Advertisement

Plant Molecular Biology Reporter

, Volume 31, Issue 1, pp 204–209 | Cite as

Apple 1-Aminocyclopropane-1-Carboxylic Acid Synthase Genes, MdACS1 and MdACS3a, are Expressed in Different Systems of Ethylene Biosynthesis

  • Dongmei Tan
  • Tianzhong Li
  • Aide Wang
Original Paper

Abstract

1-Aminocyclopropane-1-carboxylic acid synthase (ACS) is one of the key regulatory enzymes involved in the synthesis of ethylene. Climacteric fruit ripening is accompanied by increased ethylene production, in which ethylene biosynthesis is changed from system 1 to system 2. In apple, at least four members of the ACS gene family have been identified, two of which, MdACS1 and MdACS3a, have been studied extensively due to their specific expression in fruit tissue. However, the regulatory role of MdACS1 and MdACS3a in the ethylene biosynthesis system is unknown. Here we addressed this issue by investigating ACS expression in ripening apple fruits. Expression analysis in ‘Golden Delicious’ and ‘Red Fuji’ fruits, in combination with treatments of 1-MCP (1-methylcyclopropene, an ethylene inhibitor) and Ethephon (an ethylene releaser) has demonstrated that MdACS3a and MdACS1operate in system 1 and system 2 ethylene biosynthesis, respectively.

Keywords

Apple (Malus x domestica Borkh.) Fruit ripening Ethylene biosynthesis ACS System 1 System 2 

Notes

Acknowledgments

We thank Dr. Zhi Liu from the Liaoning Institute of Pomology for kindly providing the plant materials. This work was supported by the Foundation for Youth Researcher of Shenyang Agricultural University (20111002).

