The Papaya Transcription Factor CpNAC1 Modulates Carotenoid Biosynthesis through Activating Phytoene Desaturase Genes CpPDS2/4 during Fruit Ripening

Journal of Agricultural and Food Chemistry

Volumn 64, Issue 27, 2016, Pages 5454-5463

  Fu, Chang Chun ^a   Han, Yan Chao ^a   Fan, Zhong Qi ^a   Chen, Jian Ye ^a   Chen, Wei Xin ^a   Lu, Wang Jin ^a   Kuang, Jian Fei ^a  

^a SOUTH CHINA AGRICULTURAL UNIVERSITY   (China)

Author keywords

carotenoids; NAC; papaya fruit; phytoene desaturase genes; transcriptional regulation

Indexed keywords

BINS; BIOCHEMISTRY; BIOSYNTHESIS; CHEMICAL ACTIVATION; FRUITS; GENE EXPRESSION; GENES; PIGMENTS; TRANSCRIPTION FACTORS;

CAROTENOIDS; GEL MOBILITY SHIFT ASSAY; NAC TRANSCRIPTION FACTORS; PHYTOENE DESATURASE; TRANSCRIPTIONAL ACTIVATIONS; TRANSCRIPTIONAL REGULATION; TRANSCRIPTIONAL REGULATOR; TRANSIENT EXPRESSION ANALYSIS;

TRANSCRIPTION;

CAROTENOID; OXIDOREDUCTASE; PHYTOENE DEHYDROGENASE; PLANT PROTEIN; TRANSCRIPTION FACTOR;

BIOSYNTHESIS; CARICA; ENZYMOLOGY; FRUIT; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM;

CARICA; CAROTENOIDS; FRUIT; GENE EXPRESSION REGULATION, PLANT; OXIDOREDUCTASES; PLANT PROTEINS; TRANSCRIPTION FACTORS;

EID: 84978821832     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/acs.jafc.6b01020     Document Type: Article

References (56)

