Tomato facultative parthenocarpy results from SlAGAMOUS-LIKE 6 loss of function

Plant Biotechnology Journal

Volumn 15, Issue 5, 2017, Pages 634-647

  Klap, Chen ^a   Yeshayahou, Ester ^a   Bolger, Anthony M ^b   Arazi, Tzahi ^a   Gupta, Suresh K ^a   Shabtai, Sara ^a   Usadel, Björn ^b,c   Salts, Yehiam ^a   Barg, Rivka ^a  

^a VOLCANI CENTER   (Israel)

^b RWTH AACHEN UNIVERSITY   (Germany)

^c FORSCHUNGSZENTRUM JÜLICH   (Germany)

Author keywords

CRISPR Cas9; fruit set; ovary arrest; SlAGL6; Solyc01g093960; tomato fruit size

Indexed keywords

PLANT PROTEIN;

CRISPR CAS SYSTEM; FRUIT; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HEAT SHOCK RESPONSE; METABOLISM; MUTATION; PHYSIOLOGY; PLANT SEED; TOMATO; TRANSGENIC PLANT;

CRISPR-CAS SYSTEMS; FRUIT; GENE EXPRESSION REGULATION, PLANT; HEAT-SHOCK RESPONSE; LYCOPERSICON ESCULENTUM; MUTATION; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; SEEDS;

EID: 85008441684     PISSN: 14677644     EISSN: 14677652     Source Type: Journal    
DOI: 10.1111/pbi.12662     Document Type: Article

References (77)

