Holman, Tara J., Jones, Peter D., Russell, Laurel, Medhurst, Ann, Úbeda-Tomás, Susanna, Talloji, Prabhavathi, Marquez, Julietta, Schmuths, Heike, Tung, Swee-Ang, Taylor , Ian B, Footitt, Steven, Bachmair, Andreas, Theodoulou, Frederica L. and Holdsworth, Michael J.. (2009) The N-end rule pathway promotes seed germination and establishment through removal of ABA sensitivity in Arabidopsis. Proceedings of the National Academy of Sciences, Vol.10 (No.11). pp. 4549-4554. ISSN 0027-8424

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Abstract

The N-end rule pathway targets protein degradation through the identity of the amino-terminal residue of specific protein substrates. Two components of this pathway in Arabidopsis thaliana, PROTEOLYSIS6 (PRT6) and arginyl-tRNA:protein arginyltransferase (ATE), were shown to regulate seed after-ripening, seedling sugar sensitivity, seedling lipid breakdown, and abscisic acid (ABA) sensitivity of germination. Sensitivity of prt6 mutant seeds to ABA inhibition of endosperm rupture reduced with after-ripening time, suggesting that seeds display a previously undescribed window of sensitivity to ABA. Reduced root growth of prt6 alleles and the ate1 ate2 double mutant was rescued by exogenous sucrose, and the breakdown of lipid bodies and seed-derived triacylglycerol was impaired in mutant seedlings, implicating the N-end rule pathway in control of seed oil mobilization. Epistasis analysis indicated that PRT6 control of germination and establishment, as exemplified by ABA and sugar sensitivity, as well as storage oil mobilization, occurs at least in part via transcription factors ABI3 and ABI5. The N-end rule pathway of protein turnover is therefore postulated to inactivate as-yet unidentified key component(s) of ABA signaling to influence the seed-to-seedling transition.

Item Type:	Journal Article
Subjects:	S Agriculture > SB Plant culture
Divisions:	Faculty of Science > Life Sciences (2010- ) > Warwick HRI (2004-2010)
Library of Congress Subject Headings (LCSH):	Arabidopsis thaliana, Proteins -- Denaturation, Abscisic acid, Aminoacyl-tRNA, Transferases, Lipids -- Metabolism
Journal or Publication Title:	Proceedings of the National Academy of Sciences
Publisher:	National Academy of Sciences
ISSN:	0027-8424
Date:	17 March 2009
Volume:	Vol.10
Number:	No.11
Page Range:	pp. 4549-4554
Identification Number:	10.1073/pnas.0810280106
Status:	Peer Reviewed
Access rights to Published version:	Open Access
Funder:	Biotechnology and Biological Sciences Research Council (Great Britain) (BBSRC), Lawes Agricultural Trust (LAT), National Fruit and Cider Institute (Great Britain) (NFCI), University of Nottingham, Deutsche Forschungsgemeinschaft (DFG)
Grant number:	BA 1158/3/1 (DFG)
References:	1. ↵ 1. Bachmair A, 2. Finley D, 3. Varshavsky A (1986) In vivo half-life of a protein is a function of its amino-terminal residue. Science 234:179–186. 2. ↵ 1. Tasaki T, 2. Kwon YT (2007) The mammalian N-end rule pathway: New insights into its components and physiological roles. Trends Biochem Sci 32:520–528. 3. ↵ 1. Garzon M, 2. et al. (2007) PRT6/At5g02310 encodes an Arabidopsis ubiquitin ligase of the N-end rule pathway with arginine specificity and is not the CER3 locus. FEBS Lett 581:3189–3196. 4. ↵ 1. Potuschak T, 2. et al. (1998) PRT1 of Arabidopsis thaliana encodes a component of the plant N-end rule pathway. Proc Natl Acad Sci USA 95:7904–7908. 