Abstract
Fruit ripening is a complex process that is regulated by a signal network. Whereas the regulatory mechanism of abscisic acid has been studied extensively in non-climacteric fruit, little is know about other signaling pathways involved in this process. In this study, we performed that plant hormone jasmonic acid plays an important role in grape fruit coloring and softening by increasing the transcription levels of several ripening-related genes, such as the color-related genes PAL1, DFR, CHI, F3H, GST, CHS, and UFGT; softening-related genes PG, PL, PE, Cell, EG1, and XTH1; and aroma-related genes Ecar, QR, and EGS. Lastly, the fruit anthocyanin, phenol, aroma, and cell wall materials were changed. Jasmonic acid positively regulated its biosynthesis pathway genes LOS, AOS, and 12-oxophytodienoate reductase (OPR) and signal pathway genes COI1 and JMT. RNA interference of grape jasmonic acid pathway gene VvAOS in strawberry fruit appeared fruit un-coloring phenotypes; exogenous jasmonic acid rescued this phenotypes. On the contrary, overexpression of grape jasmonic acid receptor VvCOI1 in the strawberry fruit accelerated the fruit-ripening process and induced some plant defense-related gene expression level. Furthermore, jasmonic acid treatment or strong jasmonic acid signal pathway in strawberry fruit make the fruit resistance against Botrytis cinerea.
Similar content being viewed by others
References
Abeles FB, Bosshart RP, Forrence LE, Habig WH (1971) Preparation and purification of glucanase and chitinase from bean leaves. Plant Physiol 47:129–134
Alexander L, Grierson D (2002) Ethylene biosynthesis and action in tomato: a model for climacteric fruit ripening. J Exp Bot 53:2039–2055
Anastasios ID, Daryl CJ, Leon AT, Nektarios EP, Christos ID (2007) Efficacy of postharvest treatments with acibenzolar-S-methyl and methyl jasmonate against Botrytis cinerea infecting cut Freesia hybrida L. flowers. Aust Plant Pathol 36:332–340
Arnold TM, Schultz JC (2002) Induced sink strength as a prerequisite for induced tannin biosynthesis in developing leaves of Populus. Oecologia 130:585–593
Ashish R, Jyothilakshmi V, Hitendra KP, Alok P, Ramesh P, Axel M, Ramesh VS (2015) Upregulation of jasmonate biosynthesis and jasmonate-responsive genes in rice leaves in response to a bacterial pathogen mimic. Funct Integr Genomics 15:363–373
Avanci NC, Luche DD, Goldman GH, Goldman MHS (2010) Jasmonates are phytohormones with multiple functions, including plant defense and reproduction. Genet Mol Biol 9:484–505
Boter M, Ruı´z-Rivero O, Abdeen A, Prat S (2004) Conserved MYC transcription factors play a key role in jasmonate signaling both in tomato and Arabidopsis. Genes Dev 18:1577–1591
Brummell DA, Harpster MH (2001) Cell wall metabolism in fruit softening and quality and its manipulation in transgenic plants. Plant Mol Biol 47:311–340
Chen JY, Wen PF, Kong WF, Pana QH, Zhana JC, Lia JM, Wana SB, Huang WD (2006) Effect of salicylic acid on henylpropanoids and phenylalanine ammonia lyase in harvested grape berries. Postharvest Biol Technol 40(1):64–72
Cheong JJ, Choi YD (2003) Methyl jasmonate as a vital substance in plants. Trends Genet 19:409–13
Chervin C, Kereamy AE, Roustan JP, Latche A, Lamon J, Bouzayen M (2004) Ethylene seems required for the berry development and ripening in grape, a non-climacteric fruit. Plant Sci 167:1301–1305
Chini A, Fonseca S, Ferna´ndez G, Adie B, Chico JM, Lorenzo O, Garcı´a-Casado G, López-Vidriero I, Lozano FM, Ponce MR, Micol JL, Solano R (2007) The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448:666–671
Chuine I, Yiou P, Viovy N, Seguin B, Daux V, Seguin B, Daux V, Le Roy LE (2004) Grape ripening as a past climate indicator. Nature 432:289–290
Cipollini DF, Redman AM (1999) Age-dependent effects of jasmonic acid treatment and wind exposure on foliar oxidase activity and insect resistance in tomato. J Chem Ecol 25:271–281
Costantini L, Battilana J, Lamaj P, Fanizza G, Grando MS (2008) Berry and phenology-related traits in grapevine (Vitis vinifera L.): from quantitative trait loci to underlying genes. BMC Plant Biol 8:38
