Endogenous abscisic acid promotes hypocotyl growth and affects endoreduplication during dark-induced growth in tomato (Solanum lycopersicum L.)

. 2015 ; 10 (2) : e0117793. [epub] 20150219

Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid25695830

Dark-induced growth (skotomorphogenesis) is primarily characterized by rapid elongation of the hypocotyl. We have studied the role of abscisic acid (ABA) during the development of young tomato (Solanum lycopersicum L.) seedlings. We observed that ABA deficiency caused a reduction in hypocotyl growth at the level of cell elongation and that the growth in ABA-deficient plants could be improved by treatment with exogenous ABA, through which the plants show a concentration dependent response. In addition, ABA accumulated in dark-grown tomato seedlings that grew rapidly, whereas seedlings grown under blue light exhibited low growth rates and accumulated less ABA. We demonstrated that ABA promotes DNA endoreduplication by enhancing the expression of the genes encoding inhibitors of cyclin-dependent kinases SlKRP1 and SlKRP3 and by reducing cytokinin levels. These data were supported by the expression analysis of the genes which encode enzymes involved in ABA and CK metabolism. Our results show that ABA is essential for the process of hypocotyl elongation and that appropriate control of the endogenous level of ABA is required in order to drive the growth of etiolated seedlings.

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Hansen H, Grossmann K (2000) Auxin-induced ethylene triggers abscisic acid biosynthesis and growth inhibition. Plant Physiol 124: 1437–1448. PubMed PMC

Davies PJ (2010) The plant hormones: their nature, occurrence, and functions In: Davies PJ, editor. Plant hormones: biosynthesis, signal transduction, action! Dordrecht, The Netherlands: Springer. 9–11 p.

Rai MK, Shekhawat NS, Gupta AK, Phulwaria M, Ram K, et al. (2011) The role of abscisic acid in plant tissue culture: a review of recent progress. Plant Cell Tiss Org 106: 179–190.

Zhang J, Davies WJ (1990) Does ABA in the xylem control the rate of leaf growth in soil-dried maize and sunflower plants? J Exp Bot 41: 1125–1132.

Creelman RA, Mason HS, Bensen RJ, Boyer JS, Mullet JE (1990) Water deficit and abscisic acid cause differential inhibition of shoot versus root growth in soybean seedlings: Analysis of growth, sugar accumulation, and gene expression. Plant Physiol 92: 205–214. PubMed PMC

Munns R, Cramer GR (1996) Is coordination of leaf and root growth mediated by abscisic acid? Opinion. Plant Soil 185: 33–49.

Wakabayashi K, Sakurai N, Kuraishi S (1989) Role of the outer tissue in abscisic acid‐mediated growth suppression of etiolated squash hypocotyl segments. Physiol Plantarum 75: 151–156.

Hayashi Y, Takahashi K, Inoue S-I, Kinoshita T (2014) Abscisic acid suppresses hypocotyl elongation by dephosphorylating plasma membrane H(+)-ATPase in Arabidopsis thaliana. Plant Cell Physiol 55: 845–853. 10.1093/pcp/pcu028 PubMed DOI

Quarrie SA (1987) Use of genotypes differing in endogenous abscisic acid levels in studies of physiology and development In: Hoad GV, Lenton J R, Jackson MB, Atkin RK, editors. Hormone action in plant development—a critical appraisal. London: Butterworths; pp. 89–105. 10.1111/tpj.12742 DOI

Takahashi K (1972) Abscisic acid as a stimulator for rice mesocotyl growth. Nat New Biol 238: 92–93.

Saab IN, Sharp RE, Pritchard J, Voetberg GS (1990) Increased endogenous abscisic acid maintains primary root growth and inhibits shoot growth of maize seedlings at low water potentials. Plant Physiol 93: 1329–1336. PubMed PMC

Sharp RE, LeNoble ME, Else MA, Thorne ET, Gherardi F (2000) Endogenous ABA maintains shoot growth in tomato independently of effects on plant water balance: evidence for an interaction with ethylene. J Exp Bot 51: 1575–1584. PubMed

LeNoble ME, Spollen WG, Sharp RE (2004) Maintenance of shoot growth by endogenous ABA: genetic assessment of the involvement of ethylene suppression. J Exp Bot 55: 237–245. PubMed

Barrero JM, Piqueras P, González-Guzmán M, Serrano R, Rodríguez PL, et al. (2005) A mutational analysis of the ABA1 gene of Arabidopsis thaliana highlights the involvement of ABA in vegetative development. J Exp Bot 56: 2071–2083. PubMed

