Biologia Plantarum 63: 134-144, 2019 | DOI: 10.32615/bp.2019.016

Deficiency in phytochromobilin biosynthesis enhances heat-stress-induced impairments to the photosynthetic apparatus in tomato

A.J. Crispim Filho1,*, A.C. Costa2, F.R.R. Alves3, P.F. Batista2, A.A. Rodrigues4, S.C. Vasconcelos Filho4, K.J.T. Nascimento5
1 Departamento de Melhoramento Genético de Plantas, Escola de Agronomia, Universidade Federal de Goiás, Goiânia 74690-900, Goiás, Brazil
2 Laboratório de Ecofisiologia e Produtividade Vegetal, Instituto Federal Goiano, Rio Verde 75.901-970, Goiás, Brazil
3 Laboratório de Fisiologia Vegetal, Instituto de Ciências Biológicas, Universidade Federal de Goiás, Goiânia 74690-900, Goiás, Brazil
4 Laboratório de Anatomia Vegetal, Instituto Federal Goiano, Rio Verde 75.901-970, Goiás, Brazil
5 Laboratório de Sementes, Instituto Federal Goiano, Rio Verde 75.901-970, Goiás, Brazil

Plants are continuously exposed to unfavorable environmental conditions, such as heat stress, which negatively affect plant growth and productivity. There is evidence that phytochromes are involved in plant response to different abiotic stresses. We investigated the possible phytochrome-dependent responses to heat stress in photomorphogenic tomato mutants aurea (au, phytochromobilin-deficient, PΦB) and high-pigment 1 (hp1, hyperresponsive to phytochrome-mediated responses), as well as the wild-type Micro-Tom (MT). In comparison with MT, reductions in photosynthetic rate promoted by a high temperature were more pronounced in au, whereas less pronounced in hp1. All genotypes subjected to the heat stress exhibited adjustments in the capture and dissipation of energy, which were indicated by increases in the initial fluorescence and decreases in the maximum photochemical efficiency of photosystem II (PS II). The effective quantum yield of PS II and the apparent electron transport rate showed greatest alterations in the au mutant. In addition, heat-triggered anatomical changes occurred in all genotypes but were most conspicuous in the au mutant, followed by MT. Thus, phytochrome-dependent mechanisms played pivotal roles in the plant responses to the heat stress, and deficiency in phytochromobilin biosynthesis enhanced the heat-induced impairment of photosynthetic performance.

Keywords: aurea mutant, chlorophyll a fluorescence, high-pigment 1 mutant, phytochromes, thermotolerance, Solanum lycopersicum

Accepted: November 15, 2018; Prepublished online: November 15, 2018; Published online: January 19, 2019Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Crispim Filho, A.J., Costa, A.C., Alves, F.R.R., Batista, P.F., Rodrigues, A.A., Vasconcelos Filho, S.C., & Nascimento, K.J.T. (2019). Deficiency in phytochromobilin biosynthesis enhances heat-stress-induced impairments to the photosynthetic apparatus in tomato. Biologia plantarum63, 134-144. doi: 10.32615/bp.2019.016.
Download citation

