Advertisement

Protoplasma

, Volume 256, Issue 6, pp 1507–1517 | Cite as

Elevated gibberellin altered morphology, anatomical structure, and transcriptional regulatory networks of hormones in celery leaves

  • Ao-Qi Duan
  • Kai Feng
  • Jie-Xia Liu
  • Feng Que
  • Zhi-Sheng Xu
  • Ai-Sheng XiongEmail author
Original Article
  • 140 Downloads

Abstract

Gibberellins (GAs), as one of the important hormones in regulating the growth and development of higher plants, can significantly promote cell elongation and expansion. Celery is a widely grown leafy vegetable crop with rich nutritional value. However, the effect of gibberellins on celery leaves is unclear. In this paper, the celery variety “Jinnan Shiqin” plants were treated with gibberellic acid (GA3) and paclobutrazol (PBZ, a gibberellin inhibitor). Our results showed that GA3 treatment promoted the growth of celery leaves and caused lignification of celery leaf tissue. In addition, the transcript levels of genes associated with gibberellins, auxin, cytokinins, ethylene, jasmonic acid, abscisic acid, and brassinolide were altered in response to increased or decreased exogenous gibberellins or inhibitor. GA3 may regulate celery growth by interacting with other hormones through crosstalk mechanisms. This study provided a reference for further study of the regulation mechanism of gibberellins metabolism, and exerted effects on understanding the role of gibberellins in the growth and development of celery.

Keywords

Gibberellin Anatomic Hormone interaction Development Leaves Apium graveolens

Abbreviations

CPS

ent-copalyl diphosphate synthase

GA

Gibberellin

GA3

Gibberellic acid

GA20ox

GA20-oxidase

GA2ox

GA2-oxidase

GA3ox

GA3-oxidase

GGPP

Geranylgeranyl diphosphate

GID1

Gibberellin insensitive dwarf1

IPP

Isopentenyl pyrophosphate

KAO

ent-kaurenoic acid oxidase

KO

ent-kaurene oxidase

KS

ent-kaurene synthase

PBZ

Paclobutrazol

RT-qPCR

Quantitative real-time polymerase chain reaction

UV

Ultraviolet

SHI

Short internode

SLY1

Sleepy1

SPY

Spindly

Notes

Author contributions

Conceived and designed the experiments: ASX AQD. Performed the experiments: AQD KF JXL ZSX. Analyzed the data: AQD KF ASX. Contributed reagents/materials/analysis tools: ASX. Wrote the paper: AQD. Revised the paper: ASX FQ. All authors read and approved the final manuscript.

Funding information

The research was supported by Jiangsu Agricultural Science and Technology Innovation Fund [CX(18)2007], National Natural Science Foundation of China (31272175), and Priority Academic Program Development of Jiangsu Higher Education Institutions Project (PAPD).

Compliance with ethical standards

Competing interests

The authors declare that they have no conflict of interest.

