Abstract
Tomato (Solanum lycopersicum L.) plants are able to adapt to restrictive environmental conditions mainly due to hormones such as brassinosteroids (BRs) that play important roles in determining stomata conductance and leaf transpiration. However, BRs effects on morphological traits like stomata and trichome position, size, and density, as well as on physiological traits resulting in better plant water use efficiency (WUE) and productivity, remain poorly understood. The objective of this study was to better understand the 2,4-epibrassinolide (EBL) mechanisms regulating leaf transpiration and WUE that can affect fruit production in tomato plants. According to results, treating tomato plants with exogenous EBL resulted in lower leaf transpiration, mainly from 9 to 16 h during the day, as well as lower stomata conductance and aperture, higher leaf water potential, higher net CO2 assimilation rate, higher number of stomata and trichome on leaf abaxial and adaxial surfaces, and higher plant dry mass accumulation, which improved plant WUE, compared to non-treated plants. EBL treatment also increased fruit size, fruit production per plant, and fruit quality traits such as higher dry mass and soluble solids content. In conclusion, BRs can improve plant adaptation to water stress conditions by regulating important physiological and morphological mechanisms, controlling plant WUE, and leading to higher fruit production.
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References
Ali Q, Athar HR, Ashraf M (2008) Modulation of growth, photosynthetic capacity, and water relations in salt stressed wheat plants by exogenously applied 24-epibrassinolide. Plant Growth Regul 56:107–116. https://doi.org/10.1007/s10725-008-9290-7
An Z, Jing W, Liu Y, Zhang W (2008) Hydrogen peroxide generated by copper amine oxidase is involved in abscisic acid-induced stomatal closure in Vicia faba. J Exp Bot 59:815–825. https://doi.org/10.1093/jxb/erm370
Anjum SA, Wang LC, Farooq M, Hussain M, Xue LL, Zou CM (2011) Brassinolide application improves the drought tolerance in maize through modulation of enzymatic antioxidants and leaf gas exchange. J Agron Crop Sci 197:177–185. https://doi.org/10.1111/j.1439-037X.2010.00459.x
Bajguz A (2000) Effect of brassinosteroids on nucleic acid and protein content in cultured cells of Chlorella vulgaris. Plant Physiol Biochem 38:209–215. https://doi.org/10.1016/S0981-9428(00)00733-6
Bajguz A, Hayat S (2009) Effects of brassinosteroids on the plant responses to environmental stresses. Plant Physiol Biochem 47:1–8. https://doi.org/10.1016/j.plaphy.2008.10.002
Bertolino LT, Caine RS, Gray JE (2019) Impact of stomatal density and morphology on water-use efficiency in a changing world. Front Plant Sci 10:225. https://doi.org/10.3389/fpls.2019.00225
Bi H, Kovalchuk N, Langridge P, Tricker PJ, Lopato S, Borisjuk N (2017) The impact of drought on wheat leaf cuticle properties. BMC Plant Biol 17:85. https://doi.org/10.1186/s12870-017-1033-3
Caine RS, Yin X, Sloan J, Harrison EL, Mohammed U, Fulton T, Biswal AK, Dionora J, Chater CC, Coe RA, Bandyopadhyay A, Murchie EH, Swarup R, Quick WP, Gray JE (2019) Rice with reduced stomatal density conserves water and has improved drought tolerance under future climate conditions. New Phytol 221:371–384. https://doi.org/10.1111/nph.15344
Carvalho,C.R.L, Mantovani, D.M.; Carvalho, P.R.N.; Moraes, R.M. Análises químicas de alimentos (Manual Técnico). Campinas: Instituto de Tecnologia de Alimentos - ITAL, 1990. 121p
