Skip to main content
SpringerLink
Log in

Proteomic Analysis Demonstrates that Elongation of Below-Ear Internodes in Maize is Related to Three Different Hormones

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

Abstract

In many grain crops, the length of internodes below ears is related to lodging resistance in the field. To clarify the relationship between internode morphological differentiation and internode proteins during primary elongation stages in maize (Zea mays L.), we used proteomics analysis to explore factors regulating internodes in eight elite inbred maize lines: Zong3, Yu87-1, Xun9058, Xun928, Chang7-2, Zheng58, P2, and A50—the parents of four commercial hybrids in China (Yuyu22, Xundan20, Zhengdan958, and Jinsai6850). A total of 66 protein spots corresponding to 48 non-redundant proteins were identified in developing seventh to ninth leaf internodes. Of these spots, seven spots corresponding to six non-redundant proteins were related to the gibberellin (GA) pathway. Nineteen protein spots corresponding to 13 non-redundant proteins were related to the auxin (IAA) pathway, and 31 protein spots corresponding to 20 non-redundant proteins were associated with ethylene biosynthesis. A correlation analysis revealed that GA and IAA contents are negatively correlated with internode length, with the first hormone more strongly length-correlated than the second.

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

Similar content being viewed by others

References

  • Adams DO, Yang SF (1979) Ethylene biosynthesis: identification of 1-aminocyclopropane-1-carboxylic acid as an intermediate in the conversion of methionine to ethylene. Proc Natl Acad Sci 76:170–174

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alban A, David SO, Bjorkesten L, Andersson C, Sloge E, Lewis S, Currie I (2003) A novel experimental design for comparative two-dimensional gel analysis: two-dimensional difference gel electrophoresis incorporating a pooled internal standard. Proteomics 3:36–44. doi:10.1002/pmic.200390006

    Article  CAS  PubMed  Google Scholar 

  • Albermann S, Linnemannstöns P, Tudzynski B (2013) Strategies for strain improvement in Fusarium fujikuroi: overexpression and localization of key enzymes of the isoprenoid pathway and their impact on gibberellin biosynthesis. Appl Microbiol Biotechnol 97:2979–2995. doi:10.1007/s00253-012-4377-5

    Article  CAS  PubMed  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Burlini N, Facheris P, Tortora P, Guerritore A (1988) Occurrence of two phosphorylated forms of yeast fructose-1,6-bisphosphatase with different isoelectric points. Biochim Biophys Acta 972(3):353–356. doi:10.1016/0167-4889(88)90212-1

    CAS  PubMed  Google Scholar 

  • Chang XY, Gan LJ, Denny N, Xie Z, Kai X (2007) Decreased panicle-derived indole-3-acetic acid reduces gibberellin a level in the uppermost intermode, causing panicle enclosure in male sterile rice zhenshan 97 A. J Exp Bot 58:2441–2449. doi:10.1093/jxb/erm077

    Article  Google Scholar 

  • Clinkenbeard KD, Sugiyama T, Reed J (1975) Involvement of gibberellins in expression of a cysteine proteinase (SH-EP) in cotyledons of vigna mungo seedlings. BiolChem 250:3124–3135

    CAS  Google Scholar 

  • Damerval C, Vienne D, Zivy M, Thiellement H (1986) Technical improvements in two-dimensional electrophoresis increase the level of genetic variation detected in wheat-seedling proteins. Electrophoresis 7:52–54. doi:10.1002/elps.1150070108

    Article  CAS  Google Scholar 

  • Davies PJ (2010) The plant hormones: their nature, occurrence, and functions. Springer, Dordrecht, pp 1–15. doi:10.1007/978-94-009-3585-3_1

    Book  Google Scholar 

  • Duvick DN, Cassman KG (1999) Post-green revolution trends in yield potential of temperate maize in the North-Central United States. Crop Sci 39:1622–1630. doi:10.2135/cropsci1999.3961622x

    Article  Google Scholar 

  • Fang XP, Ma HS, Lu DZ, Yu H, Lai WG, Ruan SL (2011) Comparative proteomics analysis of proteins expressed in the I-1 and I-2 internodes of strawberry stolons. Proteome Sci 9:26. doi:10.1186/1477-5956-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Finnie C, Melchior S, Roepstorff P, Svensson B (2002) Proteome analysis of grain filling and seed maturation in barley. Plant Physiol 129:1308–1319. doi:10.1104/pp.003681

