A genomics approach to understanding the role of auxin in apple (Malus x domestica) fruit size control

BMC Plant Biology

Volumn 12, Issue , 2012, Pages

  Devoghalaere, Fanny ^a   Doucen, Thomas ^b   Guitton, Baptiste ^c,f   Keeling, Jeannette ^b   Payne, Wendy ^b   Ling, Toby J ^d   Ross, John J ^d   Hallett, Ian C ^a   Gunaseelan, Kularajathevan ^a   Dayatilake, GA ^e   Diak, Robert ^c   Breen, Ken C ^e   Tustin, D Stuart ^e   Costes, Evelyne ^f   Chagné, David ^c   Schaffer, Robert J ^a,b   David, Karine M ^b  

^a THE NEW ZEALAND INSTITUTE FOR PLANT AND FOOD RESEARCH LIMITED   (New Zealand)

^b UNIVERSITY OF AUCKLAND   (New Zealand)

^c PFR   (New Zealand)

^d UNIVERSITY OF TASMANIA   (Australia)

^e PFR   (New Zealand)

^f UMR AGAP   (France)

Author keywords

[No Author keywords available]

Indexed keywords

MALUS X DOMESTICA;

INDOLEACETIC ACID DERIVATIVE; VEGETABLE PROTEIN;

ARTICLE; CHROMOSOME MAP; FRUIT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GENOMICS; GROWTH, DEVELOPMENT AND AGING; MALUS; METABOLISM; PLANT GENOME; QUANTITATIVE TRAIT LOCUS;

CHROMOSOME MAPPING; FRUIT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENOME, PLANT; GENOMICS; INDOLEACETIC ACIDS; MALUS; PLANT PROTEINS; QUANTITATIVE TRAIT LOCI;

EID: 84855737923     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/1471-2229-12-7     Document Type: Article

References (70)

