Characterization of the tomato ARF gene family uncovers a multi-levels post-transcriptional regulation including alternative splicing

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Zouine, Mohamed ^a,b   Fu, Yongyao ^a,b   Chateigner Boutin, Anne Laure ^a,b   Mila, Isabelle ^a,b   Frasse, Pierre ^a,b   Wang, Hua ^a,b   Audran, Corinne ^a,b   Roustan, Jean Paul ^a,b   Bouzayen, Mondher ^a,b  

^a GRENOBLE INSTITUTE OF TECHNOLOGY   (France)

^b Centre National de la Recherche Scientifique   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ARF PROTEIN; AUXIN; ETHYLENE; SMALL INTERFERING RNA;

5' UNTRANSLATED REGION; ACUTE RESPONSE FACTOR GENE; ALTERNATIVE RNA SPLICING; ARF GENE; ARTICLE; COMPUTER MODEL; CONTROLLED STUDY; FLOWER; FRUIT; GENE CONTROL; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETIC REGULATION; GENETIC TRANSCRIPTION; MULTIGENE FAMILY; NOMENCLATURE; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PHYSIOLOGICAL PROCESS; PLANT GENE; PLANT GENOME; POSTTRANSCRIPTIONAL CONTROL; PROTEIN FUNCTION; PROTEIN STRUCTURE; REGULATORY SEQUENCE; REPRESSOR GENE; RNA SEQUENCE; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; SOLANUM; TOMATO; TRANSACTIVATION ASSAY;

5' UNTRANSLATED REGIONS; ALTERNATIVE SPLICING; CLUSTER ANALYSIS; FRUIT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; LYCOPERSICON ESCULENTUM; MULTIGENE FAMILY; OPEN READING FRAMES; ORGAN SPECIFICITY; PHYLOGENY; PLANT PROTEINS; RNA INTERFERENCE; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA STABILITY; TRANSCRIPTIONAL ACTIVATION;

EID: 84897477883     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0084203     Document Type: Article

References (57)