Champa WH, Gill MIS, Mahajan BVC, Arora NK, Bedi S (2015) Brassinosteroids improve quality of table grapes (Vitis vinifera L.) cv. Flame Seedless Trop Agric Res 26:368–379
Drake PL, Froend RH, Franks PJ (2013) Smaller, faster stomata: scaling of stomatal size, rate of response, and stomatal conductance. J Exp Bot 64(2):495–505. https://doi.org/10.1093/jxb/ers347
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. https://doi.org/10.1073/pnas.0904209106
Franks PJ, Farquhar GD (2001) The effect of exogenous abscisic acid on stomatal development, stomatal mechanics, and leaf gas exchange in Tradescantia virginiana. Plant Physiol 125:935–942. https://doi.org/10.1104/pp.125.2.935
Franks PJW, Doheny-Adams TW, Britton-Harper ZJ, Gray JE (2015) Increasing water-use efficiency directly through genetic manipulation of stomatal density. New Phytol 207:188–195. https://doi.org/10.1111/nph.13347
Galdon-Armero J, Fullana-Pericas M, Mulet PA, Conesa MA, Martin C, Galmes J (2018) The ratio of trichomes to stomata is associated with water use efficiency in tomato. Plant J 96:607–619. https://doi.org/10.1111/tpj.14055
Giuliani MM, Carucci F, Nardella E, Francavilla M, Ricciardi L, Lotti C, Gatta G (2018) Combined effects of deficit irrigation and strobilurin application on gas exchange, yield, and water use efficiency in tomato (Solanum lycopersicum L.). Sci Hortic 233:149–158. https://doi.org/10.1016/j.scienta.2018.01.052
Gomes MDMA, Campostrini E, Leal NR, Viana AP, Ferraz TM, doNascimento Siqueira L, Rosa RCC, Netto AT, Nunez-Vázquez M, Zullo MAT (2006) Brassinosteroid analogue effects on the yield of yellow passion fruit plants (Passiflora edulis f. flavicarpa). Sci Hortic 110:235–240
Gudesblat G, Schneider-Pizoń J, Betti C, Mayerhofer J, Vanhoutte I, Van Dongen W, Boeren S, Zhiponova M, de Vries S, Jonak C, Russinova E (2012) SPEECHLESS integrates brassinosteroid and stomata signalling pathways. Nat Cell Biol 14:548–554. https://doi.org/10.1038/ncb2471
Guo J, Xu W, Yu X, Shen H, Li H, Cheng D, Liu A, Liu J, Liu C, Zhao S, Song J (2016) Cuticular wax accumulation is associated with drought tolerance in wheat near-isogenic lines. Front Plant Sci 7:1809. https://doi.org/10.3389/fpls.2016.01809
Hatfield JL, Dold C (2019) Water-use efficiency: advances and challenges in a changing climate. Front Plant Sci 10:103. https://doi.org/10.3389/fpls.2019.00103
Haubrick LL, Assmann SM (2006) Brassinosteroids and plant function: some clues, more puzzles. Plant Cell Environ 29:446–457. https://doi.org/10.1111/j.1365-3040.2005.01481.x
Haubrick LL, Torsethaugen G, Assmann SM (2006) Effect of brassinolide, alone and in concert with abscisic acid, on control of stomatal aperture and potassium currents of Vicia faba guard cell protoplasts. Physiol Plant 128:134–143. https://doi.org/10.1111/j.1399-3054.2006.00708.x
Hetherington AM, Woodward FI (2003) The role of stomata in sensing and driving environmental change. Nature 424:901–908. https://doi.org/10.1038/nature01843
Hubbard KE, Siegel RS, Valerio G, Brandt B, Schroeder JI (2012) Abscisic acid and CO2 signalling via calcium sensitivity priming in guard cells, new CDPK mutant phenotypes and a method for improved resolution of stomatal stimulus-response analyses. Ann Bot 109:5–17. https://doi.org/10.1093/aob/mcr252