1. Given NK, Venis MA, Gierson D. Hormonal regulation of ripening in the strawberry, a non-climacteric fruit. Planta 1988, 174(3):402-406.
2. Nitsch JP. Growth and morphogenesis of the strawberry as related to auxin. Am J Bot 1950, 37:211-215.
3. Gorguet B, Van Heusden AW, Lindhout P. Parthenocarpic fruit development in tomato. Plant Biol 2005, 7(2):131-139. 10.1055/s-2005-837494, 15822008.
4. Agusti M, Almela V, Andreu I, Juan M, Zacarias L. Synthetic auxin 3,5,6-TPA promotes fruit development and climacteric in Prunus persica L. Batsch. J Hortic Sci Biotechnol 1999, 74(5):556-560.
5. Stern RA, Flaishman M, Applebaum S, Ben-Arie R. Effect of synthetic auxins on fruit development of 'Bing' cherry (Prunus avium L.). Sci Hortic (Amsterdam) 2007, 114(4):275-280.
6. Perrot-Rechenmann C, Napier RM. Auxins. Vitam Horm 2005, 72:203-233.
7. Woodward AW, Bartel B. Auxin: regulation, action, and interaction. Ann Bot 2005, 95(5):707-735. 10.1093/aob/mci083, 15749753.
8. Zhao Y. Auxin biosynthesis and its role in plant development. Annu Rev Plant Biol 2010, 61:49-64. 10.1146/annurev-arplant-042809-112308, 3070418, 20192736.
9. Staswick PE, Tiryaki I, Rowe ML. Jasmonate response locus JAR1 and several related Arabidopsis genes encode enzymes of the firefly luciferase superfamily that show activity on jasmonic, salicylic, and indole-3-acetic acids in an assay for adenylation. Plant Cell 2002, 14(6):1405-1415. 10.1105/tpc.000885, 150788, 12084835.
10. Bottcher C, Keyzers RA, Boss PK, Davies C. Sequestration of auxin by the indole-3-acetic acid-amido synthetase GH3-1 in grape berry (Vitis vinifera L.) and the proposed role of auxin conjugation during ripening. J Exp Bot 2010, 61(13):3615-3625. 10.1093/jxb/erq174, 20581124.
11. Ludwig-Müller J. Auxin conjugates: Their role for plant development and in the evolution of land plants. J Exp Bot 2011, 62(6):1757-1773. 10.1093/jxb/erq412, 21307383.
12. Zazímalová E, Murphy AS, Yang H, Hoyerová K, Hosek P. Auxin transporters--why so many?. Cold Spring Harbor perspectives in biology 2010, 2(3):a001552. 10.1101/cshperspect.a001552, 2829953, 20300209.
13. Gälweiler L, Guan C, Müller A, Wisman E, Mendgen K, Yephremov A, Palme K. Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 1998, 282(5397):2226-2230.
14. Nishio S, Moriguchi R, Ikeda H, Takahashi H, Fujii N, Guilfoyle TJ, Kanahama K, Kanayama Y. Expression analysis of the auxin efflux carrier family in tomato fruit development. Planta 2010, 232(3):755-764. 10.1007/s00425-010-1211-0, 20571824.
15. Abel S, Theologis A. Odyssey of auxin. Cold Spring Harb Perspect Biol 2010, 2(10):a004572. 10.1101/cshperspect.a004572, 20739413.
16. Chapman EJ, Estelle M. Mechanism of auxin-regulated gene expression in plants. Annu Rev Genet 2009, 43:265-285. 10.1146/annurev-genet-102108-134148, 19686081.
17. Shishova M, Lindberg S. A new perspective on auxin perception. J Plant Physiol 2010, 167(6):417-422. 10.1016/j.jplph.2009.12.014, 20176409.
18. Tromas A, Paponov I, Perrot-Rechenmann C. Auxin binding protein 1: functional and evolutionary aspects. Trends Plant Sci 2010, 15(8):436-446. 10.1016/j.tplants.2010.05.001, 20605513.
19. Parry G, Estelle M. Auxin receptors: A new role for F-box proteins. Curr Opin Cell Biol 2006, 18(2):152-156. 10.1016/j.ceb.2006.02.001, 16488128.
20. Leblanc N, David K, Grosclaude J, Pradier JM, Barbier-Brygoo H, Labiau S, Perrot-Rechenmann C. A novel immunological approach establishes that the auxin-binding protein, Nt-abp1, is an element involved in auxin signaling at the plasma membrane. J Biol Chem 1999, 274(40):28314-28320. 10.1074/jbc.274.40.28314, 10497189.
