Journal of Plant Growth Regulation

, Volume 37, Issue 4, pp 1099–1112 | Cite as

Brassinosteroids Positively Modulate Growth: Physiological, Biochemical and Anatomical Evidence Using Two Tomato Genotypes Contrasting to Dwarfism

  • Camille Ferreira Maia
  • Breno Ricardo Serrão da Silva
  • Allan Klynger da Silva Lobato


Growth and development are vital processes in the life cycles of plants. Brassinosteroids (BRs) are steroids that when exogenously applied can regulate several biological responses. The aim of this research was to investigate the possible interferences caused by the exogenous application of BR on growth and metabolism using two genotypes of the DWARF gene, MT-d and MT-D, that are BR-deficient and BR-efficient, respectively. The experiment had four treatments with two genotypes (BR-efficient and BR-deficient) and two levels of brassinosteroids (0 and 100 nM BR, described as − BR and + BR, respectively). This study revealed that the exogenous application of BR promoted improvement in growth, inducing increases in all variables of both genotypes evaluated. In general, BR-deficient plants sprayed with BR had effects more intense, confirming the benefits of this steroid on photosynthetic apparatus and gas exchange. The changes in the anatomical characteristics of the leaf are related to the contribution of BR on the influx and consequent fixation of CO2. In addition, modifications related to root anatomy occurred as a result of the BR action with the purpose of increasing the root protection and absorption of water and nutrients. Increases in photosynthetic pigments suggest that the role of BR is linked with chlorophyll biosynthesis and the maintenance of chloroplast integrity, resulting from associations with the increases found in the activities of antioxidant enzymes that modulate the accumulation of reactive oxygen species.


Chlorophyll fluorescence DWARF gene Gas exchange Leaf anatomy Solanum lycopersicum 24-Epibrassinolide 



This research had financial supports from Fundação Amazônia de Amparo a Estudos e Pesquisas (FAPESPA/Brazil), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq/Brazil) and Universidade Federal Rural da Amazônia (UFRA/Brazil) to AKS Lobato. In other hand, CF Maia was supported with scholarship from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq/Brazil).

Author Contributions

AKSL was advisor of this project, planning all phases of this research. CFM conducted the experiment in the greenhouse and performed physiological, biochemical and morphological determinations, while BRSS measured anatomical parameters.

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no competing interests.


