Advertisement

24-Epibrassinolide Mechanisms Regulating Blossom-End Rot Development in Tomato Fruit

  • Lucas Baiochi Riboldi
  • Salete Aparecida Gaziola
  • Ricardo Antunes Azevedo
  • Sérgio Tonetto de Freitas
  • Paulo Roberto de Camargo e Castro
Article
  • 31 Downloads

Abstract

Blossom-end rot (BER) is a physiological disorder believed to be triggered by low Ca2+ content in the distal fruit tissue. However, many other factors can also determine fruit susceptibility to BER. It is possible that during fruit growth, Ca2+ imbalance can increase membrane leakiness, which may trigger the accumulation of reactive oxygen species, leading to cell death. Brassinosteroids are a class of plant hormones involved in stress defenses, specially increasing the activity of antioxidant enzymes and the accumulation of antioxidant compounds, such as ascorbic acid. The objective of this study was to understand the mechanisms by which 24-epibrassinolide (EBL) reduces fruit susceptibility to BER. Tomato plants ‘BRS Montese’ were cultivated in a greenhouse and were weekly sprayed with water (control) or EBL (0.01 µM) after full bloom. Plants and fruits were evaluated at 15 days after pollination (DAP). According to the results, EBL treatment inhibited BER development, increased fruit diameter, length, and fresh weight. EBL-treated fruit showed higher concentrations of soluble Ca2+ and lower concentrations of cell wall-bound Ca2+. EBL-treated fruit also had higher concentrations of ascorbic acid and lower concentrations of hydrogen peroxide, compared to water-treated fruit. EBL treatment increased the activity of the three main antioxidant enzymes known as ascorbate peroxidase, catalase, and superoxide dismutase. According to the results, EBL treatment maintained higher soluble Ca2+ and antioxidant capacity, reducing fruit susceptibility to BER.

Keywords

Antioxidant capacity Blossom-end rot Brassinosteroids Calcium deficiency 24-Epibrassinolide Oxidative stress 

Notes

Acknowledgements

The Coordination of Improvement of Higher Education Personnel (CAPES) and the Department of Biological Sciences of the University of São Paulo (ESALQ/USP) supported this study. We also thank the Laboratory of Plant Ecophysiology, Laboratory of Plant Genetics and Biochemistry (ESALQ/USP), and Laboratory of Plants Mineral Nutrition (CENA/USP).

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflict of interests.