References

  1. Abeles FB, Morgan PW, Saltveit ME (1992) Ethylene in plant biology. Academic, San DiegoGoogle Scholar
  2. Bapat VA, Trivedi PK, Ghosh A, Sane VA, Ganapathi TR, Nath P (2010) Ripening of fleshy fruit, molecular insight and the role of ethylene. Biotechnol Adv 28(94):107Google Scholar
  3. Barry CS, Llop-tous MI, Grierson D (2000) The regulation of 1-aminocyclopropane-1-carboxylic acid synthase gene expression during the transition from system 1 to system 2 ethylene synthesis in tomato. Plant Physiol 123(979):986Google Scholar
  4. Capitani G, McCarthy DL, Gut H, Grutte MG, Kirsch JF (2002) Apple 1-aminocyclopropane-1-carboxylate synthase in complex with the inhibitor l-aminoethoxyvinylglycine. J Biol Chem 277(49735):49742Google Scholar
  5. Chaves ALS, de Mello-Farias PC (2006) Ethylene and fruit ripening, from illumination gas to the control of gene expression, more than a century of discoveries. Genet Mol Biol l29:508–515CrossRefGoogle Scholar
  6. Dandekar AM, Teo G, Defilippi BG, Uratsu SL, Passey AJ, Kader AA, Stow JR, Colgan RJ, James DJ (2004) Effect of down-regulation of ethylene biosynthesis on fruit flavor complex in apple fruit. Transgenic Res 13(373):384Google Scholar
  7. Fujisawa M, Nakano T, Ito Y (2011) Identification of potential target genes for the tomato fruit-ripening regulator RIN by chromatin immunoprecipitation. BMC Plant Biol 11:26PubMedCrossRefGoogle Scholar
  8. Hou J, Gao Z, Zhang Z, Chen S, Ando T, Zhang J, Wang X (2011) Isolation and characterization of an AGAMOUS homologue PmAG from the Japanese apricot (Prunus mume Sieb. et Zucc.). Plant Mol Biol Rep 29(473):480Google Scholar
  9. Kende H (1993) Ethylene biosynthesis. Annu Rev Plant Physiol 44(283):307Google Scholar
  10. Kim WT, Silverstone A, Yip WK, Dong JG, Yang SF (1992) Induction of 1-aminocyclopropane-1-carboxylate synthase mRNA by auxin in mung bean hypocotyls and cultured apple shoots. Plant Physiol 98(465):471Google Scholar
  11. Lelièvre JM, Latché A, Jones B, Bouzayen M, Pech JC (1997) Ethylene and fruit ripening. Physiol Plant 101(727):739Google Scholar
  12. Li H, Liu F, Liu G, Wang S, Guo X, Jing J (2012) Molecular cloning and expression analysis of 13 MADS-box genes in Betula platyphylla. Plant Mol Biol Rep 30(149):157Google Scholar
  13. Liang XW, Abel S, Keller JA, Shen NF, Theologis A (1992) The 1-aminocyclopropane-1-carboxylate synthase gene family of Arabidopsis thaliana. Proc Natl Acad Sci USA 89:11046–11050PubMedCrossRefGoogle Scholar
  14. Lin Z, Zhong S, Grierson D (2009) Recent advances in ethylene research. J Exp Bot 60(3311):3336Google Scholar
  15. Lincoln JE, Campbell AD, Oetiker J, Rottmann WH, Oeller PW, Shen NF, Theologis A (1993) LE-ACS4, a fruit ripening and wound-induced 1-aminocyclopropane- 1-carboxylate synthase gene of tomato (Lycopersicon esculentum). J Biol Chem 268:19422–19430PubMedGoogle Scholar
  16. Martel C, Vrebalov J, Tafelmeyer P, Giovannoni JJ (2011) The tomato MADS-Box transcription factor RIPENING INHIBITOR interacts with promoters involved in numerous ripening processes in a COLORLESS NONRIPENING-dependent manner. Plant Physiol 157(1568):1579Google Scholar
  17. Matarasso N, Schuster S, Avni A (2005) A novel plant cysteine protease has a dual function as a regulator of 1-aminocyclopropane-1-carboxylic acid synthase gene expression. Plant Cell 17(1205):1216Google Scholar
  18. Mcmurchie EJ, Mcglasson WB, Eaks IL (1972) Treatment of fruit with propylene gives information about the biogenesis of ethylene. Nature 287(235):236Google Scholar
  19. Nakatsuka A, Murachi S, Okunishi H, Shiomi S, Nakano R, Kubo Y, Inaba A (1998) Differential expression and internal feedback regulation of 1-aminocyclopropane-1-carboxylate synthase, 1-aminocyclopropane-1-carboxylate oxidase, and ethylene receptor genes in tomato fruit during development and ripening. Plant Physiol 118(1295):1305Google Scholar
  20. Ng M, Yanofsky MF (2001) Function and evolution of the plant MADS-box gene family. Nat Rev Genet 2(186):195Google Scholar
  21. Oeller PW, Min-Wong L, Taylor LP, Pike DA, Theologis A (1991) Reversible inhibition of tomato fruit senescence by antisense RNA. Science 254(437):439Google Scholar