Supplementary files

Download fileFILHO5667Suppl.pdf

File size: 91.2 kB

References

  1. Allakhverdiev, S.L., Kreslavski, V.D., Klimov, V.V., Los, D.A., Carpentier, R., Mohanty, P.: Heat stress: an overview of molecular responses in photosynthesis. - Photosynth. Res. 98: 541-550, 2008. Go to original source...
  2. Alves, F.R.R., Melo, H.C., Crispim-Filho, A.J., Costa, A. C., Nascimento, K. J. T., Carvalho, R. F.: Physiological and biochemical responses of photomorphogenic tomato mutants (cv. Micro-Tom) under water withholding. - Acta Physiol. Plant. 38: 155, 2016. Go to original source...
  3. Bianchetti, R.E., Cruz, A.B., Oliveira, B.S., Demarco, D., Purgatto, E., Peres, L.E.P., Rossi, M., Freschi, L.: Phytochromobilin deficiency impairs sugar metabolism through the regulation of cytokinin and auxin signaling in tomato fruits. - Sci. Rep. 7: 7822, 2017. Go to original source...
  4. Bilger, W., Björkman, O.: Role of xanthophyll cycle in photoprotection elucidated by measurements of light-induced absorbance changes, fluorescence and photosynthesis in leaves of Hedera canariensis. - Photosynth. Res. 25: 173-185, 1990. Go to original source...
  5. Bilger, W., Schreiber, U., Bock, M.: Determination of the quantum efficiency of photosystem II and of non-photochemical quenching of chlorophyll fluorescence in the field. - Oecologia 102: 425-432, 1995. Go to original source...
  6. Boccalandro, H.E., Ploschuk, E.L., Yanovsky, M.J., Sanchez, C.G., Casal, J.J.: Increased phytochrome B alleviates density effects on tuber yield of field potato crops. - Plant Physiol. 133: 1539-1546, 2003. Go to original source...
  7. Boccalandro, H.E., Rugnone, M.L., Moreno, J.E., Ploschuk, E.L., Serna, L., Yanovsky, M.J., Casal, J.J.: Phytochrome B enhances photosynthesis at the expense of water-use efficiency in Arabidopsis. - Plant Physiol. 150: 1083-1092, 2009. Go to original source...
  8. Carvalho, R.F., Campos, M.L., Azevedo, R.A.: The role of phytochrome in stress tolerance. - J. integr. Plant Biol. 53: 920-929, 2011a. Go to original source...
  9. Carvalho, R.F., Campos, M.L., Pino, L.E., Crestana, S.L., Zsögön, A., Lima, J.E., Benedito, V.A., Peres, L.E.: Convergence of developmental mutants into a single tomato model system: 'Micro-Tom' as an effective toolkit for plant developmental research. - Plant Methods 7: 18, 2011b. Go to original source...
  10. Chen, C., Xiao, Y., Li, X., Ni, M.: Light-regulated stomatal aperture in Arabidopsis. - Mol. Plants 5: 566-572, 2012. Go to original source...
  11. Crafts-Brandner, S.J., Salvucci, M.E.: Rubisco activase constrains the photosynthetic potential of leaves at high temperature and CO2. - Proc. nat. Acad. Sci. USA 97: 13430-13435, 2000. Go to original source...
  12. Doupis, G., Bertaki, M., Psarras, G., Kasapakis, I., Chartzoulakis, K.: Water relations, physiological behavior and antioxidant defence mechanism of olive plants subjected to different irrigation regimes. - Sci. Hort. 153: 150-156, 2013. Go to original source...
  13. Ferreira-Silva, S.L., Voigt, E.L., Silva, E.M., Maia, J.M., Fontenele, A.V., Silveira, J.A.G.: High temperature positively modulates oxidative protection in salt-stressed cashew plants. - Environ. exp. Bot. 74: 162-170, 2011. Go to original source...
  14. Galmés, J., Kapralov, M.V., Copolovici, L.O., Hermida-Carrera, C., Niinemets, Ü.: Temperature responses of the Rubisco maximum carboxylase activity across domains of life: phylogenetic signals, trade-offs, and importance for carbon gain. - Photosynth. Res. 123: 183-201, 2015. Go to original source...
  15. Genty, B., Briantais, J.M., Baker, N.R.: The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. - Biochim. biophys. Acta 990: 87-92, 1989. Go to original source...
  16. Gerganova, M., Popova, A.V., Stanoeva, D., Velitchkova, M.: Tomato plants acclimate better to elevated temperature and high light than to treatment with each factor separately. - Plant Physiol. Biochem. 104: 234-241, 2016. Go to original source...
  17. Goud, K.V., Sharma, R.: Retention of photoinduction of cytosolic enzymes in aurea mutant of tomato (Lycopersicon esculentum). - Plant Physiol. 105: 643-650, 1994. Go to original source...
  18. Goud, K.V, Sharma, R., Kendrick, R.E., Furuya, M.: Photoregulation of phenylalanine ammonia lyase is not correlated with anthocyanin induction in photomorpho-genetic mutants of tomato (Lycopersicon esculentum). - Plant Cell Physiol. 32: 1251-1258, 1991.
