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Front Plant Sci. 2016 Feb 17;7:132. doi: 10.3389/fpls.2016.00132. eCollection 2016.

Suppressor Screen and Phenotype Analyses Revealed an Emerging Role of the Monofunctional Peroxisomal Enoyl-CoA Hydratase 2 in Compensated Cell Enlargement.

Frontiers in plant science

Mana Katano, Kazuki Takahashi, Tomonari Hirano, Yusuke Kazama, Tomoko Abe, Hirokazu Tsukaya, Ali Ferjani

Affiliations

  1. Department of Biology, Tokyo Gakugei University Tokyo, Japan.
  2. Department of Biochemistry and Applied Biosciences, Miyazaki University Miyazaki, Japan.
  3. RIKEN Nishina Center Saitama, Japan.
  4. Department of Biological Sciences, Graduate School of Science, University of TokyoTokyo, Japan; Okazaki Institute for Integrative Bioscience, National Institutes of Natural SciencesOkazaki, Japan.

PMID: 26925070 PMCID: PMC4756126 DOI: 10.3389/fpls.2016.00132

Abstract

Efficient use of seed nutrient reserves is crucial for germination and establishment of plant seedlings. Mobilizing seed oil reserves in Arabidopsis involves β-oxidation, the glyoxylate cycle, and gluconeogenesis, which provide essential energy and the carbon skeletons needed to sustain seedling growth until photoautotrophy is acquired. We demonstrated that H(+)-PPase activity is required for gluconeogenesis. Lack of H(+)-PPase in fugu5 mutants increases cytosolic pyrophosphate (PPi) levels, which partially reduces sucrose synthesis de novo and inhibits cell division. In contrast, post-mitotic cell expansion in cotyledons was unusually enhanced, a phenotype called compensation. Therefore, it appears that PPi inhibits several cellular functions, including cell cycling, to trigger compensated cell enlargement (CCE). Here, we mutagenized fugu5-1 seeds with (12)C(6+) heavy-ion irradiation and screened mutations that restrain CCE to gain insight into the genetic pathway(s) involved in CCE. We isolated A#3-1, in which cell size was severely reduced, but cell number remained similar to that of original fugu5-1. Moreover, cell number decreased in A#3-1 single mutant (A#3-1sm), similar to that of fugu5-1, but cell size was almost equal to that of the wild type. Surprisingly, A#3-1 mutation did not affect CCE in other compensation exhibiting mutant backgrounds, such as an3-4 and fugu2-1/fas1-6. Subsequent map-based cloning combined with genome sequencing and HRM curve analysis identified enoyl-CoA hydratase 2 (ECH2) as the causal gene of A#3-1. The above phenotypes were consistently observed in the ech2-1 allele and supplying sucrose restored the morphological and cellular phenotypes in fugu5-1, ech2-1, A#3-1sm, fugu5-1 ech2-1, and A#3-1; fugu5-1. Taken together, these results suggest that defects in either H(+)-PPase or ECH2 compromise cell proliferation due to defects in mobilizing seed storage lipids. In contrast, ECH2 alone likely promotes CCE during the post-mitotic cell expansion stage of cotyledon development, probably by converting indolebutyric acid to indole acetic acid.

Keywords: Arabidopsis; Enoyl-CoA Hydratase 2; H+-PPase; compensation; cotyledons; gluconeogenesis; seed storage lipids

References

  1. Plant J. 2006 Nov;48(4):638-44 - PubMed
  2. Int Rev Cytol. 2002;217:1-39 - PubMed
  3. PLoS One. 2015 Nov 16;10(11):e0141247 - PubMed
  4. Prog Lipid Res. 1995;34(4):267-342 - PubMed
  5. Development. 1996 May;122(5):1589-600 - PubMed
  6. Cold Spring Harb Perspect Biol. 2015 Aug 03;7(8):a019190 - PubMed
  7. Plant Cell. 1998 Feb;10(2):183-95 - PubMed
  8. Proc Natl Acad Sci U S A. 2000 May 9;97(10):5669-74 - PubMed
  9. Annu Rev Plant Biol. 2008;59:115-42 - PubMed
  10. Plant Cell. 2011 Mar;23(3):984-99 - PubMed
  11. Prog Lipid Res. 1992;31(4):417-46 - PubMed
  12. Plant Physiol. 2007 Jun;144(2):988-99 - PubMed
  13. Plant Cell Physiol. 2013 Dec;54(12):1989-98 - PubMed
  14. Plant Cell. 2011 Aug;23(8):2895-908 - PubMed
  15. Front Plant Sci. 2011 Jul 01;2:24 - PubMed
  16. PLoS Biol. 2008 Jul 15;6(7):e174 - PubMed
  17. Dev Biol. 1999 Nov 15;215(2):407-19 - PubMed
  18. Curr Opin Plant Biol. 2007 Feb;10(1):63-9 - PubMed
  19. Bioinformatics. 2009 Aug 15;25(16):2078-9 - PubMed
  20. Curr Opin Plant Biol. 2009 Feb;12(1):17-22 - PubMed
  21. Annu Rev Plant Biol. 2006;57:477-96 - PubMed
  22. BMC Plant Biol. 2011 Nov 15;11:161 - PubMed
  23. Plant J. 2005 Jul;43(1):68-78 - PubMed
  24. J Biol Chem. 2006 Nov 24;281(47):35894-903 - PubMed
  25. J Plant Res. 2006 Jan;119(1):37-42 - PubMed
  26. Int J Dev Biol. 2005;49(5-6):547-55 - PubMed
  27. Plant Mol Biol. 2007 May;64(1-2):59-72 - PubMed
  28. Plant Cell Physiol. 2010 Jun;51(6):1046-54 - PubMed
  29. J Exp Bot. 2015 Feb;66(4):1055-63 - PubMed
  30. Bioinformatics. 2009 Nov 1;25(21):2865-71 - PubMed
  31. Curr Biol. 2013 May 6;23(9):788-92 - PubMed
  32. Plant Cell. 2014 Dec;26(12):4733-48 - PubMed
  33. Mol Plant. 2011 May;4(3):477-86 - PubMed
  34. Plant Physiol. 2000 Jun;123(2):733-42 - PubMed
  35. J Biol Chem. 2004 Oct 8;279(41):42916-23 - PubMed
  36. Plant Physiol. 2013 Jun;162(2):831-41 - PubMed
  37. Plant J. 2015 Apr;82(1):93-104 - PubMed
  38. Development. 2010 Dec;137(24):4221-7 - PubMed
  39. Planta. 2003 Oct;217(6):880-7 - PubMed
  40. Plant Signal Behav. 2013 Nov;8(11):e27204 - PubMed
  41. Curr Opin Plant Biol. 2009 Feb;12(1):9-16 - PubMed
  42. Genetics. 2008 Sep;180(1):237-51 - PubMed
  43. Plant Signal Behav. 2012 Jan;7(1):38-42 - PubMed
  44. Nat Methods. 2009 Sep;6(9):677-81 - PubMed
  45. Mutat Res. 2012 Jul 1;735(1-2):19-31 - PubMed
  46. Plant Physiol. 2010 Aug;153(4):1577-86 - PubMed
  47. Plant Cell. 2008 Dec;20(12):3227-40 - PubMed
  48. Biochem Soc Trans. 2005 Apr;33(Pt 2):380-3 - PubMed
  49. Plant Physiol. 2011 Nov;157(3):1151-62 - PubMed
  50. Plant Cell. 2009 Jul;21(7):1992-2007 - PubMed

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