Hughes J, Hepworth C, Dutton C, Dunn JA, Hunt L, Stephens J, Waugh R, Cameron DD, Gray JE (2017) Reducing stomatal density in barley improves drought tolerance without impacting on yield. Plant Physiol 174:776–787. https://doi.org/10.1104/pp.16.01844
Ichie T, Inoue Y, Takahashi N, Kamiya K, Kenzo T (2016) Ecological distribution of leaf stomata and trichomes among tree species in a Malaysian lowland tropical rain forest. J Plant Res 129:625–635. https://doi.org/10.1007/s10265-016-0795-2
Janeczko A, Koscielniak J, Pilipowicz M, Szarek-Lukaszewska G, Skoczowski A (2005) Protection of winter rape photosystem 2 by 24-epibrassinolide under cadmium stress. Photosynthetica 43:293–298. https://doi.org/10.1007/s11099-005-0048-4
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):137–144. https://doi.org/10.21273/HORTTECH.22.1.137
Jiao XC, Song XM, Zhang DL, Du QJ, Li JM (2019) Coordination between vapor pressure deficit and CO2 on the regulation of photosynthesis and productivity in greenhouse tomato production. Sci Rep 9(1):8700. https://doi.org/10.1038/s41598-019-45232-w
Khripach V, Zhabinskii V, Groot AD (2000) Twenty years of brassinosteroids: steroidal plant hormones warrant better crops for the XXI century. Ann Bot 86:441–447. https://doi.org/10.1006/anbo.2000.1227
Kim TW, Guan S, Sun Y, Deng Z, Tang W, Shang JX, Sun Y, Burlingame AL, Wang ZY (2009) Brassinosteroid signal transduction from cell-surface receptor kinases to nuclear transcription factors. Nat Cell Biol 11(10):1254–1260. https://doi.org/10.1038/ncb1970
Krishna P (2003) Brassinosteroid-mediated stress resistance. J Plant Growth Regul 22:265–275. https://doi.org/10.1186/1471-2229-10-151
Lawson T, Blatt MR (2014) Stomatal size, speed, and responsiveness impact on photosynthesis and water use efficiency. Plant Physiol 164:1556–1570. https://doi.org/10.1104/pp.114.237107
Lawson T, Vialet-Chabrand S (2019) Speedy stomata, photosynthesis, and plant water use efficiency. New Phytol 221:93–98. https://doi.org/10.1111/nph.15330
Laxmi A, Paul LK, Peters JL, Khurana JP (2004) Arabidopsis constitutive photomorphogenic mutant, bls1, displays altered brassinosteroid response and sugar sensitivity. Plant Mol Biol 56:185–201. https://doi.org/10.1007/s11103-004-2799-x
Liu L, Jia C, Zhang M, Chen D, Chen S, Guo R et al (2014) Ectopic expression of a BZR1-1D transcription factor in brassinosteroid signalling enhances carotenoid accumulation and fruit quality attributes in tomato. Plant Biotechnol J 12:105–115. https://doi.org/10.1111/pbi.12121
Liu H, Li Ning H, Zhang X, Li S, Pang J, Wang G, Sun J (2019) Optimizing irrigation frequency and amount to balance yield, fruit quality and water use efficiency of greenhouse tomato. Agric Water Manag 226:105787. https://doi.org/10.1016/j.agwat.2019.105787
Lu J, Shao G, Cui J, Wang X, Keabetswea L (2019) Yield, fruit quality and water use efficiency of tomato for processing under regulated deficit irrigation: a meta-analysis. Agric Water Manag 222:301–312. https://doi.org/10.1016/j.agwat.2019.06.008
Luan LY, Zhang ZW, Xi ZM, Huo SS, Ma LN (2016) Brassinosteroids regulate anthocyanin biosynthesis in the ripening of grape berries. S Afr J Enol Vitic 34:196–203
Medrano H, Tomás M, Martorell S, Flexas J, Hernández E, Rosselló J, Pou A, Escalona JM, Bota J (2015) From leaf to whole-plant water use efficiency (WUE) in complex canopies: limitations of leaf WUE as a selection target. Crop J 3:220–228. https://doi.org/10.1016/J.CJ.2015.04.002
