Involvement of brassinosteroids and ethylene in the control of mitochondrial electron transport chain in postharvest papaya fruit

Mazorra, Luis Miguel; Oliveira, Marcos Goes; Souza, Anderson Fernandes; Silva, Willian Batista da; Santos, Gláucia Michelle dos; Silva, Lígia Renata Almeida da; Silva, Marcelo Gomes da; Bartoli, Carlos Guillermo; Oliveira, Jurandi Gonçalves de

Abstract

The plant hormones brassinosteroids (BR) and ethylene (ET) act together to regulate plant metabolism. We used BR and 1-methylcyclopropene (1-MCP, an ET action inhibitor) to elucidate the interactions between both hormones for the regulation of mitochondrial respiratory pathways in papaya fruit. The exogenous application of the 24-epibrassinolide (epiBR) enhanced the alternative oxidase (AOX) capacity. While treatment with Brz2001 (Brz is a specific inhibitor of the BR synthesis) also enhanced AOX capacity, these effects lacked in fruit treated simultaneously with epiBR and Brz. Changing the BR level had no effect on ET emission rate in the first 24 h, but a reduction in ET emission was observed in Brz-treated fruit on the fifth day. Together with Brz, epiBR increased the ET production on the fifth day, following the day in which the treatment was carried out. When the ET sensitivity of fruit was inhibited by the application of 1-MCP, the effects of epiBR and Brz were opposite to those obtained without 1-MCP. AOX capacity was slightly inhibited by epiBR in fruit pre-treated with 1-MCP. Data suggest that BR and ET act antagonistically, therefore regulating, directly or indirectly, AOX capacity during papaya fruit ripening.

AOX capacity; (CN)-insensitive respiration; ethylene sensitivity; 1-methylcyclopropene

