Skip to main content
SpringerLink
Log in

Anatomic Structure and Expression Profiles of Related Genes: Novel Insights into Leaf Development in Celery

  • Published:
Journal of Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Celery (Apium graveolens L.) belongs to the Apiaceae family and biennial herbs. Celery is an important vegetable that is cultivated and consumed worldwide. Celery leaves, particularly the petioles, are the main edible parts. Seven genes (AgTCP1, AgTCP2, AgTCP3, AgTCP4, AgDELLA, AgLEP, and AgARGOS) that are involved in leaf growth and development were cloned from two celery cultivars (‘Liuhehuangxinqin’ and ‘Ventura’). The expression profiles of these genes were determined in different tissues and at three stages of leaf growth and development. Then, the petioles and leaf blades at the three stages were anatomically characterized. Results demonstrated that the seven genes were expressed in all tissues. The highest expression of all genes, except for AgLEP and AgTCP2, was found in the leaf blades, followed by the root, stem, and petioles. The relative expression of the genes in the petioles and leaf blades increased during the three stages. Higher gene expression was detected in ‘Ventura’ than in ‘Liuhehuangxinqin’. From Stage 1 to Stage 3, the collenchyma and vascular bundles of the petioles and leaf blades developed to be thick and large, the phloem and xylem developed extensively, and the cells grew large and tightly arranged. The growth and development of ‘Ventura’ were faster than those of ‘Liuhehuangxinqin’. The expression profiles of the seven genes (AgTCP1, AgTCP2, AgTCP3, AgTCP4, AgDELLA, AgLEP, and AgARGOS) and the anatomic characteristics of the petioles and leaf blades were used as bases to identify the related functions of potential genes at the different stages of leaf growth and development in celery. This study provided insights into the leaf regulation mechanism and development in the Apiaceae plant.

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
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Becraft PW, Bongardpierce DK, Sylvester AW, Poethig RS, Freeling M (1990) The liguleless-1 gene acts tissue specifically in maize leaf development. Dev Biol 141:220–232

    Article  CAS  PubMed  Google Scholar 

  • Cassidy A, Jones J (2014) Developments in in situ hybridisation. Methods 70:39–45

    Article  CAS  PubMed  Google Scholar 

  • Chandler PM, Harding CA (2013) ‘Overgrowth’ mutants in barley and wheat: new alleles and phenotypes of the ‘Green Revolution’ Della gene. J Exp Bot 64:1603–1613

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chen MX, Maodzeka A, Zhou LH, Ali E, Wang Z, Jiang LX (2014) Removal of DELLA repression promotes leaf senescence in Arabidopsis. Plant Sci 219:26–34

    Article  PubMed  Google Scholar 

  • Cubas P, Lauter N, Doebley J, Coen E (1999) The TCP domain: a motif found in proteins regulating plant growth and development. Plant J 18:215–222

    Article  CAS  PubMed  Google Scholar 

  • Dal Santo S, Vannozzi A, Tornielli GB, Fasoli M, Venturini L, Pezzotti M, Zenoni S (2013) Genome-wide analysis of the expansin gene superfamily reveals grapevine-specific structural and functional characteristics. PLoS One. doi:10.1371/journal.pone.0062206

    Google Scholar 

  • Danisman S et al (2013) Analysis of functional redundancies within the Arabidopsis TCP transcription factor family. J Exp Bot 64:5673–5685

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Deryabin AN, Sin’kevich MS, Klimov SV, Astakhova NV, Trunova TI (2007) CO2 exchange and structural organization of chloroplasts under hypothermia in potato plants transformed with a gene for yeast invertase Russian. J Plant Physiol 54:450–455

    CAS  Google Scholar 

  • Doebley J, Stec A, Hubbard L (1997) The evolution of apical dominance in maize. Nature 386:485–488

    Article  CAS  PubMed  Google Scholar 

  • Feng G, Qin Z, Yan J, Zhang X, Hu Y (2011) Arabidopsis ORGAN SIZE RELATED1 regulates organ growth and final organ size in orchestration with ARGOS and ARL. New Phytol 191:635–646

