Abstract
Gibberellins (GAs) are important growth regulators involved in plant development processes. However, limited information is known about the relationship between GA and xylogenesis in carrots. In this study, carrot roots were treated with GA3. The effects of applied GA3 on root growth, xylem development, and lignin accumulation were then investigated. Results indicated that GA treatment dose-dependently inhibited carrot root growth. The cell wall significantly thickened in the xylem parenchyma. Autofluorescence analysis with ultraviolet (UV) excitation indicated that these cells became lignified because of long-term GA3 treatment. Moreover, lignin content increased in the roots, and the transcripts of lignin biosynthesis genes were altered in response to applied GA3. Our data indicate that GA may play important roles in xylem growth and lignification in carrot roots. Further studies shall focus on regulating plant lignification, which may be achieved by modifying GA levels within plant tissues.
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Abbreviations
- 4CL:
-
4-coumarate-CoA ligase;
- C3ʹH:
-
p-coumaroyl shikimate/quinate 3ʹ-hydroxylase;
- C4H:
-
Cinnamate 4-hydroxylase;
- CAD:
-
Cinnamyl alcohol dehydrogenase;
- CCoAOMT:
-
Caffeoyl-CoA O-methyltransferase;
- CCR:
-
Cinnamoyl-CoA reductase;
- DAT:
-
Days after treatment;
- FW:
-
Fresh weight;
- GA:
-
Gibberellin;
- HCT:
-
Hydroxycinnamoyl-CoA shikimate/quinate hydroxycinnamoyl transferase;
- LAC:
-
Laccase;
- PAL:
-
Phenylalanine ammonia lyase;
- PER:
-
Peroxidase;
- UV:
-
Ultraviolet rays
References
Aimaretti NR, Ybalo CV, Rojas ML, Plou FJ, Yori JC (2012) Production of bioethanol from carrot discards. Bioresour Technol 123:727–732
Ali MB, McNear DH Jr (2014) Induced transcriptional profiling of phenylpropanoid pathway genes increased flavonoid and lignin content in Arabidopsis leaves in response to microbial products. BMC Plant Biol 14:84
Arana MV, SÁNchez-Lamas M, Strasser B, Ibarra SE, CerdÁN PD, Botto JF, SÁNchez RA (2014) Functional diversity of phytochrome family in the control of light and gibberellin-mediated germination in Arabidopsis. Plant Cell Environ 37:2014–2023
Beemster GT, Baskin TI (2000) Stunted plant 1 mediates effects of cytokinin, but not of auxin, on cell division and expansion in the root of Arabidopsis. Plant Physiol 124:1718–1727
Biemelt S, Tschiersch H, Sonnewald U (2004) Impact of altered gibberellin metabolism on biomass accumulation, lignin biosynthesis, and photosynthesis in transgenic tobacco plants. Plant Physiol 135:254–265
Cai C, Xu C, Li X, Ferguson I, Chen K (2006) Accumulation of lignin in relation to change in activities of lignification enzymes in loquat fruit flesh after harvest. Postharvest Biol Technol 40:163–169
Cervilla LM, Rosales MA, Rubio-Wilhelmi MM, Sánchez-Rodríguez E, Blasco B, Ríos JJ, Romero L, Ruiz JM (2009) Involvement of lignification and membrane permeability in the tomato root response to boron toxicity. Plant Sci 176:545–552
Dayan J, Schwarzkopf M, Avni A, Aloni R (2010) Enhancing plant growth and fiber production by silencing GA 2-oxidase. Plant Biotechnol J 8:425–435
Donaldson LA, Knox JP (2012) Localization of cell wall polysaccharides in normal and compression wood of radiata pine: relationships with lignification and microfibril orientation. Plant Physiol 158:642–653
Eriksson ME, Israelsson M, Olsson O, Moritz T (2000) Increased gibberellin biosynthesis in transgenic trees promotes growth, biomass production and xylem fiber length. Nat Biotechnol 18:784–788
Giacomelli L, Rota-Stabelli O, Masuero D, Acheampong AK, Moretto M, Caputi L, Vrhovsek U, Moser C (2013) Gibberellin metabolism in Vitis vinifera L. during bloom and fruit-set: functional characterization and evolution of grapevine gibberellin oxidases. J Exp Bot 64:4403–4419
Grebenstein C, Kos SP, de Jong TJ, Tamis WLM, de Snoo GR (2013) Morphological markers for the detection of introgression from cultivated into wild carrot (Daucus carota L.) reveal dominant domestication traits. Plant Biol 15:531–540
