Brassinosteroid analogue affects the senescence in two papaya genotypes submitted to drought stress

Gomes, Mara de Menezes de Assis; Torres Netto, Alena; Campostrini, Eliemar; Bressan-Smith, Ricardo; Zullo, Marco António Teixeira; Ferraz, Tiago Massi; Siqueira, Luciane do Nascimento; Leal, Nilton Rocha; Núñez-Vázquez, Miriam

Abstract

Brassinosteroids (BS) application is associated with the increase of tolerance to some kinds of stresses, such as those induced by the infection of pathogens, temperature, salt and water deficiency. In this work, the influence of a spirostanic analogue of brassinosteroid (SAB) in the leaves of papaya Golden and UENF/CALIMAN 01 (UC 01) was tested to evaluate alterations in the content of chlorophyll in plants submitted to drought stress (DS). When plants were 70 d old, SAB was applied (0,1 mg L-1) for five consecutive days in half of the plants meant for the experiment. The treatments were: control irrigated (I), I with SAB (IB), DS and DS with SAB (DSB). The evaluated leaves were marked in accordance to the age: LEAF 1 (youngest expanded leaf), LEAF 2 (insertion immediately below LEAF 1) and LEAF 3 (insertion immediately below LEAF 2). The same leaves were used throughtout the experimental period. After the thirteenth day, the chlorophyll contents of DSB (Golden and UC 01) were always lesser than the treatment DS in LEAF 2. The irrigation was restarted in stressed plants on the fifteenth day, followed by new application of SAB (IB and DSB treatments). In Golden plants, DSB showed the lowest values of chlorophyll contents after re-watering, while in UC 01, differences in chlorophyll contents between treatments DS and DSB had not occurred. Alterations in Fv/Fm relation did not occur among the treatments during stress. In genotype UC 01, the irrigated plants showed minor values of Fv/Fm at the end of the experiment, whereas the plants submitted to DS presented increments in this relation in this same time. These results indicate that SAB might have contributed to accelerate the rate of leaf senescence of the oldest leaves of stressed plants, redistributing photoassimilates and other compounds for the youngest leaves.

