Exogenous strigolactone interacts with abscisic acid-mediated accumulation of anthocyanins in grapevine berries
Jazyk angličtina Země Anglie, Velká Británie Médium print
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
29401281
PubMed Central
PMC5913642
DOI
10.1093/jxb/ery033
PII: 4833190
Knihovny.cz E-zdroje
- MeSH
- anthokyaniny metabolismus MeSH
- kyselina abscisová metabolismus MeSH
- laktony farmakologie MeSH
- ovoce účinky léků metabolismus MeSH
- regulátory růstu rostlin metabolismus farmakologie MeSH
- Vitis účinky léků metabolismus MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- anthokyaniny MeSH
- kyselina abscisová MeSH
- laktony MeSH
- regulátory růstu rostlin MeSH
Besides signalling to soil organisms, strigolactones (SLs) control above- and below-ground morphology, in particular shoot branching. Furthermore, SLs interact with stress responses, possibly thanks to a crosstalk with the abscisic acid (ABA) signal. In grapevine (Vitis vinifera L.), ABA drives the accumulation of anthocyanins over the ripening season. In this study, we investigated the effects of treatment with a synthetic strigolactone analogue, GR24, on anthocyanin accumulation in grape berries, in the presence or absence of exogenous ABA treatment. Experiments were performed both on severed, incubated berries, and on berries attached to the vine. Furthermore, we analysed the corresponding transcript concentrations of genes involved in anthocyanin biosynthesis, and in ABA biosynthesis, metabolism, and membrane transport. During the experiment time courses, berries showed the expected increase in soluble sugars and anthocyanins. GR24 treatment had no or little effect on anthocyanin accumulation, or on gene expression levels. Exogenous ABA treatment activated soluble sugar and anthocyanin accumulation, and enhanced expression of anthocyanin and ABA biosynthetic genes, and that of genes involved in ABA hydroxylation and membrane transport. Co-treatment of GR24 with ABA delayed anthocyanin accumulation, decreased expression of anthocyanin biosynthetic genes, and negatively affected ABA concentration. GR24 also enhanced the ABA-induced activation of ABA hydroxylase genes, while it down-regulated the ABA-induced activation of ABA transport genes. Our results show that GR24 affects the ABA-induced activation of anthocyanin biosynthesis in this non-climacteric fruit. We discuss possible mechanisms underlying this effect, and the potential role of SLs in ripening of non-ABA-treated berries.
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Adams DO. 2006. Phenolics and ripening in grape berries. American Journal of Enology and Viticulture 57, 249–256.
Akiyama K, Matsuzaki K, Hayashi H. 2005. Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435, 824–827. PubMed
Belhadj A, Telef N, Saigne C, Cluzet S, Barrieu F, Hamdi S, Mérillon JM. 2008. Effect of methyl jasmonate in combination with carbohydrates on gene expression of PR proteins, stilbene and anthocyanin accumulation in grapevine cell cultures. Plant Physiology and Biochemistry 46, 493–499. PubMed
Besserer A, Bécard G, Jauneau A, Roux C, Séjalon-Delmas N. 2008. GR24, a synthetic analog of strigolactones, stimulates the mitosis and growth of the arbuscular mycorrhizal fungus Gigaspora rosea by boosting its energy metabolism. Plant Physiology 148, 402–413. PubMed PMC
Boursiac Y, Léran S, Corratgé-Faillie C, Gojon A, Krouk G, Lacombe B. 2013. ABA transport and transporters. Trends in Plant Science 18, 325–333. PubMed
Bradow JM, Connick WJ Jr. 1988. Seed-germination inhibition by volatile alcohols and other compounds associated with Amaranthus palmeri residues. Journal of Chemical Ecology 14, 1633–1648. PubMed
Brewer PB, Koltai H, Beveridge CA. 2013. Diverse roles of strigolactones in plant development. Molecular Plant 6, 18–28. PubMed
Bu Q, Lv T, Shen H et al. . 2014. Regulation of drought tolerance by the F-box protein MAX2 in Arabidopsis. Plant Physiology 164, 424–439. PubMed PMC
Carra A, Gambino G, Schubert A. 2007. A cetyltrimethylammonium bromide-based method to extract low-molecular-weight RNA from polysaccharide-rich plant tissues. Analytical Biochemistry 360, 318–320. PubMed
Cheng WH, Endo A, Zhou L et al. . 2002. A unique short-chain dehydrogenase/reductase in Arabidopsis glucose signaling and abscisic acid biosynthesis and functions. The Plant Cell 14, 2723–2743. PubMed PMC
Chervin C, El-Kereamy A, Roustan J, Latche A, Lamon J, Bouzayen M. 2004. Ethylene seems required for the berry development and ripening in grape, a non-climacteric fruit. Plant Science 167, 1301–1305.