References

  1. Aktas H, Karni L, Aloni B, Bar-Tal A (2003) Physiological and biochemical mechanisms leading to blossom-end rot in greenhouse-grown peppers, irrigated with saline solution. Acta Hortic 609:81–88CrossRefGoogle Scholar
  2. Aktas H, Karni L, Chang DC, Turhan E, Bar-Tal A, Aloni B (2005) The suppression of salinity-associated oxygen radicals production in pepper (Capsicum annuum) fruit by manganese, zinc and calcium in relation to its sensitivity to blossom-end rot. Physiol Plant 123:67–74CrossRefGoogle Scholar
  3. Alexieva V, Sergiev I, Mapelli S, Karanov E (2001) The effect of drought and ultraviolet radiation on growth and stress markers in pea and wheat. Plant Cell Environ 24:1337–1344CrossRefGoogle Scholar
  4. Alves LR, Monteiro CC, Carvalho RF, Ribeiro PC, Tezotto T, Azevedo RA, Gratão PL (2017) Cadmium stress related to root-to-shoot communication depends on ethylene and auxin in tomato plants. Environ Exp Bot 134:102–115CrossRefGoogle Scholar
  5. Athar HR, Khan A, Ashraf M (2008) Exogenously applied ascorbic acid alleviates salt-induced oxidative stress in wheat. Environ Exp Bot 63:224–231CrossRefGoogle Scholar
  6. Azevedo RA, Alas RM, Smith RJ, Lea PJ (1998) Response of antioxidant enzymes to transfer from elevated carbon dioxide to air and ozone fumigation, in the leaves and roots of wild-type and a catalase-deficient mutant of barley. Physiol Plant 104:280–292CrossRefGoogle Scholar
  7. Bondada BR, Matthews MA, Shackel KA (2005) Functional xylem in the post-veraison grape berry. J Exp Bot 56:2949–2957CrossRefGoogle Scholar
  8. Borges KLR, Salvato F, Alcântara BK, Nalin RS, Piotto FA, Azevedo RA (2018) Temporal dynamic responses of roots in contrasting tomato genotypes to cadmium tolerance. Ecotoxicology 27(3):245–258CrossRefGoogle Scholar
  9. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefGoogle Scholar
  10. Campbell A, Huysamer M, Stotz HU, Greve LC, Labavitch JM (1990) Comparison of ripening processes in intact tomato fruit and excised pericarp discs. Plant Physiol 94:1582–1589CrossRefGoogle Scholar
  11. Carvalho CRL, Mantovani DMB, Carvalho PRN, Moraes RM (1990) Análises químicas de alimentos. Instituto de Tecnologia de Alimentos, Campinas, p 121Google Scholar
  12. Carvalho MEA, Piotto FA, Nogueira ML, Gomes-Junior FG, Chamma MCP, Pizzaia D, Azevedo RA (2018) Cadmium exposure triggers genotype-dependent changes in seed vigor and germination of tomato offspring. Protoplasma 255(4):989–999CrossRefGoogle Scholar
  13. Choudhury FK, Rivero RM, Blumwald E, Mittler R (2017) Reactive oxygen species, abiotic stress and stress combination. Plant J 90:856–867CrossRefGoogle Scholar
  14. Constantine GN, Ries SK (1977) Superoxide dismutases: I. occurrence in higher plants. Plant Physiol 59:309–314CrossRefGoogle Scholar
  15. Cuypers A, Hendrix S, Amaral dos, Reis R, De Smet S, Deckers J, Gielen H, Jozefczak M, Loix C, Vercampt H, Vangronsveld J, Keunen E (2016) Hydrogen peroxide, signaling in disguise during metal phytotoxicity. Front Plant Sci 7:470CrossRefGoogle Scholar
  16. De Freitas ST, Padda M, Wu Q, Park S, Mitcham E (2011a) Dynamic alterations in cellular and molecular components during blossom-end rot development in tomatoes expressing sCAX1, a constitutively active Ca2+/H+ antiporter from Arabidopsis. Plant Physiol 156:844–855CrossRefGoogle Scholar
  17. De Freitas ST, Shackel KA, Mitcham EJ (2011b) Abscisic acid triggers whole-plant and fruit-specific mechanisms to increase fruit calcium uptake and prevent blossom-end rot development in tomato fruit. J Exp Bot 62:2645–2656CrossRefGoogle Scholar
  18. De Freitas ST, Handa AK, Wu Q, Park S, Mitcham EJ (2012) Role of pectin methylesterases in cellular calcium distribution and blossom-end rot development in tomato fruit. Plant J 71:824–835CrossRefGoogle Scholar
  19. De Freitas ST, Martinelli F, Feng B, Reitz NF, Mitcham EJ (2017) Transcriptome approach to understand the potential mechanisms inhibiting or triggering blossom-end rot development in tomato fruit in response to plant growth regulators. J Plant Growth Regul 37(1):183–198CrossRefGoogle Scholar
