Role of the FUL-SHP network in the evolution of fruit morphology and function

Journal of Experimental Botany

Volumn 65, Issue 16, 2014, Pages 4505-4513

  Ferrándiz, Cristina ^a   Fourquin, Chloé ^a  

^a Ciudad Politécnica de la Innovación   (Spain)

Author keywords

Fruit dehiscence; fruit evolution; fruit morphology; FRUITFULL; MADS box; SHATTERPROOF

Indexed keywords

ARABIDOPSIS PROTEIN;

ANATOMY AND HISTOLOGY; ARABIDOPSIS; EVOLUTION; FRUIT; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYLOGENY; PHYSIOLOGY; SEED DISPERSAL;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BIOLOGICAL EVOLUTION; FRUIT; PHYLOGENY; SEED DISPERSAL;

EID: 84903700783     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/ert479     Document Type: Review

References (76)

1. Airoldi CA, Bergonzi S, Davies B. 2010. Single amino acid change alters the ability to specify male or female organ identity. Proceedings of the National Academy of Sciences, USA 107, 18898-18902.
2. Alvarez-Buylla ER, Pelaz S, Liljegren SJ, Gold SE, Burgeff C, Ditta GS, Ribas de Pouplana L, Martínez-Castilla L, Yanofsky MF. 2000. An ancestral MADS-box gene duplication occurred before the divergence of plants and animals. Proceedings of the National Academy of Sciences, USA 97, 5328-5333.
3. Arnaud N, Lawrenson T, Ostergaard L, Sablowski R. 2011. The Same Regulatory Point Mutation Changed Seed-Dispersal Structures in Evolution and Domestication. Current Biology 21, 1215-1219.
4. Avino M, Kramer EM, Donohue K, Hammel AJ, Hall JC. 2012. Understanding the basis of a novel fruit type in Brassicaceae: Conservation and deviation in expression patterns of six genes. EvoDevo 3, 20.
5. Balanzá V, Navarrete M, Trigueros M, Ferrándiz C. 2006. Patterning the female side of Arabidopsis: The importance of hormones. Journal of Experimental Botany 57, 3457-3469.
6. Becker A, Theissen G. 2003. The major clades of MADS-box genes and their role in the development and evolution of flowering plants. Molecular Phylogenetics and Evolution 29, 464-489.
7. Bemer M, Karlova R, Ballester AR, Tikunov YM, Bovy AG, Wolters-Arts M, Rossetto Pde B, Angenent GC, de Maagd RA. 2012. The tomato FRUITFULL homologs TDR4/FUL1 and MBP7/FUL2 regulate ethylene-independent aspects of fruit ripening. Plant Cell 24, 4437-4451.
8. Benlloch R, d'Erfurth I, Ferrandiz C, Cosson V, Beltrán JP, Cañas LA, Kondorosi A, Madueño F, Ratet P. 2006. Isolation of mtpim proves Tnt1 a useful reverse genetics tool in Medicago truncatula and uncovers new aspects of AP1-like functions in legumes. Plant Physiology 142, 972-983.
9. Berbel A, Ferrandiz C, Hecht V, Dalmais M, Lund OS, Sussmilch FC, Taylor SA, Bendahmane A, Ellis TH, Beltran JP, Weller JL, Madueno F. 2012. VEGETATIVE1 is essential for development of the compound inflorescence in pea. Nature Communications 3, 797.
10. Berbel A, Navarro C, Ferrandiz C, Canas LA, Madueno F, Beltran JP. 2001. Analysis of PEAM4, the pea AP1 functional homologue, supports a model for AP1-like genes controlling both floral meristem and floral organ identity in different plant species. The Plant Journal 25, 441-451.
11. Bowman JL, Alvarez J, Weigel D, Meyerowitz EM, Smyth DR. 1993. Control of flower development in Arabidopsis thaliana by APETALA1 and interacting genes. Development 119, 721-743.
