Skip to main content
SpringerLink
Log in

Evaluating the involvement and interaction of abscisic acid and miRNA156 in the induction of anthocyanin biosynthesis in drought-stressed plants

  • Review
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main conclusion

ABA is involved in anthocyanin synthesis through the regulation of microRNA156, augmenting the level of expression of anthocyanin synthesis-related genes and, therefore, increasing anthocyanin level.

Drought stress is the main cause of agricultural crop loss in the world. However, plants have developed mechanisms that allow them to tolerate drought stress conditions. At cellular level, drought stress induces changes in metabolite accumulation, including increases in anthocyanin levels due to upregulation of the anthocyanin biosynthetic pathway. Recent studies suggest that the higher anthocyanin content observed under drought stress conditions could be a consequence of a rise in the abscisic acid (ABA) concentration. This plant hormone crosses the plasma membrane by specific transporters, and it is recognized at the cytosolic level by receptors known as pyrabactin resistance (PYR)/regulatory component of ABA receptors (PYR/RCARs) that regulate downstream components. In this review, we discuss the hypothesis regarding the involvement of ABA in the regulation of microRNA156 (miRNA156), which is upregulated as part of dehydration stress responsiveness in different species. The miRNA156 upregulation produces a greater level of anthocyanin gene expression, forming the multienzyme complex that will synthesize an increased level of anthocyanins at the cytosolic face of the rough endoplasmic reticulum (RER). After synthesis, anthocyanins are transported from the RER to the vacuole by two possible models of transport: (1) membrane vesicle-mediated transport, or (2) membrane transporter-mediated transport. Thus, the aim was to analyze the recent findings on synthesis, transport and the possible mechanism by which ABA could increase anthocyanin synthesis under drought stress conditions potentially throughout microRNA156 (miRNA156).

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Agarwall P, Agarwal P, Reddy MK, Sopory S (2006) Role of DREB transcription factors in abiotic and biotic stress tolerance in plants. Plant Cell Rep 25:1263–1274. doi:10.1007/s00299-006-0204-8

    Article  CAS  Google Scholar 

  • Ahmed N, Maekawa M, Noda K (2009) Anthocyanin accumulation and expression pattern of anthocyanin biosynthesis genes in developing wheat coleoptiles. Biol Plant 53:223–228

    Article  CAS  Google Scholar 

  • Alexieva V, Sergiev I, Mapelli S, Karanov E (2001) The effect of drought and ultraviolet radiation on growth and stress markers in pea and wheat. Plant Cell Environ 24:1337–1344

    Article  CAS  Google Scholar 

  • André C, Schafleitner R, Legay S, Lefèvre I, Alvarado C, Nomberto G, Hoffmann L, Hausman JF, Larondelle Y, Evers D (2009) Gene expression changes related to the production of phenolic compounds in potato tubers grown under drought stress. Phytochem 70:1107–1116

    Article  CAS  Google Scholar 

  • Antolín MC, Ayari M, Sánchez-Díaz M (2006) Effects of partial rootzone drying on yield, ripening and berry ABA in potted Tempranillo grapevines with Split roots. Aust J Grape Wine Res 12:13–20

    Article  Google Scholar 

  • Artilip T, Wisniewski M, Arora R, Norelli J (2016) An apple rootstock overexpressing a peach CBF gene alters growth and flowering in the scion but does not impact cold hardiness or dormancy. Hortic Res 3:1–9. doi:10.1038/hortres.2016.6

    Google Scholar 

  • Asano T, Tanaka N, Yang G, Hayashi N, Komatsu S (2005) Genome-wide identification of the rice calcium-dependent protein kinase and its closely related kinase gene families: comprehensive analysis of the CDPKs gene family in rice. Plant Cell Physiol 46:356–366

    Article  CAS  PubMed  Google Scholar 

  • Bae R, Kim K (2006) Anatomical observations of anthocyanin rich cells in apple skins. Hort Sci 41:733–736

    CAS  Google Scholar 

  • Barrera-Figueroa BE, Gao L, Diop NN, Wu Z, Ehlers JD, Roberts PA, Close TJ, Zhu J, Liu R (2011) Identification and comparative analysis of drought-associated microRNAs in two cowpea genotypes. BMC Plant Biol 11:127

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berdeja M, Nicolas P, Kappel C, Wu Dai Z, Hilbert G, Peccoux A, Lafontaine N, Gomés E, Delrot S (2015) Water limitation and rootstock genotype interact to alter grape berry metabolism through transcriptome reprogramming. Hort Res 2:15012

    Article  CAS  Google Scholar 

  • Boneh U, Biton I, Schwartz A, Ben-Ari G (2012) Characterization of the ABA signal transduction pathway in Vitis vinifera. Plant Sci 187:89–96

    Article  CAS  PubMed  Google Scholar 

  • Boopathi M (2015) Plant miRNomics: novel insights in gene expression and regulation. In: PlantOmics: the omics of plant science. Springer, New Delhi, pp 181–212

  • Borsani O, Gonzalez-Neves G, Ferrer M, Monza J (2010) Anthocyanins accumulation and genes-related expression in berries of cv. Tannat (Vitis vinifera L.). J Appl Hort 12:3–9

    Google Scholar 

  • Boudet A (2007) Evolution and current status of research in phenolic compounds. Phytochem 68:2722–2735

    Article  CAS  Google Scholar 

  • Boursiac Y, Léran S, Corratgé-Faillie C, Gojon A, Krouk G, Lacombe B (2013) ABA transport and transporters. Trends Plant Sci 18:325–333

    Article  CAS  PubMed  Google Scholar 

  • Boyer J (1982) Plant productivity and environment. Science 8:218–443

    Google Scholar 

  • Bucchetti B, Matthews M, Falginella L, Peterlunger E, Castellarin S (2011) Effect of water deficit on Merlot grape tannins and anthocyanins across four seasons. Sci Hort 128:297–305