chlorophyll content; Carica papaya L.; fluorescence; water relations

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 Regulation 56:107-116.
Behnamnia M, Kalantari K, Rezanejad F (2009) Exogenous application of brassinosteroid alleviates drought-induced oxidative stress in Lycopersicon esculentum L. General and Applied Plant Physiology 35:22-34.
Campostrini E, Glenn DM (2007) Ecophysiology of papaya: a review. Brazilian Journal of Plant Physiology 19:413-424.
Clemente HS, Marler TE (1996) Drought stress influences gas-exchange responses of papaya leaves to rapid changes in irradiance. Journal of American Society of Horticultural Science 12:292-295.
Clouse SD, Sasse JM (1998) Brassinosteroids: essential regulators of plant growth and development. Annual Review of Plant Physiology and Plant Molecular Biology 49:427-451.
Carvalho RF, Monteiro CC, Caetano AC, Dourado MN, Gratão PL, Haddad CRB, Peres LEP, Azevedo RA (2013) Leaf senescence in tomato mutants as affected by irradiance and phytohormones. Biologia Plantarum 57:749-757.
Carr MKV (2013) The water relations and irrigation requirements of papaya (Carica papaya L.): a review. Experimental Agriculture 1-14.
Çag S (2007) The effects of epibrassinolide on senescence in wheat leaves. Biotechnology and Biotechnology Equipment 21:63-65.
Dhaubhadel S, Browning KS, Gallie DR, Krishna P (2002) Brassinosteroid functions to protect the translational machinery and heat-shock protein synthesis following thermal stress. The Plant Journal 29(6):681-691.
Dhaubhadel S, Chaudhary S, Dobinson KF, Krishna P (1999) Treatment with 24-epibrassinolide, a brassinosteroid, increases the basic thermotolerance of Brassica napus and tomato seedlings. Plant Molecular Biology 40:333-342.
Divi UK, Rahman T, Krishna P (2010) Brassinosteroid-mediated stress tolerance in Arabidopsis shows interactions with abscisic acid, ethylene and salicylic acid pathways. BMC Plant Biology 10:151.
Fariduddin Q, Ahmad A, Hayat S (2004) Responses of Vigna radiata to foliar application of 28-homobrassinolide and kinetin. Biologia Plantarum 48:465-468.
Gomes MMA, Campostrini E, Leal NR, Viana AP, Ferraz TM, Siqueira LN, Rosa RCC, Netto AT, Núñez-Vázquez M, Zullo MAT (2006) Brassinosteroid analogue effects on the yield of yellow passion fruit plants (Passiflora edulis f. flavicarpa). Scientia Horticulturae 110:235-240.
Gomes MMA (2011) Physiological effects related to brassinosteroid application in plants. In: Hayat S and Ahmad A (eds). Brassinosteroids: a Class of Plant Hormone, 1st Ed. Dordrecht, Heidelberg, London, New York: Springer. pp.193-242.
He YJ, Xu RJ, Zhao YJ (1996) Enhancement of senescence by epibrassinolide in leaves of mung bean seedlings. Acta Phytophysiologica Sinica 22:58-62.
He Y, Tang W, Swain JD, Green AL, Jack TP, Gan S (2001) Networking senescence-regulating pathways by using Arabidopsis enhancer trap lines. Plant Physiology 126:707-716.
Holá D (2011) Brassinosteroids and photosynthesis. In: Hayat S and Ahmad A (eds). Brassinosteroids: a Class of Plant Hormone, 1st Ed. Dordrecht, Heidelberg, London, New York: Springer. pp.143-192.
Houimli SM, Denden M, El Hadj SB (2008) Induction of salt tolerance in pepper (Capsicum anuum) by 24-epibrassinolide. EurAsian Journal of BioSciences 2:83-89.
Iwahori S, Tominaga S, Higuchi S (1990) Retardation of abscission of citrus leaf and fruitlet explants by brassinolide. Plant Growth Regulation 9:119-125.
Jager CE, Symons GM, Ross JJ, Reid JB (2008) Do brassinosteroids mediate the water stress response? Physiologia Plantarum 133: 417-425.
Kagale S, Divi UK, Krochko JE, Keller WA, Krishna P (2007) Brassinosteroid confers tolerance in Arabidopsis thaliana and Brassica napus to a range of abiotical stresses. Planta 225:353-364.
Khripach VA, Zhabinskii V, De Groot AE (2000) Twenty years of brassinosteroids: steroidal plant hormones warrant better crops for the XXI Century. Annals of Botany 86:441-447.
Krishna P (2003) Brassinosteroid-mediated stress responses. Journal of Plant Growth Regulation 22:289-297.
Li JM, Nagpal P, Vitart V, McMorris TC, Chory J (1996) A role for brassinosteroids in light dependent development of Arabidopsis Science 272:398-401.
Li KR, Wang HH, Han G, Wang QJ, Fan J (2008) Effects of brassinolide on the survival, growth and drought resistance of Robinia pseudoacacia seedlings under water-stress. New Forests 35:255-266.
Lim SH, Chang SC, Lee JS, Kim SK, Kim SY (2002) Brassinosteroids affect ethylene production in the primary roots of maize (Zea mays L.). Journal of Plant Biology 45:148-153.