Coombe BG, Hale CR. 1973. The hormone content of ripening grape berries and the effects of growth substance treatments. Plant Physiology 51, 629–634. PubMed PMC
Cutler AJ, Krochko JE. 1999. Formation and breakdown of ABA. Trends in Plant Science 4, 472–478. PubMed
Davies C, Boss PK, Robinson SP. 1997. Treatment of grape berries, a nonclimacteric fruit with a synthetic auxin, retards ripening and alters the expression of developmentally regulated genes. Plant Physiology 115, 1155–1161. PubMed PMC
Deluc LG, Grimplet J, Wheatley MD, Tillett RL, Quilici DR, Osborne C, Schooley DA, Schlauch KA, Cushman JC, Cramer GR. 2007. Transcriptomic and metabolite analyses of Cabernet Sauvignon grape berry development. BMC Genomics 8, 429. PubMed PMC
Ferrandino A, Carra A, Rolle L, Schneider A, Schubert A. 2012. Profiling of hydroxycinnamoyl tartrates and acylated anthocyanins in the skin of 34 Vitis vinifera genotypes. Journal of Agricultural and Food Chemistry 60, 4931–4945. PubMed
Ferrandino A, Guidoni S. 2010. Anthocyanins, flavonols and hydroxycinnamates: an attempt to use them to discriminate Vitis vinifera L. cv ‘Barbera’ clones. European Food Research and Technology 230, 417–427.
Floková K, Tarkowská D, Miersch O, Strnad M, Wasternack C, Novák O. 2014. UHPLC-MS/MS based target profiling of stress-induced phytohormones. Phytochemistry 105, 147–157. PubMed
Ford CM, Boss PK, Hoj PB. 1998. Cloning and characterization of Vitis vinifera UDP-glucose:flavonoid 3-O-glucosyltransferase, a homologue of the enzyme encoded by the maize Bronze-1 locus that may primarily serve to glucosylate anthocyanidins in vivo. Journal of Biological Chemistry 273, 9224–9233. PubMed
Gambetta GA, Matthews MA, Shaghasi TH, McElrone AJ, Castellarin SD. 2010. Sugar and abscisic acid signaling orthologs are activated at the onset of ripening in grape. Planta 232, 219–234. PubMed PMC
Giordano D, Provenzano S, Ferrandino A, Vitali M, Pagliarani C, Roman F, Cardinale F, Castellarin SD, Schubert A. 2016. Characterization of a multifunctional caffeoyl-CoA O-methyltransferase activated in grape berries upon drought stress. Plant Physiology and Biochemistry 101, 23–32. PubMed
Giribaldi M, Gény L, Delrot S, Schubert A. 2010. Proteomic analysis of the effects of ABA treatments on ripening Vitis vinifera berries. Journal of Experimental Botany 61, 2447–2458. PubMed PMC
Giribaldi M, Perugini I, Sauvage FX, Schubert A. 2007. Analysis of protein changes during grape berry ripening by 2-DE and MALDI-TOF. Proteomics 7, 3154–3170. PubMed
Gomez-Roldan V, Fermas S, Brewer PB et al. . 2008. Strigolactone inhibition of shoot branching. Nature 455, 189–194. PubMed
Ha C, Leyva-Gonzalez M, Osakabe Y et al. . 2014. Positive regulatory role of strigolactone in plant responses to drought and salt stress. Proceedings of the National Academy of Sciences, USA 111, 851–856. PubMed PMC
Hrazdina G, Parsons GF, Mattick LR. 1984. Physiological and biochemical events during development and maturation of grape berries. Journal of Enology and Viticulture 35, 220–227.
Ito S, Yamagami D, Umehara M et al. . 2017. Regulation of strigolactone biosynthesis by gibberellin signaling. Plant Physiology 174, 1250–1259. PubMed PMC
Jeong S, Goto-Yamamoto N, Kobayashi S, Esaka A. 2004. Effects of plant hormones and shading on the accumulation of anthocyanins and the expression of anthocyanin biosynthetic genes in grape berry skins. Plant Science 167, 247–252.