    Article  CAS  Google Scholar 

  • Buer CS, Muday GK (2004) The transparent testa4 mutation prevents flavonoid synthesis and alters auxin transport and the response of Arabidopsis roots to gravity and light. Plant Cell 16:1191–1205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buer CS, Muday G, Djordjevic M (2007) Flavonoids are differentially taken up and transported long distances in Arabidopsis. Plant Physiol 145:478–490

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Candar-Cakir B, Arican E, Zhang B (2016) Small RNA and degradome deep sequencing reveals drought-and tissue-specific microRNAs and their important roles in drought-sensitive and drought-tolerant tomato genotypes. Plant Biotech 14:1727–1746. doi:10.1111/pbi.12533

    Article  CAS  Google Scholar 

  • Castellarin S, Matthews M, Di Gaspero G, Gambetta G (2007a) Water deficits accelerate ripening and induce changes in gene expression regulating flavonoid biosynthesis in grape berries. Planta 227:101–112

    Article  CAS  PubMed  Google Scholar 

  • Castellarin S, Pfeiffer A, Sivilotti P, Degan M, Peterlunger E, Di Gaspero G (2007b) Transcriptional regulation of anthocyanin biosynthesis in ripening of grapevine under seasonal water deficit. Plant Cell Environ 30:1381–1399

    Article  CAS  PubMed  Google Scholar 

  • Chalker-Scott L (1999) Environmental significance of anthocyanins in plant stress responses. Photochem Photobiol 70:1–9

    Article  CAS  Google Scholar 

  • Chanoca A, Kovinich N, Burkel B, Stecha S, Bohorquez-Restrepo A, Ueda T, Eliceiri K, Grotewold E, Otegui M (2015) Anthocyanin vacuolar inclusions form by a microautophagy mechanism. Plan Cell 27(9):1–15

    Google Scholar 

  • Choi HI, Park HJ, Park JH (2005) Arabidopsis calcium-dependent protein kinase AtCPK32 interacts with ABF4, a transcriptional regulator of abscisic acid-responsive gene expression, and modulates its activity. Plant Physiol 139:1750–1761

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Choudhary R, Saroha AE, Swarnkar PL (2011) Effect of abscisic acid and hydrogen peroxide on antioxidant enzymes in Syzygium cumini plant. J Food Sci Technol 49(5):649–652

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Conn S, Zhang W, Franco C (2003) Anthocyanic vacuolar inclusions (AVIs) selectively bind acylated anthocyanins in Vitis vinifera L. (grapevine) suspension culture. Biotechnol Lett 25:835–839

    Article  CAS  PubMed  Google Scholar 

  • Cui B, Liang Z, Liu Y, Zhu J (2012) Effects of ABA and its inhibitor fluridone on accumulation of phenolic acids and activity of PAL and TAT hairy root of Salvia miltiorrhiza. Zhongguo Zhongyao Zazhi 37(6):754–759

    CAS  PubMed  Google Scholar 

  • Cui LG, Shan JX, Shi M, Gao JP, Lin HX (2014) The miR156-SPL9-DFR pathway coordinates the relationship between development and abiotic stress tolerance in plants. Plant J 80:1108–1117

    Article  CAS  PubMed  Google Scholar 

  • Dammann D, Ichida A, Hong B, Romanowsky S, Hrabak EM, Harmon AC, Pickard BG, Harper JF (2003) Subcellular targeting of nine calcium dependent protein kinase isoforms from Arabidopsis. Plant Physiol 132:1840–1848

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Davies WJ, Zhang J (1991) Root signals and the regulation of growth and development of plant in drying soil. Annu Rev Plant Physiol Plant Mol Biol 42:55–76

    Article  CAS  Google Scholar 

  • Deis L, Cavagnaro B, Bottini R, Wuilloud R, Silva MF (2011) Water deficit and exogenous ABA significantly affect grape and wine phenolic composition under in field and in vitro conditions. Plant Growth Regul 65:11–21

    Article  CAS  Google Scholar 

  • Deluc L, Quilici D, Decendit A, Grimplet J, Wheatley M, Schlauch K, Mérillon J, Cushman J, Cramer G (2009) Water deficit alters differentially metabolic pathways affecting important flavor and quality traits in grape berries of Cabernet Sauvignon and Chardonnay. BMC Genom 10:212

    Article  CAS  Google Scholar 

  • Ding Y, Cao J, Ni L, Zhu Y, Zhang A, Tan M, Jiang M (2013) ZmCPK11 is involved in abscisic acid-induced antioxidant defence and functions upstream of ZmMPK5 in abscisic acid signaling in maize. J Exp Bot 64:871–884

    Article  CAS  PubMed  Google Scholar 

  • Dubrovina A, Kiselev K, Khristenko V (2013) Expression of calcium-dependent protein kinase (CDPK) genes under abiotic stress conditions in wild-growing grapevine Vitis amurensis. J Plant Physiol 170:1491–1500

    Article  CAS  PubMed  Google Scholar 

  • Eldem V, Okay S, Unver T (2013) Plant microRNAs: new players in functional genomics. Turk J Agric For 37:1–21

    CAS  Google Scholar 

  • Esteban M, Villanueva M, Lissarrague R (2001) Effect of irrigation on changes in the skin of cv. Tempranillo (Vitis vinifera L.) grape berries during ripening. J Sci Food Agric 81:409–420

    Article  CAS  Google Scholar 

  • Fambrini M, Pugliesi C, Vernieri P, Giuliano G, Baroncelli S (1993) Characterization of a sunflower (Helianthus annuus L.) mutant, deficient in carotenoid synthesis and abscisic-acid content, induced by in vitro tissue culture. Theor Appl Genet 87:65–69