  1. Ahammed GJ, Yuan H-L, Ogweno JO et al (2012) Brassinosteroid alleviates phenanthrene and pyrene phytotoxicity by increasing detoxification activity and photosynthesis in tomato. Chemosphere 86:546–555. CrossRefPubMedGoogle Scholar
  2. Ahammed GJ, Choudhary SP, Chen S et al (2013a) Role of brassinosteroids in alleviation of phenanthrene–cadmium co-contamination-induced photosynthetic inhibition and oxidative stress in tomato. J Exp Bot 64:199–213. CrossRefPubMedGoogle Scholar
  3. Ahammed GJ, Ruan Y-P, Zhou J et al (2013b) Brassinosteroid alleviates polychlorinated biphenyls-induced oxidative stress by enhancing antioxidant enzymes activity in tomato. Chemosphere 90:2645–2653. CrossRefPubMedGoogle Scholar
  4. Akhtar P, Dorogi M, Pawlak K et al (2015) Pigment interactions in light-harvesting complex II in different molecular environments. J Biol Chem 290:4877–4886. CrossRefPubMedGoogle Scholar
  5. Alabadí D, Blázquez MA (2009) Molecular interactions between light and hormone signaling to control plant growth. Plant Mol Biol 69:409–417. CrossRefPubMedGoogle Scholar
  6. Aragão RM, Silva EN, Vieira CF, Silveira JAG (2012) High supply of NO3—mitigates salinity effects through an enhancement in the efficiency of photosystem II and CO2 assimilation in Jatropha curcas plants. Acta Physiol Plant 34:2135–2143. CrossRefGoogle Scholar
  7. Asmar SA, Castro EM, Pasqual M et al (2013) Changes in leaf anatomy and photosynthesis of micropropagated banana plantlets under different silicon sources. Sci Hortic 161:328–332. CrossRefGoogle Scholar
  8. Azhar N, Su N, Shabala L, Shabala S (2017) Exogenously applied 24-epibrassinolide (EBL) ameliorates detrimental effects of salinity by reducing K+ efflux via depolarization-activated K+ channels. Plant Cell Physiol 58:802–810. CrossRefPubMedGoogle Scholar
  9. Badawi GH, Yamauchi Y, Shimada E et al (2004) Enhanced tolerance to salt stress and water deficit by overexpressing superoxide dismutase in tobacco (Nicotiana tabacum) chloroplasts. Plant Sci 166:919–928. CrossRefGoogle Scholar
  10. Bai Y, Lindhout P (2007) Domestication and breeding of tomatoes: what have we gained and what can we gain in the future? Ann Bot 100:1085–1094. CrossRefPubMedPubMedCentralGoogle Scholar
  11. 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 72:248–254. CrossRefPubMedGoogle Scholar
  12. Cakmak I, Horst WJ (1991) Effect of aluminium on lipid peroxidation, superoxide dismutase, catalase, and peroxidase activities in root tips of soybean (Glycine max). Physiol Plant 83:463–468. CrossRefGoogle Scholar
  13. Cakmak I, Marschner H (1992) Magnesium deficiency and high light intensity enhance activities of superoxide dismutase, ascorbate peroxidase, and glutathione reductase in bean leaves. Plant Physiol 98:1222–1227. CrossRefPubMedPubMedCentralGoogle Scholar
  14. Calatayud A, Barreno E (2004) Response to ozone in two lettuce varieties on chlorophyll a fluorescence, photosynthetic pigments and lipid peroxidation. Plant Physiol Biochem 42:549–555. CrossRefPubMedGoogle Scholar
  15. Carvalho RF, Campos ML, Pino LE et al (2011) Convergence of developmental mutants into a single tomato model system: “Micro-Tom” as an effective toolkit for plant development research. Plant Methods 7:18. CrossRefPubMedPubMedCentralGoogle Scholar
  16. Castro EM de, Pereira FJ, Paiva R (2009) Histologia vegetal: estrutura e função dos órgãos vegetativos. UFLA, LavrasGoogle Scholar
  17. Divi UK, Krishna P (2009) Brassinosteroid: a biotechnological target for enhancing crop yield and stress tolerance. New Biotechnol 26:131–136. CrossRefGoogle Scholar
  18. Dobrikova AG, Vladkova RS, Rashkov GD et al (2014) Effects of exogenous 24-epibrassinolide on the photosynthetic membranes under non-stress conditions. Plant Physiol Biochem 80:75–82. CrossRefPubMedGoogle Scholar
  19. Elstner EF, Heupel A (1976) Inhibition of nitrite formation from hydroxylammoniumchloride: a simple assay for superoxide dismutase. Anal Biochem 70:616–620. CrossRefPubMedGoogle Scholar
  20. Ercolano MR, Sanseverino W, Carli P et al (2012) Genetic and genomic approaches for R-gene mediated disease resistance in tomato: retrospects and prospects. Plant Cell Rep 31:973–985. CrossRefPubMedPubMedCentralGoogle Scholar