12. Bowman JL, Smyth DR. 1999. CRABS CLAW, a gene that regulates carpel and nectary development in Arabidopsis, encodes a novel protein with zinc finger and helix-loop-helix domains. Development 126, 2387-2396.
13. Bowman JL, Smyth DR, Meyerowitz EM. 1991. Genetic interactions among floral homeotic genes of Arabidopsis. Development 112, 1-20.
14. Bradley D, Carpenter R, Sommer H, Hartley N, Coen E. 1993. Complementary floral homeotic phenotypes result from opposite orientations of a transposon at the plena locus of Antirrhinum. Cell 72, 85-95.
15. Causier B, Castillo R, Zhou J, Ingram R, Xue Y, Schwarz-Sommer Z, Davies B. 2005. Evolution in action: Following function in duplicated floral homeotic genes. Current Biology 15, 1508-1512.
16. Cevik V, Ryder C, Popovich A, Manning K, King GJ, Seymour GB. 2010. A FRUITFULL-like gene is associated with genetic variation for fruit flesh firmness in apple (Malus domestica Borkh.). Tree Genetics & Genomes 6, 271-279.
17. Daminato M, Guzzo F, Casadoro G. 2013. A SHATTERPROOF-like gene controls ripening in non-climacteric strawberries, and auxin and abscisic acid antagonistically affect its expression. Journal of Experimental Botany 64, 3775-3786.
18. Dardick CD, Callahan AM, Chiozzotto R, Schaffer RJ, Piagnani MC, Scorza R. 2010. Stone formation in peach fruit exhibits spatial coordination of the lignin and flavonoid pathways and similarity to Arabidopsis dehiscence. BMC Biology 8, 13.
19. Davies B, Motte P, Keck E, Saedler H, Sommer H, Schwarz-Sommer Z. 1999. PLENA and FARINELLI: Redundancy and regulatory interactions between two Antirrhinum MADS-box factors controlling flower development. EMBO Journal 18, 4023-4034.
20. Dinneny JR, Yanofsky MF. 2005. Drawing lines and borders: How the dehiscent fruit of Arabidopsis is patterned. Bioessays 27, 42-49.
21. Ferrándiz C, Gu Q, Martienssen R, Yanofsky MF. 2000a. Redundant regulation of meristem identity and plant architecture by FRUITFULL, APETALA1 and CAULIFLOWER. Development 127, 725-734.
22. Ferrándiz C, Liljegren SJ, Yanofsky MF. 2000b. Negative regulation of the SHATTERPROOF genes by FRUITFULL during Arabidopsis fruit development. Science 289, 436-438.
23. Fourquin C, del Cerro C, Victoria FC, Vialette-Guiraud A, de Oliveira AC, Ferrandiz C. 2013. A change in SHATTERPROOF protein lies at the origin of a fruit morphological novelty and a new strategy for seed dispersal in medicago genus. Plant Physiology 162, 907-917.
24. Fourquin C, Ferrandiz C. 2012. Functional analyses of AGAMOUS family members in Nicotiana benthamiana clarify the evolution of early and late roles of C-function genes in eudicots. The Plant Journal 71, 990-1001.
25. Gimenez E, Pineda B, Capel J, Anton MT, Atares A, Perez-Martin F, Garcia-Sogo B, Angosto T, Moreno V, Lozano R. 2010. Functional analysis of the Arlequin mutant corroborates the essential role of the Arlequin/TAGL1 gene during reproductive development of tomato. PLoS One 5, e14427.
26. Girin T, Stephenson P, Goldsack CMP, Kempin SA, Perez A, Pires N, Sparrow PA, Wood TA, Yanofsky MF, Østergaard L. 2010. Brassicaceae INDEHISCENT genes specify valve margin cell fate and repress replum formation. The Plant Journal 63, 329-338.
27. Groszmann M, Paicu T, Alvarez JP, Swain SM, Smyth DR. 2011. SPATULA and ALCATRAZ, are partially redundant, functionally diverging bHLH genes required for Arabidopsis gynoecium and fruit development. The Plant Journal 68, 816-829.