    Article  CAS  PubMed  Google Scholar 

  • Ferrandino A, Lovisolo C (2013) Abiotic stress effects on grapevine (Vitis vinifera L.): focus on abscisic acid-mediated consequences on secondary metabolism and berry quality. Environ Exp Bot 103:138–147

    Article  CAS  Google Scholar 

  • Finkelstein R (2013) Abscisic acid synthesis and response. Arabidopsis Book 11:e0166

    Article  PubMed  PubMed Central  Google Scholar 

  • Foreman J, Demidchik V, Bothwell J, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones J, Davies J, Dolan L (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442–446

    Article  CAS  PubMed  Google Scholar 

  • Francisco R, Regalado A, Ageorges A, Burla B, Bassin B, Eisenach C, Zarrouk O, Vialet S, Marlin T, Chaves M, Martinoia E, Nagy R (2013) ABCC1, an ATP binding cassette protein from grape berry, transports anthocyanidin 3-0-glucosides. Plant Cell 25:1840–1854

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fujita Y, Fujita M, Shinozaki K, Yamagushi-Shinozaki K (2011) ABA-mediated transcriptional regulation in response to osmotic stress in plants. J Plant Res 124:509–525. doi:10.1007/s10265-011-0412-3

    Article  CAS  PubMed  Google Scholar 

  • Furlan A, Llanes A, Luna V, Castro S (2013) Abscisic acid mediates hydrogen peroxide production in peanut induced by water stress. Biol Plant 57:555–558

    Article  CAS  Google Scholar 

  • Gao A, Wu Q, Zhang Y, Miao Y, Song C (2014) Arabidopsis calcium-dependent protein kinase CPK28 is potentially involved in the response to osmotic stress. Chin Sci Bull 59:1113–1122

    Article  CAS  Google Scholar 

  • Gilroy S, Białasek M, Suzuki N, Górecka M, Devireddy A, Karpinski S, Mittler R (2016) ROS, calcium, and electric signals: key mediators of rapid systemic signaling in plants. Plant Physiol 171(3):1606–1615

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Giordano D, Provenzano S, Ferrandino A, Vitali M, Pagliarani C, Roman F, Cardinale F, Castellarin S, Schubert A (2016) Characterization of a multifunctional caffeoyl-CoA O-methyltransferase activated in grape berries upon drought stress. Plant Physiol Biochem 101:23–32. doi:10.1016/j.plaphy.2016.01.0150

    Article  CAS  PubMed  Google Scholar 

  • Gómez C, Terrier N, Torregrosa L, Vialet S, Fournier-Level A, Verriès C, Souquet JM, Mazauric JP, Klein M (2009) Grapevine MATE-Type proteins act as vacuolar H+-dependent acylated anthocyanin transporters. Plant Physiol 150:402–415

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gómez C, Conejero G, Torregrosa L, Cheynier V, Terrier N, Ageorges A (2011) In vivo grapevine anthocyanin transport involves vesicle-mediated trafficking and the contribution of anthoMATE transporters and GST. Plant J 67:960–970

    Article  PubMed  CAS  Google Scholar 

  • Gonzalez-Guzman M, Rodriguez L, Lorenzo-Orts L, Pons C, Sarrion-Perdigones A, Fernandez M, Peirats-Llobet M, Forment J, Moreno-Alvero M, Cutler S, Alert A, Granell A, Rodriguez P (2014) Tomato PYR/PYL/RCAR abscisic acid receptors show high expression in root, differential sensitivity to the abscisic acid agonist quinabactin, and the capability to enhance plant drought resistance. J Exp Bot 65:4451–4464

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goodman C, Casati P, Walbot V (2004) A multidrug resistance-associated protein involved in anthocyanin transport in Zea mays. Plant Cell 16:1812–1826

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gou JY, Felippes F, Liu CJ, Weigel D, Wang JW (2011) Negative regulation of anthocyanin biosynthesis in Arabidopsis by a miR156-targeted SPL transcription factor. Plant Cell 23:1512–1522

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gould K, Davies K, Winefield C (2009) Anthocyanins: biosynthesis, functions, and applications. Springer Science & Business Media, New York

    Google Scholar 

  • Grotewold E, Davies K (2008) Trafficking and sequestration of anthocyanins. Nat Prod Commun 3:1251–1258

    CAS  Google Scholar 

  • Guajardo E, Correa JA, Contreras-Porcia L (2016) Role of abscisic acid (ABA) in activating antioxidant tolerance responses to desiccation stress in intertidal seaweed species. Planta 243(3):767–781

    Article  CAS  PubMed  Google Scholar 

  • Guo HS, Xie Q, Fei JF, Chua N (2005) MicroRNA directs mRNA cleavage of the transcription factor NAC1 to downregulate auxin signals for Arabidopsis lateral root development. Plant Cell 17(1376):1386

    Google Scholar 

  • Haake V, Cook D, Riechmann JL, Pineda O, Thomashow MF, Zhang JZ (2002) Transcription factor CBF4 is a regulator of drought adaptation in Arabidopsis. Plant Physiol 130:639–648

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hackenberg M, Shi BJ, Gustafson P, Langridge P (2012) A transgenic factor (TaDREB3) in barley affects the expression of microRNAs and other small non-coding RNAs. Plus One 7(8):1–21

    Google Scholar 

  • Harper JF, Beton G, Harmon A (2004) Decoding Ca2+ signals through plant protein kinases. Annu Rev Plant Biol 55:263–288

    Article  CAS  PubMed  Google Scholar 

  • Herbert K, Pimienta G, DeGregorio S, Alexandrov A, Steitz J (2013) Phosphorylation of DGCR8 increase its intracellular stability and induces a progrowth miRNA profile. Cell Rep 5:1070–1081