    Article  CAS  PubMed  Google Scholar 

  • Fernandes VF, Bezerra LdA, Mielke MS, Silva DdC, Costa LCdB (2014) Anatomia e ultraestrutura foliar de Ocimum gratissimum sob diferentes níveis de radiação luminosa. Ciênc Rural 44:1037–1042

    Article  Google Scholar 

  • Flexas J, Diaz-Espejo A, Gago J, Galle A, Galmes J, Gulias J, Medrano H (2014) Photosynthetic limitations in Mediterranean plants: a review. Environ Exp Bot 103:12–23

    Article  CAS  Google Scholar 

  • Gonzalez Padilla IM, Vidoy I, Encina CL (2009) Influence of indole-butyric acid and electro-pulse on in vitro rooting and development of olive (Olea europea L.) microshoots. Plant Cell Rep 28:1411–1420

    Article  Google Scholar 

  • Herve C et al (2009) In vivo interference with AtTCP20 function induces severe plant growth alterations and deregulates the expression of many genes important for development. Plant Physiol 149:1462–1477

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hu YX, Xie O, Chua NH (2003) The Arabidopsis auxin-inducible gene ARGOS controls lateral organ size. Plant Cell 15:1951–1961

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jiang Q, Wang F, Li MY, Hw Tan, Ma J, Xiong AS (2014) High-throughput analysis of small RNAs and characterization of novel microRNAs affected by abiotic stress in a local celery cultivar. Sci Hortic 169:36–43

    Article  CAS  Google Scholar 

  • Jones NR, Lazarus P (2014) UGT2B gene expression analysis in multiple tobacco carcinogen-targeted tissues. Drug Metab Dispos 42:529–536

    Article  PubMed Central  PubMed  Google Scholar 

  • Kosugi S, Ohashi Y (1997) PCF1 and PCF2 specifically bind to cis elements in the rice proliferating cell nuclear antigen gene. Plant Cell 9:1607–1619

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kulshrestha VK, Singh N, Saxena RC, Kohli RP (1970) A study of central pharmacological activity of alkaloid fraction of Apium graveolens Linn. Indian J Med Res 58:99–102

    CAS  PubMed  Google Scholar 

  • Lakatosova M, Holeckova B (2007) Fluorescence in situ hybridisation. Biologia 62:243–250

    Article  CAS  Google Scholar 

  • Li W, Liu B, Yu L, Feng D, Wang H, Wang J (2009) Phylogenetic analysis, structural evolution and functional divergence of the 12-oxo-phytodienoate acid reductase gene family in plants. BMC Evol Biol. doi:10.1186/1471-2148-9-90

    Google Scholar 

  • Li MY, Wang F, Jiang Q, Ma J, Xiong AS (2014a) Identification of SSRs and differentially expressed genes in two cultivars of celery (Apium graveolens L.) by deep transcriptome sequencing. Horticulture. doi:10.1038/hortres.2014.10

    Google Scholar 

  • Li MY, Wang F, Xu ZS, Jiang Q, Ma J, Tan GF, Xiong AS (2014b) High throughput sequencing of two celery varieties small RNAs identifies microRNAs involved in temperature stress response. BMC Genom 15:242

    Article  Google Scholar 

  • Lin LZ, Lu S, Harnly JM (2007) Detection and quantification of glycosylated flavonoid malonates in celery, Chinese celery, and celery seed by LC-DAD-ESI/MS. J Agr Food Chem 55:1321–1326

    Article  CAS  Google Scholar 

  • Luo D, Carpenter R, Vincent C, Copsey L, Coen E (1996) Origin of floral asymmetry in Antirrhinum. Nature 383:794–799

    Article  CAS  PubMed  Google Scholar 

  • Maydup ML, Antonietta M, Guiamet JJ, Graciano C, Lopez JR, Tambussi EA (2010) The contribution of ear photosynthesis to grain filling in bread wheat (Triticum aestivum L.). Field Crops Res 119:48–58