Morillon R, Catterou M, Sangwan RS, Sangwan BS, Lassalles JP (2001) Brassinolide may control aquaporin activities in Arabidopsis thaliana. Planta 212(2):199–204. https://doi.org/10.1007/s004250000379
Nie S, Huang S, Wang S, Cheng D, Liu J, Lv S, Li Q, Wang X (2017) Enhancing brassinosteroid signaling via overexpression of tomato (Solanum lycopersicum) SlBRI1 improves major agronomic traits. Front Plant Sci 8:1386. https://doi.org/10.3389/fpls.2017.01386
Nievola CC, Carvalho CP, Carvalho V, Rodrigues E (2017) Rapid responses of plants to temperature changes. Temperature 4(4):371–405. https://doi.org/10.1080/23328940.2017.1377812
Núñez M, Mazzafera P, Mazorra L, Siqueira WJ, Zullo MAT (2003) Influence of a brassinosteroid analogue on antioxidant enzymes in rice grown in culture medium with NaCl. Biol Plant 47:67–70. https://doi.org/10.1023/A:1027380831429
Ogweno JO, Song XS, Shi K, Hu WH, Mao WH, Zhou YH, Nogués YuJQ, S, (2008) Brassinosteroids alleviate heat-induced inhibition of photosynthesis by increasing carboxylation efficiency and enhancing antioxidant systems in Lycopersicon esculentum. J Plant Growth Regul 27:49–57. https://doi.org/10.1007/s00344-007-9030-7
Omidian M, Roein Z, Shiri MA (2021) Effect of foliar application of 24-epibrassinolide on water use efficiency and morpho-physiological characteristics of Lilium LA Hybrid under feficit irrigation. J Plant Growth Regul. https://doi.org/10.1007/s00344-021-10400-8
Ozdemir F, Bor M, Demiral T, Turkan I (2004) Effects of 24-epibrassinolide on seed germination, seedling growth, lipid peroxidation, proline content and antioxidative system of rice (Oryza sativa L.) under salinity stress. Plant Growth Regul 42:203–211. https://doi.org/10.1023/B:GROW.0000026509.25995.13
Papanatsiou M, Amtmann A, Blatt MR (2016) Stomatal spacing safeguards stomatal dynamics by facilitating guard cell ion transport independent of the epidermal solute reservoir. Plant Physiol 172(1):254–263. https://doi.org/10.1104/pp.16.00850
Pozo L, Rivera T, Noriega C, Iglesias M, Coll F, Robaina C, Velázquez B, Rodríguez OL, Rodríguez ME (1994) Algunos resultados en el cultivo de los frutales mediante la utilización de brasinoesteeroides o compuestos análogos. Cult Trop 15:79–92
Que F, Wang GL, Xu ZS, Wang F, Xiong AS (2017) Transcriptional regulation of brassinosteroid accumulation during carrot development and the potential role of brassinosteroids in petiole elongation. Front Plant Sci 8:1356. https://doi.org/10.3389/fpls.2017.01356
Raschke K (1979) Movements using turgor mechanisms: movements of stomata. In: Haupt W, Feinleib ME (eds) Encyclopedia of Plant Physiology. Springer-Verlag, Berlin, pp 383–441
Riboldi LB, Oliveira RF, Angelocci LR (2016) Leaf turgor pressure in maize plants under water stress. Aust J Crop Sci 10(6):878–886. https://doi.org/10.21475/ajcs.2016.10.06.p7602
Riboldi LB, Gaziola SA, Azevedo RA, De Freitas ST, Castro PRC (2019) 24-epibrassinolide mechanisms regulating blossom-end rot development in tomato fruit. J Plant Growth Regul 38(3):812–823. https://doi.org/10.1007/s00344-018-9892-x
Sairam RK (1994) Effect of homobrasssinolide application on plant metabolism and grain yield under irrigated and moisture-stress conditions of two wheat varieties. J Plant Growth Regul 14:173–181. https://doi.org/10.1007/BF00025220
Schroeder JI, Kwak JM, Allen GJ (2001) Guard cell abscisic acid signalling and engineering drought hardiness in plants. Nature 410:327–330. https://doi.org/10.1038/35066500