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hong-bo S, Li-Ye C, Ming-an S (2008) Calcium as a versatile plant signal transducer under soil water stress. BioEssays 30:634–641

    Article  PubMed  CAS  Google Scholar 

  • Hrabak E, Chan C, Gribskov M, Harper J, Choi J, Halford N, Kudla J, Luan S, Nimmo H, Sussman M, Thomas M, Walker-Simmons K, Zhu JK, Harmon A (2003) The Arabidopsis CDPK-SnRK superfamily of protein kinases. Plant Physiol 132:666–680

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hsieh LC, Lin SI, Shih AC, Chen JW, Lin WY, Tseng CY, Li WH, Chiou TJ (2009) Uncovering small RNA-mediated responses to phosphate deficiency in Arabidopsis by deep sequencing. Plant Physiol 151:2120–2132

    Article  PubMed  PubMed Central  Google Scholar 

  • Hu X, Zhang A, Zhang J, Jiang M (2006) Abscisic acid is a key inducer of hydrogen peroxide production in leaves of maize plants exposed to water stress. Plant Cell Physiol 47:1484–1495

    Article  CAS  PubMed  Google Scholar 

  • Hughes NM, Carpenter KL, Cannon JG (2013) Estimating contribution of anthocyanin pigments to osmotic adjustment during winter leaf reddening. J Plant Physiol 170:230–233

    Article  CAS  PubMed  Google Scholar 

  • Huits HS, Gerats AG, Kreike MM, Mol JN, Koes RE (1994) Genetic control of dihydroflavonol 4-reductase gene expression in Petunia hybrid. Planta J 6:295–310

    Article  CAS  Google Scholar 

  • Hung K, Cheng D, Hsu Y, Kao C (2008) Abscisic acid-induced hydrogen peroxide is required for anthocyanin accumulation in leaves of rice seedlings. J Plant Physiol 165:1280–1287

    Article  CAS  PubMed  Google Scholar 

  • Jaakola L, Määttä K, Pirttila AM, Törrönen R, Kärenlampi S, Hohtola A (2002) Expression of genes involved in anthocyanin biosynthesis in relation to anthocyanin, proanthocyanidin, and flavonols levels during bilberry fruit development. Plant Physiol 130:729–739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jackson D, Roberts K, Martin C (1992) Temporal and spatial control of expression of expression of anthocyanin biosynthetic genes in developing flowers of Antirrhinum majus. Plant J 2:425–434

    Article  CAS  Google Scholar 

  • Jiang Y, Joyce D (2003) ABA effects on ethylene production, PAL activity, anthocyanin and phenolic contents of strawberry fruit. Plant Growth Regul 39:171–174

    Article  Google Scholar 

  • Jones P, George A (2002) Mechanism of ABC transporters: a molecular dynamics simulation of a well characterized nucleotide-binding subunit. PNAS 99(20):12639–12644

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jopling CL, Yi M, Lancaster AM, Lemon SM, Sarnow P (2005) Modulation of hepatitis C virus RNA abundance by a liver-specific microRNA. Science 309:1577–1581

    Article  CAS  PubMed  Google Scholar 

  • Jung S (2004) Variation in antioxidant metabolism of young and mature leaves of Arabidopsis thaliana subject to drought. Plant Sci 166:459–466

    Article  CAS  Google Scholar 

  • Kadomura-Ishikawa Y, Miyawaka K, Takahashi A, Masuda T, Noji S (2014) Light and abscisic acid independently regulated FaMYB10 in Fragaria x ananassa fruit. Planta 241:953–965

    Article  PubMed  CAS  Google Scholar 

  • Kalefetoglu T, Ekmekci Y (2009) Alterations in photochemical and physiological activities of chickpea (Cicer arietinum L.) cultivars under drought stress. J Agron Crop Sci 195:335–346

    Article  CAS  Google Scholar 

  • Kang J, Hwang JU, Lee M, Kim YY, Assmann S, Martinoia E, Lee Y (2010) PDR-type ABC transporter mediates cellular uptake of the phytohormone abscisic acid. Plant Biol 107:2355–2360

    CAS  Google Scholar 

  • Kantar M, Unver T, Budak H (2010) Regulation of barley miRNAs upon dehydration stress correlated with target gene expression. Funct Integr Genom 10:493–507

    Article  CAS  Google Scholar 

  • Kennedy JA, Matthews MA, Waterhouse AL (2002) Effect of maturity and vine water status on grape skin and wine flavonoids. Am J Enol Vitic 53:268–274

    CAS  Google Scholar 

  • Kharenko O, Choudhary P, Loewen M (2013) Abscisic acid binds to recombinant Arabidopsis thaliana G-protein coupled receptor-type G 1 in Saccharomyces cerevisiae and in vitro. Plant Physiol Biochem 68:32–36

    Article  CAS  PubMed  Google Scholar 

  • Khraiwesh B, Zhu JK, Zhu J (2012) Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants. Biochim Biophys Acta 1819:137–148

    Article  CAS  PubMed  Google Scholar 

  • Kim H, Lee K, Hwang H, Bhatnagar K, Kim DY, Yoon IS, Byun MO, Kim ST, Jung KH, Kim BG (2014) Overexpression of PYL5 in rice enhances drought tolerance, inhibits growth, and modulates gene expression. J Exp Bot 65:453–464

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kimura S, Kaya H, Kawarazaki T, Hiraoka GM, Senzaki E, Michikawa M, Kuchitsu K (2012) Protein phosphorylation is a prerequisite for the Ca2+-dependet activation of Arabidopsis NADPH oxidases and may function as trigger for the positive feedback regulation of Ca2+ and reactive oxygen species. Biochim Biophys Acta Mol Cell Res 1823:398–405

