, Ban Y, Moriguchi T, Harada T (2009) Effects of auxin and jasmonates on 1-aminocyclopropane-1-carboxylate (ACC) synthase and ACC oxidase gene expression during ripening of apple fruit. Postharvest Biol Technol 51:281–284
Kondo S, Sugaya S, Sugawa S, Ninomiya M, Kittikorn M, Okawa K, Ohara H, Ueno K, Todoroki Y, Mizutani M, Hirai N (2012) Dehydration tolerance in apple seedlings is affected by an inhibitor of ABA8'-hydroxylase CYP707A. J Plant Physiol 169:234–241
Kondo S, Tomiyama H, Rodyoung A, Okawa K, Ohara H, Sugaya S, Terahara N, Hirai N (2014) Abscisic acid metabolism and anthocyanin synthesis in grape skin are affected by light emitting diode (LED) irradiation at night. J Plant Physiol 171:823–829
Kondo S, Tsukada N, Niimi Y, Seto H (2001) Interactions between jasmonates and abscisic acid in apple fruit, and stimulative effect of jasmonates on anthocyanin accumulation. J Jpn Soc Hort Sci 70:546–552
Koshiyama M, Watanabe K, Fujisawa H, Miomi M, Imamura K (2006) Development of a new plant growth regulator, prohydrojasmon. Regul Plant Growth Dev 41:24–33
Li L, Lu X, Ma H, Lyu D (2017) Jasmonic acid regulates the ascorbate-glutathione cycle in Malus baccata Borth. Roots under low root-zone temperature. Acta Physiol Plant 39:163–174
Li Y, Qiu L, Liu X, Zhang Q, Zhuansun X, Fashima T, Krugman T, Sun Q, Xie C (2020) Glycerol-induced powdery mildew resistance in wheat by regulating plant fatty acid metabolism, plant hormones cross-talk, and pathogenesis-related genes. Int J Mol Sci 21:654–673
Lv J, Ge Y, Li C, Zhang M, Li J (2017) Identification and analysis of genes involved in the jasmonate pathway in response to ethephon and 1-methylcyclopropene during the ripening of apple fruit. J Am Soc Hort Sci 142:184–191
Lysiak GP, Michalska-Giechanowska A, Wojdylo A (2020) Postharvest changes in phenolic compounds and antioxidant capacity of apples cv. Jonagold growing in different locations in Europe. Food Chem. https://doi.org/10.1016/j.foodchem2019125912
Ma C, Liang B, Chang B, Yan J, Liu L, Wang Y, Yang Y, Zhao Z (2019) Transcriptome profiling of anthocyanin biosynthesis in the peel of ‘Granny Smith’ apples (Malus domestica) after bag removal. BMC genomics 20:353. https://doi.org/10.1186/s12864-019-5730-1
Matsumoto K, Fujita T, Sato S, Moriguchi T (2018) Effects of low temperature, shading, defoliation, and crop load on the flesh coloration of the type 2 red-fleshed apple ‘Kurenainoyume’. Hort J 87:452–461
Matsuura H (2018) Metabolism of jasmonic acid and transportation to reveal its own biological activities. Regul Plant Growth Dev 53:1–9
Mimida N, Saito T, Moriguchi T, Suzuki A, Komori S, Wada M (2015) Expression of DORMANCY-ASSOCIATED MADS-BOX (DAM)-like genes in apple. Biol Plant 59:237–244
Okada K (2009) Molecular mechanism of jasmonate signaling in plants. Regul Plant Growth Dev 44:154–165
Pratiwi P, Tanaka G, Takahashi T, Xie X, Yoneyama K, Matsuura H, Takahashi K (2017) Identification of jasmonic acid and jsmonoyl-isoleucine, and characterization of AOS, AOC, OPR and JAR1 in the model Lycophyte Selaginella meellendorffii. Plant Cell Physiol 58:789–801
Sato C, Aikawa K, Sugiyama S, Nabeta K, Masuta C, Matsuura H (2011) Distal transport of exogenously applied jasmonoyl-isoleucine with wounding stress. Plant Cell Physiol 52:509–517