Grieneisen VA, Xu J, Marée AF, Hogeweg P, Scheres B (2007) Auxin transport is sufficient to generate a maximum and gradient guiding root growth. Nautilus 449:1008–1013
Hedden P, Phillips AL (2000) Gibberellin metabolism: new insights revealed by the genes. Trends Plant Sci 5:523–530
Huang Y, Li MY, Wang F, Xu ZS, Huang W, Wang GL, Ma J, Xiong AS (2015) Heat shock factors in carrot: genome-wide identification, classification, and expression profiles response to abiotic stress. Mol Biol Rep 42:893–905
Israelsson M, Eriksson M, Hertzberg M, Aspeborg H, Nilsson P, Moritz T (2003) Changes in gene expression in the wood-forming tissue of transgenic hybrid aspen with increased secondary growth. Plant Mol Biol 52:893–903
Jia XL, Wang GL, Xiong F, Yu XR, Xu ZS, Wang F, Xiong AS (2015) De novo assembly, transcriptome characterization, lignin accumulation, and anatomic characteristics: novel insights into lignin biosynthesis during celery leaf development. Sci Rep 5:8259
Jiang S, Xu K, Wang YZ, Ren YP, Gu S (2008) Role of GA3, GA4 and uniconazole-P in controlling gravitropism and tension wood formation in Fraxinus mandshurica Rupr. Var. japonica maxim. Seedlings. J Integr Plant Biol 50:19–28
Jourdan M, Gagné S, Dubois-Laurent C, Maghraoui M, Huet S, Suel A, Hamama L, Briard M, Peltier D, Geoffriau E (2015) Carotenoid content and root color of cultivated carrot: a candidate-gene association study using an original broad unstructured population. PLoS One 10:e0116674
Jung JK, McCouch S (2013) Getting to the roots of it: genetic and hormonal control of root architecture. Front Plant Sci 4:186
Kende H, Zeevaart J (1997) The five “classical” plant hormones. Plant Cell 9:1197–1210
Lee Y, Lee WS, Kim SH (2013) Hormonal regulation of stem cell maintenance in roots. J Exp Bot 64:1153–1165
Lindsey K, Rowe J, Liu J (2014) Hormonal crosstalk for root development: a combined experimental and modelling perspective. Front Plant Sci 5:116
Little CHA, MacDonald JE (2003) Effects of exogenous gibberellin and auxin on shoot elongation and vegetative bud development in seedlings of Pinus sylvestris and Picea glauca. Tree Physiol 23:73–83
Liu J, Mehdi S, Topping J, Friml J, Lindsey K (2013) Interaction of PLS and PIN and hormonal crosstalk in Arabidopsis root development. Front Plant Sci 4:75
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408
Luby CH, Maeda HA, Goldman IL (2014) Genetic and phenological variation of tocochromanol (vitamin E) content in wild (Daucus carota L. var. carota) and domesticated carrot (D. carota L. var. sativa). Hortic Res 1:14015
Mauriat M, Moritz T (2009) Analyses of GA20ox- and GID1-over-expressing aspen suggest that gibberellins play two distinct roles in wood formation. Plant J 58:989–1003
Michel-Wolwertz MR, Sironval C (1963) Inhibition of growth and accumulation of β-carotene in carrot roots by gibberellic acid. Phytochemistry 2:183–187
Ogawa M, Hanada A, Yamauchi Y, Kuwahara A, Kamiya Y, Yamaguchi S (2003) Gibberellin biosynthesis and response during Arabidopsis seed germination. Plant Cell 15:1591–1604
Okuno A, Hirano K, Asano K, Takase W, Masuda R, Morinaka Y, Ueguchi-Tanaka M, Kitano H, Matsuoka M (2014) New approach to increasing rice lodging resistance and biomass yield through the use of high gibberellin producing varieties. PLoS One 9:e86870
Ragni L, Nieminen K, Pacheco-Villalobos D, Sibout R, Schwechheimer C, Hardtke CS (2011) Mobile gibberellin directly stimulates Arabidopsis hypocotyl xylem expansion. Plant Cell 23:1322–1336
Reinecke DM, Wickramarathna AD, Ozga JA, Kurepin LV, Jin AL, Good AG, Pharis RP (2013) Gibberellin 3-oxidase gene expression patterns influence gibberellin biosynthesis, growth, and development in pea. Plant Physiol 163:929–945
Sakamoto T, Morinaka Y, Ishiyama K, Kobayashi M, Itoh H, Kayano T, Iwahori S, Matsuoka M, Tanaka H (2003) Genetic manipulation of gibberellin metabolism in transgenic rice. Nat Biotechnol 21:909–913
Shan C, Mei Z, Duan J, Chen H, Feng H, Cai W (2014) OsGA2ox5, a gibberellin metabolism enzyme, is involved in plant growth, the root gravity response and salt stress. PLoS One 9:e87110