Arsovski AA, Galstyan A, Guseman JM, Nemhauser JL (2012) Photomorphogenesis. In The Arabidopsis Book. e0147. 10.1199/tab.0147 PubMed DOI PMC

Barrero JM, Rodríguez PL, Quesada V, Alabadí D, Blázquez MA, et al. (2008) The ABA1 gene and carotenoid biosynthesis are required for late skotomorphogenic growth in Arabidopsis thaliana . Plant Cell Environ 31: 227–234. PubMed

Taylor IB, Linforth RST, Al-Naieb RJ, Bowman WR, Marples BA (1988) The wilty tomato mutants flacca and sitiens are impaired in the oxidation of ABA-aldehyde to ABA. Plant Cell Environ 11: 739–745.

Tal M, Nevo Y (1973) Abnormal stomatal behavior and root resistance, and hormonal imbalance in three wilty mutants of tomato. Biochem Genet 3: 291–300. PubMed

Neill SJ, Horgan R (1985) Abscisic acid production and water relations in wilty tomato mutants subjected to water deficiency. J Exp Bot 36: 1222–1231.

Burbidge A, Grieve TM, Jackson A, Thompson A, McCarty DR, et al. (1999) Characterization of the ABA‐deficient tomato mutant notabilis and its relationship with maize Vp14. Plant J 17: 427–431. PubMed

Thompson AJ, Thorne ET, Burbidge A, Jackson AC, Sharp RE, et al. (2004) Complementation of notabilis, an abscisic acid-deficient mutant of tomato: Importance of sequence context and utility of partial complementation. Plant Cell Environ 27: 459–471.

Murashige T, Skoog A (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plantarum 15: 473–497.

Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9: 671–675. PubMed PMC

Pěnčík A, Rolčík J, Novák O, Magnus V, Barták P, et al. (2009) Isolation of novel indole-3-acetic acid conjugates by immunoaffinity extraction. Talanta 80: 651–655. 10.1016/j.talanta.2009.07.043 PubMed DOI

Hoyerová K, Gaudinová A, Malbeck J, Dobrev PI, Kocábek T, et al. (2006) Efficiency of different methods of extraction and purification of cytokinins. Phytochem 67: 1151–1159. PubMed

Dobrev PI, Kamínek M (2002) Fast and efficient separation of cytokinins from auxin and abscisic acid and their purification using mixed-mode solidphase extraction. J Chromatogr A 950: 21–29. PubMed

Svačinová J, Novák O, Plačková L, Lenobel R, Holík J, et al. (2012) A new approach for cytokinin isolation from Arabidopsis tissues using miniaturized purification: pipette tip solid-phase extraction. Plant Methods 8: 17 10.1186/1746-4811-8-17 PubMed DOI PMC

Dekkers BJ, Willems L, Bassel GW, van Bolderen-Veldkamp RP, Ligterink W, et al. (2012) Identification of reference genes for RT-qPCR expression analysis in Arabidopsis and tomato seeds. Plant Cell Physiol 53: 28–37. 10.1093/pcp/pcr113 PubMed DOI

Doležel J, Greilhuber J, Suda J (2007) Estimation of nuclear DNA content in plants using flow cytometry. Nat Protoc 2: 2233–2244. PubMed

Parks BM, Cho MH, Spalding EP (1998) Two genetically separable phases of growth inhibition induced by blue light in Arabidopsis seedlings. Plant Physiol 118: 609–615. PubMed PMC

Parks BM, Spalding EP (1999) Sequential and coordinated action of phytochromes A and B during Arabidopsis stem growth revealed by kinetic analysis. P Natl Acad Sci USA 96: 14142–14146. PubMed PMC

Kitahata N, Asami T (2011) Chemical biology of abscisic acid. J Plant Res 124: 549–557. 10.1007/s10265-011-0415-0 PubMed DOI

Nitsch LM, Oplaat C, Feron R, Ma Q, Wolter-Arts M, et al. (2009) Abscisic acid levels in tomato ovaries are regulated by LeNCED1 and SlCYP707A1 . Planta 299: 1335–1346. PubMed

Traas J, Hülskamp M, Gendreau E, Höfte H (1998) Endoreduplication and development: rule without dividing? Curr Opin Plant Biol 1: 498–503. PubMed

Bergougnoux V, Zalabák D, Jandová M, Novák O, Wiese-Klinkenberg A, et al. (2012) Effect of blue light on endogenous isopentenyladenine and endoreduplication during photomorphogenesis and de-etiolation of tomato (Solanum lycopersicum L.) seedlings. PLoS One. 7, e45255 10.1371/journal.pone.0045255 PubMed DOI PMC