1. Ampomah-Dwamena, C., Morris, B.A., Sutherland, P., Veit, B. and Yao, J.-L. (2002) Down-regulation of TM29, a tomato SEPALLATA homolog, causes parthenocarpic fruit development and floral reversion. Plant Physiol. 130, 605–617.
2. Ariizumi, T., Shinozaki, Y. and Ezura, H. (2013) Genes that influence yield in tomato. Breed. Sci. 63, 3–13.
3. Barg, R., Pilowsky, M., Shabtai, S., Carmi, N., Szechtman, A.D., Dedicova, B. and Salts, Y. (1997) The TYLCV-tolerant tomato line MP-1 is characterized by superior transformation competence. J. Exp. Bot. 48, 1919–1923.
4. Bassel, G.W., Mullen, R.T. and Bewley, J.D. (2008) procera is a putative DELLA mutant in tomato (Solanum lycopersicum): effects on the seed and vegetative plant. J. Exp. Bot. 59, 585–593.
5. Beraldi, D., Picarella, M.E., Soressi, G.P. and Mazzucato, A. (2004) Fine mapping of the parthenocarpic fruit (pat) mutation in tomato. Theor. Appl. Genet. 108, 209–216.
6. Bohner, J. and Bangerth, F. (1988) Cell number, cell size and hormone levels in semi-isogenic mutants of Lycopersicon pimpinellifolium differing in fruit size. Physiologia Plant. 72, 316–320.
7. Bolger, A., Scossa, F., Bolger, M.E., Lanz, C., Maumus, F., Tohge, T., Quesneville, H. et al. (2014a) The genome of the stress-tolerant wild tomato species Solanum pennellii. Nat. Genet. 46, 1034–1038.
8. Bolger, A.M., Lohse, M. and Usadel, B. (2014b) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics, 30, 2114–2120.
9. Carmi, N., Salts, Y., Dedicova, B., Shabtai, S. and Barg, R. (2003) Induction of parthenocarpy in tomato via specific expression of the rolB gene in the ovary. Planta, 217, 726–735.
10. Carrera, E., Ruiz-Rivero, O., Peres, L/E., Atares, A. and Garcia-Martinez, J.L. (2012) Characterization of the procera tomato mutant shows novel functions of the SlDELLA protein in the control of flower morphology, cell division and expansion, and the auxin-signaling pathway during fruit-set and development. Plant Physiol. 160, 1581–1596.
11. Casas Diaz, A.V., Hewitt, J.D. and Lapushner, D. (1987) Effects of parthenocarpy on fruit quality in tomato. J. Am. Soc. Hort. Sci. 112, 634–637.
12. Chandrasekaran, J., Brumin, M., Wolf, D., Leibman, D., Klap, C., Pearlsman, M., Sherman, A. et al. (2016) Development of broad virus resistance in non-transgenic cucumber using CRISPR/Cas9 technology. Mol. Plant Pathol. 17, 1140–1153.
13. Chevalier, C., Bourdon, M., Pirrello, J., Cheniclet, C., Gévaudant, F. and Frangne, N. (2014) Endoreduplication and fruit growth in tomato: evidence in favour of the karyoplasmic ratio theory. J. Exp. Bot. 65, 2731–2746.
14. Coen, E.S. and Meyerowitz, E.M. (1991) The war of the whorls - genetic interactions controlling flower development. Nature, 353, 31–37.
15. Damodharan, S., Zhao, D. and Arazi, T. (2016) A common miRNA160-based mechanism regulates ovary patterning, floral organ abscission and lamina outgrowth in tomato. Plant J. 86, 458–471.
16. Dreni, L. and Kater, M.M. (2014) MADS reloaded: evolution of the AGAMOUS subfamily genes. New Phytol. 201, 717–732.
17. Dreni, L. and Zhang, D. (2016) Flower development: the evolutionary history and functions of the AGL6 subfamily MADS-box genes. J. Exp. Bot. 67, 1625–1638.
18. Duan, Y., Xing, Z., Diao, Z., Xu, W., Li, S., Du, X., Wu, G. et al. (2012) Characterization of Osmads6-5, a null allele, reveals that OsMADS6 is a critical regulator for early flower development in rice (Oryza sativa L.). Plant Mol. Biol. 80, 429–442.
19. El Ahmadi, A.B. and Stevens, M.A. (1979) Reproductive responses of heat-tolerant tomatoes to high temperatures. J. Amer. Soc. Hort. Sci. 104, 686–691.