1. Fraser, P. D.; Bramley, P. M. The biosynthesis and nutritional uses of carotenoids Prog. Lipid Res. 2004, 43, 228-265 10.1016/j.plipres.2003.10.002
2. Lu, S.; Li, L. Carotenoid metabolism: biosynthesis, regulation, and beyond J. Integr. Plant Biol. 2008, 50, 778-785 10.1111/j.1744-7909.2008.00708.x
3. Bartley, G. E.; Scolnik, P. A. Plant carotenoids: pigments for photoprotection, visual attraction, and human health Plant Cell 1995, 7, 1027 10.2307/3870055
4. Blas, A. L.; Ming, R.; Liu, Z.; Veatch, O. J.; Paull, R. E.; Moore, P. H.; Yu, Q. Cloning of the papaya chromoplast-specific lycopene β-cyclase, CpCYC-b, controlling fruit flesh color reveals conserved microsynteny and a recombination hot spot Plant Physiol. 2010, 152, 2013-2022 10.1104/pp.109.152298
5. Nisar, N.; Li, L.; Lu, S.; Khin, N. C.; Pogson, B. J. Carotenoid metabolism in plants Mol. Plant 2015, 8, 68-82 10.1016/j.molp.2014.12.007
6. Scolnik, P. A.; Bartley, G. E. Phytoene desaturase from Arabidopsis Plant Physiol. 1993, 103, 1475 10.1104/pp.103.4.1475
7. Hable, W. E.; Oishi, K. K. Maize phytoene desaturase maps near the viviparous5 locus Plant Physiol. 1995, 108, 1329 10.1104/pp.108.3.1329
8. Kita, M.; Komatsu, A.; Omura, M.; YANo, M.; Ikoma, Y.; Moriguchi, T. Cloning and expression of CitPDS1, a gene encoding phytoene desaturase in citrus Biosci., Biotechnol., Biochem. 2001, 65, 1424-1428 10.1271/bbb.65.1424
9. Just, B. J.; Santos, C. A. F.; Fonseca, M. E. N.; Boiteux, L. S.; Oloizia, B. B.; Simon, P. W. Carotenoid biosynthesis structural genes in carrot (Daucus carota): isolation, sequence-characterization, single nucleotide polymorphism (SNP) markers and genome mapping Theor. Appl. Genet. 2007, 114, 693-704 10.1007/s00122-006-0469-x
10. Yan, P.; Gao, X. Z.; Shen, W. T.; Zhou, P. Cloning and expression analysis of phytoene desaturase and -carotene desaturase genes in Carica papaya Mol. Biol. Rep. 2011, 38, 785-791 10.1007/s11033-010-0167-2
11. Pecker, I.; Chamovitz, D.; Linden, H.; Sandmann, G.; Hirschberg, J. A single polypeptide catalyzing the conversion of phytoene to zeta-carotene is transcriptionally regulated during tomato fruit ripening Proc. Natl. Acad. Sci. U. S. A. 1992, 89, 4962-4966 10.1073/pnas.89.11.4962
12. Fraser, P. D.; Truesdale, M. R.; Bird, C. R.; Schuch, W.; Bramley, P. M. Carotenoid biosynthesis during tomato fruit development (evidence for tissue-specific gene expression) Plant Physiol. 1994, 105, 405-413 10.1104/pp.105.1.405
13. Rodrigo, M. J.; Marcos, J. F.; Zacarías, L. Biochemical and molecular analysis of carotenoid biosynthesis in flavedo of orange (Citrus sinensis L.) during fruit development and maturation J. Agric. Food Chem. 2004, 52, 6724-6731 10.1021/jf049607f
14. Fu, X.; Kong, W.; Peng, G.; Zhou, J.; Azam, M.; Xu, C.; Grierson, D.; Chen, K. Plastid structure and carotenogenic gene expression in red- and white-fleshed loquat (Eriobotrya japonica) fruits J. Exp. Bot. 2012, 63, 341-354 10.1093/jxb/err284
15. Welsch, R.; Maass, D.; Voegel, T.; DellaPenna, D.; Beyer, P. Transcription factor RAP2. 2 and its interacting partner SINAT2: stable elements in the carotenogenesis of Arabidopsis leaves Plant Physiol. 2007, 145, 1073-1085 10.1104/pp.107.104828
16. Toledo-Ortiz, G.; Huq, E.; Rodríguez-Concepción, M. Direct regulation of phytoene synthase gene expression and carotenoid biosynthesis by phytochrome-interacting factors Proc. Natl. Acad. Sci. U. S. A. 2010, 107, 11626-11631 10.1073/pnas.0914428107