  21. Farooq M, Wahid A, Basra SMA, Islam-ud-Din (2009) Improving water relations and gas exchange with brassinosteroids in rice under drought stress. J Agron Crop Sci 195:262–269. CrossRefGoogle Scholar
  22. Flores P, Hernández V, Hellín P et al (2016) Metabolite profile of the tomato dwarf cultivar Micro-Tom and comparative response to saline and nutritional stresses with regard to a commercial cultivar. J Sci Food Agric 96:1562–1570. CrossRefPubMedGoogle Scholar
  23. Franks PJ, Beerling DJ (2009) Maximum leaf conductance driven by CO2 effects on stomatal size and density over geologic time. Proc Natl Acad Sci USA 106:10343–10347. CrossRefPubMedGoogle Scholar
  24. Genisel M, Turk H, Erdal S (2013) Exogenous progesterone application protects chickpea seedlings against chilling-induced oxidative stress. Acta Physiol Plant 35:241–251. CrossRefGoogle Scholar
  25. Gerlach D (1977) Botanische mikrotechnik: eine einführung, 2nd edn. Georg Thieme, StuttgartGoogle Scholar
  26. Gerszberg A, Hnatuszko-Konka K (2017) Tomato tolerance to abiotic stress: a review of most often engineered target sequences. Plant Growth Regul 83:175–198. CrossRefGoogle Scholar
  27. Gerszberg A, Hnatuszko-Konka K, Kowalczyk T, Kononowicz AK (2015) Tomato (Solanum lycopersicum L.) in the service of biotechnology. Plant Cell Tissue Organ Cult 120:881–902. CrossRefGoogle Scholar
  28. Giannopolitis CN, Ries SK (1977) Superoxide dismutases: I. Occurrence in higher plants. Plant Physiol 59:309–314CrossRefGoogle Scholar
  29. Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930. CrossRefPubMedGoogle Scholar
  30. Gong M, Li Y-J, Chen S-Z (1998) Abscisic acid-induced thermotolerance in maize seedlings is mediated by calcium and associated with antioxidant systems. J Plant Physiol 153:488–496. CrossRefGoogle Scholar
  31. Guo HX, Liu WQ, Shi YC (2006) Effects of different nitrogen forms on photosynthetic rate and the chlorophyll fluorescence induction kinetics of flue-cured tobacco. Photosynthetica 44:140–142CrossRefGoogle Scholar
  32. Hameed M, Ashraf M, Naz N (2009) Anatomical adaptations to salinity in cogon grass [Imperata cylindrica (L.) Raeuschel] from the Salt Range, Pakistan. Plant Soil 322:229–238. CrossRefGoogle Scholar
  33. Havir EA, McHale NA (1987) Biochemical and developmental characterization of multiple forms of catalase in tobacco leaves. Plant Physiol 84:450–455. CrossRefPubMedPubMedCentralGoogle Scholar
  34. Hu WH, Wu Y, Zeng JZ et al (2010) Chill-induced inhibition of photosynthesis was alleviated by 24-epibrassinolide pretreatment in cucumber during chilling and subsequent recovery. Photosynthetica 48:537–544. CrossRefGoogle Scholar
  35. Javelle M, Vernoud V, Rogowsky PM, Ingram GC (2011) Epidermis: the formation and functions of a fundamental plant tissue. New Phytol 189:17–39. CrossRefPubMedGoogle Scholar
  36. Johansen DA (1940) Plant microtechnique, 1st edn. Springer, New YorkGoogle Scholar
  37. Joo S-H, Jang M-S, Kim MK et al (2015) Biosynthetic relationship between C28-brassinosteroids and C29-brassinosteroids in rice (Oryza sativa) seedlings. Phytochemistry 111:84–90. CrossRefPubMedGoogle Scholar
  38. Kocsy G, Tari I, Vanková R et al (2013) Redox control of plant growth and development. Plant Sci 211:77–91. CrossRefPubMedGoogle Scholar
  39. Krouk G, Ruffel S, Gutiérrez RA et al (2011) A framework integrating plant growth with hormones and nutrients. Trends Plant Sci 16:178–182. CrossRefPubMedGoogle Scholar
  40. Li J, Yang P, Gan Y et al (2015) Brassinosteroid alleviates chilling-induced oxidative stress in pepper by enhancing antioxidation systems and maintenance of photosystem II. Acta Physiol Plant 37:222. CrossRefGoogle Scholar
  41. Li J, Khan ZU, Tao X et al (2017) Effects of exogenous auxin on pigments and primary metabolite profile of postharvest tomato fruit during ripening. Sci Hortic 219:90–97. CrossRefGoogle Scholar
  42. Lichtenthaler HK, Buschmann C (2001) Chlorophylls and carotenoids: measurement and characterization by UV-VIS spectroscopy. In: Current protocols in food analytical chemistry. Wiley, Hoboken, pp 431–438Google Scholar
  43. Lima JV, Lobato AKS (2017) Brassinosteroids improve photosystem II efficiency, gas exchange, antioxidant enzymes and growth of cowpea plants exposed to water deficit. Physiol Mol Biol Plants 23:59–72. CrossRefPubMedPubMedCentralGoogle Scholar