Tanimoto E (1987) Gibberellin-dependent root elongation in Lactuca sativa: recovery from growth retardant-suppressed elongation with thickening by low concentration of GA3. Plant Cell Physiol 28:963–973
Tanimoto E (1988) Gibberellin regulation of root growth with change in galactose content of cell walls in Pisum sativum. Plant Cell Physiol 29:269–280
Tanimoto E (1994) Interaction of gibberellin A3 and ancymidol in the growth and cell-wall extensibility of dwarf pea roots. Plant Cell Physiol 35:1019–1028
Tanimoto E (2005) Regulation of root growth by plant hormones-roles for auxin and gibberellin. Crit Rev Plant Sci 24:249–265
Tian C, Jiang Q, Wang F, Wang GL, Xu ZS, Xiong AS (2015) Selection of suitable reference genes for qPCR normalization under abiotic stresses and hormone stimuli in carrot leaves. PLoS One 10:e0117569
Tokuji Y, Kuriyama K (2003) Involvement of gibberellin and cytokinin in the formation of embryogenic cell clumps in carrot (Daucus carota). J Plant Physiol 160:133–141
Tokunaga N, Uchimura N, Sato Y (2006) Involvement of gibberellin in tracheary element differentiation and lignification in Zinnia elegans xylogenic culture. Protoplasma 228:179–187
Wadenbäck J, von Arnold S, Egertsdotter U, Walter M, Grima-Pettenati J, Goffner D, Gellerstedt G, Gullion T, Clapham D (2008) Lignin biosynthesis in transgenic Norway spruce plants harboring an antisense construct for cinnamoyl CoA reductase (CCR). Transgenic Res 17:379–392
Wang GL, Jia XL, Xu ZS, Wang F, Xiong AS (2015a) Sequencing, assembly, annotation, and gene expression: novel insights into the hormonal control of carrot root development revealed by a high-throughput transcriptome. Mol Gen Genomics 290:1379–1391
Wang GL, Xiong F, Que F, Xu ZS, Wang F, Xiong AS (2015b) Morphological characteristics, anatomical structure, and gene expression: novel insights into gibberellin biosynthesis and perception during carrot growth and development. Hortic Res 2:15028
Wang GL, Xu ZS, Wang F, Li MY, Tan GF, Xiong AS (2015c) Regulation of ascorbic acid biosynthesis and recycling during root development in carrot (Daucus carota L.). Plant Physiol Biochem 94:10–18
Wuddineh WA, Mazarei M, Zhang J, Poovaiah CR, Mann DGJ, Ziebell A, Sykes RW, Davis MF, Udvardi MK, Stewart CN (2015) Identification and overexpression of gibberellin 2-oxidase (GA2ox) in switchgrass (Panicum virgatum L.) for improved plant architecture and reduced biomass recalcitrance. Plant Biotechnol J 13:636–647
Xu ZS, Huang Y, Wang F, Song X, Wang GL, Xiong AS (2014a) Transcript profiling of structural genes involved in cyanidin-based anthocyanin biosynthesis between purple and non-purple carrot (Daucus carota L.) cultivars reveals distinct patterns. BMC Plant Biol 14:262
Xu ZS, Tan HW, Wang F, Hou XL, Xiong AS (2014b) CarrotDB: a genomic and transcriptomic database for carrot. Database 2014: bau096
Yazawa K, Takahata K, Kamada H (2004) Isolation of the gene encoding carrot leafy cotyledon1 and expression analysis during somatic and zygotic embryogenesis. Plant Physiol Biochem 42:215–223
Yuan H, Zhang J, Nageswaran D, Li L (2015) Carotenoid metabolism and regulation in horticultural crops. Hortic Res 2:15036
Zhao XY, Zhu DF, Zhou B, Peng WS, Lin JZ, Huang XQ, He RQ, Zhuo YH, Peng D, Tang DY, Li MF, Liu XM (2010) Over-expression of the AtGA2ox8 gene decreases the biomass accumulation and lignification in rapeseed (Brassica napus L.). J Zhejiang Univ Sci B 11:471–481
Acknowledgments
The research was supported by the Jiangsu Natural Science Foundation (BK20130027) and the Priority Academic Program Development of Jiangsu Higher Education Institutions.
Authors’ contribution
ASX and GLW initiated and designed the research. GLW and FQ performed the experiments. GLW, ZSX, and FW analyzed the data. GLW wrote the paper. ASX and GLW revised the paper. All authors read and approved the final manuscript.
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Wang, GL., Que, F., Xu, ZS. et al. Exogenous gibberellin enhances secondary xylem development and lignification in carrot taproot. Protoplasma 254, 839–848 (2017). https://doi.org/10.1007/s00709-016-0995-6
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DOI: https://doi.org/10.1007/s00709-016-0995-6