    Article  CAS  Google Scholar 

  • Klein M, Weissenbock G, Dufaud A, Gaillard C, Kreuz K, Martinoia E (1996) Different energization mechanism drive the vacuolar uptake of a flavonoid glucoside and a herbicide glucoside. J Biol Chem 271:29666–29671

    Article  CAS  PubMed  Google Scholar 

  • Kong X, Jiang W, Zhang D, Cai G, Pan J, Li D (2013) Genome-wide identification and expression analysis of calcium-dependent protein kinase in maize. BMC Genom 14:433

    Article  CAS  Google Scholar 

  • Kuo H-F, Chiou T-J (2011) The role of microRNA in phosphorus deficiency signaling. Plant Physiol 156:1016–1024

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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. Proc Natl Acad Sci 107:2361–2366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kuromori T, Sugimoto E, Shinozaki K (2011) Arabidopsis mutants of AtABCG22, an ABC transporter gene, increase water transpiration and drought susceptibility. Plant J 67:885–894

    Article  CAS  PubMed  Google Scholar 

  • Levitt J (1980) Responses of plants to environmental stresses. Academic Press, New York

    Google Scholar 

  • Li A, Zhu Y, Tan X, Wang X, Wei B, Guo H, Zhang Z, Chen X, Zhao G, Kong X, Jia J, Mao L (2008) Evolutionary and functional study of the CDPK gene family in wheat (Triticum aestivum L.). Plant Mol Biol 66:429–443

    Article  CAS  PubMed  Google Scholar 

  • Li H, Dong Y, Yin H, Wang N, Yang J, Liu X, Wang Y, Wu J, Li X (2011) Characterization of the stress associated microRNAs in Glycine max by deep sequencing. BMC Plant Biol 11:170–174

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li Q, Chen P, Dai S, Sun Y, Kai W, Pei Y, He S, Liang B, Zhang Y, Leng P (2015) PacCYP707A2 negatively regulates cherry fruit ripening while PacCYP707A1 mediates drought tolerance. J Exp Bot 66(13):3765–3774

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li J, Lv X, Wang L, Qiu Z, Song X, Lin J, Chen W (2017a) Transcriptome analysis reveals the accumulation mechanism of anthocyanins in Zijuan tea (Camellia sinensis var. asssamica (Masters) kitamura) leaves. Plant Growth Regul 81:51–61

    Article  CAS  Google Scholar 

  • Li Z, Yu J, Peng Y, Huang B (2017b) Metabolic pathways regulated by abscisic acid, salicylic acid and y-aminobutyric acid in association with improved drought tolerance in creeping bentgrass (Agrostis stolonifera). Physiol Plant 159(1):42–58. doi:10.1111/ppl.12483

    Article  CAS  PubMed  Google Scholar 

  • Liu HH, Tian X, Li YJ, Wu CA, Zheng CC (2008) Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana. RNA 14:836–843

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Llave C, Xie Z, Kasschau KD, Carrington JC (2002) Cleavage of Scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA. Science 297:2053–2056

    Article  CAS  PubMed  Google Scholar 

  • Lotkowska M, Tohge T, Fernie A, Xue GP, Balazadeh S, Mueller-Roeber B (2015) The Arabidopsis transcription factor MYB112 promotes anthocyanin formation during salinity and under high light stress. Plant Physiol 169(3):1862–1880. doi:10.1104/pp.15.00605

    PubMed  PubMed Central  Google Scholar 

  • Marrs KA, Alfenito MR, Lloyd AM, Walbolt V (1995) A glutathione S-transferase involved in vacuolar transfer encoded by the maize gene bronze-2. Nature 375:397–400

    Article  CAS  PubMed  Google Scholar 

  • Martínez-Lüscher J, Sánchez-Díaz M, Delrot S, Aguirreolea J, Pascual I, Gomés E (2014) Ultraviolet-B radiation and water deficit interact to alter flavonol and anthocyanin profiles in grapevine berries through transcriptomic regulation. Plant Cell Physiol 55(11):1–12

    Article  CAS  Google Scholar 

  • Matthews MA, Anderson M (1988) Fruit ripening in Vitis vinifera L.: responses to seasonal water deficit. Am J Enol Vitic 39:313–320

    Google Scholar 

  • McCarty D, Carson C, Stinard P, Robertson D (1989) Molecular analysis of viviparous-1: an abscisic acid-insensitive mutant of maize. Plant Cell 1:523–532

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Medina-Puche L, Cumplido-Laso G, Amil-Ruiz F, Hoffman T, Ring L, Rodriguez-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 x ananassa fruits. J Exp Bot 65(2):401–417

    Article  CAS  PubMed  Google Scholar 

  • Miyakawa T, Fujita Y, Yamaguchi-Shinozaki K, Tanokura M (2013) Structure and function of abscisic acid receptors. Trends Plant Sci 18:259–266

    Article  CAS  PubMed  Google Scholar 

  • Moreno L (2009) Plant responses to water deficit stress. Agron Colomb 27:179–191

    Google Scholar 

  • Mori I, Murata Y, Yang Y, Munemasa S, Wang YF, Andreoli S, Tiriac H, Alonso J, Harper J, Ecker J, Kwak J, Schroeder J (2006) CDPKs CPK6 and CPK3 function in ABA regulation of guard cell S-type anion and Ca2+-permeable channels and stomatal closure. Plos 4:1749–1762

    Article  CAS  Google Scholar 

  • Nagabhushana I, Reddy A (2004) Rice flavonoid pathway genes, OsDfr and OsAns, are induced by dehydration, high salt and ABA, and contain stress responsive promoter elements that interact with the transcription activator, OsC1-MYB. Plant Sci 166:1505–1513

