Illuminating colors: regulation of carotenoid biosynthesis and accumulation by light

Current Opinion in Plant Biology

Volumn 37, Issue , 2017, Pages 49-55

  Llorente, Briardo ^a   Martinez Garcia, Jaime F ^a,b   Stange, Claudia ^c   Rodriguez Concepcion, Manuel ^a  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^b INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

^c UNIVERSITY OF CHILE   (Chile)

Author keywords

[No Author keywords available]

Indexed keywords

CAROTENOID;

ARABIDOPSIS; BIOSYNTHESIS; CARROT; GENE EXPRESSION REGULATION; LIGHT; METABOLISM; RADIATION RESPONSE; TOMATO;

ARABIDOPSIS; CAROTENOIDS; DAUCUS CAROTA; GENE EXPRESSION REGULATION, PLANT; LIGHT; LYCOPERSICON ESCULENTUM;

EID: 85017309957     PISSN: 13695266     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbi.2017.03.011     Document Type: Review

References (47)

1. 1•• Kromdijk, J., Glowacka, K., Leonelli, L., Gabilly, S.T., Iwai, M., Niyogi, K.K., Long, S.P., Improving photosynthesis and crop productivity by accelerating recovery from photoprotection. Science 354 (2016), 857–861 A neat example of how manipulating carotenoid-dependent photoprotection mechanisms can improve the plant response to natural shading events and increase crop productivity.
2. 2 Nisar, N., Li, L., Lu, S., Khin, N.C., Pogson, B.J., Carotenoid metabolism in plants. Mol. Plant 8 (2015), 68–82.
3. 3 Hou, X., Rivers, J., Leon, P., McQuinn, R.P., Pogson, B.J., Synthesis and function of apocarotenoid signals in plants. Trends Plant Sci. 21 (2016), 792–803.
4. 4 Ruiz-Sola, M.A., Rodriguez-Concepcion, M., Carotenoid biosynthesis in Arabidopsis: a colorful pathway. Arabidopsis Book, 10, 2012, e0158.
5. 5 Azari, R., Tadmor, Y., Meir, A., Reuveni, M., Evenor, D., Nahon, S., Shlomo, H., Chen, L., Levin, I., Light signaling genes and their manipulation towards modulation of phytonutrient content in tomato fruits. Biotechnol. Adv. 28 (2010), 108–118.
6. 6 Rodriguez-Concepcion, M., Stange, C., Biosynthesis of carotenoids in carrot: an underground story comes to light. Arch. Biochem. Biophys. 539 (2013), 110–116.
7. 7 Garcia-Mas, J., Rodriguez-Concepcion, M., The carrot genome sequence brings colors out of the dark. Nat. Genet. 48 (2016), 589–590.
8. 8 Llorente, B., D'Andrea, L., Rodriguez-Concepcion, M., Evolutionary recycling of light signaling components in fleshy fruits: new insights on the role of pigments to monitor ripening. Front. Plant Sci., 7, 2016, 263.
9. 9 Meier, S., Tzfadia, O., Vallabhaneni, R., Gehring, C., Wurtzel, E.T., A transcriptional analysis of carotenoid, chlorophyll and plastidial isoprenoid biosynthesis genes during development and osmotic stress responses in Arabidopsis thaliana. BMC Syst. Biol., 5, 2011, 77.
10. 10• Toledo-Ortiz, G., Huq, E., Rodriguez-Concepcion, M., Direct regulation of phytoene synthase gene expression and carotenoid biosynthesis by phytochrome-interacting factors. Proc. Natl. Acad. Sci. U. S. A. 107 (2010), 11626–11631 This article reports the first example of a light-regulated transcription factor directly controlling the expression of a carotenoid biosynthesis gene in coordination with photosynthetic development.
11. 11•• Toledo-Ortiz, G., Johansson, H., Lee, K.P., Bou-Torrent, J., Stewart, K., Steel, G., Rodriguez-Concepcion, M., Halliday, K.J., The HY5-PIF regulatory module coordinates light and temperature control of photosynthetic gene transcription. PLoS Genet., 10, 2014, e1004416 The relevance of antagonistic modules for the control of carotenoid biosynthesis and accumulation in Arabidopsis was nicely described in this work. They also show that the HY5-PIF module can integrate light and temperature cues.
12. 12 Leivar, P., Monte, E., PIFs: systems integrators in plant development. Plant Cell 26 (2014), 56–78.
13. 13 Lau, O.S., Deng, X.W., The photomorphogenic repressors COP1 and DET1: 20 years later. Trends Plant Sci. 17 (2012), 584–593.
14. 14 Casal, J.J., Photoreceptor signaling networks in plant responses to shade. Annu. Rev. Plant Biol. 64 (2013), 403–427.
15. 15 Roig-Villanova, I., Bou-Torrent, J., Galstyan, A., Carretero-Paulet, L., Portoles, S., Rodriguez-Concepcion, M., Martinez-Garcia, J.F., Interaction of shade avoidance and auxin responses: a role for two novel atypical bHLH proteins. EMBO J. 26 (2007), 4756–4767.