  20. Dobrikova AG, Vladkova RS, Rashkov GD, Todinova SJ, Krumova SB, Apostolova EL (2014) Effects of exogenous 24-epibrassinolide on the photosynthetic membranes under non-stress conditions. Plant Physiol Biochem 80:75–82CrossRefGoogle Scholar
  21. Gallie DR (2013) L-ascorbic acid: a multifunctional molecule supporting plant growth and development. Scientifica.  https://doi.org/10.1155/2013/795964 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Gratão PL, Polle A, Lea PJ, Azevedo RA (2005) Making the life of heavy metal- stressed plants a little easier. Funct Plant Biol 32:481–494CrossRefGoogle Scholar
  23. Gratão PL, Monteiro CC, Tezotto T, Carvalho RF, Alves LR, Peters LP, Azevedo RA (2015) Cadmium stress antioxidant responses and root-to-shoot communication in grafted tomato plants. Biometals 28:803–816CrossRefGoogle Scholar
  24. Heath RL, Packer L (1968) Photoperoxidation in isoled chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:11CrossRefGoogle Scholar
  25. Hepler PK, Winship LJ (2010) Calcium at the cell wall-cytoplast interface. J Integr Plant Biol 52:147–160CrossRefGoogle Scholar
  26. Ho LC, White PJ (2005) A cellular hypothesis for the induction of blossom-end rot in tomato fruit. Ann Bot 95:571–581CrossRefGoogle Scholar
  27. Ho LC, Belda R, Brown M, Andrews J, Adams P (1993) Uptake and transport of calcium and the possible causes of blossom end rot in tomato. J Exp Bot 44:509–518CrossRefGoogle Scholar
  28. Ikeda H, Shibuya T, Nishiyama M, Nakata Y, Kanayama Y (2017) Physiological mechanisms accounting for the lower incidence of blossom-end rot in tomato introgression line IL8-3 fruit. Hortic J 86(3):327–333CrossRefGoogle Scholar
  29. Jiang W, Bai J, Yang X, Yu H, Liu Y (2012) Exogenous application of abscisic acid, putrescine, or 2,4-epibrassinolide at appropriate concentration effectively alleviate damage to tomato seedlings from suboptimal temperature stress. Horttechnology 22(1):137–144Google Scholar
  30. Kraus TE, Fletcher RA, Evans RC, Pauls KP (1995) Paclobutrazol enhances tolerance to increased levels of UV-B radiation in soybean (Glycine max) seedlings. Can J Bot 73:797–806CrossRefGoogle Scholar
  31. Liu Y, Zhao Z, Si J, Di C, Han J, An L (2009) Brassinosteroids alleviate chilling-induced oxidative damage by enhancing antioxidant defense system in suspension cultured cells of Chorispora bungeana. Plant Growth Regul 59:207–214CrossRefGoogle Scholar
  32. Maia CF, Silva BRS, Lobato AKS (2018) J Plant Growth Regul.  https://doi.org/10.1007/s00344-018-9802-2 CrossRefGoogle Scholar
  33. Malavolta E, Vitti GC, Oliveira AS (1997) Avaliação do estado nutricional das plantas- princípios e aplicações. 2 ed, POTAFOS, Piracicaba, p 309Google Scholar
  34. Mestre TC, Garcia-Sanchez F, Rubio F, Martinez V, Rivero RM (2012) Glutathione homeostasis as an important and novel factor controlling blossom-end rot development in calcium-deficient tomato fruits. J Plant Physiol 169:1719–1727CrossRefGoogle Scholar
  35. Nagata N, Asami T, Yoshida S (2001) Brassinazole, an inhibitor of brassinosteroid biosynthesis, inhibits development of secondary xylem in cress plants (Lepidium sativum). Plant Cell Physiol 42:1006–1011CrossRefGoogle Scholar
  36. Nakano Y, Asada K (1981) Hydrogen-peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880Google Scholar
  37. Ogweno JO, Song XS, Shi K, HU WH, Mao WH, Zhou YH, YU JQ, Nogués S (2008) Brassinosteroids alleviate heat-induced inhibition of photosynthesis by increasing carboxylation efficiency and enhancing antioxidant systems in Lycopersicon esculentum. J Plant Growth Regul 27:49–57CrossRefGoogle Scholar
  38. Peaucelle A, Braybrook SA, Höfte H (2012) Cell wall mechanics and growth control in plants: the role of pectins revisited. Front Plant Sci 3:121CrossRefGoogle Scholar
  39. Pompeu GB, Vilhena MB, Gratão PL, Carvalho RF, Rossi ML, Martinelli AP, Azevedo RA (2017) Abscisic acid-deficient sit tomato mutant responses to cadmium-induced stress. Protoplasma 254(2):771–783CrossRefGoogle Scholar