Creelman RA, Mullet JE (1995) Jasmonic acid distribution and action in plants: regulation during development and response to biotic and abiotic stress. Proc Natl Acad Sci U S A 92:4114–4119
Creelman RA, Mullet JE (1997) Biosynthesis and action of jasmonates in plants. Annu Rev Plant Physiol Plant Mol Biol 48:355–381
Delker C, Stenzel I, Hause B, Miersch O, Feussner I, Wasternack C (2006) Jasmonate biosynthesis in Arabidopsis thaliana—enzymes, products, regulation. Plant Biol 8:297–306
Dong J, Zhang YT, Tang XW, Jin WM, Han ZH (2013) Differences in volatile ester composition between Fragaria × ananassa and F. vesca and implications for strawberry aroma patterns. Sci Horti 150:47–53
Encarna G, Adrian M, José L (1995) Changes in volatile compounds during maturation of some grape varieties. J Sci Food Agric 67(2):229–233
Fan J, Mattheis P, Fellman JK, Patterson ME (1997) Effect of methyl jasmonate on ethylene and volatile production by summered apple depends on fruit developmental stage. J Agric Food Chem 45:208–211
Fan X, Mattheis JP, Fellman JK (1998) A role for jasmonates in climacteric fruit ripening. Planta 204:444–449
Farmer EE, Ryan CA (1992) Octadecanoid precursors of jasmonic acid activate the synthesis of wound-inducible proteinase-inhibitors. Plant Cell 4:129–134
Feng S, Ma L, Wang X, Xie D, Dinesh-Kumar SP, Wei N, Deng XW (2003) The COP9 signalosome interacts physically with SCFCOI1 and modulates jasmonate responses. Plant Cell 15:1083–1094
Fonseca S, Chico JM, Solano R (2009) The jasmonate pathway: the ligand, the receptor and the core signalling module. Curr Opin Plant Biol 12:539–547
Franco RR, Andrés G, María M, Fernando MR, María EG, Isidro GC, Fernando LP (2011) The sesquiterpene botrydial produced by Botrytis cinerea induces the hypersensitive response on plant tissues and its action is modulated by salicylic acid and jasmonic acid signaling. MPMI 24(8):888–896
Fujisawa M, Shima Y, Nakagawa H, Kitagawa M, Kimbara J, Nakano T, Kasumi T, Ito Y (2014) Transcriptional regulation of fruit ripening by tomato FRUITFULL homologs and associated MADS box proteins. Plant Cell 26:89–101
Gansser D, Latza S, Berger RG (1997) Methyl jasmonates in developing strawberry fruit (Fragaria × ananassa Duch. cv. Kent). J Agric Food Chem 45:2477–2480
Gfeller A, Liechti R, Farmer EE (2010) Arabidopsis jasmonate signaling pathway. Sci Signal 3: cm3
Ghasemi PA, Sajjadi SE, Parang K (2014) A review (research and patent) on jasmonic acid and its derivatives. Arch Pharm 347:229–239
Griesser M, Hoffmann T, Bellido ML, Rosati C, Fink B, Kurtzer R, Aharoni A, Muñóz-Blanco J, Schwab W (2008) Redirection of flavonoid biosynthesis through the downregulation of an anthocyanidin glucosyltransferase in ripening strawberry (Fragaria × ananassa) fruit. Plant Physiol 146:1528–1539
Hofmann E, Pollmann S (2008) Molecular mechanism of enzymatic allene oxide cyclization in plants. Plant Physiol Biochem 46:302–308
Jane AA, James ER, Hashmath IH, David MC (2013) Transcriptional profiling of Zea mays roots reveals roles for jasmonic acid and terpenoids in resistance against Phytophthora cinnamomi. Funct Integr Genomics 13:217–228
Jeong SW, Das PK, Jeoung SC, Song JY, Lee HK, Kim YK, Kim WJ, Park Y, Yoo SD, Choi SB, Choi G, Park Y (2010) Ethylene suppression of sugar-induced anthocyanin pigmentation in Arabidopsis. Plant Physiol 154:1514–1531
Jia H, Chai Y, Li C, Lu D, Luo J, Qin L, YuanYue S (2011) Abscisic acid plays an important role in the regulation of strawberry fruit ripening. Plant Physiol 157:188–199
Jiang Y, Joyce DC (2003) ABA effects on ethylene production, PAL activity, anthocyanin and phenolic contents of strawberry fruit. Plant Growth Regul 39:171–174
Jin P, Zheng YH, Tang SS, Rui HJ, Wang CY (2009) Enhancing disease resistance in peach fruit with methyl jasmonate. J Sci Food Agric 89:802–808
Kang JH, Wang L, Giri A, Baldwin IT (2006) Silencing threonine deaminase and JAR4 in Nicotiana attenuata impairs jasmonic acid-isoleucine mediated defenses against Manduca sexta. Plant Cell 18:3303–3320