16. 16• Bou-Torrent, J., Toledo-Ortiz, G., Ortiz-Alcaide, M., Cifuentes-Esquivel, N., Halliday, K.J., Martinez-Garcia, J.F., Rodriguez-Concepcion, M., Regulation of carotenoid biosynthesis by shade relies on specific subsets of antagonistic transcription factors and cofactors. Plant Physiol. 169 (2015), 1584–1594 Analysis of the role of PIFs on the regulation of carotenoid biosynthesis by shade unveils new antagonistic modules in Arabidopsis.
17. 17 Galstyan, A., Cifuentes-Esquivel, N., Bou-Torrent, J., Martinez-Garcia, J.F., The shade avoidance syndrome in Arabidopsis: a fundamental role for atypical basic helix-loop-helix proteins as transcriptional cofactors. Plant J. 66 (2011), 258–267.
18. 18 Zhou, P., Song, M., Yang, Q., Su, L., Hou, P., Guo, L., Zheng, X., Xi, Y., Meng, F., Xiao, Y., et al. Both PHYTOCHROME RAPIDLY REGULATED1 (PAR1) and PAR2 promote seedling photomorphogenesis in multiple light signaling pathways. Plant Physiol. 164 (2014), 841–852.
19. 19 Welsch, R., Beyer, P., Hugueney, P., Kleinig, H., von Lintig, J., Regulation and activation of phytoene synthase, a key enzyme in carotenoid biosynthesis, during photomorphogenesis. Planta 211 (2000), 846–854.
20. 20 Rodriguez-Villalon, A., Gas, E., Rodriguez-Concepcion, M., Phytoene synthase activity controls the biosynthesis of carotenoids and the supply of their metabolic precursors in dark-grown Arabidopsis seedlings. Plant J. 60 (2009), 424–435.
21. 21•• Alvarez, D., Voss, B., Maass, D., Wust, F., Schaub, P., Beyer, P., Welsch, R., Carotenogenesis is regulated by 5′UTR-mediated translation of phytoene synthase splice variants. Plant Physiol. 172 (2016), 2314–2326 This is a very elegant work and one of the very few examples of post-transcriptional control of carotenoid gene expression to meet regular and extraordinary carotenoid needs.
22. 22•• Zhou, X., Welsch, R., Yang, Y., Alvarez, D., Riediger, M., Yuan, H., Fish, T., Liu, J., Thannhauser, T.W., Li, L., Arabidopsis OR proteins are the major posttranscriptional regulators of phytoene synthase in controlling carotenoid biosynthesis. Proc. Natl. Acad. Sci. U. S. A. 112 (2015), 3558–3563 A landmark work showing that OR proteins, previously known to promote carotenoid accumulation by triggering the differentiation of chromoplasts, also regulate carotenoid biosynthesis by direct interaction with PSY to post-translationally increase the amount of active enzyme.
23. 23 Park, S., Kim, H.S., Jung, Y.J., Kim, S.H., Ji, C.Y., Wang, Z., Jeong, J.C., Lee, H.S., Lee, S.Y., Kwak, S.S., Orange protein has a role in phytoene synthase stabilization in sweetpotato. Sci. Rep., 6, 2016, 33563.
24. 24 Chayut, N., Yuan, H., Ohali, S., Meir, A., Saar, U., Tzuri, G., Zheng, Y., Mazourek, M., Gepstein, S., Zhou, X., et al. Distinct mechanisms of the ORANGE protein in controlling carotenoid flux. Plant Physiol. 173 (2017), 376–389.
25. 25 Klee, H.J., Giovannoni, J.J., Genetics and control of tomato fruit ripening and quality attributes. Annu. Rev. Genet. 45 (2011), 41–59.
26. 26 Giliberto, L., Perrotta, G., Pallara, P., Weller, J.L., Fraser, P.D., Bramley, P.M., Fiore, A., Tavazza, M., Giuliano, G., Manipulation of the blue light photoreceptor cryptochrome 2 in tomato affects vegetative development, flowering time, and fruit antioxidant content. Plant Physiol. 137 (2005), 199–208.
27. 27 Weller, J.L., Schreuder, M.E., Smith, H., Koornneef, M., Kendrick, R.E., Physiological interactions of phytochromes A, B1 and B2 in the control of development in tomato. Plant J. 24 (2000), 345–356.
28. 28 Davuluri, G.R., van Tuinen, A., Fraser, P.D., Manfredonia, A., Newman, R., Burgess, D., Brummell, D.A., King, S.R., Palys, J., Uhlig, J., et al. Fruit-specific RNAi-mediated suppression of DET1 enhances carotenoid and flavonoid content in tomatoes. Nat. Biotechnol. 23 (2005), 890–895.
29. 29 Liu, Y., Roof, S., Ye, Z., Barry, C., van Tuinen, A., Vrebalov, J., Bowler, C., Giovannoni, J., Manipulation of light signal transduction as a means of modifying fruit nutritional quality in tomato. Proc. Natl. Acad. Sci. U. S. A. 101 (2004), 9897–9902.