  19. Grover, A., Mittal, D., Negi, M., Lavania, D.: Generating high temperature tolerant transgenic plants: achievements and challenges. - Plant Sci. 205-206: 38-47, 2013. Go to original source...
  20. Ingraham, R.H., Lau, S.Y.M., Taneja, A.K., Hodges, R.S.: Denaturation and the effects of temperature on hydrophobic-interaction and reversed-phase high-performance liquid chromatography of proteins: Bio-gel tsk-phenyl-5-pw column. - J. Chromatogr. 327: 77-92, 1985. Go to original source...
  21. Kalaji, H.M., Schansker, G., Ladle, R.J., Goltsev, V., Bosa, K., Allakhverdiev, S.I., Brestic, M., Bussotti, F., Calatayud, A., Dąbrowski, P., Elsheery, N.I., Ferroni, L., Guidi, L., Hogewoning, S.W., Jajoo, A., Misra, A.N., Nebauer, S.G., Pancaldi, S., Penella, C., Poli, D., Pollastrini, M., Romanowska-Duda, Z.B., Rutkowska, B., Serôdio, J., Suresh, K., Szulc, W., Tambussi, E., Yanniccari, M., Zivcak, M.: Frequently asked questions about in vivo chlorophyll fluorescence: practical issue. - Photosynth. Res. 122: 121-158, 2014. Go to original source...
  22. Karnovsky, M.J.: A formaldehyde-glutaraldehyde fixative of high osmolarity for use in electron microscopy. - J. cell. Biol. 27: 137-138, 1965.
  23. Khudyakova, A.Y., Kreslavski, V.D., Shirshikova, G.N., Zharmukhamedov, S.K., Kosobryukhov, A.A., Allakhverdiev, S.I.: Resistance of Arabidopsis thaliana L. photosynthetic apparatus to UV-B is reduced by deficit of phytochromes B and A. - J. Photochem. Photobiol. B 169: 41-46, 2017. Go to original source...
  24. Kreslavski, V.D., Carpentier, R., Klimov, V.V., Murata, N., Allakhverdiev, S.I.: Molecular mechanisms of stress resistance of the photosynthetic apparatus. - Biochem. (Moscow) 1 Suppl. Ser. A: 185-205, 2007. Go to original source...
  25. Krüger, T.P.J., Ilioaia, C., Johnson, M.P., Ruban, A.V., Grondelle, R.V.: Disentangling the low-energy states of the major light-harvesting complex of plants and their role in photoprotection. - Biochim. biophys. Acta 1837: 1027-1038, 2014.
  26. Latif, H.H., Mohamed, H.I.: Exogenous applications of moringa leaf extract effect on retrotransposon, ultrastructural and biochemical contents of common bean plants under environmental stresses. - S. Afr. J. Bot. 106: 221-231, 2016. Go to original source...
  27. Liu, Y., Roof, S., Ye, Z., Barry, C., Tuinen, A.V., Vrebalov, J., Bowler, C., Giovannoni, J.: Manipulation of light signal transduction as a means of modifying fruit nutritional quality in tomato. - Proc. nat. Acad. Sci. USA 101: 9897-9902, 2004. Go to original source...
  28. Lubovská, Z., Dobrá, J., Štorchová, H., Wilhelmová, N., Vanková, R.: Cytokinin oxidase/dehydrogenase over-expression modifies antioxidant defense against heat, drought and their combination in Nicotiana tabacum plants. - J. Plant Physiol. 171: 1625-1633, 2014. Go to original source...
  29. Mathur, S., Agrawal, D., Jajoo, A.: Photosynthesis: response to high temperature stress. - J. Photochem. Photobiol. B. 137: 116-126, 2014. Go to original source...
  30. McCormac, A.C., Fischer, A., Kumar, A.M., Söll, D., Terry, M.J.: Regulation of HEMA1 expression by phytochrome and a plastid signal during de-etiolation in Arabidopsis thaliana. - Plant. J. 25: 549-561, 2001. Go to original source...
  31. Melo, H.C., Castro, E.M., Alves, E., Perina, F.J.: [Leaf anatomy of micro-tomato phytochrome-mutants and chloroplast ultra-structure]. - Ciênc. Agrotec. 35: 11-18, 2011. [In Port.] Go to original source...
  32. Meneguelli-Souza, A.C., Vitória, A.P., Vieira, T.O., Degli-Esposti, M.S.O., Souza, C.M.M.: Ecophysiological responses of Eichhornia crassipes (Mart.) Solms to As5+ under different stress conditions. - Photosynthetica 54: 243-250, 2016. Go to original source...
  33. Merzlyak, M.N., Solovchenko, A.E.: Photostability of pigments in ripening apple fruit: a possible photoprotective role of carotenoids during plant senescence. - Plant Sci. 163: 881-888, 2002. Go to original source...
  34. Moon, J., Zhu, L., Shen, H., Huq, E.: PIF1 directly and indirectly regulates chlorophyll biosynthesis to optimize the greening process in Arabidopsis. - Proc. nat. Acad. Sci. USA 105: 9433-9438, 2008. Go to original source...
  35. Müller, P., Li, X., Niyogi, K.K.: Non-photochemical quenching. A response to excess light energy. - Plant Physiol. 125: 1558-1566, 2001. Go to original source...