Lim PO, Kim HJ, Nam HG (2007) Leaf senescence. Annual Review of Plant Biology 58:115-136.
Mahouachi J, Arbona V, Gómez-Cadenas A (2007) Hormonal changes in papaya seedlings subjected to progressive water stress and re-watering. Plant Growth Regulation 53:43-51.
Mahouachi J, Socorro AR, Talon M (2006) Responses of papaya seedlings (Carica papaya L.) to water stress and re-hydration: growth, photosynthesis and mineral nutrient imbalance. Plant Soil 281:137-146.
Mahouachi J, Argamasilla R, Gómez-Cadenas A (2012) Influence of exogenous glycine betaine and abscisic acid on papaya in responses to water-deficit stress. Journal of Plant Growth Regulation 31:1-10.
Malo SE, Campbell CW (1986) The Papaya. Gainesville: University of Florida, Cooperative Extension Service Fruits Crops Fact Sheet FC.
Mandava NB (1988) Plant growth-promoting brassinosteroids. Physiology and Plant Molecular Biology 39:23-52.
Müssig C, Altmann T (1999) Physiology and molecular mode of action of brassinosteroids. Plant Physiology and Biochemistry 37:363-372.
Müssig C, Fischer S, Altman T (2002) Brassinosteroid-regulated gene expression. Plant Physiology 129:1241-1251.
Nakashita H, Yasuda M, Nitta T, Asami T, Fujioka S, Arai Y, Sekimata K, Takatsuto S, Yamaguchi I, Yoshida S (2003) Brassinosteroid functions in a broad range of disease resistance in tobacco and rice. The Plant Journal 33(5):887-898.
Nemhauser JL, Hong F, Chory J (2006) Different plant hormones regulate similar processes through largely nonoverlapping transcriptional responses. Cell 126:467-475.
Noodén, LD (1988) Senescence and aging in plants In: Noodén LN, Leopold AC, editors. The phenomenon of senescence and aging San diego: Academic Press. pp. 1-50.
Ogweno JO, Song XS, Shi K, Hu WH, Mao WH, Zhou YH, Yu JQ, Nogues S (2008) Brassinosteroids alleviate heat-induced inhibition of photosynthesis by increasing carboxylation efficiency and enhancing antioxidant systems in Lycopersicon esculentum Journal of Plant Growth Regulation 27:49-57.
Rodríguez CMR, Zullo MAT, Queiróz HM, Azevedo MBM, Becerra EA, Manchado FC (2006) The preparation of spirostanic analogues of brassinolide and castasterone. Polish Journal of Chemistry 80:637-646.
Sairam RK (1994) Effects of homobrassinolide application on plant metabolism and grain yield under irrigated and moisture stress conditions of two wheat varieties. Plant Growth Regulation 14:173-181.
Schlagnhaufer C, Arteca RN, Yopp JH (1984) Evidence that brassinosteroid stimulates auxin-induced ethylene synthesis in mung bean hypocotyls between S-adenosylmethionine and 1-aminocyclopropane 1-carboxylic acid. Physiologia Plantarum 61:555-558.
Smart CM (1994) Gene expression during leaf senescence. New Phytologist 126:419-448.
Sugiyama K, Kuraishi S (1989) Stimulation of fruit set of "Morita" navel orange with brassinolide. Acta Horticulturae 239:345-348.
Torres Netto A, Campostrini E, Oliveira JG, Yamanishi OK (2002) Portable chlorophyll meter for the quantification of photosynthetic pigments, nitrogen and the possible use for assessment of the photochemical process in Carica papaya L. Brazilian Journal of Plant Physiology 14:203-210.
Torres Netto A, Campostrini E, Azevedo LC, Souza MA, Ramalho JC, Chaves MM (2009) Morphological analysis and photosynthetic performance of improved papaya genotypes. Brazilian Journal of Plant Physiology 21:209-222.
Vardhini BV, Rao SSR (2002) Acceleration of ripening of tomato pericarp discs by brassinosteroids. Phytochemistry 16:843-847.
Xia XJ, Huang LF, Zhou YH, Mao WH, Shi K, Wu JX, Asami T, Chen Z, Yu JQ (2009) Brassinosteroids promote photosynthesis and growth by enhancing activation of Rubisco and expression of photosynthetic genes in Cucumis sativus Planta 230:1185-1196.
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 Journal of Experimental Botany 55:1135-1143.
Zhang MC, Zhai ZX, Tian XL, Duan LS, Li ZH (2008) Brassinolide alleviated the adverse effect of water deficits on photosynthesis and the antioxidant of soybean (Glycine max L.). Plant Growth Regulation 56:257-264.
Zhao YJ, Luo WH, Wang YQ, Xu RJ (1987) Retarding effects of brassinolide on maturation and senescence of hypocotyls segments of mungbean seedlings. Acta Physiologica Sinica 13:129-135.
Zhao YJ, Xu RJ, Cuo WH (1990) Inhibitory effects of abscisic acid on epibrassinolide-induced senescence of detached cotyledons in cucumber seedlings. Chinese Science Bulletin 35:928-931.
Zullo MAT, Adam G (2002) Brassinosteroids phytohormones-structure, bioactivity and applications. Brazilian Journal of Plant Physiology 14:143-181.