Katsir L, Schilmiller AL, Staswick PE, He SY, Howe GA (2008) COI1 is a critical component of a receptor for jasmonate and the bacterial virulence factor coronatine. Proc Natl Acad Sci U S A 105:7100–7105
Kochba J, Lavee S, Spiegel-Roy P (1997) Difference in peroxidase activity and isoenzymes in embryogenic and non-embryogenic “Shamouti” orange ovular callus lines. Plant Cell Physiol 18:463–467
Kondo S (2006) The role of jasmonates in fruit color development and chilling injury. Acta Hortic 727:45–56
Kondo S, Yamada H, Setha S (2007) Effect of jasmonates differed at fruit ripening stages on 1-aminocyclopropane-1-carboxylate (ACC) synthase and ACC oxidase gene expression in pears. J Am Soc Hortic Sci 132:120–125
Lee S, Chung EJ, Joung YH, Choi D (2010) Non-climacteric fruit ripening in pepper: increased transcription of EIL-like genes normally regulated by ethylene. Func Integr Genomics 10:135–146
Lester GE, Dunlap JR (1985) Physiological changes during development and ripening of Terlita’ musk melon fruits. Scientia Hoxticalture 2:323–331
Li C, Schilmiller AL, Liu G, Lee GI, Jayanty S, Sageman C, Vrebalov J, Giovannoni JJ, Yagi K, Kobayashi Y, Howe GA (2005) Role of beta-oxidation in jasmonate biosynthesis and systemic wound signaling in tomato. Plant Cell 17:971–986
Lorenzo O, Chico JM, Sa´nchez-Serrano JJ, Solano R (2004) JASMONATEINSENSITIVE1 encodes a MYC transcription factor essential to discriminate between different jasmonate-regulated defense responses in Arabidopsis. Plant Cell 16:1938–1950
Manning K (1998) Isolation of a set of ripening-related genes from strawberry: their identification and possible relationship to fruit quality traits. Planta 205:622–631
Martínez G, Chaves A, Añón M (1996) Effect of exogenous application of gibberellic acid on color change and phenylalanine ammonia-lyase, chlorophyllase, and peroxidase activities during ripening of strawberry fruit (Fragaria × ananassa Duch.). J Plant Growth Regul 15:139–146
McConn M, Creelman RA, Bell E, Mullet JE, Browse J (1997) Jasmonate is essential for insect defense in Arabidopsis. Proc Natl Acad Sci U S A 94:5473–5477
Memelink J, Verpoorte R, Kijne JW (2001) ORC anization of jasmonate responsive gene expression in alkaloid metabolism. Trends Plant Sci 6:212–221
Meng XH, Han J, Wang Q, Tian SP (2009) Changes in physiology and quality of peach fruits treated by methyl jasmonate under low temperature stress. Food Chem 114:1028–1035
Mukkun L, Singh Z (2009) Methyl jasmonate plays a role in fruit ripening of “Pajaro” strawberry through stimulation of ethylene biosynthesis. Sci Hortic 123:5–10
Peña-Cortés H, Barrios P, Dorta F, Polanco V, Sánchez C, Sánchez E, Ramírez I (2004) Involvement of jasmonic acid and derivatives in plant response to pathogen and insects and in fruit ripening. J Plant Growth Regul 23:246–260
Rudell DR, Mattheis JP, Fan X, Fellman JK (2002) Methyl jasmonate enhances anthocyanin accumulation and modifies production of phenolics and pigments in “Fuji” apples. J Am Soc Hortic Sci 127:435–441
Sandra CD, Lucı́a CL, Esperanza FG, M. Luisa GP (2003) Aromatic composition of the Vitis vinifera grape Albariño. LWT - Food Sci Technol 36(6):585–590
Sasaki Y, Asamizu E, Shibata D, Nakamura Y, Kaneko T, Awai K, Amagai M, Kuwata C, Tsugane T, Masuda T, Shimada H, Takamiya K, Ohta H, Tabata S (2001) Monitoring of methyl jasmonate-responsive genes in Arabidopsis by cDNA macroarray: self-activation of jasmonic acid biosynthesis and crosstalk with other phytohormone signaling pathways. DNA Res 8:153–161
Scalschi L, Vicedo B, Camas G, Fernandez-Crespo E, Lape L, González-Bosch C, García-Aqustín P (2013) Hexanoic acid is a resistance inducer that protects tomato plants against Pseudomonas syringae by priming the jasmonic acid and salicylic acid pathways. Mol Plant Pathol 14:342–355
Seo HS, Song JT, Cheong JJ, Lee YH, Lee YW, Hwang I, Lee JS, Choi YD (2001) Jasmonic acid carboxyl methyltransferase: a key enzyme for jasmonate-regulated plant responses. Proc Natl Acad Sci 98:4788–4793
Serkan S, Turgut C (2003) Effect of contact on the aroma composition of the musts of Vitis vinifera L.cv. Muscat of Bornova and Narince grown in Turkey. F00d Chem 81: 341–347.