21. Tromas A, Braun N, Muller P, Khodus T, Paponov IA, Palme K, Ljung K, Lee JY, Benfey P, Murray JA, et al. The AUXIN BINDING PROTEIN 1 is required for differential auxin responses mediating root growth. PLoS One 2009, 4(9):e6648. 10.1371/journal.pone.0006648, 2744284, 19777056.
22. David KM, Couch D, Braun N, Brown S, Grosclaude J, Perrot-Rechenmann C. The auxin-binding protein 1 is essential for the control of cell cycle. Plant J 2007, 50(2):197-206. 10.1111/j.1365-313X.2007.03038.x, 17376160.
23. Chen JG, Ullah H, Young JC, Sussman MR, Jones AM. ABP1 is required for organized cell elongation and division in Arabidopsis embryogenesis. Genes Dev 2001, 15(7):902-911. 10.1101/gad.866201, 312669, 11297513.
24. Balbi V, Lomax TL. Regulation of early tomato fruit development by the diageotropica gene. Plant Physiol 2003, 131(1):186-197. 10.1104/pp.010132, 166799, 12529527.
25. Christian M, Steffens B, Schenck D, Lüthen H. The diageotropica mutation of tomato disrupts a signalling chain using extracellular auxin binding protein 1 as a receptor. Planta 2003, 218(2):309-314. 10.1007/s00425-003-1090-8, 12928901.
26. de Jong M, Wolters-Arts M, Feron R, Mariani C, Vriezen WH. The Solanum lycopersicum auxin response factor 7 (SlARF7) regulates auxin signaling during tomato fruit set and development. Plant J 2009, 57(1):160-170. 10.1111/j.1365-313X.2008.03671.x, 18778404.
27. Wang H, Jones B, Li Z, Frasse P, Delalande C, Regad F, Chaabouni S, Latche A, Pech JC, Bouzayen M. The tomato Aux/IAA transcription factor IAA9 is involved in fruit development and leaf morphogenesis. Plant Cell 2005, 17(10):2676-2692. 10.1105/tpc.105.033415, 1242265, 16126837.
28. Guillon F, Philippe S, Bouchet B, Devaux MF, Frasse P, Jones B, Bouzayen M, Lahaye M. Down-regulation of an Auxin Response Factor in the tomato induces modification of fine pectin structure and tissue architecture. J Exp Bot 2008, 59(2):273-288. 10.1093/jxb/erm323, 18267945.
29. Jones B, Frasse P, Olmos E, Zegzouti H, Li ZG, Latche A, Pech JC, Bouzayen M. 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 J 2002, 32(4):603-613. 10.1046/j.1365-313X.2002.01450.x, 12445130.
30. Janssen BJ, Thodey K, Schaffer RJ, Alba R, Balakrishnan L, Bishop R, Bowen JH, Crowhurst RN, Gleave AP, Ledger S, et al. Global gene expression analysis of apple fruit development from the floral bud to ripe fruit. BMC Plant Biol 2008, 8:16. 10.1186/1471-2229-8-16, 2287172, 18279528.
31. Mousdale DMA, Knee M. Indolyl-3-acetic acid and ethylene levels in ripening apple fruits. J Exp Bot 1981, 32(4):753-758.
32. Treharne KJ, Quinlan JD, Knight JN, Ward DA. Hormonal regulation of fruit development in apple: 'A mini-review'. Plant Growth Regul 1985, 3(2):125-132.
33. Newcomb RD, Crowhurst RN, Gleave AP, Rikkerink EH, Allan AC, Beuning LL, Bowen JH, Gera E, Jamieson KR, Janssen BJ, et al. Analyses of expressed sequence tags from apple. Plant Physiol 2006, 141(1):147-166. 10.1104/pp.105.076208, 1459330, 16531485.
34. Schaffer RJ, Friel EN, Souleyre EJ, Bolitho K, Thodey K, Ledger S, Bowen JH, Ma JH, Nain B, Cohen D, et al. A genomics approach reveals that aroma production in apple is controlled by ethylene predominantly at the final step in each biosynthetic pathway. Plant Physiol 2007, 144(4):1899-1912. 10.1104/pp.106.093765, 1949883, 17556515.
35. Johnston JW, Gunaseelan K, Pidakala P, Wang M, Schaffer RJ. Co-ordination of early and late ripening events in apples is regulated through differential sensitivities to ethylene. J Exp Bot 2009, 60(9):2689-2699. 10.1093/jxb/erp122, 2692014, 19429839.
36. Espley RV, Hellens RP, Putterill J, Stevenson DE, Kutty-Amma S, Allan AC. Red colouration in apple fruit is due to the activity of the MYB transcription factor, MdMYB10. Plant J 2007, 49(3):414-427. 10.1111/j.1365-313X.2006.02964.x, 1865000, 17181777.