Publication Dates

Publication in this collection
02 Dec 2013
Date of issue
2013

History

Received
20 Dec 2012
Accepted
26 Sept 2013

This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

[1] 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 Regulation 56:107-116.

[2] Behnamnia M, Kalantari K, Rezanejad F (2009) Exogenous application of brassinosteroid alleviates drought-induced oxidative stress in Lycopersicon esculentum L. General and Applied Plant Physiology 35:22-34.

[4] Campostrini E, Glenn DM (2007) Ecophysiology of papaya: a review. Brazilian Journal of Plant Physiology 19:413-424.

[5] Clemente HS, Marler TE (1996) Drought stress influences gas-exchange responses of papaya leaves to rapid changes in irradiance. Journal of American Society of Horticultural Science 12:292-295.

[6] Clouse SD, Sasse JM (1998) Brassinosteroids: essential regulators of plant growth and development. Annual Review of Plant Physiology and Plant Molecular Biology 49:427-451.

[7] Carvalho RF, Monteiro CC, Caetano AC, Dourado MN, Gratão PL, Haddad CRB, Peres LEP, Azevedo RA (2013) Leaf senescence in tomato mutants as affected by irradiance and phytohormones. Biologia Plantarum 57:749-757.

[8] Carr MKV (2013) The water relations and irrigation requirements of papaya (Carica papaya L.): a review. Experimental Agriculture 1-14.

[9] Çag S (2007) The effects of epibrassinolide on senescence in wheat leaves. Biotechnology and Biotechnology Equipment 21:63-65.

[10] Dhaubhadel S, Browning KS, Gallie DR, Krishna P (2002) Brassinosteroid functions to protect the translational machinery and heat-shock protein synthesis following thermal stress. The Plant Journal 29(6):681-691.

[11] Dhaubhadel S, Chaudhary S, Dobinson KF, Krishna P (1999) Treatment with 24-epibrassinolide, a brassinosteroid, increases the basic thermotolerance of Brassica napus and tomato seedlings. Plant Molecular Biology 40:333-342.

[12] Divi UK, Rahman T, Krishna P (2010) Brassinosteroid-mediated stress tolerance in Arabidopsis shows interactions with abscisic acid, ethylene and salicylic acid pathways. BMC Plant Biology 10:151.

[13] Fariduddin Q, Ahmad A, Hayat S (2004) Responses of Vigna radiata to foliar application of 28-homobrassinolide and kinetin. Biologia Plantarum 48:465-468.

[14] Gomes MMA, Campostrini E, Leal NR, Viana AP, Ferraz TM, Siqueira LN, Rosa RCC, Netto AT, Núñez-Vázquez M, Zullo MAT (2006) Brassinosteroid analogue effects on the yield of yellow passion fruit plants (Passiflora edulis f. flavicarpa). Scientia Horticulturae 110:235-240.

[15] Gomes MMA (2011) Physiological effects related to brassinosteroid application in plants. In: Hayat S and Ahmad A (eds). Brassinosteroids: a Class of Plant Hormone, 1st Ed. Dordrecht, Heidelberg, London, New York: Springer. pp.193-242.

[16] He YJ, Xu RJ, Zhao YJ (1996) Enhancement of senescence by epibrassinolide in leaves of mung bean seedlings. Acta Phytophysiologica Sinica 22:58-62.