20. Falavigna, A., Badino, M. and Soressi, G.P. (1978) Potential of the monomendelian factor pat in the tomato breeding for industry. Genetica Agraria, 32, 159–160.
21. Ficcadenti, N., Sestili, S., Pandolfini, T., Cirillo, C., Rotino, G.L. and Spena, A. (1999) Genetic engineering of parthenocarpic fruit development in tomato. Mol. Breeding, 5, 463–470.
22. Firon, N., Pressman, E., Meir, S., Khoury, R. and Altahan, L. (2012) Ethylene is involved in maintaining tomato (Solanum lycopersicum) pollen quality under heat-stress conditions. AoB. Plants, 2012, pls024.
23. Gillaspy, G., Ben-David, H. and Gruissem, W. (1993) Fruits: a developmental perspective. Plant Cell, 5, 1439–1451.
24. Gimenez, E., Castañeda, L., Pineda, B., Pan, I.L., Moreno, V., Angosto, T. and Lozano, R. (2016) TOMATO AGAMOUS1 and ARLEQUIN/TOMATO AGAMOUS-LIKE1 MADS-box genes have redundant and divergent functions required for tomato reproductive development. Plant Mol. Biol. 91, 513–531.
25. Gorguet, B., van Heusden, A.W. and Lindhout, P. (2005) Parthenocarpic fruit development in tomato. Plant Biol. 7, 131–139.
26. Gorguet, B., Eggink, P.M., Ocana, J., Tiwari, A., Schipper, D., Finkers, R., Visser, R.G.F. et al. (2008) Mapping and characterization of novel parthenocarpy QTLs in tomato. Theor. Appl. Genet. 116, 755–767.
27. Hazra, P. and Dutta, A.K. (2010) Inheritance of parthenocarpy in tomato (Solanum lycopersicum) and its association with two marker characters. Int. J. Plant Sci. 1, 144–149.
28. Huang, X., Effgen, S., Meyer, R.C., Theres, K. and Koornneef, M. (2012) Epistatic natural allelic variation reveals a function of AGAMOUS-LIKE6 in axillary bud formation in Arabidopsis. Plant Cell, 24, 2364–2379.
29. Imanshi, S. and Hiura, I. (1975) Relationship between fruit weight and seed content in the tomato. J. Jpn. Soc. Hort. Sci. 44, 33–40.
30. Koo, S.C., Bracko, O., Park, M.S., Schwab, R., Chun, H.J., Park, K.M., Seo, J.S. et al. (2010) Control of lateral organ development and flowering time by the Arabidopsis thaliana MADS-box Gene AGAMOUS-LIKE6. Plant J. 62, 807–816.
31. Li, H. and Durbin, R. (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics, 25, 1754–1760.
32. Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G. et al. and 1000 Genome Project Data Processing Subgroup. (2009) The sequence alignment/map format and SAMtools. Bioinformatics, 25, 2078–2079.
33. Li, H., Liang, W., Hu, Y., Zhu, L., Yin, C., Xu, J., Dreni, L. et al. (2011) Rice MADS6 interacts with the floral homeotic genes SUPERWOMAN1, MADS3, MADS58, MADS13, and DROOPING LEAF in specifying floral organ identities and meristem fate. Plant Cell, 23, 2536–2552.
34. Lin, S., George, W.L. and Splittstoesser, W.E. (1984) Expression and inheritance of parthenocarpy in ‘Severianin’ tomato. J. Hered. 75, 62–66.
35. Lippman, Z. and Tanksley, S.D. (2001) Dissecting the genetic pathway to extreme fruit size in tomato using a cross between the small-fruited wild species Lycopersicon pimpinellifolium and L. esculentum var, Giant Heirloom. Genetics, 158, 413–422.
36. Mazzucato, A., Taddei, A.R. and Soressi, G.P. (1998) The parthenocarpic fruit (pat) mutant of tomato (Lycopersicon esculentum Mill.) sets seedless fruits and has aberrant anther and ovule development. Development, 125, 107–114.
37. Mazzucato, A., Cellini, F., Bouzayen, M., Zouine, M., Mila, I., Minoia, S., Petrozza, A. et al. (2015) A TILLING allele of the tomato Aux/IAA9 gene offers new insights into fruit set mechanisms and perspectives for breeding seedless tomatoes. Mol. Breeding, 35, 22.