1. Quint M, Gray WM (2006) Auxin signaling. Curr Opin Plant Biol 9: 448-453. (Pubitemid 44292053)
2. Teale WD, Ditengou FA, Dovzhenko AD, Li X, Molendijk AM, et al. (2008) Auxin as a model for the integration of hormonal signal processing and transduction. Mol Plant 1: 229-237.
3. Wang H, Schauer N, Usadel B, Frasse P, Zouine M, et al. (2009) Regulatory features underlying pollination-dependent and -independent tomato fruit set revealed by transcript and primary metabolite profiling. Plant Cell 21: 1428-1452.
4. Sagar M, Chervin C, Mila I, Hao Y, Roustan JP, et al. (2013) SlARF4, an auxin response factor involved in the control of sugar metabolism during tomato fruit development. Plant Physiol 161: 1362-1374.
5. Sagar M, Chervin C, Bouzayen M, Zouine M (2013) Under-expression of the Auxin Response Factor Sl-ARF4 improves post-harvest behavior of tomato fruits. Plant Signal Behav 8.
6. Theologis A, Huynh TV, Davis RW (1985) Rapid induction of specific mRNAs by auxin in pea epicotyl tissue. J Mol Biol 183: 53-68.
7. Guilfoyle T, Hagen G, Ulmasov T, Murfett J (1998) How does auxin turn on genes? Plant Physiol 118: 341-347. (Pubitemid 128652926)
8. Tiwari SB, Hagen G, Guilfoyle T (2003) The roles of auxin response factor domains in auxin-responsive transcription. Plant Cell 15: 533-543. (Pubitemid 36230003)
9. Hayashi K (2012) The interaction and integration of auxin signaling components. Plant Cell Physiol 53: 965-975.
10. Szemenyei H, Hannon M, Long JA (2008) TOPLESS mediates auxin-dependent transcriptional repression during Arabidopsis embryogenesis. Science 319: 1384-1386. (Pubitemid 351354872)
11. Causier B, Lloyd J, Stevens L, Davies B (2012) TOPLESS co-repressor interactions and their evolutionary conservation in plants. Plant Signal Behav 7: 325-328.
12. Ulmasov T, Murfett J, Hagen G, Guilfoyle TJ (1997) Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9: 1963-1971. (Pubitemid 28174069)
13. Wang L, Kim J, Somers DE (2013) Transcriptional corepressor TOPLESS complexes with pseudoresponse regulator proteins and histone deacetylases to regulate circadian transcription. Proc Natl Acad Sci U S A 110: 761-766.
14. Audran-Delalande C, Bassa C, Mila I, Regad F, Zouine M, et al. (2012) Genome-wide identification, functional analysis and expression profiling of the Aux/IAA gene family in tomato. Plant Cell Physiol 53: 659-672.
15. Rademacher EH, Lokerse AS, Schlereth A, Llavata-Peris CI, Bayer M, et al. (2012) Different auxin response machineries control distinct cell fates in the early plant embryo. Dev Cell 22: 211-222.
16. Cole M, Chandler J, Weijers D, Jacobs B, Comelli P, et al. (2009) DORNROSCHEN is a direct target of the auxin response factor MONOPTEROS in the Arabidopsis embryo. Development 136: 1643-1651.
17. Lim PO, Lee IC, Kim J, Kim HJ, Ryu JS, et al. (2010) Auxin response factor 2 (ARF2) plays a major role in regulating auxin-mediated leaf longevity. J Exp Bot 61: 1419-1430.
18. Wilmoth JC, Wang S, Tiwari SB, Joshi AD, Hagen G, et al. (2005) NPH4/ARF7 and ARF19 promote leaf expansion and auxin-induced lateral root formation. Plant J 43: 118-130. (Pubitemid 40962740)
19. Ellis CM, Nagpal P, Young JC, Hagen G, Guilfoyle TJ, et al. (2005) AUXIN RESPONSE FACTOR1 and AUXIN RESPONSE FACTOR2 regulate senescence and floral organ abscission in Arabidopsis thaliana. Development 132: 4563-4574. (Pubitemid 41632234)
20. Marin E, Jouannet V, Herz A, Lokerse AS, Weijers D, et al. (2010) miR390, Arabidopsis TAS3 tasiRNAs, and their AUXIN RESPONSE FACTOR targets define an autoregulatory network quantitatively regulating lateral root growth. Plant Cell 22: 1104-1117.
21. Yoon EK, Yang JH, Lee WS (2010) Auxin and Abscisic Acid Responses of Auxin Response Factor 3 in Arabidopsis Lateral Root Development. Journal of Plant Biology 53: 150-154.
22. Varaud E, Brioudes F, Szecsi J, Leroux J, Brown S, et al. (2011) AUXIN RESPONSE FACTOR8 regulates Arabidopsis petal growth by interacting with the bHLH transcription factor BIGPETALp. Plant Cell 23: 973-983.
23. Goetz M, Vivian-Smith A, Johnson SD, Koltunow AM (2006) AUXIN RESPONSE FACTOR8 is a negative regulator of fruit initiation in Arabidopsis. Plant Cell 18: 1873-1886. (Pubitemid 44260184)
24. Goetz M, Hooper LC, Johnson SD, Rodrigues JC, Vivian-Smith A, et al. (2007) Expression of aberrant forms of AUXIN RESPONSE FACTOR8 stimulates parthenocarpy in Arabidopsis and tomato. Plant Physiol 145: 351-366. (Pubitemid 47575133)
25. Guillon F, Philippe S, Bouchet B, Devaux MF, Frasse P, et al. (2008) Downregulation of an Auxin Response Factor in the tomato induces modification of fine pectin structure and tissue architecture. J Exp Bot 59: 273-288. (Pubitemid 351651371)
26. de Jong M, Wolters-Arts M, Feron R, Mariani C, Vriezen WH (2009) The Solanum lycopersicum auxin response factor 7 (SlARF7) regulates auxin signaling during tomato fruit set and development. Plant J 57: 160-170.
27. Li H, Johnson P, Stepanova A, Alonso JM, Ecker JR (2004) Convergence of signaling pathways in the control of differential cell growth in Arabidopsis. Dev Cell 7: 193-204. (Pubitemid 39149159)
28. Jain M, Khurana JP (2009) Transcript profiling reveals diverse roles of auxin-responsive genes during reproductive development and abiotic stress in rice. Febs Journal 276: 3148-3162.