    Article  CAS  Google Scholar 

  • Nageshbabu U, Jyothi MN, Sharadamma N, Rai DV, Devaraj VR (2013a) Expression of miRNAs confers enhanced tolerance to drought and salt stress in Finger millet (Eleusine coracona). J Stress Physiol Biochem 9:22–231

    Google Scholar 

  • Nageshbabu U, Jyothi MN, Sharadamma N, Rai DV, Devaraj VR (2013b) Expression of miRNAs regulates growth and development of French bean (Phaseolus vulgaris) under salt and drought stress conditions. Int Res J Biol Sci 2:52–56

    Google Scholar 

  • Nagira Y, Ikegami K, Koshiba T, Ozeki Y (2006) Effect of ABA upon anthocyanin synthesis in regenerated torenia shoots. J Plant Res 119:137–144

    Article  CAS  PubMed  Google Scholar 

  • Neufeld H, Poindexter D, Murakami P, Schaberg P (2011) Observations on the relationship between above- and below-ground anthocyanin production in Galax urceolata (Poir.) Brummitt growing in sun-exposed and shaded locations. Castanea 76(1):84–98

    Article  Google Scholar 

  • Ollé D, Guiraud JL, Souquet JM, Terrier N, Ageorges A, Cheynier V, Verries C (2011) Effect of pre- and post-veraison water deficit on proanthocyanidin and anthocyanin accumulation during Shiraz berry development. Aust J Grape Wine Res 17:90–100

    Article  CAS  Google Scholar 

  • Orom UA, Nielsen FC, Lund AH (2008) MicroRNA-10a bins the 5`UTR of ribosomal protein mRNAs and enhances their translation. Mol Cell 30:460–471

    Article  PubMed  CAS  Google Scholar 

  • Pandey S, Nelson DC, Assman SM (2009) Two novel GPCR-Type G proteins are abscisic acid receptors in Arabidopsis. Cell 136:136–148

    Article  CAS  PubMed  Google Scholar 

  • Park SY, Fung P, Nishimura N, Jensen D, Fujii H, Zhao Y, Lumba S, Santiago J, Rodrigues A, Chow TF, Alfred S, Bonetta D, Finkelstein R, Provart N, Desveaux D, Rodriguez P, McCourt P, Zhu JK, Schroeder J, Volkman B, Cutler S (2009) Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of star proteins. Science 324:1068–1071

    CAS  PubMed  PubMed Central  Google Scholar 

  • Paroo Z, Ye X, Chen S, Liu Q (2009) Phosphorylation of the human microRNA-generating complex mediates MAPK/Erk signaling. Cell 139:112–122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pecket RC, Small CJ (1980) Occurrence, location and development of anthocyanoplast. Phytochem 19:2571–2576

    Article  Google Scholar 

  • Pei Z, Murata Y, Benning G, Thomine S, Klüsener B, Allen G, Grill E, Schroeder J (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signaling in guard cells. Nature 406:731–734

    Article  CAS  PubMed  Google Scholar 

  • Pelletier MK, Shirley BW (1996) Analysis of flavanone3-hydroxylase in Arabidopsis seedlings. Plant Physiol 11:339–345

    Article  Google Scholar 

  • Pessarakli M (2010) Plant and crop stress, 3rd edn. Print ISBN: 978-1-4398-1396-6. eBook ISBN: 978-1-4398-1399-7

  • Portnoy V, Huang V, Place R, Li LC (2011) Small RNA and transcriptional upregulation. Wiley Interdiscip Rev RNA 2:748–760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Poustka F, Irani NG, Feller A, Lu Y, Pourcel L, Frame K, Grotewold E (2007) A trafficking pathway for anthocyanins overlaps with the endoplasmic reticulum-to-vacuole protein-sorting route in Arabidopsis and contributes to the formation of vacuolar inclusions. Plant Physiol 145:1323–1335

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rajagopalan R, Vaucheret H, Trejo J, Bartel D (2006) A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana. Genes Dev 20:3407–3425

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Risk JM, Day CL, Macknight RC (2009) Reevaluation of abscisic acid-binding assays shows that G-protein-Coupled Receptor2 does not bind abscisic acid. Plant Physiol 150:6–11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roby G, Harbertson F, Adams D, Matthews M (2004) Berry and vine water deficits as factors in winegrape composition: anthocyanins and tannins. Aust J Grape Wine Res 10:100–107

    Article  CAS  Google Scholar 

  • Sanchita Singh R, Mishra A, Shawan S, Shirke P, Gupta M, Sharma A (2015) Physiological performance, secondary metabolite and expression profiling of genes associated with drought tolerance in Withania somnifera. Protoplasma 252(6):1439–1450. doi:10.1007/s00709-015-0771-z

    Article  CAS  PubMed  Google Scholar 

  • Santesteban LG, Miranda C, Royo JB (2011) Regulated deficit irrigation effects on growth, yield, grape quality and individual anthocyanin composition in Vitis vinifera L. cv. “Tempranillo”. Agric Water Manag 98:1171–1179

    Article  Google Scholar 

  • Saslowsky D, Warek U, Winkel B (2005) Nuclear localization of flavonoid enzymes in Arabidopsis. J Biol Chem 280:23735–23740

    Article  CAS  PubMed  Google Scholar 

  • Schwinn K, Ngo H, Kenel F, Brummell D, Albert N, McCallum J, Pither-Joyce M, Crowhurst R, Eady C, Davies K (2016) The onion (Allium cepa L. R2R3-MYB Gene MYB1 regulates anthocyanin biosynthesis. Front Plant Sci 7:1865. doi:10.3389/fpls.2016.01865

    Article  PubMed  PubMed Central  Google Scholar 

  • Shen YY, Wang XF, Wu FQ, Du SY, Cao Z, Shang Y, Wang XL, Peng CC, Yu XC, Zhu SY (2006) The Mg-chelatase H subunit is an abscisic acid receptor. Nature 443:823–826