Segatto FB, Bisognin DA, Benedetti M (2004) Técnica para o estudo da anatomia da epiderme foliar de batata. Cienc Rural 34(5):1597–1601. https://doi.org/10.1590/S0103-84782004000500042
Shahzad B, Tanveer M, Che Z, Rehman A, Cheema SA, Sharma A, Zhaorong D (2018) Role of 24-epibrassinolide (EBL) in mediating heavy metal and pesticide induced oxidative stress in plants: a review. Ecotox Environ Safe 147:935–944. https://doi.org/10.1016/j.ecoenv.2017.09.066
Sharma A, Kumar V, Singh R, Thukral AK, Bhardwaj R (2016) Effect of seed pre-soaking with 24-epibrassinolide on growth and photosynthetic parameters of Brassica juncea L. in imidacloprid soil. Ecotoxicol Environ Safe 133:195–201. https://doi.org/10.1016/j.ecoenv.2016.07.008
Shi C, Qi C, Ren H, Huang A, Hei S, She X (2015) Ethylene mediates brassinosteroid-induced stomatal closure via Gα protein-activated hydrogen peroxide and nitric oxide production in Arabidopsis. Plant J 82:280–301. https://doi.org/10.1111/tpj.12815
Suhita D, Raghavendra AS, Kwak JM, Vavasseur A (2004) Cytoplasmic alkalization precedes reactive oxygen species production during methyl jasmonate- and abscisic acid-induced stomatal closure. Plant Physiol 134:1536–1545. https://doi.org/10.1104/pp.103.032250
Vale FXR, Fernandes Filho EI, Liberato JR (2003) Quant: a software plant disease severity assessment. 8th International Congress of Plant Pathology, Christchurch New Zealand, p105.
Vesala T, Sevanto S, Grönholm T, Salmon Y, Nikinmaa E, Hari P, Hölttä T (2017) Effect of leaf water potential on internal humidity and CO2 dissolution: reverse transpiration and improved water use efficiency under negative pressure. Front Plant Sci 8:54. https://doi.org/10.3389/fpls.2017.00054
Vialet-Chabrand S, Matthews JSA, Simkin AJ, Raines CA, Lawson T (2017) Importance of fluctuations in light on the acclimation of Arabidopsis thaliana. Plant Physiol 173:2163–2179. https://doi.org/10.1104/pp.16.01767
Wang CF, You Y, Chen FXS, Wang J, Wang JS (2004) Adjusting effect of brassinolide and GA (4) on the orange growth. Acta Agric Univ Jiangxiensis 26:759–762
Wang C, Wu S, Tankari M, Zhang X, Li L, Gong D, Hao W, Zhang Y, Mei X, Wang Y, Liu F, Wang Y (2018) Stomatal aperture rather than nitrogen nutrition determined water use efficiency of tomato plants under nitrogen fertigation. Agric Water Manag 209:94–101. https://doi.org/10.1016/j.agwat.2018.07.020
Wani AS, Hayat S, Ahmad A, Tahir I (2017) Efficacy of brassinosteroid analogues in the mitigation of toxic effects of salt stress in Brassica juncea plants. J Environ Biol 34:27–36. https://doi.org/10.22438/jeb/38/1/MS-196
Xia JX, Huang LF, Zhou YH, Mao HW, Shi K, Wu JX, Asami T, Chen ZX, Yu JQ (2009a) Brassinosteroids promote photosynthesis and growth by enhancing activation of Rubisco and expression of photosynthetic genes in Cucumis sativus. Planta 230:1185–1196. https://doi.org/10.1007/s00425-009-1016-1
Xia XJ, Wang YJ, Zhou YH, Tao Y, Mao WH, Shi K, Asami T, Chen ZX, Yu JQ (2009b) Reactive oxygen species are involved in brassinosteroid-induced stress tolerance in cucumber. Plant Physiol 150:801–814. https://doi.org/10.1104/pp.109.138230
Xia XJ, Gao CJ, Song LX, Zhou YH, Shi K, Yu Q (2014) Role of H2O2 dynamics in brassinosteroid-induced stomatal closure and opening in Solanum lycopersicum. Plant Cell Environ 37:2036–2050. https://doi.org/10.1111/pce.12275
Xu Z, Jiang Y, Jia B, Zhou G (2016) Elevated-CO2 response of stomata and its dependence on environmental factors. Front Plant Sci 7:657. https://doi.org/10.3389/fpls.2016.00657