[17] He Y, Tang W, Swain JD, Green AL, Jack TP, Gan S (2001) Networking senescence-regulating pathways by using Arabidopsis enhancer trap lines. Plant Physiology 126:707-716.

[18] Holá D (2011) Brassinosteroids and photosynthesis. In: Hayat S and Ahmad A (eds). Brassinosteroids: a Class of Plant Hormone, 1st Ed. Dordrecht, Heidelberg, London, New York: Springer. pp.143-192.

[19] Houimli SM, Denden M, El Hadj SB (2008) Induction of salt tolerance in pepper (Capsicum anuum) by 24-epibrassinolide. EurAsian Journal of BioSciences 2:83-89.

[20] Iwahori S, Tominaga S, Higuchi S (1990) Retardation of abscission of citrus leaf and fruitlet explants by brassinolide. Plant Growth Regulation 9:119-125.

[21] Jager CE, Symons GM, Ross JJ, Reid JB (2008) Do brassinosteroids mediate the water stress response? Physiologia Plantarum 133: 417-425.

[22] Kagale S, Divi UK, Krochko JE, Keller WA, Krishna P (2007) Brassinosteroid confers tolerance in Arabidopsis thaliana and Brassica napus to a range of abiotical stresses. Planta 225:353-364.

[23] Khripach VA, Zhabinskii V, De Groot AE (2000) Twenty years of brassinosteroids: steroidal plant hormones warrant better crops for the XXI Century. Annals of Botany 86:441-447.

[24] Krishna P (2003) Brassinosteroid-mediated stress responses. Journal of Plant Growth Regulation 22:289-297.

[25] Li JM, Nagpal P, Vitart V, McMorris TC, Chory J (1996) A role for brassinosteroids in light dependent development of Arabidopsis Science 272:398-401.

[26] Li KR, Wang HH, Han G, Wang QJ, Fan J (2008) Effects of brassinolide on the survival, growth and drought resistance of Robinia pseudoacacia seedlings under water-stress. New Forests 35:255-266.

[27] Lim SH, Chang SC, Lee JS, Kim SK, Kim SY (2002) Brassinosteroids affect ethylene production in the primary roots of maize (Zea mays L.). Journal of Plant Biology 45:148-153.

[28] Lim PO, Kim HJ, Nam HG (2007) Leaf senescence. Annual Review of Plant Biology 58:115-136.

[29] Mahouachi J, Arbona V, Gómez-Cadenas A (2007) Hormonal changes in papaya seedlings subjected to progressive water stress and re-watering. Plant Growth Regulation 53:43-51.

[30] Mahouachi J, Socorro AR, Talon M (2006) Responses of papaya seedlings (Carica papaya L.) to water stress and re-hydration: growth, photosynthesis and mineral nutrient imbalance. Plant Soil 281:137-146.

[31] Mahouachi J, Argamasilla R, Gómez-Cadenas A (2012) Influence of exogenous glycine betaine and abscisic acid on papaya in responses to water-deficit stress. Journal of Plant Growth Regulation 31:1-10.

[32] Malo SE, Campbell CW (1986) The Papaya. Gainesville: University of Florida, Cooperative Extension Service Fruits Crops Fact Sheet FC.

[33] Mandava NB (1988) Plant growth-promoting brassinosteroids. Physiology and Plant Molecular Biology 39:23-52.

[35] Müssig C, Altmann T (1999) Physiology and molecular mode of action of brassinosteroids. Plant Physiology and Biochemistry 37:363-372.

[36] Müssig C, Fischer S, Altman T (2002) Brassinosteroid-regulated gene expression. Plant Physiology 129:1241-1251.

[37] Nakashita H, Yasuda M, Nitta T, Asami T, Fujioka S, Arai Y, Sekimata K, Takatsuto S, Yamaguchi I, Yoshida S (2003) Brassinosteroid functions in a broad range of disease resistance in tobacco and rice. The Plant Journal 33(5):887-898.