Wang H, Qi Q, Schorr P, Cutler AJ, Crosby WL, et al. (1998) ICK1, a cyclin-dependent protein kinase inhibitor from Arabidopsis thaliana interacts with both Cdc2a and CycD3, and its expression is induced by abscisic acid. Plant J 15: 501–510. PubMed

Bisbis B, Delmas F, Joubés J, Sicard A, Hernould M, et al. (2006) Cyclin-dependent kinase (CDK) inhibitors regulate the CDK-cyclin complex activities in endoreduplicating cells of developing tomato fruit. J Biol Chem 281: 7374–7383. PubMed

Nafati M, Fragne N, Hernould M, Chevalier C, Gévaudant F (2010) Functional characterization of the tomato cyclin-dependent kinase inhibitor SlKRP1 domains involved in protein-protein interactions. New Phytol 188: 136–149. 10.1111/j.1469-8137.2010.03364.x PubMed DOI

Chen H, Zhang J, Neff MM, Hong S-W, Zhang H, et al. (2008) Integration of light and abscisic acid signaling during seed germination and early seedling development. P Natl Acad Sci USA 105: 4495–4500 10.1073/pnas.0710778105 PubMed DOI PMC

Mäkelä P, Munns R, Colmer TD, Peltonen‐Sainio P (2003) Growth of tomato and an ABA‐deficient mutant (sitiens) under saline conditions. Physiol Plantarum: 117: 58–63.

Aroca R, Del Mar Alguacil M, Vernieri P, Ruiz-Lozano JM (2008) Plant responses to drought stress and exogenous ABA application are modulated differently by mycorrhization in tomato and an ABA-deficient mutant (sitiens). Microb Ecol 56: 704–719. 10.1007/s00248-008-9390-y PubMed DOI

Sharp RE (2002) Interaction with ethylene: changing views on the role of abscisic acid in root and shoot growth responses to water stress. Plant Cell Environ 25: 211–222. PubMed

Taiz L, Zeiger E (2006) Plant Physiology, fourth edition Sunderland, Massachusetts: Sinauer Associates, Inc., Publishers; Pp. 485–486. 10.1016/j.ijsu.2006.06.025 DOI

Dolezal K, Popa I, Krystof V, Spíchal L, Fojtíková M, et al. (2006) Preparation and biological activity of 6-benzylaminopurine derivatives in plants and human cancer cells. Bioorg Med Chem 14: 875–884. PubMed

Jones HG, Sharp CS, Higgs KH (1987). Growth and water relations of wilty mutants of tomato (Lycopersicon esculentum Mill.). J Exp Bot 38: 1848–1856.

Sindhu RK, Walton DC (1988) Xanthoxin metabolism in cell-free preparations from wild type and wilty mutants of tomato. Plant Physiol 88: 178–182. PubMed PMC

Groot SP, Yperen II, Karssen CM (1991) Strongly reduced levels of endogenous abscisic acid in developing seeds of tomato mutant sitiens do not influence in vivo accumulation of dry matter and storage proteins. Physiol Plantarum 81: 73–78.

Leung J, Giraudat J (1998) Abscisic acid signal transduction. Annu Rev Plant Physiol Plant Mol Biol 49: 199–222. PubMed

Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR (2010) Abscisic acid: emergence of a core signaling network. Annu Rev Plant Biol 61: 651–679. 10.1146/annurev-arplant-042809-112122 PubMed DOI

Rushton DL, Tripathi P, Rabara RC, Lin J, Ringler P, et al. (2012) WRKY transcription factors: key components in abscisic acid signalling. Plant Biotechnol J 10: 2–11. 10.1111/j.1467-7652.2011.00634.x PubMed DOI

Finkelstein R (2013) Abscisic acid synthesis and response. Arabidopsis Book 11: e0166 10.1199/tab.0166 PubMed DOI PMC

Brocard-Gifford I, Lynch TJ, Garcia ME, Malhotra B, Finkelstein RR (2004) The Arabidopsis thaliana ABSCISIC ACID-INSENSITIVE8 locus encodes a novel protein mediating abscisic acid and sugar responses essential for growth. Plant Cell 16: 406–421. PubMed PMC

Gonzalez-Guzman M, Pizzio GA, Antoni R, Vera-Sirera F, Merilo E, et al. (2012) Arabidopsis PYR/PYL/RCAR receptors play a major role in quantitative regulation of stomatal aperture and transcriptional response to abscisic acid. Plant Cell 24: 2483–2496. 10.1105/tpc.112.098574 PubMed DOI PMC

Kraepiel Y, Rousselin P, Sotta B, Kerhoas L, Einhorn J, et al. (1994) Analysis of phytochrome- and ABA-deficient mutants suggests that ABA degradation is controlled by light in Nicotiana plumbaginifolia. Plant J 6: 665–672.