28. Gu Q, Ferrandiz C, Yanofsky MF, Martienssen R. 1998. The FRUITFULL MADS-box gene mediates cell differentiation during Arabidopsis fruit development. Development 125, 1509-1517.
29. Hands P, Vosnakis N, Betts D, Irish VF, Drea S. 2011. Alternate transcripts of a floral developmental regulator have both distinct and redundant functions in opium poppy. Annals of Botany 107, 1557-1566.
30. Heijmans K, Ament K, Rijpkema AS, Zethof J, Wolters-Arts M, Gerats T, Vandenbussche M. 2012. Redefining C and D in the petunia ABC. Plant Cell 24, 2305-2317.
31. Heisler M, Atkinson A, Bylstra Y, Walsh R, Smyth D. 2001. SPATULA, a gene that controls development of carpel margin tissues in Arabidopsis, encodes a bHLH protein. Development 128, 1089-1098.
32. Hileman LC, Drea S, Martino G, Litt A, Irish VF. 2005. Virus-induced gene silencing is an effective tool for assaying gene function in the basal eudicot species Papaver somniferum (opium poppy). The Plant Journal 44, 334-341.
33. Huijser P, Klein J, Lönnig WE, Meijer H, Saedler H, Sommer H. 1992. Bracteomania, an inflorescence anomaly, is caused by the loss of function of the MADS-box gene squamosa in Antirrhinum majus. EMBO Journal 11, 1239-1249.
34. Immink RG, Hannapel DJ, Ferrario S, Busscher M, Franken J, Lookeren Campagne MM, Angenent GC. 1999. A petunia MADS box gene involved in the transition from vegetative to reproductive development. Development 126, 5117-5126.
35. Irish VF, Litt A. 2005. Flower development and evolution: Gene duplication, diversification and redeployment. Current Opinion in Genetics & Development 15, 454-460.
36. Irish VF, Sussex IM. 1990. Function of the apetala-1 gene during Arabidopsis floral development. Plant Cell 2, 741-751.
37. Isemura T, Kaga A, Tabata S, Somta P, Srinives P, Shimizu T, Jo U, Vaughan DA, Tomooka N. 2012. Construction of a genetic linkage map and genetic analysis of domestication related traits in mungbean (Vigna radiata). PLoS One 7, e41304.
38. Itkin M, Seybold H, Breitel D, Rogachev I, Meir S, Aharoni A. 2009. The TOMATO AGAMOUS-LIKE 1 is a Component of the Fruit Ripening Regulatory Network. The Plant Journal 60, 1081-1095.
39. Jaakola L, Poole M, Jones MO, Kamarainen-Karppinen T, Koskimaki JJ, Hohtola A, Haggman H, Fraser PD, Manning K, King GJ, Thomson H, Seymour GB. 2010. A SQUAMOSA MADS box gene involved in the regulation of anthocyanin accumulation in bilberry fruits. Plant Physiology 153, 1619-1629.
40. Kay P, Groszmann M, Ross JJ, Parish RW, Swain SM. 2012. Modifications of a conserved regulatory network involving INDEHISCENT controls multiple aspects of reproductive tissue development in Arabidopsis. The New Phytologist 197, 73-87.
41. Konishi S, Izawa T, Lin SY, Ebana K, Fukuta Y, Sasaki T, Yano M. 2006. An SNP caused loss of seed shattering during rice domestication. Science 312, 1392-1396.
42. Kramer EM, Jaramillo MA, Di Stilio VS. 2004. Patterns of gene duplication and functional evolution during the diversification of the AGAMOUS subfamily of MADS box genes in angiosperms. Genetics 166, 1011-1023.
43. Lenser T, Theissen G. 2013. Conservation of fruit dehiscence pathways between Lepidium campestre and Arabidopsis thaliana sheds light on the regulation of INDEHISCENT. The Plant Journal 76, 545-556.