17. Llorente, B.; D'Andrea, L.; Ruiz-Sola, M. A.; Botterweg, E.; Pulido, P.; Andilla, J.; Loza-Alvarez, P.; Rodriguez-Concepcion, M. Tomato fruit carotenoid biosynthesis is adjusted to actual ripening progression by a light-dependent mechanism Plant J. 2016, 85, 107-119 10.1111/tpj.13094
18. Fujisawa, M.; Nakano, T.; Shima, Y.; Ito, Y. A large-scale identification of direct targets of the tomato MADS box transcription factor RIPENING INHIBITOR reveals the regulation of fruit ripening Plant Cell 2013, 25, 371-386 10.1105/tpc.112.108118
19. Shima, Y.; Kitagawa, M.; Fujisawa, M.; Nakano, T.; Kato, H.; Kimbara, J.; Kasumi, T.; Ito, Y. Tomato FRUITFULL homologues act in fruit ripening via forming MADS-box transcription factor complexes with RIN Plant Mol. Biol. 2013, 82, 427-438 10.1007/s11103-013-0071-y
20. Fujisawa, M.; Shima, Y.; Nakagawa, H.; Kitagawa, M.; Kimbara, J.; Nakano, T.; Kasumi, T.; Ito, Y. Transcriptional regulation of fruit ripening by tomato FRUITFULL homologs and associated MADS box proteins Plant Cell 2014, 26, 89-101 10.1105/tpc.113.119453
21. Shan, W.; Kuang, J. F.; Chen, L.; Xie, H.; Peng, H. H.; Xiao, Y. Y.; Li, X. P.; Chen, W. X.; Chen, J. Y.; Lu, W. J.; He, Q.-g. Molecular characterization of banana NAC transcription factors and their interactions with ethylene signalling component EIL during fruit ripening J. Exp. Bot. 2012, 63, 5171-5187 10.1093/jxb/ers178
22. Zhang, K.; Gan, S. S. An abscisic acid-AtNAP transcription factor-SAG113 protein phosphatase 2C regulatory chain for controlling dehydration in senescing Arabidopsis leaves Plant Physiol. 2012, 158, 961-969 10.1104/pp.111.190876
23. Shan, W.; Kuang, J. F.; Lu, W. J.; Chen, J. Y. Banana fruit NAC transcription factor MaNAC1 is a direct target of MaICE1 and involved in cold stress through interacting with MaCBF1 Plant, Cell Environ. 2014, 37, 2116-2127 10.1111/pce.12303
24. Ma, N. N.; Feng, H. L.; Meng, X.; Li, D.; Yang, D. Y.; Wu, C. A.; Meng, Q. W. Overexpression of tomato SlNAC1 transcription factor alters fruit pigmentation and softening BMC Plant Biol. 2014, 14, 351 10.1186/s12870-014-0351-y
25. Zhu, M. K.; Chen, G. P.; Zhou, S.; Tu, Y.; Wang, Y.; Dong, T. T.; Hu, Z. L. A new tomato NAC (NAM/ATAF1/2/CUC2) transcription factor, SlNAC4, functions as a positive regulator of fruit ripening and carotenoid accumulation Plant Cell Physiol. 2014, 55, 119-135 10.1093/pcp/pct162
26. Zhou, H.; Lin-Wang, K.; Wang, H. L.; Gu, C.; Dare, A. P.; Espley, R. V.; He, H. P.; Allan, A. C.; Han, Y. P. Molecular genetics of blood-fleshed peach reveals activation of anthocyanin biosynthesis by NAC transcription factors Plant J. 2015, 82, 105-121 10.1111/tpj.12792
27. Oliveira, D. D. S.; Lobato, A. L.; Ribeiro, S. M. R.; Santana, A. M. C.; Chaves, J. B. P.; Pinheiro-Sant'Ana, H. M. Carotenoids and vitamin C during handling and distribution of guava (Psidium guajava L.), mango (Mangifera indica L.), and papaya (Carica papaya L.) at commercial restaurants J. Agric. Food Chem. 2010, 58, 6166-6172 10.1021/jf903734x
28. Nguyen, T. T. T.; Shaw, P. N.; Parat, M. O.; Hewavitharana, A. K. Anticancer activity of Carica papaya: A review Mol. Nutr. Food Res. 2013, 57, 153-164 10.1002/mnfr.201200388