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Foo E, Ross JJ, Davies NW, Reid JB, Weller JL (2006) A role for ethylene in the phytochrome-mediated control of vegetative development. Plant J 46:911–921. doi:10.1111/j.1365-313X.2006.02754.x

    Article  CAS  PubMed  Google Scholar 

  • Fu Z, Jin X, Ding D, Li Y, Fu Z, Tang J (2011) Proteomic analysis of heterosis during maize seed germination. Proteomics 11:1462–1472. doi:10.1002/pmic.201000481

    Article  CAS  PubMed  Google Scholar 

  • Fujioka S, Yamane H, Spray CR, Phinney BO, Gaskin P, MacMillan J, Takahashi N (1990) Gibberellin A3 is biosynthesized from gibberellin A20 via gibberellin A5 in shoots of Zea mays L. Plant Physiol 94:127–131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gallardo K, Job C, Groot SP, Puype M, Demol H, Vandekerckhove J, Job D (2001) Proteomic analysis of Arabidopsis seed germination and priming. Plant Physiol 126:835–848

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Graebe JE (1987) Gibberellin biosynthesis and control. Annu Rev Plant Physiol 38:419–465

    Article  CAS  Google Scholar 

  • Grierson D (2013) 3 Ethylene and the control of fruit ripening. Mol Biol Biochem Fruit Ripen 6:43–71. doi:10.1002/9781118593714.ch3

    Article  Google Scholar 

  • Guillard M, Wada Y, Hansikova H, Yuasa I, Vesela K, Ondruskova N, Kadoya M, Janssen A, Heuvel LPWJVD, Morava E, Zeman J, Wevers RA, Lefeber DJ (2011) Transferrin mutations at the glycosylation site complicate diagnosis of congenital disorders of glycosylation type I. J Inherited Metabol Dis 34,901–906. doi:10.1007/s10545-011-9311-y.

    Article  CAS  Google Scholar 

  • Hamano M, Yamato Y, Yamazaki H, Miura H (2002) Endogenous gibberellins and their effects on flowering and stem elongation in cabbage (Brassica oleracea var. capitata). J Hortic Sci Biotechnol 77:220–225. doi:10.1080/14620316.2002.11511483

    Article  CAS  Google Scholar 

  • Hedden P (2003) The genes of the green revolution. Trends Genet 19:5–9

    Article  CAS  PubMed  Google Scholar 

  • Hirano T, Uchida N, Azuma T, Yasuda T (1996) Effect of submergence on distribution of photoassimilates and activities of sucrose metabolizing enzymes in sink organs of floating rice [Oryza sativa]. Jpn J Crop Sci 65:540–548. doi:10.1626/jcs.65.540

    Article  CAS  Google Scholar 

  • Isaacson T, Damasceno CM, Saravanan RS, He Y, Catalá C, Saladié M, Rose JK (2006) Sample extraction techniques for enhanced proteomic analysis of plant tissues. Nat Protoc 1:769–774. doi:10.1038/nprot.2006.102

    Article  CAS  PubMed  Google Scholar 

  • Jackson MB (2008) Ethylene-promoted elongation: an adaptation to submergence stress. Ann Bot (Lond) 101:229–248

    Article  CAS  Google Scholar 

  • Kang GZ, Li GZ, Xu W, Peng XQ, Han QX, Zhu YJ, Guo T (2012) Proteomics reveals the effects of salicylic acid on growth and tolerance to subsequent drought stress in wheat. J Proteome Res 11:6066–6079. doi:10.1021/pr300728y

    Article  CAS  PubMed  Google Scholar 

  • Konishi H, Kitano H, Komatsu S (2005) Identification of rice root proteins regulated by gibberellin using proteome analysis. Plant Cell Environ 28:328–339. doi:10.1111/j.1365-3040.2005.01269.x

    Article  CAS  Google Scholar 

  • Kushwah S, Jones AM, Laxmi A (2011) Cytokinin interplay with ethylene, auxin, and glucose signaling controls arabidopsis seedling root directional growth. Am Soc Plant Biol 156:1186–1851. doi:10.1104/pp.111.175794

    Google Scholar 

  • Lomax TL, Muday GK, Rubery PH (1995) Auxin transport. In: Davies PJ (ed) Plant hormones: physiology, biochemistry, and molecular biology. Kluwer, Dordrecht, Netherlands, pp 509–530