Jia H, Zhang C, Pervaiz T, Zhao P, Liu Z, Wang B, Wang C, Zhang L, Fang J, Qian J. 2016. Jasmonic acid involves in grape fruit ripening and resistance against Botrytis cinerea. Functional and Integrative Genomics 16, 79–94. PubMed
Kadomura-Ishikawa Y, Miyawaki K, Takahashi A, Masuda T, Noji S. 2015. Light and abscisic acid independently regulated FaMYB10 in Fragaria × ananassa fruit. Planta 241, 953–965. PubMed
Kalua C, Boss P. 2010. Comparison of major volatile compounds from Riesling and Cabernet Sauvignon grapes (Vitis vinifera L.) from fruitset to harvest. Australian Journal of Grape and Wine Research 16, 337–348.
Kang J, Hwang J, Lee M, Kim Y, Assmann S, Martinoia E, Lee Y. 2010. PDR-type ABC transporter mediates cellular uptake of the phytohormone abscisic acid. Proceedings of the National Academy of Sciences, USA 107, 2355–2360. PubMed PMC
Kang J, Yim S, Choi H, Kim A, Lee KP, Lopez-Molina L, Martinoia E, Lee Y. 2015. Abscisic acid transporters cooperate to control seed germination. Nature Communications 6, 8113. PubMed PMC
Kohlen W, Charnikhova T, Lammers M et al. . 2012. The tomato CAROTENOID CLEAVAGE DIOXYGENASE8 (SlCCD8) regulates rhizosphere signaling, plant architecture and affects reproductive development through strigolactone biosynthesis. New Phytologist 196, 535–547. PubMed
Kuromori T, Miyaji T, Yabuuchi H, Shimizu H, Sugimoto E, Kamiya A, Moriyama Y, Shinozaki K. 2010. ABC transporter AtABCG25 is involved in abscisic acid transport and responses. Proceedings of the National Academy of Sciences, USA 107, 2361–2366. PubMed PMC
Kushiro T, Okamoto M, Nakabayashi K, Yamagishi K, Kitamura S, Asami T, Hirai N, Koshiba T, Kamiya Y, Nambara E. 2004. The Arabidopsis cytochrome P450 CYP707A encodes ABA 8'-hydroxylases: key enzymes in ABA catabolism. EMBO Journal 23, 1647–1656. PubMed PMC
Lashbrooke JG, Young PR, Dockrall SJ, Vasanth K, Vivier MA. 2013. Functional characterisation of three members of the Vitis vinifera L. carotenoid cleavage dioxygenase gene family. BMC Plant Biology 13, 156. PubMed PMC
Lechat MM, Pouvreau JB, Péron T et al. . 2012. PrCYP707A1, an ABA catabolic gene, is a key component of Phelipanche ramosa seed germination in response to the strigolactone analogue GR24. Journal of Experimental Botany 63, 5311–5322. PubMed PMC
Ledger SE, Janssen BJ, Karunairetnam S, Wang T, Snowden KC. 2010. Modified CAROTENOID CLEAVAGE DIOXYGENASE8 expression correlates with altered branching in kiwifruit (Actinidia chinensis). New Phytologist 188, 803–813. PubMed
Lee KH, Piao HL, Kim HY, Choi SM, Jiang F, Hartung W, Hwang I, Kwak JM, Lee IJ, Hwang I. 2006. Activation of glucosidase via stress-induced polymerization rapidly increases active pools of abscisic acid. Cell 126, 1109–1120. PubMed
Li G, Xin H, Zheng XF, Li S, Hu Z. 2012. Identification of the abscisic acid receptor VvPYL1 in Vitis vinifera. Plant Biology 14, 244–248. PubMed
Liu J, He H, Vitali M et al. . 2015. Osmotic stress represses strigolactone biosynthesis in Lotus japonicus roots: exploring the interaction between strigolactones and ABA under abiotic stress. Planta 241, 1435–1451. PubMed
Liu J, Novero M, Charnikhova T, Ferrandino A, Schubert A, Ruyter-Spira C, Bonfante P, Lovisolo C, Bouwmeester HJ, Cardinale F. 2013. Carotenoid cleavage dioxygenase 7 modulates plant growth, reproduction, senescence, and determinate nodulation in the model legume Lotus japonicus. Journal of Experimental Botany 64, 1967–1981. PubMed PMC
López-Ráez JA, Kohlen W, Charnikhova T et al. . 2010. Does abscisic acid affect strigolactone biosynthesis?New Phytologist 187, 343–354. PubMed