  44. Liu Y, Zhao Z, Si J et al (2009) Brassinosteroids alleviate chilling-induced oxidative damage by enhancing antioxidant defense system in suspension cultured cells of Chorispora bungeana. Plant Growth Regul 59:207–214. CrossRefGoogle Scholar
  45. Ma CC, Gao YB, Guo HY, Wang JL (2004) Photosynthesis, transpiration, and water use efficiency of Caragana microphylla, C. intermedia, and C. korshinskii. Photosynthetica 42:65–70. CrossRefGoogle Scholar
  46. Marti E, Gisbert C, Bishop GJ et al (2006) Genetic and physiological characterization of tomato cv. Micro-Tom. J Exp Bot 57:2037–2047. CrossRefPubMedGoogle Scholar
  47. Meyer CJ, Peterson CA, Steudle E (2011) Permeability of Iris germanica’s multiseriate exodermis to water, NaCl, and ethanol. J Exp Bot 62:1911–1926. CrossRefPubMedGoogle Scholar
  48. Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880Google Scholar
  49. Nie S, Huang S, Wang S et al (2017) Enhancing brassinosteroid signaling via overexpression of tomato (Solanum lycopersicum) SlBRI1 improves major agronomic traits. Front Plant Sci 8:1–20. CrossRefGoogle Scholar
  50. Noguchi T, Fujioka S, Choe S et al (1999) Brassinosteroid-insensitive dwarf mutants of arabidopsis accumulate brassinosteroids. Plant Physiol 121:743–752. CrossRefPubMedPubMedCentralGoogle Scholar
  51. Ogweno JO, Song XS, Shi K et al (2008) Brassinosteroids alleviate heat-induced inhibition of photosynthesis by increasing carboxylation efficiency and enhancing antioxidant systems in Lycopersicon esculentum. J Plant Growth Regul 27:49–57. CrossRefGoogle Scholar
  52. Oh K, Yamada K, Asami T, Yoshizawa Y (2012) Synthesis of novel brassinosteroid biosynthesis inhibitors based on the ketoconazole scaffold. Bioorg Med Chem Lett 22:1625–1628. CrossRefPubMedGoogle Scholar
  53. Pereira MP, Rodrigues LC, de A, Corrêa FF, et al (2016) Cadmium tolerance in Schinus molle trees is modulated by enhanced leaf anatomy and photosynthesis. Trees 30:807–814. CrossRefGoogle Scholar
  54. Pereira-Netto AB, Roessner U, Fujioka S et al (2009) Shooting control by brassinosteroids: metabolomic analysis and effect of brassinazole on Malus prunifolia, the Marubakaido apple rootstock. Tree Physiol 29:607–620. CrossRefPubMedGoogle Scholar
  55. Qiu Z, Wang L, Zhou Q (2013) Effects of bisphenol A on growth, photosynthesis and chlorophyll fluorescence in above-ground organs of soybean seedlings. Chemosphere 90:1274–1280. CrossRefPubMedGoogle Scholar
  56. Rady MM, Rehman H ur (2016) Supplementing organic biostimulants into growing media enhances growth and nutrient uptake of tomato transplants. Sci Hortic 203:192–198. CrossRefGoogle Scholar
  57. Ramakrishna B, Rao SSR (2015) Foliar application of brassinosteroids alleviates adverse effects of zinc toxicity in radish (Raphanus sativus L.) plants. Protoplasma 252:665–677. CrossRefPubMedGoogle Scholar
  58. Salas Fernandez MG, Becraft PW, Yin Y, Lübberstedt T (2009) From dwarves to giants? Plant height manipulation for biomass yield. Trends Plant Sci 14:454–461. CrossRefPubMedGoogle Scholar
  59. Segatto FB, Bisognin DA, Benedetti M et al (2004) Técnica para o estudo da anatomia da epiderme foliar de batata. Ciência Rural 34:1597–1601. CrossRefGoogle Scholar
  60. Sha Valli Khan PS, Kozai T, Nguyen QT et al (2003) Growth and water relations of Paulownia fortunei under photomixotrophic and photoautotrophic conditions. Biol Plant 46:161–166. CrossRefGoogle Scholar
  61. Shahbaz M, Ashraf M, Athar H-R (2008) Does exogenous application of 24-epibrassinolide ameliorate salt induced growth inhibition in wheat (Triticum aestivum L.)? Plant Growth Regul 55:51–64. CrossRefGoogle Scholar
  62. Shi Y, Zhang Y, Yao H et al (2014) Silicon improves seed germination and alleviates oxidative stress of bud seedlings in tomato under water deficit stress. Plant Physiol Biochem 78:27–36. CrossRefPubMedGoogle Scholar
  63. Shu S, Tang Y, Yuan Y et al (2016) The role of 24-epibrassinolide in the regulation of photosynthetic characteristics and nitrogen metabolism of tomato seedlings under a combined low temperature and weak light stress. Plant Physiol Biochem 107:344–353. CrossRefPubMedGoogle Scholar
  64. Silva EN, Ribeiro RV, Ferreira-Silva SL et al (2012) Coordinate changes in photosynthesis, sugar accumulation and antioxidative enzymes improve the performance of Jatropha curcas plants under drought stress. Biomass Bioenerg 45:270–279. CrossRefGoogle Scholar