  • Mang HG, Kang EO, Shim JH, Kim SY, Park KY, Kim YS, Bahk YY, Kim WT (2004) A proteomic analysis identifies glutathione S-transferase isoforms whose abundance is differentially regulated by ethylene during the formation of early root epidermis in Arabidopsis seedlings. Biochim Biophys Acta (BBA) 1676:231–239. doi:10.1016/j.bbaexp.2003.12.005

    Article  CAS  Google Scholar 

  • McQueen-Mason SJ, Rochange F (1999) Expansins in plant growth and development: an update on an emerging topic. Plant Biol 1:19–25. doi:10.1055/s-2007-978484

    Article  Google Scholar 

  • Migné C, Prensier G, Grenet E (1994) Immunogold labelling of xylans and arabinoxylans in the plant cell walls of maize stem. Biol Cell 81:267–276. doi:10.1016/0248-4900(94)90009-4

    Article  Google Scholar 

  • Nakayama N, Smith RS, Mandel T, Robinson S, Kimura S, Boudaoud A, Kuhlemeier C (2012) Mechanical regulation of auxin-mediated growth. Curr Biol 22:635–637. doi:10.1016/j.cub.2012.06.050

    Article  Google Scholar 

  • Neuhoff V, Arold N, Taube D, Ehrhardt W (1988) Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using Coomassie Brilliant Blue G-250 and R-250. Electrophoresis 9:255–262. doi:10.1002/elps.1150090603

    Article  CAS  PubMed  Google Scholar 

  • Phillips IDJ (1971) Effect of relative hormone concentration on auxin-gibberellin interaction in correlative inhibition of axillary buds. Planta 96:27–34. doi:10.1007/BF00397901

    Article  CAS  PubMed  Google Scholar 

  • Porubleva L, VanderVeelden K, Korthari S, Oliver DJ, Chitnis PR (2001) The proteome of maize leaves: use of gene sequences and expressed sequence tag data for identification of proteins with peptide mass fingerprints. Electrophoresis 22:1724–1738. doi:10.1002/1522-2683(200105)22:9<1724::AID-ELPS1724>3.0.CO;2-2

    Article  CAS  PubMed  Google Scholar 

  • Rayle DL, Cleland RE (1992) The acid growth theory of auxin-induced cell elongation is alive and well. Plant Physiol 99:1271–1274

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ritchie SW, Hanway JJ, Benson GO (1989) How a corn plant develops. Iowa State University of Science and Technology, Cooperative Extension Service, lowa, special report, 48

  • Rodweli VW, Monamarn DJ, Shapiro DJA (1973) Gibberellin A (4/7) enhanced cone production in tsuga heterophylla: the influence of Gibberellin A (4/7) on seed-and pollen-cone production. Enzymd 38:373–412. doi:10.1086/297019

    Google Scholar 

  • Romeo T, Gong M, Liu MY (1993) Identification and molecular characterization of csrA, a pleiotropic gene from Escherichia coli that affects glycogen biosynthesis, gluconeogenesis, cell size, and surface properties. J Bacteriol 175:4744–4755

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sauter M, Kende H (1992) Gibberellin-induced growth and regulation of the cell division cycle in deepwater rice. Planta 188(3):362–368. doi:10.1007/BF00192803

    Article  CAS  PubMed  Google Scholar 

  • Schaller GE (2012) Ethylene and the regulation of plant development. BMC Biol 10:9–11. doi:10.1186/1741-7007-10-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sharma VK, Malik MK, Maheshwari SC, Khurana JP (1997) Light-Induced changes in phosphorylation status of low molecular weight wheat nuclear proteins. J Plant Biochem Biotechnol 6(1):9–12. doi:10.1007/BF03263001

    Article  CAS  Google Scholar 

  • Shibaoka H (1994) Plant hormone-induced changes in the orientation of cortical microtubules: alterations in the cross-linking between microtubules and the plasma membrane. Annu Rev Plant Biol 45:527–544. doi:10.1146/annurev.pp.45.060194.002523

    Article  CAS  Google Scholar 

  • Skylas DJ, Mackintosh JA, Cordwell SJ, Basseal DJ, Walsh BJ, Harry J, Blumenthal C, Copeland L, Wrigley CW, Rathmell W (2000) Proteome approach to the characterisation of protein composition in the developing and mature wheat-grain endosperm. J Cereal Sci 32:169–188. doi:10.1006/jcrs.2000.0321

    Article  CAS  Google Scholar 

  • Smith TA (1990) Plant polyamines: metabolism and function. Curr Topics Plant Physiol 5:1–23