[38] Nemhauser JL, Hong F, Chory J (2006) Different plant hormones regulate similar processes through largely nonoverlapping transcriptional responses. Cell 126:467-475.

[39] Noodén, LD (1988) Senescence and aging in plants In: Noodén LN, Leopold AC, editors. The phenomenon of senescence and aging San diego: Academic Press. pp. 1-50.

[40] Ogweno JO, Song XS, Shi K, Hu WH, Mao WH, Zhou YH, Yu JQ, Nogues S (2008) Brassinosteroids alleviate heat-induced inhibition of photosynthesis by increasing carboxylation efficiency and enhancing antioxidant systems in Lycopersicon esculentum Journal of Plant Growth Regulation 27:49-57.

[41] Rodríguez CMR, Zullo MAT, Queiróz HM, Azevedo MBM, Becerra EA, Manchado FC (2006) The preparation of spirostanic analogues of brassinolide and castasterone. Polish Journal of Chemistry 80:637-646.

[42] Sairam RK (1994) Effects of homobrassinolide application on plant metabolism and grain yield under irrigated and moisture stress conditions of two wheat varieties. Plant Growth Regulation 14:173-181.

[43] Schlagnhaufer C, Arteca RN, Yopp JH (1984) Evidence that brassinosteroid stimulates auxin-induced ethylene synthesis in mung bean hypocotyls between S-adenosylmethionine and 1-aminocyclopropane 1-carboxylic acid. Physiologia Plantarum 61:555-558.

[44] Smart CM (1994) Gene expression during leaf senescence. New Phytologist 126:419-448.

[45] Sugiyama K, Kuraishi S (1989) Stimulation of fruit set of "Morita" navel orange with brassinolide. Acta Horticulturae 239:345-348.

[46] Torres Netto A, Campostrini E, Oliveira JG, Yamanishi OK (2002) Portable chlorophyll meter for the quantification of photosynthetic pigments, nitrogen and the possible use for assessment of the photochemical process in Carica papaya L. Brazilian Journal of Plant Physiology 14:203-210.

[47] Torres Netto A, Campostrini E, Azevedo LC, Souza MA, Ramalho JC, Chaves MM (2009) Morphological analysis and photosynthetic performance of improved papaya genotypes. Brazilian Journal of Plant Physiology 21:209-222.

[48] Vardhini BV, Rao SSR (2002) Acceleration of ripening of tomato pericarp discs by brassinosteroids. Phytochemistry 16:843-847.

[49] Xia XJ, Huang LF, Zhou YH, Mao WH, Shi K, Wu JX, Asami T, Chen Z, Yu JQ (2009) Brassinosteroids promote photosynthesis and growth by enhancing activation of Rubisco and expression of photosynthetic genes in Cucumis sativus Planta 230:1185-1196.

[50] 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 Journal of Experimental Botany 55:1135-1143.

[51] Zhang MC, Zhai ZX, Tian XL, Duan LS, Li ZH (2008) Brassinolide alleviated the adverse effect of water deficits on photosynthesis and the antioxidant of soybean (Glycine max L.). Plant Growth Regulation 56:257-264.

[52] Zhao YJ, Luo WH, Wang YQ, Xu RJ (1987) Retarding effects of brassinolide on maturation and senescence of hypocotyls segments of mungbean seedlings. Acta Physiologica Sinica 13:129-135.

[53] Zhao YJ, Xu RJ, Cuo WH (1990) Inhibitory effects of abscisic acid on epibrassinolide-induced senescence of detached cotyledons in cucumber seedlings. Chinese Science Bulletin 35:928-931.

[54] Zullo MAT, Adam G (2002) Brassinosteroids phytohormones-structure, bioactivity and applications. Brazilian Journal of Plant Physiology 14:143-181.

Brasil

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Brassinosteroid analogue affects the senescence in two papaya genotypes submitted to drought stress

Abstract

Publication Dates

History