    Article  CAS  PubMed  Google Scholar 

  • Shen X, Zhao K, Liu L, Zhang K, Yuan H, Liao X, Wang Q, Guo X, Li F, Li T (2014) A role for PacMYBA in aBA-regulated anthocyanin in red-colored sweet cherry cv. Hong Deng (Prunus avium L.). Plant Cell Physiol 55(5):862–880

    Article  CAS  PubMed  Google Scholar 

  • Shi BJ, Hussain S (2016) miRNA/siRNA-based approaches to enhance drought tolerance of barley and wheat under drought stress. In: Ahmad P (ed) Water stress and crop plants: a sustainable approach, 1st edn. Wiley & Sons, UK, p 248–260

    Chapter  Google Scholar 

  • Shin DH, Choi MG, Lee HK, Cho M, Choi SB, Choi G, Park YI (2013) Calcium dependet sucrose uptake links sugar signaling to anthocyanin biosynthesis in Arabidopsis. Biochem Biophys Res Commun 430:634–639

    Article  CAS  PubMed  Google Scholar 

  • Sirichandra C, Gu D, Hu HC, Davanture M, Lee S, Djaoui M, Valot B, Zivy M, Leung J, Merlot S, Kwak J (2009) Phosphorylation of the Arabidopsis AtrbohF NADPH oxidase by OST1 protein kinase. FEBS Lett 583:2982–2986

    Article  CAS  PubMed  Google Scholar 

  • Snyder B, Nicholson R (1990) Synthesis of phytoalexins in sorghum as a site-specific response to fungal ingress. Science 248:1637–1639

    Article  CAS  PubMed  Google Scholar 

  • Sperdouli I, Moustakas M (2014) Interaction of proline, sugars, and anthocyanins during photosynthetic acclimation of Arabidopsis thaliana to drought stress. J Plant Physiol 169:577–585

    Article  CAS  Google Scholar 

  • Steyn W, Wand S, Holcroft D, Jacobs G (2002) Anthocyanins in vegetative tissues: a proposed unified function in photoprotection. New Phytol 155:349–361

    Article  CAS  Google Scholar 

  • Sudha G, Ravishankar G (2003) The role of calcium channels in anthocyanin production in callus cultures of Daucus carota. Plant Growth Regul 40:163–169

    Article  CAS  Google Scholar 

  • Sun G, Stewart C, Xiao P, Zhang B (2012a) MicroRNA expression analysis in the cellulosic biofuel crop switchgrass (Panicum virgatum) under abiotic stress. PLoS One 7:1–7

    Google Scholar 

  • Sun Y, Li H, Huang JR (2012b) Arabidopsis TT19 functions as a carrier to transport anthocyanin from the cytosol to tonoplast. Mol Plant 5:387–400

    Article  CAS  PubMed  Google Scholar 

  • Sunkar R, Kapoor A, Zhu JK (2006) Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance. Plant Cell 18:2051–2065

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tadeo F, Gómez-Cadenas A (2008) Fisiología de las plantas y el estrés. In: Azón-Bieto J, Talón M (eds) Fundamentos de Fisiología Vegetal, 2a edn. McGraw Hill, España, p 577–598

    Google Scholar 

  • Taiz L, Zeiger E (2002) Plant Physiology, 3rd edn. Sinauer Associates Inc., Publishers Sunderland, Massachusetts

    Google Scholar 

  • Taiz L, Zeiger E (2010) Plant physiology, 5th edn. Sinauer Associates Inc., Publishers Sunderland, Massachusetts

    Google Scholar 

  • Taiz L, Zeiger E, Moller M, Murphy A (2016) Plant physiology, 6th edn. Sinauer Associates Inc., Publishers Sunderland, Massachusetts

    Google Scholar 

  • Teixeira A, Eiras-Dias J, Castellarin SD, Gerós H (2013) Berry phenolics of grapevine under challenging environments. Int J Mol Sci 14:18711–18739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tian L, Wan S, Pan Q, Zheng Y, Huang W (2008) A novel plastid localization of chalcone synthase in developing grape berry. Plant Sci 175:431–436

    Article  CAS  Google Scholar 

  • Toda K, Kuroiwa H, Senthil K, Shimada N, Aoki T, Ayabe S, Shimada S, Sakuta M, Miyazaki Y, Takahashi R (2012) The soybean F3’ H protein is localized to the tonoplast in the seed coat hilum. Planta 236:79–89

    Article  CAS  PubMed  Google Scholar 

  • Trindade I, Capitao C, Dalmay T, Fevereiro MP, Santos DM (2010) miR398 and miR408 are up-regulated in response to water deficit in Medicago Truncalata. Planta 231:705–716

    Article  CAS  PubMed  Google Scholar 

  • United Nations (2014) World Water Development Report 2014. In: 6th World Water Forum “Solution for Water”, Marseille, France

  • Verweij W, Spelt C, Di Sansebastiano GP, Vermeer J, Reale L, Ferrantil F, Koes R, Quattrocchio F (2008) An H+ P-ATPase on the tonoplast determines vacuolar pH and flower colour. Nat Cell Biol 10:1456–1462

    Article  CAS  PubMed  Google Scholar 

  • Vitrac X, Larronde F, Krisa S, Decendit A, Deffiex G, Mérillon JM (2000) Sugar sensing and Ca2+-calmodulin requirement in Vitis vinifera cells producing anthocyanins. Phytochemistry 53:659–665

    Article  CAS  PubMed  Google Scholar 

  • Vogt T (2010) Phenylpropanoid biosynthesis. Mol Plant 3:2–20

    Article  CAS  PubMed  Google Scholar 

  • Wang T, Chen L, Zhao M, Tian Q, Zhang WH (2011) Identification of drought-responsive microRNAs in Medicago truncatula by genome-wide high-throughput sequencing. BMC Genom 12:367