38. Mesihovic, A., Iannacone, R., Firon, N. and Fragkostefanakis, S. (2016) Heat stress regimes for the investigation of pollen thermotolerance in crop plants. Plant Reprod. 29, 93–105.
39. Michelmore, R.W., Paran, I. and Kesseli, R.V. (1991) Identification of markers linked to disease-resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. Proc. Natl Acad. Sci. USA, 88, 9828–9832.
40. Nuez, F., Costa, J. and Cuartero, J. (1986) Genetics of the parthenocarpy for tomato varieties “Sub-Artic Plenty”, “75/59” and “Severianı́n”. Z. Pflanzenzucht, 96, 200–206.
41. Nunome, T., Honda, I., Ohyama, A., Miyatake, K., Yamaguchi, H. and Fukuoka, H. (2014) Map based cloning of tomato parthenocarpic fruit-2 (pat-2) gene. Procs. XVIIIth EUCARPIA meeting, Avignon, France, 70 (abst.).
42. Ohmori, S., Kimizu, M., Sugita, M., Miyao, A., Hirochika, H., Uchida, E., Nagato, Y. et al. (2009) MOSAIC FLORAL ORGANS1, an AGL6-like MADS box gene, regulates floral organ identity and meristem fate in rice. Plant Cell, 21, 3008–3025.
43. Pan, I.L., McQuinn, R., Giovannoni, J.J. and Irish, V.F. (2010) Functional diversification of AGAMOUS lineage genes in regulating tomato flower and fruit development. J. Exp. Bot. 61, 1795–1806.
44. Park, S.J., Jiang, K., Schatz, M.C. and Lippman, Z.B. (2012) Rate of meristem maturation determines inflorescence architecture in tomato. Proc. Natl Acad. Sci. USA, 109, 639–644.
45. Pattison, R.J., Csukasi, F., Zheng, Y., Fei, Z., van der Knaap, E. and Catalá, C. (2015) Comprehensive tissue-specific transcriptome analysis reveals distinct regulatory programs during early tomato fruit development. Plant Physiol. 168, 1684–1701.
46. Perry, F.E. (1915) The inheritance of size in tomatoes. Ohio Naturalist, 15, 473–497.
47. Philouze, J. (1989) Natural parthenocarpy in tomato. IV. A study of the polygenic control of parthenocarpy in line 75/59. Agronomie, 9, 63–75.
48. Philouze, J. and Maisonneuve, B. (1978) Heredity of the natural ability to set parthenocarpic fruits in a German line. Tomato Genet. Coop. 28, 12.
49. Picken, A.J.F. (1984) A review of pollination and fruit set in the tomato (Lycopersicon esculentum Mill.). J. Hort. Sci. 59, 1–13.
50. Pnueli, L., Hareven, D., Rounsley, S.D., Yanofsky, M.F. and Lifschitz, E. (1994) Isolation of the tomato AGAMOUS gene TAG1 and analysis of its homeotic role in transgenic plants. Plant Cell, 6, 163–173.
51. Rijpkema, A.S., Zethof, J., Gerats, T. and Vandenbussche, M. (2009) The petunia AGL6 gene has a SEPALLATA-like function in floral patterning. Plant J. 60, 1–9.
52. Ruan, Y.L., Patrick, J.W., Bouzayen, M., Osorio, S. and Fernie, A.R. (2012) Molecular regulation of seed and fruit set. Trends Plant Sci. 17, 656–665.
53. Saito, T., Ariizumi, T., Okabe, Y., Asamizu, E., Hiwasa-Tanase, K., Fukuda, N., Mizoguchi, T. et al. (2011) TOMATOMA: a novel tomato mutant database distributing Micro-Tom mutant collections. Plant Cell Physiol. 52, 283–896.
54. Sato, S., Kamiyama, M., Iwata, T., Makita, N., Furukawa, H. and Ikeda, H. (2006) Moderate increase of mean daily temperature adversely affects fruit set of Lycopersicon esculentum by disrupting specific physiological processes in male reproductive development. Ann. Bot. Lond. 97, 731–738.
55. Schauer, S.E., Schlüter, P.M., Baskar, R., Gheyselinck, J., Bolaños, A., Curtis, M.D. and Grossniklaus, U. (2009) Intronic regulatory elements determine the divergent expression patterns of AGAMOUS-LIKE6 subfamily members in Arabidopsis. Plant J. 59, 987–1000.
56. Schneeberger, K., Ossowski, S., Lanz, C., Juul, T., Petersen, A.H., Nielsen, K.L., Jørgensen, J.E. et al. (2009) SHOREmap: simultaneous mapping and mutation identification by deep sequencing. Nat. Methods, 6, 550–551.