  40. Rached M, Pierre B, Yves G, Matsukura C, Ariizumi T, Ezura H, Fukuda N (2018) Differences in blossom-end rot resistance in tomato cultivars is associated with total ascorbate rather than calcium concentration in the distal end part of fruits per se. Hortic J.  https://doi.org/10.2503/hortj.OKD-150 CrossRefGoogle Scholar
  41. Riboldi LB, Araújo SHC, De Freitas ST, Castro PRC (2018a) Blossom-end rot incidence in elongated tomato fruit. Botany 96(10):663–673CrossRefGoogle Scholar
  42. Riboldi LB, Araújo SHC, De Freitas ST, Castro PRC (2018b) Fruit shape regulates susceptibility of tomato to blossom-end rot. Acta Sci AgronGoogle Scholar
  43. Riboldi LB, Araújo SHC, Múrcia JAG, De Freitas ST, Castro PRC (2018c) Abscisic acid (ABA) and 24-epibrassinolide regulate blossom-end rot (BER) development in tomato fruit under Ca2+ deficiency’. Aust J Crop Sci 12(9):1440–1446CrossRefGoogle Scholar
  44. Saltveit ME (2002) The rate of ion leakage from chilling-sensitive tissue does not immediately increase upon exposure to chilling temperatures. Postharvest Biol Technol 26:295–304CrossRefGoogle Scholar
  45. Saure MC (2001) Blossom-end rot of tomato (Lycopersicon esculentum Mill.): a calcium or a stress-related disorder? Sci Hortic 90:193–208CrossRefGoogle Scholar
  46. Saure MC (2014) Why calcium deficiency is not the cause of blossom-end rot in tomato and pepper fruit–a reappraisal. Sci Hortic 174:151–154CrossRefGoogle Scholar
  47. Shahzad B, Tanveera M, Cheb Z, Rehmanc A, Cheemac SA, Sharmad A, Songb H, Rehmane S, Singh I, Shono M (2005) Physiological and molecular effects of 24-epibrassinolide, a brassinosteroid on thermotolerance of tomato. Plant Growth Regul 47:111–119CrossRefGoogle Scholar
  48. Soares C, De Sousa A, Pinto A, Azenha M, Teixeira J, Azevedo RA, Fidalgo F (2016) Effect of 24-epibrassinolide on ROS content, antioxidant system, lipid peroxidation and Ni uptake in Solanum nigrum L. under Ni stress. Environ Exp Bot 122:115–125CrossRefGoogle Scholar
  49. Turhan E, Karni L, Aktas H, Deventurero G, Chang DC, Bar-Tal A, Aloni B (2006) Apoplastic antioxidants in pepper (Capsicum annuum L.) fruit and their relationship to blossom-end rot. J Hortic Sci Biotechnol 81:661–667CrossRefGoogle Scholar
  50. Van Breusegem F, Dat JF (2006) Reactive oxygen species in plant cell death. Plant Physiol 141:384–390CrossRefGoogle Scholar
  51. Wu W, Zhang Q, Ervin EH, Yang Z, Zhang X (2017) Physiological mechanism of enhancing salt stress tolerance of perennial ryegrass by 24-epibrassinolide. Front Plant Sci 8:1017CrossRefGoogle Scholar
  52. Xia X-J, Wang Y-J, Zhou Y-H, Tao Y, Mao W-H, Shi K, Asami T, Chen Z, Yu J-Q (2009) Reactive oxygen species are involved in brassinosteroid-induced stress tolerance in cucumber. Plant Physiol 150(2):801–814CrossRefGoogle Scholar
  53. Yadav S, Hayat S, Wani AS, Irfan M, Ahmad A (2012) Comparison of the influence of 28-homobrassinolide and 24-epibrassinolide on nitrate reductase activity, proline content, and antioxidant enzymes of tomato. Int J Veg Sci 18(2):161–170CrossRefGoogle Scholar
  54. Yamauchi Y, Furutera A, Seki K, Toyoda Y, Tanaka K, Sugimoto Y (2008) Malondialdehyde generated from peroxidized linolenic acid causes protein modification in heat-stressed plants. Plant Physiol Biochem 46:786–793CrossRefGoogle Scholar
  55. Zheng Q, Liu J, Liu R, Wu H, Jiang C, Wang C, Guan Y (2016) Temporal and spatial distributions of sodium and polyamines regulated by brassinoesteroids in enhancing tomato salt resistance. Plant Soil 400:147–164CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Biological Sciences Department, “Luiz de Queiroz” College of AgricultureUniversity of São PauloPiracicabaBrazil
  2. 2.Genetics and Plant Breeding Department, “Luiz de Queiroz” College of AgricultureUniversity of São PauloPiracicabaBrazil
  3. 3.Postharvest Biology and TechnologySérgio Tonetto de FreitasBrazilian Agricultural Research CorporationPetrolinaBrazil

Personalised recommendations