29. de Jong M, Wolters-Arts M, Garcia-Martinez JL, Mariani C, Vriezen WH (2011) The Solanum lycopersicum AUXIN RESPONSE FACTOR 7 (SlARF7) mediates cross-talk between auxin and gibberellin signalling during tomato fruit set and development. J Exp Bot 62: 617-626.
30. Li J, Dai X, Zhao Y (2006) A role for auxin response factor 19 in auxin and ethylene signaling in Arabidopsis. Plant Physiol 140: 899-908. (Pubitemid 43956244)
31. Liu ZH, Yu YC, Xiang FN (2011) [Auxin response factors and plant growth and development]. Yi Chuan 33: 1335-1346.
32. Vert G, Walcher CL, Chory J, Nemhauser JL (2008) Integration of auxin and brassinosteroid pathways by Auxin Response Factor 2. Proc Natl Acad Sci U S A 105: 9829-9834. (Pubitemid 352031385)
33. Guilfoyle TJ, Hagen G (2007) Auxin response factors. Curr Opin Plant Biol 10: 453-460. (Pubitemid 47505406)
34. Guilfoyle TJ, Hagen G (2001) Auxin response factors. Journal of Plant Growth Regulation 20: 281-291. (Pubitemid 34088623)
35. Ulmasov T, Hagen G, Guilfoyle TJ (1999) Activation and repression of transcription by auxin-response factors. Proceedings of the National Academy of Sciences of the United States of America 96: 5844-5849. (Pubitemid 29234706)
36. Nagpal P, Ellis CM, Weber H, Ploense SE, Barkawi LS, et al. (2005) Auxin response factors ARF6 and ARF8 promote jasmonic acid production and flower maturation. Development 132: 4107-4118. (Pubitemid 41488860)
37. Jones B, Frasse P, Olmos E, Zegzouti H, Li ZG, et al. (2002) Down-regulation of DR12, an auxin-response-factor homolog, in the tomato results in a pleiotropic phenotype including dark green and blotchy ripening fruit. Plant Journal 32: 603-613. (Pubitemid 36814966)
38. Wang DK, Pei KM, Fu YP, Sun ZX, Li SJ, et al. (2007) Genome-wide analysis of the auxin response factors (ARF) gene family in rice (Oryza sativa). Gene 394: 13-24.
39. Kalluri UC, Difazio SP, Brunner AM, Tuskan GA (2007) Genome-wide analysis of Aux/IAA and ARF gene families in Populus trichocarpa. BMC Plant Biol 7: 59.
40. Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, et al. (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457: 551-556.
41. Xing H, Pudake RN, Guo G, Xing G, Hu Z, et al. (2011) Genome-wide identification and expression profiling of auxin response factor (ARF) gene family in maize. BMC Genomics 12: 178.
42. Kumar R, Tyagi AK, Sharma AK (2011) Genome-wide analysis of auxin response factor (ARF) gene family from tomato and analysis of their role in flower and fruit development. Molecular Genetics and Genomics 285: 245-260.
43. Wu J, Wang F, Cheng L, Kong F, Peng Z, et al. (2011) Identification, isolation and expression analysis of auxin response factor (ARF) genes in Solanum lycopersicum. Plant Cell Reports 30: 2059-2073.
44. Ottenschlager I, Wolff P, Wolverton C, Bhalerao RP, Sandberg G, et al. (2003) Gravity-regulated differential auxin transport from columella to lateral root cap cells. Proc Natl Acad Sci U S A 100: 2987-2991. (Pubitemid 36297610)
45. Maza E, Frasse P, Senin P, Bouzayen M, Zouine M (2013) Comparison of normalization methods for differential gene expression analysis in RNA-Seq experiments: A matter of relative size of studied transcriptomes. Communicative & Integrative Biology 6.
46. (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485: 635-641.
47. Serrani JC, Ruiz-Rivero O, Fos M, Garcia-Martinez JL (2008) Auxin-induced fruit-set in tomato is mediated in part by gibberellins. Plant Journal 56: 922-934.
48. de Jong M, Mariani C, Vriezen WH (2009) The role of auxin and gibberellin in tomato fruit set. Journal of Experimental Botany 60: 1523-1532.
49. Wang H, Jones B, Li Z, Frasse P, Delalande C, et al. (2005) The tomato Aux/IAA transcription factor IAA9 is involved in fruit development and leaf morphogenesis. Plant Cell 17: 2676-2692.
50. Devoghalaere F, Doucen T, Guitton B, Keeling J, Payne W, et al. (2012) A genomics approach to understanding the role of auxin in apple (Malus x domestica) fruit size control. BMC Plant Biol 12: 7.
51. Wang JW, Wang LJ, Mao YB, Cai WJ, Xue HW, et al. (2005) Control of root cap formation by MicroRNA-targeted auxin response factors in Arabidopsis. Plant Cell 17: 2204-2216.
52. Williams L, Carles CC, Osmont KS, Fletcher JC (2005) A database analysis method identifies an endogenous trans-acting short-interfering RNA that targets the Arabidopsis ARF2, ARF3, and ARF4 genes. Proc Natl Acad Sci U S A 102: 9703-9708. (Pubitemid 40981744)
53. Wu MF, Tian Q, Reed JW (2006) Arabidopsis microRNA167 controls patterns of ARF6 and ARF8 expression, and regulates both female and male reproduction. Development 133: 4211-4218. (Pubitemid 44830665)
54. Zhou F, Roy B, von Arnim AG (2010) Translation reinitiation and development are compromised in similar ways by mutations in translation initiation factor eIF3h and the ribosomal protein RPL24. BMC Plant Biol 10: 193.
55. Rosado A, Li R, van de Ven W, Hsu E, Raikhel NV (2012) Arabidopsis ribosomal proteins control developmental programs through translational regulation of auxin response factors. Proc Natl Acad Sci U S A 109: 19537-19544.
56. Abel S, Theologis A (1994) Transient transformation of Arabidopsis leaf protoplasts: a versatile experimental system to study gene expression. Plant J 5: 421-427.
57. Hamilton AJ, Lycett GW, Grierson D (1990) Antisense Gene That Inhibits Synthesis of the Hormone Ethylene in Transgenic Plants. Nature 346: 284-287. (Pubitemid 120005886)