References

  1. Achard P, Vriezen WH, Van Der Straeten D, Harberd NP (2003) Ethylene regulates Arabidopsis development via the modulation of DELLA protein growth repressor function. Plant Cell 15(12):2816–2825PubMedPubMedCentralGoogle Scholar
  2. Achard P, Cheng H, De Grauwe L, Decat J, Schoutteten H, Moritz T, Van Der Straeten D, Peng J, Harberd NP (2006) Integration of plant responses to environmentally activated phytohormonal signals. Science 311(5757):91–94PubMedGoogle Scholar
  3. Achard P, Gusti A, Cheminant S, Alioua M, Dhondt S, Coppens F, Beemster GTS, Genschik P (2009) Gibberellin signaling controls cell proliferation rate in Arabidopsis. Curr Biol 19(14):1188–1193PubMedGoogle Scholar
  4. Bai MY, Shang JX, Oh E, Fan M, Bai Y, Zentella R, Sun TP, Wang ZY (2012) Brassinosteroid, gibberellin and phytochrome impinge on a common transcription module in Arabidopsis. Nat Cell Biol 14(8):810–817PubMedPubMedCentralGoogle Scholar
  5. Chen S, Wang XJ, Zhang LY, Lin SS, Liu DC, Wang QZ, Cai SY, El-Tanbouly R, Gan LJ, Wu H, Li Y (2016) Identification and characterization of tomato gibberellin 2-oxidases (GA2oxs) and effects of fruit-specific SlGA2ox1 overexpression on fruit and seed growth and development. Hortic Res 3:16059PubMedPubMedCentralGoogle Scholar
  6. Coles JP, Phillips AL, Croker SJ, García-Lepe R, Lewis MJ, Hedden P (1999) Modification of gibberellin production and plant development in Arabidopsis by sense and antisense expression of gibberellin 20-oxidase genes. Plant J 17(5):547–556PubMedGoogle Scholar
  7. Eunkyoo O, Shinjiro Y, Jianhong H, Jikumaru Y, Byunghyuck J, Inyup P, Hee-Seung L, Tai-Ping S, Yuji K, Giltsu C (2007) PIL5, a phytochrome-interacting bHLH protein, regulates gibberellin responsiveness by binding directly to the GAI and RGA promoters in Arabidopsis seeds. Plant Cell 19(4):1192–1208Google Scholar
  8. Feng K, Hou XL, Li MY, Jiang Q, Xu ZS, Liu JX, Xiong AS (2018) CeleryDB: a genomic database for celery. Database (Oxford) 2018.  https://doi.org/10.1093/database/bay070
  9. Gallego-Bartolomé J, Minguet EG, Grau-Enguix F, Abbas M, Locascio A, Thomas SG, Alabadí D, Blázquez MA (2012) Molecular mechanism for the interaction between gibberellin and brassinosteroid signaling pathways in Arabidopsis. Proc Natl Acad Sci U S A 109(33):13446–13451PubMedPubMedCentralGoogle Scholar
  10. Gao XH, Xiao SL, Yao QF, Wang YJ, Fu XD (2011) An updated GA signaling ‘relief of repression’ regulatory model. Mol Plant 4(4):601–606PubMedGoogle Scholar
  11. Hedden P (2001) Gibberellin metabolism and its regulation. J Plant Growth Regul 20(4):317–318PubMedGoogle Scholar
  12. Hedden P, Phillips AL (2000) Gibberellin metabolism: new insights revealed by the genes. Trends Plant Sci 5(12):523–530PubMedGoogle Scholar
  13. Helliwell CA, Sheldon CC, Olive MR, Walker AR, Zeevaart JA, Peacock WJ, Dennis ES (1998) Cloning of the Arabidopsis ent-kaurene oxidase gene GA3. Proc Natl Acad Sci U S A 95(15):9019–9024PubMedPubMedCentralGoogle Scholar
  14. Helliwell CA, Poole A, Peacock WJ, Dennis ES (1999) Arabidopsis ent-kaurene oxidase catalyzes three steps of gibberellin biosynthesis. Plant Physiol 119(2):507–510PubMedPubMedCentralGoogle Scholar
  15. Helliwell CA, Chandler PM, Poole A, Dennis ES, Peacock WJ (2001) The CYP88A cytochrome P450, ent-kaurenoic acid oxidase, catalyzes three steps of the gibberellin biosynthesis pathway. Proc Natl Acad Sci U S A 98(4):2065–2070PubMedPubMedCentralGoogle Scholar
  16. Huang S, Raman AS, Ream JE, Fujiwara H, Cerny RE, Brown SM (1998) Overexpression of 20-oxidase confers a gibberellin-overproduction phenotype in Arabidopsis. Plant Physiol 118(3):773–781PubMedPubMedCentralGoogle Scholar
  17. Jasinski S, Piazza P, Craft J, Hay A, Woolley L, Rieu I, Phillips A, Hedden P, Tsiantis M (2005) KNOX action in Arabidopsis is mediated by coordinate regulation of cytokinin and gibberellin activities. Curr Biol 15(17):1560–1565PubMedGoogle Scholar
  18. Li MY, Wang F, Jiang Q, Ma J, Xiong AS (2014) Identification of SSRs and differentially expressed genes in two cultivars of celery (Apium graveolens L.) by deep transcriptome sequencing. Hortic Res 1:10PubMedPubMedCentralGoogle Scholar
  19. Li MY, Wang F, Jiang Q, Wang GL, Tian C, Xiong AS (2016) Validation and comparison of reference genes for qPCR normalization of celery (Apium graveolens) at different development stages. Front Plant Sci 7:313PubMedPubMedCentralGoogle Scholar