References

Almeida AM, Jarmuszkiewicz W, Khomsi H, Arruda P, Vercesi AE, Sluse FE (1999) Cyanide-resistant, ATP-synthesis-sustained, and uncoupling-protein-sustained respiration during postharvest ripening of tomato fruit. Plant Physiology 119:1323-1330.
Arteca RN, Arteca JM (2008) Effects of brassinosteroid, auxin, and cytokinin on ethylene production in Arabidopsis thaliana plants. Journal of Experimental Botany 59:3019-3026.
Asami T, Mizutani M, Fujioka S, Goda H, Min YK, Shimada Y, Nakano T, Takatsuto S, Matsuyama T, Nagata N, Sakata K, Yoshida S (2001) Selective interaction of triazole derivatives with DWF4, a cytochrome P450 monooxygenase of the brassinosteroid biosynthetic pathway, correlates with brassinosteroid deficiency in planta. Journal of Biological Chemistry 276:25687-25691.
Asami T, Nakano T, Nakashita H, Sekimata K, Shimada Y, Yoshida S (2003) The influence of chemical genetics on plant science: shedding light on functions and mechanism of action of brassinosteroids using biosynthesis inhibitors. Journal of Plant Growth Regulation 22:336-349.
Beavis AD, Vercesi AE (1992) Anion uniport in plant mitochondria is mediated by a Mg(2+)-insensitive inner membrane anion channel. Journal of Biological Chemistry 267:3079-3087.
Blankenship SM, Dole JM (2003) 1-Methylcyclopropene: a review. Postharvest Biology and Technology 28:1-25.
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72:248-254.
Bron IU, Jacomino AP (2006) Ripening and quality of 'Golden' papaya fruit harvested at different maturity stages. Brazilian Journal of Plant Physiology 18:389-396.
Calegario FF, Cosso RG, Fagian MM, Almeida FV, Jardim WF, Jezek P, Arruda P, Vercesi AE (2003) Stimulation of potato tuber respiration by cold stress is associated with an increased capacity of both plant uncoupling mitochondrial protein (PUMP) and alternative oxidase. Journal of Bioenergetics and Biomembranes 35:211-220.
Carré JE, Affourtit C, Moore AL (2011) Interaction of purified alternative oxidase from thermogenic Arum maculatum with pyruvate. FEBS Letters 585:397-401.
Considine MJ, Daley DO, Whelan J (2001) The expression of alternative oxidase and uncoupling protein during fruit ripening in mango. Plant Physiology 126:1619-1629.
De Grauwe L, Vandenbussche F, Tietz O, Palme K, Van Der Straeten D (2005) Auxin, ethylene and brassinosteroids: tripartite control of growth in the Arabidopsis hypocotyl. Plant and Cell Physiology 46:827-836.
Deslauriers SD, Larsen PB (2010) FERONIA is a key modulator of brassinosteroid and ethylene responsiveness in Arabidopsis hypocotyls. Molecular Plant 3:626-640.
Duque P, Arrabaça JD (1999) Respiratory metabolism during cold storage of apple fruit. II. Alternative oxidase is induced at the climacteric. Physiologia Plantarum 107:24-31.
Fabi JP, Mendes LRBC, Lajolo FM, Nascimento JRO (2010) Transcript profiling of papaya fruit reveals differentially expressed genes associated with fruit ripening. Plant Science 179:225-233.
Fabi JP, Cordenunsi BR, de Mattos Barreto GP, Mercadante AZ, Lajolo FM, Oliveira do Nascimento JR (2007) Papaya fruit ripening: response to ethylene and 1-methylcyclopropene (1-MCP). Journal of Agricultural and Food Chemistry 55:6118-6123.
Fu FQ, Mao WH, Shi K, Zhou YH, Asami T, Yu JQ (2008) A role of brassinosteroids in early fruit development in cucumber. Journal of Experimental Botany 59:2299-2308.
Gendron JM, Haque A, Gendron N, Chang T, Asami T, Wang ZY (2008) Chemical genetic dissection of brassinosteroid-ethylene interaction. Molecular Plant 1:368-379.
Goda H, Shimada Y, Asami T, Fujioka S, Yoshida S (2002) Microarray analysis of brassinosteroid-regulated genes in Arabidopsis. Plant Physiology 130:1319-1334.
Jarmuszkiewicz W, Almeida AM, Vercesi AE, Sluse FE, Sluse-Goffart CM (2000) Proton re-uptake partitioning between uncoupling protein and ATP synthase during benzohydroxamic acid-resistant state 3 respiration in tomato fruit mitochondria. Journal of Biological Chemistry 275:13315-13320.
Lalel HJD, Singh Z, Tan SC (2003) Glycosidically-bound aroma volatile compounds in the skin and pulp of 'Kensington Pride' mango fruit at different stages of maturity. Postharvest Biology and Technology 29:205-218.
Manenoi A, Bayogan ERV, Thumdee S, Paull RE (2007) Utility of 1-methylcyclopropene as a papaya postharvest treatment. Postharvest Biology and Technology 44:55-62.
Manenoi A, Paull RE (2007) Papaya fruit softening, endoxylanase gene expression, protein and activity. Physiologia Plantarum 131:470-480.
Martins IS, Carnieri EGS, Vercesi AE (1993) Mechanisms of Ca²⁺ and anion transport across the inner membrane of plant mitochondria. Current Topics in Plant Physiology 1:211-217.
Moller IM, Bérczi A, van der Plas LHW, Lambers H (1988) Measurement of the activity and capacity of the alternative pathway in intact plant tissues: identification of problems and possible solutions. Physiologia Plantarum 72:642-649.
Oliveira JG, Vitoria AP (2011) Papaya: nutritional and pharmacological characterization, and quality loss due to physiological disorders. An overview. Food Research International 44:1306-1313.
Sekimata K, Kimura T, Kaneko I, Nakano T, Yoneyama K, Takeuchi Y, Yoshida S, Asami T (2001) A specific brassinosteroid biosynthesis inhibitor, Brz2001: evaluation of its effects on Arabidopsis, cress, tobacco, and rice. Planta 213:716-721.
Silva MG, Santos EO, Sthel MS, Cardoso SL, Cavalli A, Monteiro AR, Oliveira JG, Pereira MG, Vargas H (2003) Effect of heat treatment on ethylene and CO2 emissions rates during papaya (Carica papaya L.) fruit ripening. Review of Scientific Instruments 74:703-705.
Souza MS, Azevedo IG, Corrêa SF, Silva MG, Pereira MG, Oliveira JG (2009) Responses of 1-MCP applications in 'Golden' papaya fruits on different maturation stages. Revista Brasileira de Fruticultura 31:693-700.
Symons GM, Chua YJ, Ross JJ, Quittenden LJ, Davies NW, Reid JB (2012) Hormonal changes during non-climacteric ripening in strawberry. Journal of Experimental Botany 63:4741-4750.
Tanaka K, Asami T, Yoshida S, Nakamura Y, Matsuo T, Okamoto S (2005) Brassinosteroid homeostasis in Arabidopsis is ensured by feedback expressions of multiple genes involved in its metabolism. Plant Physiology 138:1117-1125.
Vanlerberghe GC (2013) Alternative oxidase: a mitochondrial respiratory pathway to maintain metabolic and signaling homeostasis during abiotic and biotic stress in plants. International Journal of Molecular Sciences 14:6805-6847.
Vardhini BV, Rao SS (2002) Acceleration of ripening of tomato pericarp discs by brassinosteroids. Phytochemistry 16:843-847.
Voesenek LA, Harren FJ, Bögemann GM, Blom CW, Reuss J (1990) Ethylene production and petiole growth in rumex plants induced by soil waterlogging: the application of a continuous flow system and a laser driven intracavity photoacoustic detection system. Plant Physiology 94:1071-1077.
Wills RBH, Widjanarko SB (1995) Changes in physiology, composition and sensory characteristics of Australian papaya during ripening. Australian Journal of Experimental Agriculture 35:1173-1176.
Zaharah SS, Singh Z, Symons GM, Reid JB (2012) Role of brassinosteroids, ethylene, abscisic acid, and indole-3-acetic acid in mango fruit ripening. Journal of Plant Growth Regulation 31:363-372.