  36. Muramoto, T., Kami, C., Kataoka, H., Iwata, N., Linley, P.J., Mukougawa, K., Yokota, A., Kohchi, T.: The tomato photomorphogenetic mutant aurea is deficient in phytochromobilin synthase for phytochrome chromophore biosynthesis. - Plant Cell Physiol. 46: 661-665, 2005. Go to original source...
  37. Murchie, E.H., Horton, P.: Acclimation of photosynthesis to irradiance and spectral quality in British plant species: chlorophyll content, photosynthetic capacity and habitat preference. - Plant Cell Environ. 20: 438-448, 1997. Go to original source...
  38. Mutava, R.N., Prince, S.J.K., Syed, N.H., Song, L., Valliyodan, B., Chen, W., Nguyen, H.T.: Understanding abiotic stress tolerance mechanisms in soybean: A comparative evaluation of soybean response to drought and flooding stress. - Plant Physiol. Biochem. 86: 109-120, 2015. Go to original source...
  39. O'brien, T.P., Feder, N., Mccully, M.E.: Polychromatic staining of plant cell walls by toluidine blue O. - Protoplasma 59: 368-373, 1964.
  40. Peters, J.L., Széll, M., Kendrick, R.E.: The expression of light-regulated genes in the high-pigment-1 mutant of tomato. - Plant Physiol. 117: 797-807, 1998. Go to original source...
  41. Possart, A., Fleck, C., Hiltbrunner, A.: Shedding (far-red) light on phytochrome mechanisms and responses in land plants. - Plant Sci. 217-218: 36-46, 2014. Go to original source...
  42. Rizhsky, L., Liang, H., Mittler, R.: The combined effect of drought stress and heat shock on gene expression in tobacco. - Plant Physiol. 130: 1143-1151, 2002. Go to original source...
  43. Sajid, M., Rashid, B., Ali, Q., Husnain, T.: Mechanisms of heat sensing and responses in plants. It is not all about Ca2+ ions. - Biol. Plant. 62: 409-420, 2018. Go to original source...
  44. Salvucci, M.E., Crafts-Brandner, S.J.: Relationship between the heat tolerance of photosynthesis and the thermal stability of Rubisco activase in plants from contrasting thermal environments. - Plant Physiol. 134: 1460-1470, 2004. Go to original source...
  45. Schittenhelm, S., Menge-Hartmann, U., Oldenburg, E.: Photosynthesis, carbohydrate metabolism, and yield of phytochrome-B-overexpressing potatoes under different light regimes. - Crop Sci. 44: 131-143, 2004. Go to original source...
  46. Scholander, P.F., Hammel, H.T., Bradstreet, E.D., Hemmingsen, E.A.: Sap pressure in vascular plants: negative hydrostatic pressure can be measured in plants. - Science 148: 339-346, 1965. Go to original source...
  47. Sharma, L., Priya, M., Bindumadhava, H., Nair, R.M., Nayyar, H.: Influence of high temperature stress on growth, phenology and yield performance of mungbean [Vigna radiata (L.) Wilczek] under managed growth conditions. - Sci. Hort. 213: 379-391, 2016. Go to original source...
  48. Soto, A., Hernández, L., Quiles, M.J.: High root temperature affects the tolerance to high light intensity in Spathiphyllum plants. - Plant Sci. 227: 84-89, 2014. Go to original source...
  49. Terry, M.J., Kendrick, R.E.: The aurea and yellow-green-2 mutants of tomato are deficient in phytochrome chromophore synthesis. - J. Biol. Chem. 271: 21681-21686, 1996. Go to original source...
  50. Teskey, R., Wertin, T., Bauweraerts, I., Ameye, M., Mcguire, M.A., Steppe, K.: Responses of tree species to heat waves and extreme heat events. - Plant Cell Environ. 38: 1699-1712, 2014.
  51. Wang, F.F., Lian, H., Kang, C., Yang, H.: Phytochrome B is involved in mediating red light-induced stomatal opening in Arabidopsis thaliana. - Mol. Plant 3: 246-259, 2010. Go to original source...
  52. Wellburn, A.R.: The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. - J. Plant Physiol. 144: 307-313, 1997.
  53. Zhang, G.L., Chen, L.Y., Zhang, S.T., Zheng, H., Liu, G.H. Effects of high temperature stress on microscopic and ultrastructural characteristics of mesophyll cells in flag leaves of rice. - Rice Sci. 16: 65-71, 2009. Go to original source...
  54. Zhang, J., Stankey, R.J., Vierstra, R.D.: Structure-guided engineering of plant phytochrome B with altered photochemistry and light signaling. - Plant Physiol. 161: 1445-1457, 2013. Go to original source...
  55. Zhou, S., Sun, H., Zheng, B., Li, R., Zangh, W.: Cell cycle transcription factor E2F2 mediates non-stress temperature response of AtHSP70-4 in Arabidopsis. - Biochem. biophys. Res. Commun. 455: 139-146, 2014. Go to original source...