  22. Oraguzie NC, Iwanami H, Soejima J, Harada T, Hall A (2004) Inheritance of Md-ACS1 gene and its relationship to fruit softening in apple (Malus × domestica Borkh). Theor Appl Genet 108(1526):1533Google Scholar
  23. Oraguzie NC, Volz RK, Whitworth CJ, Bassett HCM, Hall AJ, Gardiner SE (2007) Influence of Md-ACS1 allelotype and harvest season within an apple germplasm collection on fruit softening during cold air storage. Postharvest Biol Technol 44(212):219Google Scholar
  24. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45PubMedCrossRefGoogle Scholar
  25. Rosenfield CL, Kiss E, Hrazdina G (1996) MdACS-2 (Accession No U73815) and Md-ACS3 (Accession No U73816), two new 1-aminocyclopropane-1-carboxylate synthases in ripening apple fruit. Plant Physiol 112:1735CrossRefGoogle Scholar
  26. Seymour GB, Taylor JE, Tucke GA (1993) Biochemistry of fruit ripening. Chapman & Hall, LondonCrossRefGoogle Scholar
  27. Soria-Guerra RE, Rosales-Mendoza S, Gasic K, Wisniewski ME, Band M, Korban SS (2011) Gene expression is highly regulated in early developing fruit of apple. Plant Mol Biol Rep 29(885):897Google Scholar
  28. Sunako T, Sakuraba W, Senda M, Akada S, Ishikawa R, Niizeki M, Harada T (1999) An allele of the ripening-specific 1-aminocyclopropane-1-carboxylate synthase gene (ACS1) in apple fruit with a long storage life. Plant Physiol 119(1297):1303Google Scholar
  29. Sunako T, Ishikawa R, Senda M, Akada S, Niizeki M, Harada T (2000) MdACS-5A (Accession No AB034992) and 5B (Accession No AB034993) Two wound-responsive genes encoding 1-aminocyclopropane-1-carboxylate synthase in apple. Plant Physiol 122:620Google Scholar
  30. Varanasi V, Shin S, Mattheis J, Rudell D, Zhu Y (2011) Expression profiles of the MdACS3 gene suggest a function as an accelerator of apple (Malus × domestica) fruit ripening. Postharvest Biol Technol 62(141):148Google Scholar
  31. Velasco R, Zharkikh A, Affourtit J, Dhingra A, Estaro A, Kalyanaraman A et al (2010) The genome of the domesticated apple (Malus × domestica Borkh). Nat Genet 42(833):839Google Scholar
  32. Wakasa Y, Kudo H, Ishikawa R, Akada S, Senda M, Niizeki M, Harada T (2006) Low expression of an endopolygalacturonase gene in apple fruit with long-term storage potential. Postharvest Biol Technol 39(193):198Google Scholar
  33. Wang A, Tan D, Tatsuki M, Kasai A, Li T, Saito H, Harada T (2009a) Molecular mechanism of distinct ripening profiles in ‘Fuji’ apple fruit and its early maturing sports. Postharvest Biol Technol 52(38):43Google Scholar
  34. Wang A, Yamakake J, Kudo H, Wakasa Y, Hatsuyama Y, Igarashi M, Kasai A, Li T, Harada T (2009b) Null mutation of the MdACS3 gene, coding for a ripening-specific 1-aminocyclopropane-1-carboxylate synthase, leads to long shelf life in apple fruit. Plant Physiol 151(391):399Google Scholar
  35. Wang A, Li T, Harada T (2011) The regulation of 1-aminocyclopropan-1- carboxylate synthase genes on fruit shelf life of apple. Eur J Hortic Sci 76(S77):83Google Scholar
  36. Wiersma PA, Zhang H, Lu C, Quail A, Toivonen PMA (2007) Survey of the expression of genes for ethylene synthesis and perception during maturation and ripening of ‘Sunrise’ and ‘Golden Delicious’ apple fruit. Postharvest Biol Technol 44(204):211Google Scholar
  37. Wilkinson JQ, Lanahan MB, Yen HC, Giovannoni JJ, Klee HJ (1995) An ethylene-inducible component of signal transduction encoded by Never-ripe. Science 270:1807–1809PubMedCrossRefGoogle Scholar
  38. Yang SF, Hoffman NE (1984) Ethylene biosynthesis and its regulation in higher plants. Annu Rev Plant Physiol 35(155):189Google Scholar
  39. Zhang Y, Zhu J, Dai H (2012) Characterization of transcriptional differences between columnar and standard apple trees using RNA-Seq. Plant Mol Biol Rep. doi: 10.1007/s11105-011-0396-0

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  1. 1.Fruit Development and Metabolic Biology Laboratory, College of HorticultureShenyang Agricultural UniversityShenyangPeople’s Republic of China
  2. 2.Laboratory of Fruit Cell and Molecular Breeding, College of Agronomy and Bio-techChina Agricultural UniversityBeijingPeople’s Republic of China

Personalised recommendations