  65. Singh AP, Savaldi-Goldstein S (2015) Growth control: brassinosteroid activity gets context. J Exp Bot 66:1123–1132. CrossRefPubMedGoogle Scholar
  66. Smeekens S, Ma J, Hanson J, Rolland F (2010) Sugar signals and molecular networks controlling plant growth. Curr Opin Plant Biol 13:273–278. CrossRefGoogle Scholar
  67. Sorin C, Musse M, Mariette F et al (2015) Assessment of nutrient remobilization through structural changes of palisade and spongy parenchyma in oilseed rape leaves during senescence. Planta 241:333–346. CrossRefPubMedGoogle Scholar
  68. Steel RG, Torrie JH, Dickey DA (2006) Principles and procedures of statistics: a biometrical approach, 3rd edn. Academic Internet Publishers, MoorparkGoogle Scholar
  69. Suresh BV, Roy R, Sahu K et al (2014) Tomato genomic resources database: an integrated repository of useful tomato genomic information for basic and applied research. PLoS ONE 9:e86387. CrossRefPubMedPubMedCentralGoogle Scholar
  70. Thussagunpanit J, Jutamanee K, Kaveeta L et al (2015a) Comparative effects of brassinosteroid and brassinosteroid mimic on improving photosynthesis, lipid peroxidation, and rice seed set under heat stress. J Plant Growth Regul 34:320–331. CrossRefGoogle Scholar
  71. Thussagunpanit J, Jutamanee K, Sonjaroon W et al (2015b) Effects of brassinosteroid and brassinosteroid mimic on photosynthetic efficiency and rice yield under heat stress. Photosynthetica 53:312–320. CrossRefGoogle Scholar
  72. Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants protective role of exogenous polyamines. Plant Sci 151:59–66. CrossRefGoogle Scholar
  73. Verhoef N, Yokota T, Shibata K et al (2013) Brassinosteroid biosynthesis and signalling in Petunia hybrida. J Exp Bot 64:2435–2448. CrossRefPubMedPubMedCentralGoogle Scholar
  74. Wang Z, Zheng P, Meng J, Xi Z (2015) Effect of exogenous 24-epibrassinolide on chlorophyll fluorescence, leaf surface morphology and cellular ultrastructure of grape seedlings (Vitis vinifera L.) under water stress. Acta Physiol Plant 37:1729. CrossRefGoogle Scholar
  75. Wei Z, Li J (2016) Brassinosteroids regulate root growth, development, and symbiosis. Mol Plant 9:86–100. CrossRefPubMedGoogle Scholar
  76. Wu Q-S, Xia R-X, Zou Y-N (2006) Reactive oxygen metabolism in mycorrhizal and non-mycorrhizal citrus (Poncirus trifoliata) seedlings subjected to water stress. J Plant Physiol 163:1101–1110. CrossRefPubMedGoogle Scholar
  77. Wu XX, Ding HD, Chen JL et al (2015) Amelioration of oxidative damage in Solanum melongena seedlings by 24-epibrassinolide during chilling stress and recovery. Biol Plant 59:350–356. CrossRefGoogle Scholar
  78. Xia X-J, Huang L-F, Zhou Y-H et al (2009) Brassinosteroids promote photosynthesis and growth by enhancing activation of Rubisco and expression of photosynthetic genes in Cucumis sativus. Planta 230:1185–1196. CrossRefPubMedGoogle Scholar
  79. Yuan GF, Jia CG, Li Z et al (2010) Effect of brassinosteroids on drought resistance and abscisic acid concentration in tomato under water stress. Sci Hortic 126:103–108. CrossRefGoogle Scholar
  80. Zhang YP, Zhu XH, Ding HD et al (2013) Foliar application of 24-epibrassinolide alleviates high-temperature-induced inhibition of photosynthesis in seedlings of two melon cultivars. Photosynthetica 51:341–349. CrossRefGoogle Scholar
  81. Zhang J, Liu X, Li S et al (2014) The rice semi-dwarf mutant sd37, caused by a mutation in CYP96B4, plays an important role in the fine-tuning of plant growth. PLoS ONE 9:e88068. CrossRefPubMedPubMedCentralGoogle Scholar
  82. Zheng Q, Liu J, Liu R et al (2016) Temporal and spatial distributions of sodium and polyamines regulated by brassinosteroids in enhancing tomato salt resistance. Plant Soil 400:147–164. CrossRefGoogle Scholar
  83. Zhiponova MK, Vanhoutte I, Boudolf V et al (2013) Brassinosteroid production and signaling differentially control cell division and expansion in the leaf. New Phytol 197:490–502. CrossRefPubMedGoogle Scholar

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Authors and Affiliations

  1. 1.Núcleo de Pesquisa Vegetal Básica e AplicadaUniversidade Federal Rural da Amazônia, ParagominasParagominasBrazil

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