57. Scutt, C.P., Vinauger-Douard, M., Fourquin, C., Finet, C. and Dumas, C. (2006) An evolutionary perspective on the regulation of carpel development. J. Exp. Bot. 57, 2143–2152.
58. Selleri, L. (2011) Ph. D. Thesis http://hdl.handle.net/2067/2501.
59. Smaczniak, C., Immink, R.G., Angenent, G.C. and Kaufmann, K. (2012) Developmental and evolutionary diversity of plant MADS-domain factors: insights from recent studies. Development, 139, 3081–3098.
60. Soressi, G.P. and Salamini, F. (1975) A monomendelian gene inducing parthenocarpic fruits. Rep. Tomato Genet. Coop. 25, 22.
61. Tang, N., Deng, W., Hu, G., Hu, N. and Li, Z. (2015) Transcriptome profiling reveals the regulatory mechanism underlying pollination dependent and parthenocarpic fruit set mainly mediated by auxin and gibberellin. PLoS ONE, 10, e0125355.
62. Tanksley, S.D. (2004) The genetic, developmental, and molecular bases of fruit size and shape variation in tomato. Plant Cell, 16, 181–189.
63. Theissen, G. (2001) Development of floral organ identity: stories from the MADS house. Curr. Opin. Plant Biol. 4, 75–85.
64. Theissen, G. and Saedler, H. (2001) Plant biology: floral quartets. Nature, 409, 469–471.
65. Tomato Genome Consortium (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature, 485, 635–641.
66. Vardy, E., Lapushner, D., Genizi, A. and Hewitt, J. (1989) Genetics of parthenocarpy in tomato under a low temperature regime: II. Cultivar “Severianin”. Euphytica, 41, 9–15.
67. Varga, A. and Bruinsma, J. (1976) Roles of seeds and auxins in tomato fruit growth. Z. Pflanzenphysiol. 80, 95–104.
68. Varga, A. and Bruinsma, J. (1986) Tomato. In CRC Handbook of Fruit Set and Development (Monselise, S.P., Ed.), pp. 461–481. CRC Press Inc, Boca Raton, FL.
69. Varoquaux, F., Blanvillain, R., Delseny, M. and Gallois, P. (2000) Less is better: new approaches for seedless fruit production. Trends Biotechnol. 18, 233–242.
70. Wang, H., Schauer, N., Usadel, B., Frasse, P., Zouine, M., Hernould, M., Latché, A. 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.
71. Wang, P., Liao, H., Zhang, W., Yu, X., Zhang, R., Shan, H., Duan, X. et al. (2015) Flexibility in the structure of spiral flowers and its underlying mechanisms. Nat. Plants, 2, 15188.
72. Yao, J., Dong, Y. and Morris, B.A. (2001) Parthenocarpic apple fruit production conferred by transposon insertion mutations in a MADS-box transcription factor. Proc. Natl Acad. Sci. USA, 98, 1306–1311.
73. Ye, J., Parra, E.J., Sosnoski, D.M., Hiester, K., Underhill, P.A. and Shriver, M.D. (2002) Melting curve SNP (McSNP) genotyping: a useful approach for diallelic genotyping in forensic science. J. Forensic Sci. 47, 593–600.
74. Yoo, S.K., Wu, X., Lee, J.S. and Ahn, J.H. (2011) AGAMOUS-LIKE 6 is a floral promoter that negatively regulates the FLC/MAF clade genes and positively regulates FT in Arabidopsis. Plant J. 65, 62–76.
75. Zahn, L.M., Leebens-Mack, J.H., Arrington, J.M., Hu, Y., Landherr, L.L., dePamphilis, C.W., Becker, A. et al. (2006) Conservation and divergence in the AGAMOUS subfamily of MADS-box genes: evidence of independent sub- and neofunctionalization events. Evol. Dev. 8, 30–45.
76. Zhang, J., Nallamilli, B.R., Mujahid, H. and Peng, Z. (2010) OsMADS6 plays an essential role in endosperm nutrient accumulation and is subject to epigenetic regulation in rice (Oryza sativa). Plant J. 64, 604–617.
77. Zhang, S., Xu, M., Qiu, Z., Wang, K., Du, Y., Gu, L. and Cui, X. (2016) Spatiotemporal transcriptome provides insights into early fruit development of tomato (Solanum lycopersicum). Sci. Rep. 6, 23173.