5. ↵ 1. Yoshida S, 2. Ito M, 3. Callis J, 4. Nishida I, 5. Watanabe A (2002) A delayed leaf senescence mutant is defective in arginyl-tRNA: Protein arginyltransferase, a component of the N-end rule pathway in Arabidopsis. Plant J 32:129–137. 6. ↵ 1. Stary S, 2. et al. (2003) PRT1 of Arabidopsis is a ubiquitin protein ligase of the plant N-end rule pathway with specificity for aromatic amino-terminal residues. Plant Physiol 133:1360–1366. 7. ↵ 1. Ditzel M, 2. et al. (2003) Degradation of DIAP1 by the N-end rule pathway is essential for regulating apoptosis. Nat Cell Biol 5:467–473. 8. ↵ 1. Lee MJ, 2. et al. (2005) RGS4 and RGS5 are in vivo substrates of the N-end rule pathway. Proc Natl Acad Sci USA 102:15030–15035. 9. ↵ 1. Takemoto D, 2. Jones DA (2005) Membrane release and destabilization of Arabidopsis RIN4 following cleavage by Pseudomonas syringae AvrRpt2. Mol Plant Microbe Interact 18:1258–1268. 10. ↵ 1. Finch-Savage WE, 2. Leubner-Metzger G (2006) Seed dormancy and the control of germination. New Phytol 171:501–523. 11. ↵ 1. Holdsworth MJ, 2. Soppe WJJ, 3. Bentsink L (2008) Molecular networks regulating Arabidopsis seed maturation, after-ripening, dormancy and germination. New Phytol 179:33–54. 12. ↵ 1. Kucera B, 2. Cohn MA, 3. Leubner-Metzger G (2005) Plant hormone interactions during seed dormancy release and germination. Seed Sci Res 15:281–307. 13. ↵ 1. Carrera E, 2. et al. (2008) Seed after-ripening is a discrete developmental pathway associated with specific gene networks in Arabidopsis. Plant J 53:214–224. 14. ↵ 1. Kushiro T, 2. et al. (2004) The Arabidopsis cytochrome P450CYP707A encodes ABA 8′- hydroxylases: Key enzymes in ABA catabolism. EMBO J 23:1647–1656. 15. ↵ 1. Okamoto M, 2. et al. (2006) CYP707A1 and CYP707A2, which encode abscisic acid 8′-hydroxylases, are indispensable for proper control of seed dormancy and germination in Arabidopsis. Plant Physiol 141:97–107. 16. ↵ 1. Lopez-Molina L, 2. Mongrand B, 3. McLachlin DT, 4. Chait BT, 5. Chua NH (2002) ABI5 acts downstream of ABI3 to execute an ABA-dependent growth arrest during germination. Plant J 32:317–328. 17. ↵ 1. Penfield S, 2. Li Y, 3. Gilday AD, 4. Graham S, 5. Graham IA (2006) Arabidopsis ABA INSENSITIVE4 regulates lipid mobilization in the embryo and reveals repression of seed germination by the endosperm. Plant Cell 18:1887–1899. 18. ↵ 1. Stone SL, 2. Williams LA, 3. Farmer LM, 4. Vierstra RD, 5. Callis J (2006) KEEP ON GOING, a RING E3 ligase essential for Arabidopsis growth and development, is involved in abscisic acid signaling. Plant Cell 18:3415–3428. 19. ↵ 1. Zhang XR, 2. Garreton V, 3. Chua NH (2005) The AIP2 E3 ligase acts as a novel negative regulator of ABA signaling by promoting ABI3 degradation. Genes Dev 19:1532–1543. 20. ↵ 1. Dekkers BJW, 2. Schuurmans J, 3. Smeekens SCM (2008) Interaction between sugar and abscisic acid signalling during early seedling development in Arabidopsis. Plant Mol Biol 67:151–167. 21. ↵ 1. Finkelstein RR, 2. Gibson SI (2002) ABA and sugar interactions regulating development: Cross-talk or voices in a crowd? Curr Opin Plant Biol 5:26–32. 22. ↵ 1. Russell L, 2. Larner V, 3. Kurup S, 4. Bougourd S, 5. Holdsworth MJ (2000) The Arabidopsis COMATOSE locus regulates germination potential. Development 127:3759–3767. 