44. Liljegren SJ, Ditta GS, Eshed Y, Savidge B, Bowman JL, Yanofsky MF. 2000. SHATTERPROOF MADS-box genes control seed dispersal in Arabidopsis. Nature 404, 766-770.
45. Liljegren SJ, Roeder AHK, Kempin SA, Gremski K, Østergaard L, Guimil S, Reyes DK, Yanofsky MF. 2004. Control of fruit patterning in Arabidopsis by INDEHISCENT. Cell 116, 843-853.
46. Liu B, Fujita T, Yan Z, Sakamoto S, Xu D, Abe J. 2007. QTL Mapping of Domestication-related Traits in Soybean (Glycine max). Annals of Botany 100, 1027-1038.
47. Mandel MA, Yanofsky MF. 1995. The Arabidopsis AGL8 MADS box gene is expressed in inflorescence meristems and is negatively regulated by APETALA1. Plant Cell 7, 1763-1771.
48. Melzer S, Lens F, Gennen J, Vanneste S, Rohde A, Beeckman T. 2008. Flowering-time genes modulate meristem determinacy and growth form in Arabidopsis thaliana. Nature Genetics 40, 1489-1492.
49. Muhlhausen A, Lenser T, Mummenhoff K, Theissen G. 2013. Evidence that an evolutionary transition from dehiscent to indehiscent fruits in Lepidium (Brassicaceae) was caused by a change in the control of valve margin identity genes. The Plant Journal 73, 824-835.
50. Ostergaard L, Kempin SA, Bies D, Klee HJ, Yanofsky MF. 2006. Pod shatter-resistant Brassica fruit produced by ectopic expression of the FRUITFULL gene. Plant Biotechnology Journal 4, 45-51.
51. Ostergaard L. 2008. Don't 'leaf' now. The making of a fruit. Current Opinion in Plant Biology 12, 36-41.
52. Pabon-Mora N, Ambrose BA, Litt A. 2012. Poppy APETALA1/FRUITFULL orthologs control flowering time, branching, perianth identity, and fruit development. Plant Physiology 158, 1685-1704.
53. Pabon-Mora N, Hidalgo O, Gleissberg S, Litt A. 2013a. Assessing duplication and loss of APETALA1/FRUITFULL homologs in Ranunculales. Frontiers in Plant Science 4, 358.
54. Pabon-Mora N, Litt A. 2011. Comparative anatomical and developmental analysis of dry and fleshy fruits of Solanaceae. American Journal of Botany 98, 1415-1436.
55. Pabon-Mora N, Sharma B, Holappa LD, Kramer EM, Litt A. 2013b. The Aquilegia FRUITFULL-like genes play key roles in leaf morphogenesis and inflorescence development. The Plant Journal 74, 197-212.
56. Pan IL, McQuinn R, Giovannoni JJ, Irish VF. 2010. Functional diversification of AGAMOUS lineage genes in regulating tomato flower and fruit development. Journal of Experimental Botany 61, 1795-1806.
57. Pnueli L, Hareven D, Rounsley SD, Yanofsky MF, Lifschitz E. 1994. Isolation of the tomato AGAMOUS gene TAG1 and analysis of its homeotic role in transgenic plants. Plant Cell 6, 163-173.
58. Rajani S, Sundaresan V. 2001. The Arabidopsis myc/bHLH gene ALCATRAZ enables cell separation in fruit dehiscence. Current Biology 11, 1914-1922.
59. Roeder A, Yanofsky M. 2005. Fruit Development in Arabidopsis. The Arabidopsis Book. (ed. E. Meyerowitz and CR Somerville), Rockville, MD. doi/10.1199/tab.0074.
60. Roeder AH, Ferrandiz C, Yanofsky MF. 2003. The role of the REPLUMLESS homeodomain protein in patterning the Arabidopsis fruit. Current Biology 13, 1630-1635.
61. Sessions A, Nemhauser JL, McColl A, Roe JL, Feldmann KA, Zambryski PC. 1997. ETTIN patterns the Arabidopsis floral meristem and reproductive organs. Development 124, 4481-4491.