  20. Li MY, Hou XL, Wang F, Tan GF, Xu ZS, Xiong AS (2018) Advances in the research of celery, an important Apiaceae vegetable crop. Crit Rev Biotechnol 38(2):172–183PubMedGoogle Scholar
  21. Mikihiro O, Atsushi H, Yukika Y, Ayuko K, Yuji K, Shinjiro Y (2003) Gibberellin biosynthesis and response during Arabidopsis seed germination. Plant Cell 15(7):1591–1604Google Scholar
  22. Olszewski N, Sun TP, Gubler F (2002) Gibberellin signaling: biosynthesis, catabolism, and response pathways. Plant Cell 14:Suppl:S61–Suppl:S80PubMedGoogle Scholar
  23. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29(9):e45PubMedPubMedCentralGoogle Scholar
  24. Phillips AL, Ward DA, Uknes S, Appleford NE, Lange T, Huttly AK, Gaskin P, Graebe JE, Hedden P (1995) Isolation and expression of three gibberellin 20-oxidase cDNA clones from Arabidopsis. Plant Physiol 108(3):1049–1057PubMedPubMedCentralGoogle Scholar
  25. Ross JJ, O’Neill DP (2002) Auxin regulation of the gibberellin pathway in pea. Plant Physiol 130(4):1974–1982PubMedPubMedCentralGoogle Scholar
  26. Ross JJ, O’Neill DP, Smith JJ, Kerckhoffs LH, Elliott RC (2010) Evidence that auxin promotes gibberellin A1 biosynthesis in pea. Plant J 21(6):547–552Google Scholar
  27. Silverstone AL, Sun T (2000) Gibberellins and the green revolution. Trends Plant Sci 5(1):1–2PubMedGoogle Scholar
  28. Susana UT, Fernán F, Ilda C, Beemster GTS, Rishikesh B, Ranjan S, Peter D, Jim H, Bennett MJ (2009) Gibberellin signaling in the endodermis controls Arabidopsis root meristem size. Curr Biol 19(14):1194–1199Google Scholar
  29. Thomas SG, Phillips AL, Hedden P (1999) Molecular cloning and functional expression of gibberellin 2- oxidases, multifunctional enzymes involved in gibberellin deactivation. Proc Natl Acad Sci U S A 96(8):4698–4703PubMedPubMedCentralGoogle Scholar
  30. Ubeda-Tomás S, Federici F, Casimiro I, Beemster GTS, Bhalerao R, Swarup R, Doerner P, Haseloff J, Bennett MJ (2009) Gibberellin signaling in the endodermis controls Arabidopsis root meristem size. Curr Biol 19(14):1194–1199PubMedGoogle Scholar
  31. Wang GL, Feng Q, Xu ZS, Feng W, Xiong AS (2015a) Exogenous gibberellin altered morphology, anatomic and transcriptional regulatory networks of hormones in carrot root and shoot. BMC Plant Biol 15:290PubMedPubMedCentralGoogle Scholar
  32. 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 2:15028PubMedPubMedCentralGoogle Scholar
  33. Wang GL, Huang Y, Zhang XY, Xu ZS, Wang F, Xiong AS (2016) Transcriptome-based identification of genes revealed differential expression profiles and lignin accumulation during root development in cultivated and wild carrots. Plant Cell Rep 35(8):1743–1755PubMedGoogle Scholar
  34. Wolbang CM, Ross JJ (2001) Auxin promotes gibberellin biosynthesis in decapitated tobacco plants. Planta 214(1):153–157PubMedGoogle Scholar
  35. Wolbang CM, Chandler PM, Smith JJ, Ross JJ (2004) Auxin from the developing inflorescence is required for the biosynthesis of active gibberellins in barley stems. Plant Physiol 134(2):769–776PubMedPubMedCentralGoogle Scholar
  36. Yaarit GW, Inbar M, Roy B, John A, Neil O, Naomi O, Yuval E, David W (2005) Cross talk between gibberellin and cytokinin: the Arabidopsis GA response inhibitor SPINDLY plays a positive role in cytokinin signaling. Plant Cell 17(1):92–102Google Scholar
  37. Yanai O, Shani E, Dolezal K, Tarkowski P, Sablowski R, Sandberg G, Samach A, Ori N (2005) Arabidopsis KNOXI proteins activate cytokinin biosynthesis. Curr Biol 15(17):1566–1571PubMedGoogle Scholar
  38. Yukika Y, Mikihiro O, Ayuko K, Atsushi H, Yuji K, Shinjiro Y (2004) Activation of gibberellin biosynthesis and response pathways by low temperature during imbibition of Arabidopsis thaliana seeds. Plant Cell 16(2):367–378Google Scholar
  39. Zentella R, Zhang Z, Park M, Thomas SG, Endo A, Murase K, Fleet C, Jikumaru Y, Nambara E, Kamiya Y (2007) Global analysis of DELLA direct targets in early gibberellin signaling in Arabidopsis. Plant Cell 19(10):3037–3057PubMedPubMedCentralGoogle Scholar
  40. Zhuang WB, Gao ZH, Wen LH, Huo XM, Cai BH, Zhang Z (2015) Metabolic changes upon flower bud break in Japanese apricot are enhanced by exogenous GA4. Hortic Res 2:15046PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2019

Authors and Affiliations

  1. 1.State Key Laboratory of Crop Genetics and Germplasm Enhancement, Ministry of Agriculture and Rural Affairs Key Laboratory of Biology and Germplasm Enhancement of Horticultural Crops in East China, College of HorticultureNanjing Agricultural UniversityNanjingChina

Personalised recommendations