23. ↵ 1. Lemieux B, 2. Miquel M, 3. Somerville C, 4. Browse J (1990) Mutants of Arabidopsis with alterations in seed lipid fatty-acid composition. Theor Appl Genet 80:234–240. 24. ↵ 1. Lee SC, 2. et al. (2002) Gibberellin regulates Arabidopsis seed germination via RGL2, a GAI/RGA-like gene whose expression is up-regulated following imbibition. Genes Dev 16:646–658. 25. ↵ 1. Koornneef M, 2. Jorna ML, 3. Brinkhorst Van der Swan DLC, 4. Karssen CM (1982) The isolation of Abscisic Acid (ABA) deficient mutants by selection of induced revertants in non-germinating gibberellin sensitive lines of Arabidopsis thaliana (L) Heynh. Theor Appl Genet 61:385–393. 26. ↵ 1. Koornneef M, 2. Reuling G, 3. Karssen CM (1984) The isolation and characterization of abscisic acid insensitive mutants of Arabidopsis thaliana. Physiol Plant 61:377–383. 27. ↵ 1. Finkelstein RR, 2. Lynch TJ (2000) The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor. Plant Cell 12:599–609. 28. ↵ 1. Nambara E, 2. et al. (2002) A screen for genes that function in abscisic acid signaling in Arabidapsis thaliana. Genetics 161:1247–1255. 29. ↵ 1. Baker A, 2. Graham IA, 3. Holdsworth M, 4. Smith SM, 5. Theodolou FL (2006) Chewing the fat: Beta-oxidation in signalling and development. Trends Plant Sci 11:124–132. 30. ↵ 1. Eastmond PJ (2007) MONODEHYROASCORBATE REDUCTASE4 is required for seed storage oil hydrolysis and postgerminative growth in Arabidopsis. Plant Cell 19:1376–1387. 31. ↵ 1. Carrera E, 2. et al. (2007) Gene expression profiling reveals defined functions of the ABC transporter COMATOSE late in phase II of germination. Plant Physiol 143:1669–1679. Abstract/FREE Full Text 32. ↵ 1. Tyler L, 2. et al. (2004) DELLA proteins and gibberellin-regulated seed germination and floral development in Arabidopsis. Plant Physiol 135:1008–1019. 33. ↵ 1. Seo M, 2. et al. (2006) Regulation of hormone metabolism in Arabidopsis seeds: Phytochrome regulation of abscisic acid metabolism and abscisic acid regulation of gibberellin metabolism. Plant J 48:354–366. 34. ↵ 1. Bethke PC, 2. et al. (2007) The Arabidopsis aleurone layer responds to nitric oxide, gibberellin, and abscisic acid and is sufficient and necessary for seed dormancy. Plant Physiol 143:1173–1188. 35. ↵ 1. Footitt S, 2. et al. (2006) Analysis of the role of COMATOSE and peroxisomal beta-oxidation in the determination of germination potential in Arabidopsis. J Exp Bot 57:2805–2814. 36. 1. Hugouvieux V, 2. Kwak JM, 3. Schroeder JI (2001) An mRNA cap binding protein, ABH1, modulates early abscisic acid signal transduction in Arabidopsis. Cell 106:477–487. 37. 1. Nishimura N, 2. et al. (2004) Isolation and characterization of novel mutants affecting the abscisic acid sensitivity of Arabidopsis germination and seedling growth. Plant Cell Physiol 45:1485–1499. 38. 1. Parcy F, 2. Giraudat J (1997) Interactions between the ABI1 and the ectopically expressed ABI3 genes in controlling abscisic acid responses in Arabidopsis vegetative tissues. Plant J 11:693–702. 39. 1. Brocard-Gifford I, 2. Lynch TJ, 3. Garcia ME, 4. Malhotra B, 5. Finkelstein RR (2004) The Arabidopsis thaliana ABSCISIC ACID-INSENSITIVE8 locus encodes a novel protein mediating abscisic acid and sugar responses essential for growth. Plant Cell 16:406–421.
URI:	http://wrap.warwick.ac.uk/id/eprint/880

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