    Article  Google Scholar 

  • McConnell JR, Barton MK (1998) Leaf polarity and meristem formation in Arabidopsis. Development 125:2935–2942

    CAS  PubMed  Google Scholar 

  • Mizukami Y (2001) A matter of size: developmental control of organ size in plants. Curr Opin Plant Biol 4:533–539

    Article  CAS  PubMed  Google Scholar 

  • Mizukami Y, Fischer RL (2000) Plant organ size control: AINTEGUMENTA regulates growth and cell numbers during organogenesis. Proc Natl Acad Sci USA 97:942–947

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Momin RA, Nair MG (2002) Antioxidant, cyclooxygenase and topoisomerase inhibitory compounds from Apium graveolens Linn. seeds. Phytomedicine 9:312–318

    Article  CAS  PubMed  Google Scholar 

  • Moore RC, Purugganan MD (2003) The early stages of duplicate gene evolution. Proc Natl Acad Sci USA 100:15682–15687

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Olofsson L, Engstrom A, Lundgren A, Brodelius PE (2011) Relative expression of genes of terpene metabolism in different tissues of Artemisia annua L. BMC Plant Biol. doi:10.1186/1471-2229-11-45

    PubMed Central  PubMed  Google Scholar 

  • Olson JM (2006) Photosynthesis in the Archean era. Photosynth Res 88:109–117

    Article  CAS  PubMed  Google Scholar 

  • Park SH et al (2007) A Ds-insertion mutant of OSH6 (Oryza sativa Homeobox 6) exhibits outgrowth of vestigial leaf-like structures, bracts, in rice. Planta 227:1–12

    Article  CAS  PubMed  Google Scholar 

  • Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. doi:10.1093/nar/29.9.e45

    PubMed Central  PubMed  Google Scholar 

  • Ponnala L, Wang Y, Sun Q, van Wijk KJ (2014) Correlation of mRNA and protein abundance in the developing maize leaf. Plant J 78:424–440

    Article  CAS  PubMed  Google Scholar 

  • Riedel A, Lang R, Rohm B, Rubach M, Hofmann T, Somoza V (2014) Structure-dependent effects of pyridine derivatives on mechanisms of intestinal fatty acid uptake: regulation of nicotinic acid receptor and fatty acid transporter expression. J Nutr Biochem 25:750–757

    Article  CAS  PubMed  Google Scholar 

  • Sentoku N, Sato Y, Matsuoka M (2000) Overexpression of rice OSH genes induces ectopic shoots on leaf sheaths of transgenic rice. Devl Biol 220:358–364

    Article  CAS  Google Scholar 

  • Snyman HA (2014) Influence of water stress on root development of Opuntia ficus-indica and O. robusta. Arid Land Res Manag 28:447–463

    Article  CAS  Google Scholar 

  • Spurr AR (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26:31–43

    Article  CAS  PubMed  Google Scholar 

  • Suzuki T, Sakurai K, Ueguchi C, Mizuno T (2001) Two types of putative nuclear factors that physically interact with histidine-containing phosphotransfer (Hpt) domains, signaling mediators in His-to-Asp phosphorelay, in Arabidopsis thaliana. Plant Cell Physiol 42:37–45

    Article  CAS  PubMed  Google Scholar 

  • Sylvester AW, Cande WZ, Freeling M (1990) Division and differentiation during normal and liguleless-1 maize leaf development. Development 110:985–1000

    CAS  PubMed  Google Scholar 

  • Tippmann HF (2004) Analysis for free: comparing programs for sequence analysis. Brief Bioinform 5:82–87

    Article  CAS  PubMed  Google Scholar 

  • Tsukaya H (1995) Developmental genetics of leaf morphogenesis in dicotyledonous plants. J Plant Res 108:407–416

    Article  Google Scholar 

  • Tsukaya H (2003) Organ shape and size: a lesson from studies of leaf morphogenesis. Curr Opin Plant Biol 6:57–62