Publication Dates

Publication in this collection
08 Nov 2013
Date of issue
2013

History

Received
15 May 2013
Accepted
01 Aug 2013

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

[1] Almeida AM, Jarmuszkiewicz W, Khomsi H, Arruda P, Vercesi AE, Sluse FE (1999) Cyanide-resistant, ATP-synthesis-sustained, and uncoupling-protein-sustained respiration during postharvest ripening of tomato fruit. Plant Physiology 119:1323-1330.

[2] Arteca RN, Arteca JM (2008) Effects of brassinosteroid, auxin, and cytokinin on ethylene production in Arabidopsis thaliana plants. Journal of Experimental Botany 59:3019-3026.

[3] Asami T, Mizutani M, Fujioka S, Goda H, Min YK, Shimada Y, Nakano T, Takatsuto S, Matsuyama T, Nagata N, Sakata K, Yoshida S (2001) Selective interaction of triazole derivatives with DWF4, a cytochrome P450 monooxygenase of the brassinosteroid biosynthetic pathway, correlates with brassinosteroid deficiency in planta. Journal of Biological Chemistry 276:25687-25691.

[4] Asami T, Nakano T, Nakashita H, Sekimata K, Shimada Y, Yoshida S (2003) The influence of chemical genetics on plant science: shedding light on functions and mechanism of action of brassinosteroids using biosynthesis inhibitors. Journal of Plant Growth Regulation 22:336-349.

[5] Beavis AD, Vercesi AE (1992) Anion uniport in plant mitochondria is mediated by a Mg(2+)-insensitive inner membrane anion channel. Journal of Biological Chemistry 267:3079-3087.

[6] Blankenship SM, Dole JM (2003) 1-Methylcyclopropene: a review. Postharvest Biology and Technology 28:1-25.

[7] Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72:248-254.

[8] Bron IU, Jacomino AP (2006) Ripening and quality of 'Golden' papaya fruit harvested at different maturity stages. Brazilian Journal of Plant Physiology 18:389-396.

[9] Calegario FF, Cosso RG, Fagian MM, Almeida FV, Jardim WF, Jezek P, Arruda P, Vercesi AE (2003) Stimulation of potato tuber respiration by cold stress is associated with an increased capacity of both plant uncoupling mitochondrial protein (PUMP) and alternative oxidase. Journal of Bioenergetics and Biomembranes 35:211-220.

[10] Carré JE, Affourtit C, Moore AL (2011) Interaction of purified alternative oxidase from thermogenic Arum maculatum with pyruvate. FEBS Letters 585:397-401.

[11] Considine MJ, Daley DO, Whelan J (2001) The expression of alternative oxidase and uncoupling protein during fruit ripening in mango. Plant Physiology 126:1619-1629.