62. Seymour G, Poole M, Manning K, King GJ. 2008. Genetics and epigenetics of fruit development and ripening. Current Opinion in Plant Biology 11, 58-63.
63. Shan H, Zhang N, Liu C, Xu G, Zhang J, Chen Z, Kong H. 2007. Patterns of gene duplication and functional diversification during the evolution of the AP1/SQUA subfamily of plant MADS-box genes. Molecular Phylogenetics and Evolution 44, 26-41.
64. Shima Y, Kitagawa M, Fujisawa M, Nakano T, Kato H, Kimbara J, Kasumi T, Ito Y. 2013. Tomato FRUITFULL homologues act in fruit ripening via forming MADS-box transcription factor complexes with RIN. Plant Molecular Biology 82, 427-438.
65. Smykal P, Gennen J, De Bodt S, Ranganath V, Melzer S. 2007. Flowering of strict photoperiodic Nicotiana varieties in non-inductive conditions by transgenic approaches. Plant Molecular Biology 65, 233-242.
66. Soltis DE, Ma H, Frohlich MW, Soltis PS, Albert VA, Oppenheimer DG, Altman NS, dePamphilis C, Leebens-Mack J. 2007. The floral genome: An evolutionary history of gene duplication and shifting patterns of gene expression. Trends in Plant Science 12, 358-367.
67. Tadiello A, Pavanello A, Zanin D, Caporali E, Colombo L, Rotino GL, Trainotti L, Casadoro G. 2009. A PLENA-like gene of peach is involved in carpel formation and subsequent transformation into a fleshy fruit. Journal of Experimental Botany 60, 651-661.
68. Tani E, Polidoros AN, Tsaftaris AS. 2007. Characterization and expression analysis of FRUITFULL-and SHATTERPROOF-like genes from peach (Prunus persica) and their role in split-pit formation. Tree Physiology 27, 649-659.
69. Tani E, Tsaballa A, Stedel C, Kalloniati C, Papaefthimiou D, Polidoros A, Darzentas N, Ganopoulos I, Flemetakis E, Katinakis P, Tsaftaris A. 2011. The study of a SPATULA-like bHLH transcription factor expressed during peach (Prunus persica) fruit development. Plant Physiology Biochem 49, 654-663.
70. Theissen G, Becker A, Di Rosa A, Kanno A, Kim JT, Münster T, Winter KU, Saedler H. 2000. A short history of MADS-box genes in plants. Plant Molecular Biology 42, 115-149.
71. Vrebalov J, Pan IL, Arroyo AJM, McQuinn R, Chung M, Poole M, Rose J, Seymour G, Grandillo S, Giovannoni J, Irish VF. 2009. Fleshy fruit expansion and ripening are regulated by the Tomato SHATTERPROOF gene TAGL1. Plant Cell 21, 3041-3062.
72. Vrebalov J, Ruezinsky D, Padmanabhan V, White R, Medrano D, Drake R, Schuch W, Giovannoni J. 2002. A MADS-box gene necessary for fruit ripening at the tomato ripening-inhibitor (rin) locus. Science 296, 343-346.
73. Weeden NF, Brauner S, Przyborowski JA. 2002. Genetic analysis of pod dehiscence in pea (Pisum sativum L.). Cellular & Molecular Biology Letters 7, 657-663.
74. Wege S, Scholz A, Gleissberg S, Becker A. 2007. Highly Efficient Virus-induced Gene Silencing (VIGS) in California Poppy (Eschscholzia californica): An Evaluation of VIGS as a Strategy to Obtain Functional Data from Non-model Plants. Annals of Botany 100, 641-649.
75. Yanofsky MF, Ma H, Bowman JL, Drews GN, Feldmann KA, Meyerowitz EM. 1990. The protein encoded by the Arabidopsis homeotic gene agamous resembles transcription factors. Nature 346, 35-39.
76. Yellina AL, Orashakova S, Lange S, Erdmann R, Leebens-Mack J, Becker A. 2010. Floral homeotic C function genes repress specific B function genes in the carpel whorl of the basal eudicot California poppy (Eschscholzia californica). Evodevo 1, 13.