    Google Scholar 

  • Szabados L, Savouré A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15:89–97. doi:10.1016/j.tplants.2009.11.009

    Article  CAS  PubMed  Google Scholar 

  • Tang JH, Teng WT, Ma XQ, Yan JB, Meng YJ, Li JS (2007) The genetic dissection of plant height using a set of RIL population in maize. Euphytica 155:117–124. doi:10.1007/s10681-006-9312-3

    Article  CAS  Google Scholar 

  • Van Noorden GE, Kerim T, Goffard N, Wiblin R, Pellerone FI, Rolfe BG, Mathesius U (2007) Overlap of proteome changes in Medicago truncatula in response to auxin and Sinorhizobium meliloti. Plant Physiol 144:1115–1131. doi:10.1104/pp.107.099978

    Article  PubMed  PubMed Central  Google Scholar 

  • Van der Straeten D, Zhou ZY, Prinsen E, Van Onckelen HA, Van Montagu MC (2001) A comparative molecular-physiological study of submergence response in lowland and deepwater rice. Plant Physiol 125:955–968

    Article  Google Scholar 

  • Vogler H, Kuhlemeier C (2003) Simple hormones but complex signalling: growth and development. Curr Opin Plant Biol 6:51–56. doi:10.1016/S1369-5266(02)00013-4

    Article  CAS  PubMed  Google Scholar 

  • Voss T, Haberl P (2000) Observations on the reproducibility and matching efficiency of two-dimensional electrophoresis gels: consequences for comprehensive data analysis. Electrophoresis 21:3345–3350. doi:10.1002/1522-2683(20001001)21:16<3345::AID-ELPS3345>3.0.CO;2-Z

    Article  CAS  PubMed  Google Scholar 

  • Xu N, York K, Miller P, Cheikh N (2004) Co-regulation of ear growth and internode elongation in corn. Plant Growth Regul 44:231–241. doi:10.1007/s10725-004-5935-3

    Article  CAS  Google Scholar 

  • Xu SB, Li T, Deng ZY, Chong K, Xue YB, Wang T (2008) Dynamic proteomic analysis reveals a switch between central carbon metabolism and alcoholic fermentation in rice filling grains. Plant Physiol 148:908–925. doi:10.1104/pp.108.125633

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang SF, Dong JG (1993) Recent progress in research of ethylene biosynthesis. Bot Bull Acad Sin 34:89–101

    CAS  Google Scholar 

  • Zarembinski TI, Theologis A (1997) Expression characteristics of OS-ACS1 and OS-ACS2, two members of the 1-aminocyclopropane-1-carboxylate synthase gene family in rice (Oryza sativa L. cv. Habiganj Aman II) during partial submergence. Plant Mol Biol 33:71–77. doi:10.1023/B:PLAN.0000009693.26740.c3

    Article  CAS  PubMed  Google Scholar 

  • Zhang MX, He JX, Wang BX (1997) Effect of osmotic stress and Co++ on ethylene production and endogenous polyamine content in wheat seedlings. Acta Bot Boreal 17:67–71

    Google Scholar 

  • Zhao P, Ding D, Zhang FF, Zhao XF, Xue YD, Li WH, Fu ZY, Li HC, Tang JH (2015) Investigating the molecular genetic basis of heterosis for internode expansion in maize by microRNA transcriptomic deep sequencing. Funct Integr Genom 15:261–270. doi:10.1007/s10142-014-0411-2

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Key Laboratory of Physiological Ecology and Genetic Improvement of Food Crops in Henan Province, Department of Agronomy, College of Agronomy, Henan Agricultural University, 95 Wenhua Road, Zhengzhou, 450002, China

    Zhihui Ma, Yongqiang Chen, Canran Sun, Jiao Jin, Zhanyong Guo & Zhiyuan Fu

  2. Postdoctoral Research Base of Henan Institute of Science and Technology, Xinxiang, 453000, China

    Zhihui Ma

Authors
  1. Zhihui Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yongqiang Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Canran Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jiao Jin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zhanyong Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Zhiyuan Fu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zhiyuan Fu.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ma, Z., Chen, Y., Sun, C. et al. Proteomic Analysis Demonstrates that Elongation of Below-Ear Internodes in Maize is Related to Three Different Hormones. J Plant Growth Regul 37, 144–155 (2018). https://doi.org/10.1007/s00344-017-9714-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-017-9714-6

Keywords

Search

Navigation