Sato H, Otagaki S, Saelai P, Kondo S, Shiratake K, Matsumoto S (2017) Varietal differences in phenolic compounds metabolism of type 2 red-fleshed apples. Scientia Hort 219:1–9
Sheng L, Shen D, Luo Y, Sun X, Wang J, Luo T, Zeng Y, Xu J, Deng X, Cheng Y (2017) Exogenous g-aminobutyric acid treatment affects citrate and amino acid accumulation to improve fruit quality and storage performance of postharvest citrus fruit. Food Chem 216:138–145
Staswick PE, Tiryaki I (2004) The oxylipin signal jasmonic acid is activated by an enzyme that conjugates it to isoleucine in Arabidopsis. Plant Cell 16:2117–2127
Suktawee S, Shishido M, Wang S, Saito T, Okawa K, Ohara H, Nimitkeatkai H, Ikeura H, Kondo S (2019) n-Propyl dihydrojasmonates influence ethylene signal transduction in infected apple fruit by Botrytis cinerea. Hort J 88:41–49
Torrigiani P, Fregolaa F, Ziosi V, Ruiza KB, Kondo S, Costa G (2012) Differential expression of allene oxide synthase (AOS), and jasmonate relationship with ethylene biosynthesis in seed and mesocarp of developing peach fruit. Postharvest Biol Technol. 63:67–73
Wakuta S, Suzuki E, Saburi W, Matsuura H, Nabeta K, Imai R, Matsui H (2011) OsJAR1 and OsJAR2 are jasmonyl-isoleucine synthases involved in wound- and pathogen-induced jasmonic acid signaling. Biochem Biophys Res Communi 409:634–639
Wang N, Qu C, Jiang S, Chen Z, Xu H, Fang H, Su M, Zhang J, Wang Y, Liu W, Zhang Z, Lu N, Chen X (2018) The proanthocyanidin-specific transcription factor MdMYBPA1 initiates anthocyanin synthesis under low-temperature conditions in red-fleshed apples. Plant J 96:39–55
Yanfang Y, Kaikai Z, Liyin Y, Xing Y, Ying W, Hongwei L, Qiang L, Duanfen C, Deyou Q (2018) Identification and characterization of MYC transcription factors in Taxus sp. Gene 675:1–8
Yang L, Li J, Ji J, Li P, Yu L, Abd-Allah EF, Luo Y, Hu L, Hu X (2016) High temperature induces expression of tobacco transcription factor NtMYC2a to regulate nicotine and JA biosynthesis. Frontn Physiol 465:1–13. https://doi.org/10.3389/tphys.2016.00465
Zhang F, Yao J, Ke J, Zhang L, Lam VQ, Xin XF, Zhou E, Chen J, Brunzelle J, Griffin PR, Zhou M, Xu HE, Melcher K, He SY (2015) Structural basis of JAZ resression of MYC transcription factors in jasmonate signaling. Nature 525:269–275
Ziosi V, Bonghi C, Bregori AM, Trainotti L, Biondi S, Sutthiwal S, Kondo S, Costa G, Torrigiani P (2008) Jasmonate-induced transcriptional changes suggest a negative interference with the ripening syndrome in peach fruit. J Exp Bot 59:563–573
Acknowledgements
This study was supported by Ajinomoto Co.
Author information
Authors and Affiliations
Contributions
SK designed the study and wrote the paper. HT and PO performed GC–MS, LC–MS, and PCR analyses. RK sprayed Ile and PDJ to the tree and collected sample. TS, KO, and HO revised the article. HM provided JA-L-Ile. YL and DI provided L-Ile.
Corresponding author
Ethics declarations
Conflict of interest
There is no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Kondo, S., Tomiyama, H., Opio, P. et al. l-Isoleucine (Ile) Promotes Anthocyanin Accumulation in Apples. J Plant Growth Regul 40, 541–549 (2021). https://doi.org/10.1007/s00344-020-10117-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00344-020-10117-0