    Article  PubMed  Google Scholar 

  • Tsukaya H, Beemster GTS (2006) Genetics, cell cycle and cell expansion in organogenesis in plants. J Plant Res 119:1–4

    Article  PubMed  Google Scholar 

  • Tsukaya H, Tsuge T, Uchimiya H (1994) The cotyledon: a superior system for studies of leaf development. Planta 195:309–312

    Article  CAS  Google Scholar 

  • Tsukaya H, Kozuka T, Kim GT (2002) Genetic control of petiole length in Arabidopsis thaliana. Plant Cell Physiol 43:1221–1228

    Article  CAS  PubMed  Google Scholar 

  • van der Graaff E, Den Dulk-Ras A, Hooykaas PJJ, Keller B (2000) Activation tagging of the LEAFY PETIOLE gene affects leaf petiole development in Arabidopsis thaliana. Development 127:4971–4980

    PubMed  Google Scholar 

  • Ward JM et al (2006) A new role for the Arabidopsis AP2 transcription factor, LEAFY PETIOLE, in gibberellin-induced germination is revealed by the misexpression of a homologous gene, SOB2/DRN-LIKE. Plant Cell 18:29–39

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Weijschede J, Antonise K, de Caluwe H, de Kroon H, Huber H (2008) Effects of cell number and cell size on petiole length variation in a stoloniferous herb. Am J Bot 95:41–49

    Article  PubMed  Google Scholar 

  • Wilkins MR and others (1999) Protein identification and analysis tools in the ExPASy server. Methods in molecular biology. 2-D proteome analysis protocols, vol 112, pp 531–552

  • Xiong A-S et al (2008) Gene duplication and transfer events in plant mitochondria genome. Biochem Biophys Res Commun 376:1–4

    Article  CAS  PubMed  Google Scholar 

  • Xiong AS et al (2009) Gene duplication, transfer, and evolution in the chloroplast genome. Biotechnol Adv 27:340–347

    Article  CAS  PubMed  Google Scholar 

  • Xiong F et al (2014) The influence of nitrogen on the development and accumulation of protein bodies in the developing endosperm of wheat caryopses. Mol Biol Rep 41:689–695

    Article  CAS  PubMed  Google Scholar 

  • Young ND et al (2011) The Medicago genome provides insight into the evolution of rhizobial symbioses. Nature 480:520–524

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yuan J et al (1999) MULTICLUSTAL: a systematic method for surveying Clustal W alignment parameters. Bioinformatics 15:862–863

    Article  CAS  PubMed  Google Scholar 

  • Zentella R et al (2007) Global analysis of DELLA direct targets in early gibberellin signaling in Arabidopsis. Plant Cell 19:3037–3057

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhuang J, Zhu B (2014) Analysis of Brassica napus ESTs: gene discovery and expression patterns of AP2/ERF-family transcription factors. Mol Biol Rep 41:45–56

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The research was supported by the National Natural Science Foundation of China (31272175); New Century Excellent Talents in University (NCET-11-0670); Jiangsu Natural Science Foundation (BK20130027); Priority Academic Program Development of Jiangsu Higher Education Institutions.

Conflict of interests

The authors declare that there are no competing interests.

Author information

Authors and Affiliations

  1. State Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Horticulture, Nanjing Agricultural University, Nanjing, 210095, China

    Xiao-Ling Jia, Guang-Long Wang, Feng Wang, Yan Li, Zhi-Sheng Xu & Ai-Sheng Xiong

Authors
  1. Xiao-Ling Jia
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Guang-Long Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Feng Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yan Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zhi-Sheng Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ai-Sheng Xiong
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ai-Sheng Xiong.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 3632 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jia, XL., Wang, GL., Wang, F. et al. Anatomic Structure and Expression Profiles of Related Genes: Novel Insights into Leaf Development in Celery. J Plant Growth Regul 34, 519–531 (2015). https://doi.org/10.1007/s00344-015-9487-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-015-9487-8

Keywords

Search

Navigation