Lv S, Zhang Y, Li C et al. . 2018. Strigolactone-triggered stomatal closure requires hydrogen peroxide synthesis and nitric oxide production in an abscisic acid-independent manner. New Phytologist 217, 290–304. PubMed
McCarty DR, Carson CB, Stinard PS, Robertson DS. 1989. Molecular analysis of viviparous-1: an abscisic acid-insensitive mutant of maize. The Plant Cell 1, 523–532. PubMed PMC
Moskowitz AH, Hrazdina G. 1981. Vacuolar contents of fruit subepidermal cells from Vitis species. Plant Physiology 68, 686–692. PubMed PMC
Nambara E, Marion-Poll A. 2005. Abscisic acid biosynthesis and catabolism. Annual Review of Plant Biology 56, 165–185. PubMed
Okamoto M, Kuwahara A, Seo M, Kushiro T, Asami T, Hirai N, Kamiya Y, Koshiba T, Nambara E. 2006. CYP707A1 and CYP707A2, which encode abscisic acid 8'-hydroxylases, are indispensable for proper control of seed dormancy and germination in Arabidopsis. Plant Physiology 141, 97–107. PubMed PMC
Okamoto M, Tanaka Y, Abrams SR, Kamiya Y, Seki M, Nambara E. 2009. High humidity induces abscisic acid 8'-hydroxylase in stomata and vasculature to regulate local and systemic abscisic acid responses in Arabidopsis. Plant Physiology 149, 825–834. PubMed PMC
Pagliarani C, Vitali M, Ferrero M, Vitulo N, Incarbone M, Lovisolo C, Valle G, Schubert A. 2017. The accumulation of miRNAs differentially modulated by drought stress is affected by grafting in grapevine. Plant Physiology 173, 2180–2195. PubMed PMC
Park SY, Fung P, Nishimura N et al. . 2009. Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324, 1068–1071. PubMed PMC
Peláez-Vico MA, Bernabéu-Roda L, Kohlen W, Soto MJ, López-Ráez JA. 2016. Strigolactones in the Rhizobium–legume symbiosis: stimulatory effect on bacterial surface motility and down-regulation of their levels in nodulated plants. Plant Science 245, 119–127. PubMed
Pilati S, Perazzolli M, Malossini A, Cestaro A, Demattè L, Fontana P, Dal Ri A, Viola R, Velasco R, Moser C. 2007. Genome-wide transcriptional analysis of grapevine berry ripening reveals a set of genes similarly modulated during three seasons and the occurrence of an oxidative burst at vèraison. BMC Genomics 8, 428. PubMed PMC
Pirie A, Mullins MG. 1976. Changes in anthocyanin and phenolics content of grapevine leaf and fruit tissues treated with sucrose, nitrate, and abscisic acid. Plant Physiology 58, 468–472. PubMed PMC
Ruiz-Lozano JM, Aroca R, Zamarreño ÁM, Molina S, Andreo-Jiménez B, Porcel R, García-Mina JM, Ruyter-Spira C, López-Ráez JA. 2016. Arbuscular mycorrhizal symbiosis induces strigolactone biosynthesis under drought and improves drought tolerance in lettuce and tomato. Plant, Cell and Environment 39, 441–452. PubMed
Ruyter-Spira C, Al-Babili S, van der Krol S, Bouwmeester H. 2013. The biology of strigolactones. Trends in Plant Science 18, 72–83. PubMed
Ruyter-Spira C, Kohlen W, Charnikhova T et al. . 2011. Physiological effects of the synthetic strigolactone analog GR24 on root system architecture in Arabidopsis: another belowground role for strigolactones?Plant Physiology 155, 721–734. PubMed PMC
Saito S, Hirai N, Matsumoto C, Ohigashi H, Ohta D, Sakata K, Mizutani M. 2004. Arabidopsis CYP707As encode (+)-abscisic acid 8'-hydroxylase, a key enzyme in the oxidative catabolism of abscisic acid. Plant Physiology 134, 1439–1449. PubMed PMC
Sandhu AK, Gray DJ, Lu J, Gu L. 2011. Effect of exogenous abscisic acid on antioxidant capacities, anthocyanin, and flavonol content of muscadine grape (Vitis rotundifolia) skins. Food Chemistry 126, 982–988.