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):161–170. https://doi.org/10.1080/19315260.2011.593614
Yu JQ, Huang LF, Hu WH, Zhou YH, Mao WH, Ye SF, Nogués S (2004) A role for brassinosteroids in the regulation of photosynthesis in Cucumis sativus. J Exp Bot 55:1135–1143. https://doi.org/10.1093/jxb/erh124
Yusuf M, Fariduddin Q, Varshney P, Ahmad A (2012) Salicylic acid minimizes nickel and/or salinity-induced toxicity in Indian mustard (Brassica juncea) through an improved antioxidant system. Environ Sci Pollut Res Int 19(1):8–18. https://doi.org/10.1007/s11356-011-0531-3
Zeisler-Diehl V, Müller Y, Schreiber L (2018) Epicuticular wax on leaf cuticles does not establish the transpiration barrier, which is essentially formed by intracuticular wax. J Plant Physiol 227:66–74. https://doi.org/10.1016/j.jplph.2018.03.018
Zhao G, Xu H, Zhang P, Su X, Zhao H (2017) Effects of 2,4-epibrassinolide on photosynthesis and Rubisco activase gene expression in Triticum aestivum L. seedlings under a combination of drought and heat stress. Plant Growth Regul 81:377–384. https://doi.org/10.1007/s10725-016-0214-7
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 brassinosteroids in enhancing tomato salt resistance. Plant Soil 400:147–164. https://doi.org/10.1007/s11104-015-2712-1
Zhu T, Tan WR, Deng XG, Zheng T, Zhang DW, Lin HH (2015) Effects of brassinosteroids on quality attributes and ethylene synthesis in postharvest tomato fruit. Postharvest Biol Technol 100:196–204. https://doi.org/10.1016/j.postharvbio.2014.09.016
Zimmermann D, Reuss R, Westhoff M, Gessner P, Bauer W, Bamberg E, Bentrup FW, Zimmermann U (2008) A novel, non-invasive, online monitoring, versatile and easy plant-based probe for measuring leaf water status. J Exp Bot 59:3157–3167. https://doi.org/10.1093/jxb/ern171
Zimmermann U, Bitter R, Marchiori PER, Rüger S, Ehrenberger W, Sukhorukov VL, Schüttler A, Ribeiro RV (2013) A non-invasive plant-based probe for continuous monitoring of water stress in real time: a new tool for irrigation scheduling and deeper insight into drought and salinity stress physiology. Theor Exp Plant Phys 25(1):2–11. https://doi.org/10.1590/S2197-00252013000100002
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We thank the Department of Biological Sciences at University of São Paulo (ESALQ/USP), particularly the Laboratory of Plant Ecophysiology, (ESALQ/USP), Laboratory of Morphogenesis and Reproductive Biology (ESALQ/USP), and Laboratory of Neurophysiology and Plants under Stress (LEPSE).
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This study was supported by the Coordination for the Improvement of Higher Education Personnel (CAPES). The authors have no relevant financial or non-financial interests to disclose.
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LBR was responsible for the experiment, data processing, and writing the manuscript, RZD was responsible to process microscopy data analysis, and PRCC and STF were responsible for mentoring, writing, and correcting the manuscript.
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Riboldi, L.B., Dias, R.Z., de Camargo e Castro, P.R. et al. 2,4-Epibrassinolide mechanisms regulating water use efficiency and fruit production in tomato plants. Braz. J. Bot 44, 617–627 (2021). https://doi.org/10.1007/s40415-021-00745-5
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DOI: https://doi.org/10.1007/s40415-021-00745-5