30. 30 Wang, S., Liu, J., Feng, Y., Niu, X., Giovannoni, J., Liu, Y., Altered plastid levels and potential for improved fruit nutrient content by downregulation of the tomato DDB1-interacting protein CUL4. Plant J. 55 (2008), 89–103.
31. 31•• 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. 85 (2016), 107–119 This paper describes the adaptation of a shade-regulated PIF1-dependent pathway to monitor ripening progression in tomato fruits.
32. 32 Alba, R., Cordonnier-Pratt, M.M., Pratt, L.H., Fruit-localized phytochromes regulate lycopene accumulation independently of ethylene production in tomato. Plant Physiol. 123 (2000), 363–370.
33. 33 Powell, A.L., Nguyen, C.V., Hill, T., Cheng, K.L., Figueroa-Balderas, R., Aktas, H., Ashrafi, H., Pons, C., Fernandez-Munoz, R., Vicente, A., et al. Uniform ripening encodes a Golden 2-like transcription factor regulating tomato fruit chloroplast development. Science 336 (2012), 1711–1715.
34. 34 Tang, X., Miao, M., Niu, X., Zhang, D., Cao, X., Jin, X., Zhu, Y., Fan, Y., Wang, H., Liu, Y., et al. Ubiquitin-conjugated degradation of golden 2-like transcription factor is mediated by CUL4-DDB1-based E3 ligase complex in tomato. New Phytol. 209 (2016), 1028–1039.
35. 35 Galpaz, N., Wang, Q., Menda, N., Zamir, D., Hirschberg, J., Abscisic acid deficiency in the tomato mutant high-pigment 3 leading to increased plastid number and higher fruit lycopene content. Plant J. 53 (2008), 717–730.
36. 36 Kilambi, H.V., Kumar, R., Sharma, R., Sreelakshmi, Y., Chromoplast-specific carotenoid-associated protein appears to be important for enhanced accumulation of carotenoids in hp1 tomato fruits. Plant Physiol. 161 (2013), 2085–2101.
37. 37 Simpson, K., Cerda, A., Stange, C., Carotenoid biosynthesis in Daucus carota. Subcell. Biochem. 79 (2016), 199–217.
38. 38• Fuentes, P., Pizarro, L., Moreno, J.C., Handford, M., Rodriguez-Concepcion, M., Stange, C., Light-dependent changes in plastid differentiation influence carotenoid gene expression and accumulation in carrot roots. Plant Mol. Biol. 79 (2012), 47–59 The central relevance of light-dependent plastid development for carotenoid accumulation in carrot roots was first described in this paper.
39. 39 Clotault, J., Peltier, D., Berruyer, R., Thomas, M., Briard, M., Geoffriau, E., Expression of carotenoid biosynthesis genes during carrot root development. J. Exp. Bot. 59 (2008), 3563–3573.
40. 40 Baranska, M., Baranski, R., Schulz, H., Nothnagel, T., Tissue-specific accumulation of carotenoids in carrot roots. Planta 224 (2006), 1028–1037.
41. 41 Kim, J.E., Rensing, K.H., Douglas, C.J., Cheng, K.M., Chromoplasts ultrastructure and estimated carotene content in root secondary phloem of different carrot varieties. Planta 231 (2010), 549–558.
42. 42 Stange, C., Fuentes, P., Handford, M., Pizarro, L., Daucus carota as a novel model to evaluate the effect of light on carotenogenic gene expression. Biol. Res. 41 (2008), 289–301.
43. 43•• Iorizzo, M., Ellison, S., Senalik, D., Zeng, P., Satapoomin, P., Huang, J., Bowman, M., Iovene, M., Sanseverino, W., Cavagnaro, P., et al. A high-quality carrot genome assembly provides new insights into carotenoid accumulation and asterid genome evolution. Nat. Genet. 48 (2016), 657–666 This article provides interesting evidence that the carotenoid cultivars selected by their high carotenoid contents might actually be photomorphogenic mutants.
44. 44 Lado, J., Cronje, P., Alquezar, B., Page, A., Manzi, M., Gomez-Cadenas, A., Stead, A.D., Zacarias, L., Rodrigo, M.J., Fruit shading enhances peel color, carotenes accumulation and chromoplast differentiation in red grapefruit. Physiol. Plant. 154 (2015), 469–484.
45. 45 Maass, D., Arango, J., Wust, F., Beyer, P., Welsch, R., Carotenoid crystal formation in Arabidopsis and carrot roots caused by increased phytoene synthase protein levels. PLoS One, 4, 2009, e6373.
46. 46 Shi, H., Wang, X., Mo, X., Tang, C., Zhong, S., Deng, X.W., Arabidopsis DET1 degrades HFR1 but stabilizes PIF1 to precisely regulate seed germination. Proc. Natl. Acad. Sci. U. S. A. 112 (2015), 3817–3822.
47. 47 Dong, J., Tang, D., Gao, Z., Yu, R., Li, K., He, H., Terzaghi, W., Deng, X.W., Chen, H., Arabidopsis DE-ETIOLATED1 represses photomorphogenesis by positively regulating phytochrome-interacting factors in the dark. Plant Cell 26 (2014), 3630–3645.