Seymour GB, Cross KC (1996) Cell wall disassembly and fruit softening. Postharvest News Inform 7:45–52
Shan X, Zhang Y, Peng W, Wang Z, Xie D (2009) Molecular mechanism for jasmonate-induction of anthocyanin accumulation in Arabidopsis. J Exp Bot 60:3849–3860
Shima Y, Fujisawa M, Kitagawa M, Nakano T, Kimbara J, Nakamura N, Shiina T, Sugiyama J, Nakamura T, Kasumi T, Ito Y (2014) Tomato FRUITFULL homologs regulate fruit ripening via ethylene biosynthesis. Biosci Biotechnol Biochem 78(2):231–237
Soma SM, Singh VK (2012) LOX genes in blast fungus (Magnaporthe grisea) resistance in rice. Funct Integr Genomics 12:265–275
Sun L, Yuan B, Zhang M, Wang L, Cui MM, Wang Q, Leng P (2012) Fruit-specific RNAi-mediated suppression of SlNCED1increases both lycopene and b–carotene contents in tomato fruit. J Exp Bot 63:3097–3108
Suza WP, Staswick PE (2008) The role of JAR1 in Jasmonoyl-L:-isoleucine production during Arabidopsis wound response. Planta 227:1221–1232
Tamari G, Borochov A, Atzorn R, Weiss D (1995) Methyl jasmonate induces pigmentation and flavonoid gene expression in petunia corollas: a possible role in wound response. Physiol Plant 94:45–50
Thaler JS, Stout MJ, Karban R, Duffey SS (1996) Exogenous jasmonates simulate insect wounding in tomato plants (Lycopersicon esculentum) in the laboratory and field. J Chem Ecol 22:1767–1781
Thines B, Katsir L, MelottoM NY, Mandaokar A, Liu G, Nomura K, He SY, Howe GA, Browse J (2007) JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling. Nature 448:661–665
Tian MS, Prakash S, Elgar HJ, Young H, Burmeister DM, Ross GS (2000) Responses of strawberry fruit to 1-methylcyclopropene (1-MCP) and ethylene. Plant Growth Regul 32:83–90
Ueda J, Kato J (1980) Isolation and identification of a senescence-promoting substance from wormwood (Artemisia absinthium L.). Plant Physiol 66:246–249
Vijayan P, Shockey J, Lévesque CA, Cook RJ, Browse J (1998) A role for jasmonate in pathogen defense of Arabidopsis. Proc Natl Acad Sci U S A 95:7209–7214
Wang CY, Buta JG (1994) Methyl jasmonate reduces chilling injury in Cucurbita pepo through its regulation of abscisic acid and polyamine levels. Environ Exp Bot 34:427–432
Wang SY, Zheng W (2005) Preharvest application of methyl jasmonate increases fruit quality and antioxidant capacity in raspberries. Int J Food Sci Technol 40:187–195
Wang SY, Bowman L, Ding M (2008) Methyl jasmonate enhances antioxidant activity and flavonoid content in blackberries (Rubus sp.) and promotes antiproliferation of human cancer cells. Food Chem 107:1261–1269
Wang KT, Cao SF, Jin P (2010) Effect of hot air treatment on postharvest decay of Chinese bayberry fruit. Int J Food Microbiol 141:11–16
Wasternack C, Hanse B (2013) Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. Ann Bot 111:1021–1058
Wasternack C, Parthier B (1997) Jasmonate-signalled plant gene expression. Trends Plant Sci 2:302–307
Williamson BT, Tudzynski B, Pvan Kan JAL (2007) Botrytis cinerea: the cause of grey mould disease. Mol Plant Pathol 8:561–580
Wu J, Wang L, Baldwin IT (2008) Methyl jasmonate-elicited herbivore resistance: does MeJA function as a signal without being hydrolyzed to JA. Planta 227:1161–1168