Snowden KC, Simkin AJ, Janssen BJ, Templeton KR, Loucas HM, Simons JL, Karunairetnam S, Gleave AP, Clark DG, Klee HJ. 2005. The Decreased apical dominance1/Petunia hybrida CAROTENOID CLEAVAGE DIOXYGENASE8 gene affects branch production and plays a role in leaf senescence, root growth, and flower development. The Plant Cell 17, 746–759. PubMed PMC
Speirs J, Binney A, Collins M, Edwards E, Loveys B. 2013. Expression of ABA synthesis and metabolism genes under different irrigation strategies and atmospheric VPDs is associated with stomatal conductance in grapevine (Vitis vinifera L. cv Cabernet Sauvignon). Journal of Experimental Botany 64, 1907–1916. PubMed PMC
Sun J, Dong Y, Li C, Shen Y. 2015. Transcription and enzymatic analysis of beta-glucosidase VvBG1 in grape berry ripening. Plant Growth Regulation 75, 67–73.
Sun L, Zhang M, Ren J, Qi J, Zhang G, Leng P. 2010. Reciprocity between abscisic acid and ethylene at the onset of berry ripening and after harvest. BMC Plant Biology 10, 257. PubMed PMC
Symons GM, Davies C, Shavrukov Y, Dry IB, Reid JB, Thomas MR. 2006. Grapes on steroids. Brassinosteroids are involved in grape berry ripening. Plant Physiology 140, 150–158. PubMed PMC
Thompson AJ, Jackson AC, Parker RA, Morpeth DR, Burbidge A, Taylor IB. 2000. Abscisic acid biosynthesis in tomato: regulation of zeaxanthin epoxidase and 9-cis-epoxycarotenoid dioxygenase mRNAs by light/dark cycles, water stress and abscisic acid. Plant Molecular Biology 42, 833–845. PubMed
Umehara M, Hanada A, Yoshida S et al. . 2008. Inhibition of shoot branching by new terpenoid plant hormones. Nature 455, 195–200. PubMed
Villalobos-González L, Peña-Neira A, Ibáñez F, Pastenes C. 2016. Long-term effects of abscisic acid (ABA) on the grape berry phenylpropanoid pathway: gene expression and metabolite content. Plant Physiology and Biochemistry 105, 213–223. PubMed
Visentin I, Vitali M, Ferrero M, Zhang Y, Ruyter-Spira C, Novák O, Strnad M, Lovisolo C, Schubert A, Cardinale F. 2016. Low levels of strigolactones in roots as a component of the systemic signal of drought stress in tomato. New Phytologist 212, 954–963. PubMed
Vogel JT, Walter MH, Giavalisco P et al. . 2010. SlCCD7 controls strigolactone biosynthesis, shoot branching and mycorrhiza-induced apocarotenoid formation in tomato. The Plant Journal 61, 300–311. PubMed
Walker AR, Lee E, Bogs J, McDavid DA, Thomas MR, Robinson SP. 2007. White grapes arose through the mutation of two similar and adjacent regulatory genes. The Plant Journal 49, 772–785. PubMed
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. Australian Journal of Grape and Wine Research 15, 195–204.
Xu ZJ, Nakajima M, Suzuki Y, Yamaguchi I. 2002. Cloning and characterization of the abscisic acid-specific glucosyltransferase gene from adzuki bean seedlings. Plant Physiology 129, 1285–1295. PubMed PMC
Yang YZ, Tan BC. 2014. A distal ABA responsive element in AtNCED3 promoter is required for positive feedback regulation of ABA biosynthesis in Arabidopsis. PLoS One 9, e87283. PubMed PMC
Yoneyama K, Xie X, Kusumoto D, Sekimoto H, Sugimoto Y, Takeuchi Y, Yoneyama K. 2007. Nitrogen deficiency as well as phosphorus deficiency in sorghum promotes the production and exudation of 5-deoxystrigol, the host recognition signal for arbuscular mycorrhizal fungi and root parasites. Planta 227, 125–132. PubMed
Young PR, Lashbrooke JG, Alexandersson E, Jacobson D, Moser C, Velasco R, Vivier MA. 2012. The genes and enzymes of the carotenoid metabolic pathway in Vitis vinifera L. BMC Genomics 13, 243. PubMed PMC
Zhang M, Leng P, Zhang G, Li X. 2009. Cloning and functional analysis of 9-cis-epoxycarotenoid dioxygenase (NCED) genes encoding a key enzyme during abscisic acid biosynthesis from peach and grape fruits. Journal of Plant Physiology 166, 1241–1252. PubMed