29. Ramos-Parra, P. A.; García-Salinas, C.; Hernández-Brenes, C.; Díaz de la Garza, R. I. Folate levels and polyglutamylation profiles of papaya (Carica papaya cv. Maradol) during fruit development and ripening J. Agric. Food Chem. 2013, 61, 3949-3956 10.1021/jf305364x
30. Maisarah, A. M.; Asmah, R.; Fauziah, O. Proximate analysis, antioxidant and antiproliferative activities of different parts of Carica papaya J. Nutr. Food Sci. 2014, 4, 267 10.4172/2155-9600.1000267
31. Yuan, H.; Zhang, J. X.; Nageswaran, D.; Li, L. Carotenoid metabolism and regulation in horticultural crops Hortic. Res. 2015, 2, 15036 10.1038/hortres.2015.36
32. Skelton, R. L.; Yu, Q.; Srinivasan, R.; Manshardt, R.; Moore, P. H.; Ming, R. Tissue differential expression of lycopene β-cyclase gene in papaya Cell Res. 2006, 16, 731-739 10.1038/sj.cr.7310081
33. Devitt, L. C.; Fanning, K.; Dietzgen, R. G.; Holton, T. A. Isolation and functional characterization of a lycopene β-cyclase gene that controls fruit colour of papaya (Carica papaya L.) J. Exp. Bot. 2010, 61, 33-39 10.1093/jxb/erp284
34. Burg, S. P.; Burg, E. A. Molecular requirements for the biological activity of ethylene Plant Physiol. 1967, 42, 144-152 10.1104/pp.42.1.144
35. Zou, Y.; Zhang, L.; Rao, S.; Zhu, X. Y.; Ye, L. L.; Chen, W. X.; Li, X. P. The relationship between the expression of ethylene-related genes and papaya fruit ripening disorder caused by chilling injury PLoS One 2014, 9, e116002 10.1371/journal.pone.0116002
36. Jing, G. X.; Li, T. T.; Qu, H. X.; Yun, Z.; Jia, Y. X.; Zheng, X. L.; Jiang, Y. M. Carotenoids and volatile profiles of yellow-and red-fleshed papaya fruit in relation to the expression of carotenoid cleavage dioxygenase genes Postharvest Biol. Technol. 2015, 109, 114-119 10.1016/j.postharvbio.2015.06.006
37. Wan, C. Y.; Wilkins, T. A. A modified hot borate method significantly enhances the yield of high-quality RNA from cotton (Gossypium hirsutum L.) Anal. Biochem. 1994, 223, 7-12 10.1006/abio.1994.1538
38. Zhu, X. Y.; Li, X. P.; Chen, W. X.; Chen, J. Y.; Lu, W. J.; Chen, L.; Fu, D. W. Evaluation of new referece genes in papaya for accurate transcript normalization under different experimental conditions PLoS One 2012, 7, e44405 10.1371/journal.pone.0044405
39. -ΔΔCT method Methods 2001, 25, 402-408 10.1006/meth.2001.1262
40. Han, Y. C.; Fu, C. C.; Kuang, J. F.; Chen, J. Y.; Lu, W. J. Two banana fruit ripening-related C2H2 zinc finger proteins are transcriptional repressors of ethylene biosynthetic genes Postharvest Biol. Technol. 2016, 116, 8-15 10.1016/j.postharvbio.2015.12.029
41. Hellens, R. P.; Allan, A. C.; Friel, E. N.; Bolitho, K.; Grafton, K.; Templeton, M. D.; Karunairetnam, S.; Gleave, A. P.; Laing, W. A. Transient expression vectors for functional genomics, quantification of promoter activity and RNA silencing in plants Plant Methods 2005, 1, 13 10.1186/1746-4811-1-13
42. Sainsbury, F.; Thuenemann, E. C.; Lomonossoff, G. P. pEAQ: versatile expression vectors for easy and quick transient expression of heterologous proteins in plants Plant Biotechnol. J. 2009, 7, 682-693 10.1111/j.1467-7652.2009.00434.x
43. Ba, L. J.; Kuang, J. F.; Chen, J. Y.; Lu, W. J. MaJAZ1 attenuates the MaLBD5-mediated transcriptional activation of jasmonate biosynthesis gene MaAOC2 in regulating cold tolerance of banana fruit J. Agric. Food Chem. 2016, 64, 738-745 10.1021/acs.jafc.5b05005
44. Kou, X.; Watkins, C. B.; Gan, S. S. Arabidopsis AtNAP regulates fruit senescence J. Exp. Bot. 2012, 63, 6139-6147 10.1093/jxb/ers266