Weatherwax SC, Ong MS, Degenhardt J, Bray EA, Tobin EM (1996) The interaction of light in the regulation of plant gene expression. Plant Physiol 111: 363–370. PubMed PMC

Symons GM, Reid JB (2003) Hormone levels and response during de-etiolation in pea. Planta 216: 422–431. PubMed

Nagel OW, Konings H, Lambers H (1994) Growth rate, plant development and water relations of the ABA deficient tomato mutant sitiens . Physiol Plantarum 92: 102–108.

Perrot-Rechenmann C (2010) Cellular responses to auxin: division versus expansion. Cold Spring Harb Perspect Biol. 2: a001446 10.1101/cshperspect.a001446 PubMed DOI PMC

Wen B, Nieuwland J, Murray JAH (2013) The Arabidopsis CDK inhibitor ICK3/KRP5 is rate limiting for primary root growth and promotes growth through cell elongation and endoreduplication. J Exp Bot 64: 1–13. 10.1093/jxb/ers358 PubMed DOI PMC

del Castellano M, Boniotti MB, Caro E, Schnittiger A, Gutierrez C (2004) DNA replication licensing affects cell proliferation or endoreplication in a cell type-specific manner. Plant Cell 16: 2380–2393. PubMed PMC

Pettko-Szandtner A, Meszaros T, Horvath GV, Bako L, Csordas-Toth E, et al. (2006) Activation of an alfalfa cyclin-dependent kinase inhibitor by calmodulin-like domain protein kinase. Plant J 46: 111–123. PubMed

Alabadí D, Gallego-Bartolomé J, García-Cárcel L, Orlando L, Rubio V, et al. (2008) Gibberellins modulate light signalling pathways to prevent Arabidopsis seedling de-etiolation in darkness. Plant J 53: 324–335. PubMed

Yamburenko MV, Zubo YO, Vankova R, Kusnetsov VV, Kulaeva ON, et al. (2013) Abscisic acid represses the transcription of chloroplast genes. J Exp Bot 64: 4491–4502. 10.1093/jxb/ert258 PubMed DOI PMC

Guan C, Wang X, Feng J, Hong S, Liang Y, et al. (2014) Cytokinin antagonizes abscisic acid-mediated inhibition of cotyledon greening of promoting the degradation of ABSCISIC ACID INSENSITIVE5 protein in Arabidopsis. Plant Physiol 164: 1515–1526. 10.1104/pp.113.234740 PubMed DOI PMC

Valente P, Tao W, Verbelen JP (1998). Auxins and cytokinins control DNA endoreduplication and deduplication in single cells of tobacco. Plant Sci 134: 207–215.

Scofield S, Dewitte W, Nieuwland J, Murray JA (2013) The Arabidopsis homeobox gene SHOOT MERISTEMLESS has cellular and meristem‐organisational roles with differential requirements for cytokinin and CYCD3 activity. Plant J 75: 53–66. 10.1111/tpj.12198 PubMed DOI

Takahashi N, Kajihara T, Okamura C, Kim Y, Katagiri Y, et al. (2013) Cytokinins Control Endocycle Onset by Promoting the Expression of an APC/C Activator in Arabidopsis Roots. Curr Biol 23: 1812–1817. 10.1016/j.cub.2013.07.051 PubMed DOI

Brugiere N, Jiao S, Hantke S, Zinselmeier C, Roessler JA, et al. (2003) Cytokinin oxidase gene expression in maize is localized to the vasculature, and is induced by cytokinins, abscisic acid, and abiotic stress. Plant Physiol 132: 1228–1240. PubMed PMC

Rivero RM, Gimeno J, Van Deynze A, Harkamal W, Blumwald E (2010) Enhanced cytokinin synthesis in tobacco plants expressing PSARK:: IPT prevents the degradation of photosynthetic protein complexes during drought. Plant Cell Physiol 51: 1929–1941. 10.1093/pcp/pcq143 PubMed DOI

Nambara E, Marion-Poll A (2005) Abscisic acid biosynthesis and catabolism. Annu Rev Plant Biol 56: 165–185.oamdg. PubMed

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