37. Atkinson RG, Schroder R, Hallett IC, Cohen D, MacRae EA. Overexpression of polygalacturonase in transgenic apple trees leads to a range of novel phenotypes involving changes in cell adhesion. Plant Physiol 2002, 129(1):122-133. 10.1104/pp.010986, 155877, 12011344.
38. Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A, Kalyanaraman A, Fontana P, Bhatnagar SK, Troggio M, Pruss D, et al. The genome of the domesticated apple (Malus × domestica Borkh.). Nat Genet 2010, 42(10):833-839. 10.1038/ng.654, 20802477.
39. Gustafson FG. Auxin distribution in fruits and its significance in fruit development. Am J Bot 1939, 26:189-194.
40. Shulaev V, Sargent DJ, Crowhurst RN, Mockler TC, Folkerts O, Delcher AL, Jaiswal P, Mockaitis K, Liston A, Mane SP, et al. The genome of woodland strawberry (Fragaria vesca). Nat Genet 2011, 43(2):109-116. 10.1038/ng.740, 21186353.
41. Remington DL, Vision TJ, Guilfoyle TJ, Reed JW. Contrasting modes of diversification in the Aux/IAA and ARF gene families. Plant Physiol 2004, 135(3):1738-1752. 10.1104/pp.104.039669, 519086, 15247399.
42. Kalluri UC, Difazio SP, Brunner AM, Tuskan GA. Genome-wide analysis of Aux/IAA and ARF gene families in Populus trichocarpa. BMC Plant Biol 2007, 7:59. 10.1186/1471-2229-7-59, 2174922, 17986329.
43. Wang Y, Deng D, Bian Y, Lv Y, Xie Q. Genome-wide analysis of primary auxin-responsive Aux/IAA gene family in maize (Zea mays. L.). Mol Biol Rep 2010, 37(8):3991-4001. 10.1007/s11033-010-0058-6, 20232157.
44. Xing H, Pudake RN, Guo G, Xing G, Hu Z, Zhang Y, Sun Q, Ni Z. Genome-wide identification and expression profiling of auxin response factor (ARF) gene family in maize. BMC Genomics 2011, 12:178. 10.1186/1471-2164-12-178, 3082248, 21473768.
45. Kumar R, Tyagi AK, Sharma AK. Genome-wide analysis of auxin response factor (ARF) gene family from tomato and analysis of their role in flower and fruit development. Mol Genet Genomics 2011, 285(3):245-260. 10.1007/s00438-011-0602-7, 21290147.
46. Srivastava A, Handa AK. Hormonal regulation of tomato fruit development: A molecular perspective. J Plant Growth Regul 2005, 24(2):67-82.
47. Liebhard R, Kellerhals M, Pfammatter W, Jertmini M, Gessler C. Mapping quantitative physiological traits in apple (Malus × domestica Borkh.). Plant Mol Biol 2003, 52(3):511-526. 10.1023/A:1024886500979, 12956523.
48. Bertin N, Causse M, Brunel B, Tricon D, Génard M. Identification of growth processes involved in QTLs for tomato fruit size and composition. J Exp Bot 2009, 60(1):237-248. 3071768, 19033553.
49. Grandillo S, Ku HM, Tanksley SD. Identifying the loci responsible for natural variation in fruit size and shape in tomato. Theor Appl Genet 1999, 99(6):978-987.
50. Harada T, Kurahashi W, Yanai M, Wakasa Y, Satoh T. Involvement of cell proliferation and cell enlargement in increasing the fruit size of Malus species. Sci Hortic 2005, 105(4):447-456.
51. McAtee PA, Hallett IC, Johnston JW, Schaffer RJ. A rapid method of fruit cell isolation for cell size and shape measurements. Plant Methods 2009, 5(1):5. 10.1186/1746-4811-5-5, 2685799, 19402911.
52. Malladi A, Hirst PM. Increase in fruit size of a spontaneous mutant of 'Gala' apple (Malus × domestica Borkh.) is facilitated by altered cell production and enhanced cell size. J Exp Bot 2010, 61(11):3003-3013. 10.1093/jxb/erq134, 2892151, 20484321.
53. Mallory AC, Bartel DP, Bartel B. MicroRNA-directed regulation of Arabidopsis Auxin Response Factor17 is essential for proper development and modulates expression of early auxin response genes. Plant Cell 2005, 17(5):1360-1375. 10.1105/tpc.105.031716, 1091760, 15829600.
54. Trewavas AJ, Cleland RE. Is plant development regulated by changes in the concentration of growth substances or by changes in the sensitivity to growth substances?. Trends Biochem Sci 1983, 8(10):354-357.