45. Yokotani, N.; Tsuchida-Mayama, T.; Ichikawa, H.; Mitsuda, N.; Ohme-Takagi, M.; Kaku, H.; Minami, E.; Nishizawa, Y. OsNAC111, a blast disease-responsive transcription factor in rice, positively regulates the expression of defense-related genes Mol. Plant-Microbe Interact. 2014, 27, 1027-1034 10.1094/MPMI-03-14-0065-R
46. Shan, W.; Chen, J. Y.; Kuang, J. F.; Lu, W. J. Banana fruit NAC transcription factor MaNAC5 cooperates with MaWRKYs to enhance the expression of pathogenesis-related genes against Colletotrichum musae Mol. Plant Pathol. 2016, 17, 330-338 10.1111/mpp.12281
47. Schweiggert, R. M.; Steingass, C. B.; Mora, E.; Esquivel, P.; Carle, R. Carotenogenesis and physico-chemical characteristics during maturation of red fleshed papaya fruit (Carica papaya L.) Food Res. Int. 2011, 44, 1373-1380 10.1016/j.foodres.2011.01.029
48. Schweiggert, R. M.; Steingass, C. B.; Heller, A.; Esquivel, P.; Carle, R. Characterization of chromoplasts and carotenoids of red- and yellow-fleshed papaya (Carica papaya L.) Planta 2011, 234, 1031-1044 10.1007/s00425-011-1457-1
49. Olsen, A. N.; Ernst, H. A.; Leggio, L. L.; Skriver, K. DNA-binding specificity and molecular functions of NAC transcription factors Plant Sci. 2005, 169, 785-797 10.1016/j.plantsci.2005.05.035
50. Kjaersgaard, T.; Jensen, M. K.; Christiansen, M. W.; Gregersen, P.; Kragelund, B. B.; Skriver, K. Senescence-associated barley NAC (NAM, ATAF1, 2, CUC) transcription factor interacts with radical-induced cell death 1 through a disordered regulatory domain J. Biol. Chem. 2011, 286, 35418-35429 10.1074/jbc.M111.247221
51. McQuinn, R. P.; Giovannoni, J. J.; Pogson, B. J. More than meets the eye: from carotenoid biosynthesis, to new insights into apocarotenoid signaling Curr. Opin. Plant Biol. 2015, 27, 172-179 10.1016/j.pbi.2015.06.020
52. Grassi, S.; Piro, G.; Lee, J. M.; Zheng, Y.; Fei, Z.; Dalessandro, G.; Giovannoni, J. J.; Lenucci, M. S. Comparative genomics reveals candidate carotenoid pathway regulators of ripening watermelon fruit BMC Genomics 2013, 14, 781 10.1186/1471-2164-14-781
53. Ye, J.; Hu, T. X.; Yang, C. M.; Li, H. X.; Yang, M. Z.; Ijaz, R.; Ye, Z. B.; Zhang, Y. Y. Transcriptome profiling of tomato fruit development reveals transcription factors associated with ascorbic acid, carotenoid and flavonoid biosynthesis PLoS One 2015, 10, e0130885 10.1371/journal.pone.0130885
54. Chung, M. Y.; Vrebalov, J.; Alba, R.; Lee, J.; McQuinn, R.; Chung, J. D.; Klein, P.; Giovannoni, J. A tomato (Solanum lycopersicum) APETALA2/ERF gene, SlAP2a, is a negative regulator of fruit ripening Plant J. 2010, 64, 936-947 10.1111/j.1365-313X.2010.04384.x
55. Karlova, R.; Rosin, F. M.; Busscher-Lange, J.; Parapunova, V.; Do, P. T.; Fernie, A. R.; Fraser, P. D.; Baxter, C.; Angenent, G. C.; de Maagd, R. A. Transcriptome and metabolite profiling show that APETALA2a is a major regulator of tomato fruit ripening Plant Cell 2011, 23, 923-941 10.1105/tpc.110.081273
56. Lee, J. M.; Joung, J. G.; McQuinn, R.; Chung, M. Y.; Fei, Z.; Tieman, D.; Klee, H.; Giovannoni, J. Combined transcriptome, genetic diversity and metabolite profiling in tomato fruit reveals that the ethylene response factor SlERF6 plays an important role in ripening and carotenoid accumulation Plant J. 2012, 70, 191-204 10.1111/j.1365-313X.2011.04863.x