Yan J, Zhang C, Gu M, Bai Z, Zhang W, Qi T, Cheng Z, Peng W, Luo H, Nan F, Wang Z, Xie D (2009) The Arabidopsis CORONATINE INSENSITIVE1 protein is a jasmonate receptor. Plant Cell 21:2220–2236
Yao HJ, Tian SP (2005) Effects of a biocontrol agent and methyl jasmonate on postharvest diseases of peach fruit and the possible mechanisms involved. J Appl Microbiol 98:941–950
Yu MM, Shen L, Fan B, Zhao DY, Zheng Y, Sheng JP (2009) The effect of MeJA on ethylene biosynthesis and induced disease resistance to Botrytis cinerea in tomato. Postharvest Biol Technol 54(3):153–158
Yu M, Shen L, Zhang A, She J (2011) Methyl jasmonate-induced defense responses are associated with elevation of 1-aminocyclopropane-1-carboxylate oxidase in Lycopersicon esculentum fruit. J Plant Physiol 168:1820–1827
Zhou ML, Yang XB, Zhang Q, Zhou M, Zhao EZ, Tang YX, Zhu XM, Shao JR, Wu YM (2013) Induction of annexin by heavy metals and jasmonic acid in Zea mays. Funct Integr Genomics 13:241–251
Ziosi V, Bonghi C, Bregoli 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
Zucker M (1968) Sequential induction of phenylalanine ammonia lyase and a lyase inactivating system in potato tuber disks. Plant Physiol 43(3):365–374
Acknowledgments
We would like to express our gratitude to Jiangsu Academy of Agricultural Sciences for providing the grape and strawberry fruit materials. We also thank all laboratory members for their help, advice, and discussion.
Funding
This work was supported by the China National Natural Science Fund (31401847), Jiangsu Natural Science Fund (BK20140707), China Postdoctoral Science Fund (2014 M561663), and Central University Basic Research and Operating Expenses of Special Funding (KJQN201541).
Disclosures
The authors have no conflicts of interest to declare.
Author information
Authors and Affiliations
Corresponding authors
Additional information
Haifeng Jia, Cheng Zhang and Zhongjie Liu contributed equally to this article.
ESM
Below is the link to the electronic supplementary material.
ESM 1
Fig. S1. Changes of LOX, AOS, OPR3, COI1, and JMT mRNA levels during grape fruit development. Transcript levels were measured by quantitative real-time PCR (qRT-PCR) using Vv18s as an internal control. Error bars represent the standard error (SE) (n = 3) (TIFF 155 kb)
ESM 2
Fig. S2. Changes of ethylene content after MeJA application in grape. Asterisks indicated statistically significant differences at P < 0.05 as determined by Student’s test. (TIFF 19 kb)
ESM 3
Fig. S3. Methyl jasmonic acid treatment enhances the strawberry fruit resistance against B. cinerea. Comparison of sensitivity to gray mold fungus at 25 °C and 95 % relative humidity between control fruits (water treatment) and methyl jasmonic acid (10 μm) treatment fruit. The full ripening strawberry fruits were inoculated with fungal spore concentration of 104/μl. The pictures were got in 0, 2, 3, 4, and 8 days after inoculated with B. cinerea. (TIFF 5600 kb)
ESM 4
Supplement Table S1. Primers used in the article. (DOCX 25 kb)
Rights and permissions
About this article
Cite this article
Jia, H., Zhang, C., Pervaiz, T. et al. Jasmonic acid involves in grape fruit ripening and resistant against Botrytis cinerea . Funct Integr Genomics 16, 79–94 (2016). https://doi.org/10.1007/s10142-015-0468-6
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10142-015-0468-6