55. Stern RA, Ben-Arie R. Pre-harvest drop control of 'Red Delicious' and 'Jonathan' apple (Malus domestica) as affected by the synthetic auxin 3,5,6-TPA. J Hortic Sci Biotech 2006, 81(6):943-948.
56. Percy AE, Jameson PE, Melton LD. Expansion during early apple fruit development induced by auxin and N-(2-chloro-4-pyridyl)-N'-phenylurea: effect on cell wall hemicellulose. Plant Growth Regul 1998, 26(1):1-6.
57. Goetz M, Vivian-Smith A, Johnson SD, Koltunow AM. AUXIN RESPONSE FACTOR8 is a negative regulator of fruit initiation in Arabidopsis. Plant Cell 2006, 18(8):1873-1886. 10.1105/tpc.105.037192, 1533983, 16829592.
58. Goetz M, Hooper LC, Johnson SD, Rodrigues JC, Vivian-Smith A, Koltunow AM. Expression of aberrant forms of AUXIN RESPONSE FACTOR8 stimulates parthenocarpy in Arabidopsis and tomato. Plant Physiol 2007, 145(2):351-366. 10.1104/pp.107.104174, 2048734, 17766399.
59. Zhang J, Chen R, Xiao J, Qian C, Wang T, Li H, Ouyang B, Ye Z. A single-base deletion mutation in SlIAA9 gene causes tomato (Solanum lycopersicum) entire mutant. J Plant Res 2007, 120(6):671-678. 10.1007/s10265-007-0109-9, 17955175.
60. Liu K, Kang BC, Jiang H, Moore SL, Li H, Watkins CB, Setter TL, Jahn MM. A GH3-like gene, CcGH3, isolated from Capsicum chinense L. fruit is regulated by auxin and ethylene. Plant Mol Biol 2005, 58(4):447-464. 10.1007/s11103-005-6505-4, 16021332.
61. Trainotti L, Tadiello A, Casadoro G. The involvement of auxin in the ripening of climacteric fruits comes of age: the hormone plays a role of its own and has an intense interplay with ethylene in ripening peaches. J Exp Bot 2007, 58(12):3299-3308. 10.1093/jxb/erm178, 17925301.
62. Chaabouni S, Jones B, Delalande C, Wang H, Li Z, Mila I, Frasse P, Latche A, Pech JC, Bouzayen M. Sl-IAA3, a tomato Aux/IAA at the crossroads of auxin and ethylene signalling involved in differential growth. J Exp Bot 2009, 60(4):1349-1362. 10.1093/jxb/erp009, 2657550, 19213814.
63. Tacken E, Ireland H, Gunaseelan K, Karunairetnam S, Wang D, Schultz K, Bowen J, Atkinson RG, Johnston JW, Putterill J, et al. The role of ethylene and cold temperature in the regulation of the apple POLYGALACTURONASE1 gene and fruit softening. Plant Physiol 2010, 153(1):294-305. 10.1104/pp.109.151092, 2862417, 20237022.
64. Günl M, Liew EF, David K, Putterill J. Analysis of a post-translational steroid induction system for GIGANTEA in Arabidopsis. BMC Plant Biology 2009, 9:141. 10.1186/1471-2229-9-141, 2789081, 19943973.
65. R development Core team R: A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna: R Foundation for Statistical Computing 2009, R development Core team.
66. Segura V, Denancé C, Durel CE, Costes E. Wide range QTL analysis for complex architectural traits in a 1-year-old apple progeny. Genome 2007, 50(2):159-171. 10.1139/G07-002, 17546081.
67. Guitton B, Kelner JJ, Velasco R, Gardiner SE, Chagné D, Costes E. Genetic control of biennial bearing in apple. J Exp Bot 2012, 63(1):131-149. 10.1093/jxb/err261, 3245460, 21963613.
68. van Oojen J, Voorips R. JoinMap 3.0, Software for the calculation of genetic linkage maps. Plant Research International 2001, Wageningen: The Netherlands.
69. Liew M, Pryor R, Palais R, Meadows C, Erali M, Lyon E, Wittwer C. Genotyping of single-nucleotide polymorphisms by high-resolution melting of small amplicons. Clin Chem 2004, 50(7):1156-1164. 10.1373/clinchem.2004.032136, 15229148.
70. Chagne D, Gasic K, Crowhurst RN, Han Y, Bassett HC, Bowatte DR, Lawrence TJ, Rikkerink EH, Gardiner SE, Korban SS. Development of a set of SNP markers present in expressed genes of the apple. Genomics 2008, 92(5):353-358. 10.1016/j.ygeno.2008.07.008, 18721872.