    Article  CAS  Google Scholar 

  • Wang Y, Chen ZH, Zhang B, Hills A, Blatt M (2013) PYR/PYL/RCAR abscisic acid receptors regulate K+ and Cl− channels through reactive oxygen species-mediated activation of Ca2+ channels at the plasma membrane of intact Arabidopsis guard cells. Plant Physiol 163:566–577

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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. Aus J Grape Wine Res 15:195–204

    Article  CAS  Google Scholar 

  • Winkel-Shirley B (1999) Evidence for enzyme complexes in the phenylpropanoid and flavonoid pathways. Physiol Plant 107:142–149

    Article  CAS  Google Scholar 

  • Winkel-Shirley B (2004) Metabolic channeling in plants. Annu Rev Plant Biol 55:85–107

    Article  CAS  Google Scholar 

  • Winkel-Shirley B (2006) The biosynthesis of flavonoids. In: Grotewold E (ed) The science of flavonoids, 1st edn. Springer, New York, p 71–95

    Chapter  Google Scholar 

  • Yazaki K (2005) Transporters of secondary metabolites. Curr Opin Plant Biol 8:301–307

    Article  CAS  PubMed  Google Scholar 

  • Yoon GM, Cho HS, Ha HJ, Liu JR, Lee HS (1999) Characterization of NtCDPK1, a calcium-dependent protein kinase gene in Nicotiana tabacum, and the activity of its encoded protein. Plant Mol Biol 39:991–1001

    Article  CAS  PubMed  Google Scholar 

  • Zarrouk O, Francisco R, Pinto-Marijuan M, Brossa R, Santos R, Pinheiro C, Costa J, Lopes C, Chaves M (2012) Impact of irrigation regime on berry development and flavonoids composition in Aragonez (Sy. Tempranillo) grapevine. Agric Water Manag 114:18–29

    Article  Google Scholar 

  • Zhang X, Zhang L, Dong F, Gao J, Galbraith D, Song C (2001) Hydrogen peroxide is involved in Abscisic acid-induced stomatal closure in Vicia faba. Plant Physiol 126:1438–1448

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang H, Wang L, Deroles S, Bennett R, Davies K (2006) New insight into the vesicles and formation of anthocyanic vacuolar inclusions in flower petals. BMC Plant Biol 6:29

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang J, Chen Ch, Zhang D, Li H, Li P, Ma F (2014) Reactive oxygen species produced via plasma membrane NADPH oxidase regulate anthocyanin synthesis in apple peel. Planta 240:1023–1035

    Article  CAS  PubMed  Google Scholar 

  • Zhang XL, Jiang L, Xin Q, Liu Y, Tan JX, Chen ZZ (2015) Structural basis and functions of abscisic acid receptors PYLs. Front Plant Sci 6:88

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang C, Guo Q, Liu Y, Liu H, Wang F, Jia C (2017) Molecular cloning and functional analysis of a flavanone 3-hydroxylase gene from blueberry. J Hortic Sci Biotechnol 92:57–64

    Article  CAS  Google Scholar 

  • Zhao J, Dixon R (2010) The ‘ins’ and ‘outs’ of flavonoid transport. Trends Plant Sci 15:72–80

    Article  CAS  PubMed  Google Scholar 

  • Zhao J, Huhman D, Shadle G, He XZ, Sumner L, Tang Y, Dixon R (2011) MATE2 mediates vacuolar sequestration of flavonoid glycosides and glycoside malonates in Medicago truncatula. Plant Cell 23:1536–1555

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu SY, Yu XC, Wang XJ (2007) Two calcium-dependent protein kinases CPK4 and CPK11, regulate abscisic acid signal transduction in Arabidopsis. Plant Cell 19:3019–3036

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zou JJ, Wei FJ, Wang C, Wu JJ, Ratnasekera D, Liu WX, Wu WH (2010) Arabidopsis calcium-dependent protein kinase CPK10 functions in abscisic acid- and Ca2+-mediated stomatal regulation in response to drought stress. Plant Physiol 154:1232–1243

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We would like to thank to Dr. Jerry Cohen (University of Minnesota, Twin Cities) for critical review and comments and Comisión Nacional de Investigación Científica y Tecnológica (CONICYT) of the Government of Chile by Doctoral Scholarship and Fondecyt 1120917 Project.

Author information

Authors and Affiliations

  1. Doctoral Program in Science of Natural Resources, Universidad de La Frontera, P.O. Box 54-D, Temuco, Chile

    Jorge González-Villagra

  2. Department of Biology and The Biotron Centre for Experimental Climate Change Research, Western University, London, ON, N6A 5B7, Canada

    Leonid V. Kurepin

  3. Departamento de Ciencias Químicas y Recursos Naturales, Facultad de Ingeniería y Ciencias, Universidad de La Frontera, P.O. Box 54-D, Temuco, Chile

    Marjorie M. Reyes-Díaz

  4. Center of Plant, Soil Interaction and Natural Resources Biotechnology, Scientific and Technological Bioresource Nucleus (BIOREN), Universidad de La Frontera, P.O. Box 54-D, Temuco, Chile

    Marjorie M. Reyes-Díaz

Authors
  1. Jorge González-Villagra
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Leonid V. Kurepin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Marjorie M. Reyes-Díaz
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marjorie M. Reyes-Díaz.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

González-Villagra, J., Kurepin, L.V. & Reyes-Díaz, M.M. Evaluating the involvement and interaction of abscisic acid and miRNA156 in the induction of anthocyanin biosynthesis in drought-stressed plants. Planta 246, 299–312 (2017). https://doi.org/10.1007/s00425-017-2711-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-017-2711-y

Keywords

Search

Navigation