[12] De Grauwe L, Vandenbussche F, Tietz O, Palme K, Van Der Straeten D (2005) Auxin, ethylene and brassinosteroids: tripartite control of growth in the Arabidopsis hypocotyl. Plant and Cell Physiology 46:827-836.

[13] Deslauriers SD, Larsen PB (2010) FERONIA is a key modulator of brassinosteroid and ethylene responsiveness in Arabidopsis hypocotyls. Molecular Plant 3:626-640.

[14] Duque P, Arrabaça JD (1999) Respiratory metabolism during cold storage of apple fruit. II. Alternative oxidase is induced at the climacteric. Physiologia Plantarum 107:24-31.

[15] Fabi JP, Mendes LRBC, Lajolo FM, Nascimento JRO (2010) Transcript profiling of papaya fruit reveals differentially expressed genes associated with fruit ripening. Plant Science 179:225-233.

[16] Fabi JP, Cordenunsi BR, de Mattos Barreto GP, Mercadante AZ, Lajolo FM, Oliveira do Nascimento JR (2007) Papaya fruit ripening: response to ethylene and 1-methylcyclopropene (1-MCP). Journal of Agricultural and Food Chemistry 55:6118-6123.

[17] Fu FQ, Mao WH, Shi K, Zhou YH, Asami T, Yu JQ (2008) A role of brassinosteroids in early fruit development in cucumber. Journal of Experimental Botany 59:2299-2308.

[18] Gendron JM, Haque A, Gendron N, Chang T, Asami T, Wang ZY (2008) Chemical genetic dissection of brassinosteroid-ethylene interaction. Molecular Plant 1:368-379.

[19] Goda H, Shimada Y, Asami T, Fujioka S, Yoshida S (2002) Microarray analysis of brassinosteroid-regulated genes in Arabidopsis. Plant Physiology 130:1319-1334.

[20] Jarmuszkiewicz W, Almeida AM, Vercesi AE, Sluse FE, Sluse-Goffart CM (2000) Proton re-uptake partitioning between uncoupling protein and ATP synthase during benzohydroxamic acid-resistant state 3 respiration in tomato fruit mitochondria. Journal of Biological Chemistry 275:13315-13320.

[21] Lalel HJD, Singh Z, Tan SC (2003) Glycosidically-bound aroma volatile compounds in the skin and pulp of 'Kensington Pride' mango fruit at different stages of maturity. Postharvest Biology and Technology 29:205-218.

[22] Manenoi A, Bayogan ERV, Thumdee S, Paull RE (2007) Utility of 1-methylcyclopropene as a papaya postharvest treatment. Postharvest Biology and Technology 44:55-62.

[23] Manenoi A, Paull RE (2007) Papaya fruit softening, endoxylanase gene expression, protein and activity. Physiologia Plantarum 131:470-480.

[24] Martins IS, Carnieri EGS, Vercesi AE (1993) Mechanisms of Ca²⁺ and anion transport across the inner membrane of plant mitochondria. Current Topics in Plant Physiology 1:211-217.

[25] Moller IM, Bérczi A, van der Plas LHW, Lambers H (1988) Measurement of the activity and capacity of the alternative pathway in intact plant tissues: identification of problems and possible solutions. Physiologia Plantarum 72:642-649.

[26] Oliveira JG, Vitoria AP (2011) Papaya: nutritional and pharmacological characterization, and quality loss due to physiological disorders. An overview. Food Research International 44:1306-1313.

[27] Sekimata K, Kimura T, Kaneko I, Nakano T, Yoneyama K, Takeuchi Y, Yoshida S, Asami T (2001) A specific brassinosteroid biosynthesis inhibitor, Brz2001: evaluation of its effects on Arabidopsis, cress, tobacco, and rice. Planta 213:716-721.

[28] Silva MG, Santos EO, Sthel MS, Cardoso SL, Cavalli A, Monteiro AR, Oliveira JG, Pereira MG, Vargas H (2003) Effect of heat treatment on ethylene and CO2 emissions rates during papaya (Carica papaya L.) fruit ripening. Review of Scientific Instruments 74:703-705.

[29] Souza MS, Azevedo IG, Corrêa SF, Silva MG, Pereira MG, Oliveira JG (2009) Responses of 1-MCP applications in 'Golden' papaya fruits on different maturation stages. Revista Brasileira de Fruticultura 31:693-700.

[30] Symons GM, Chua YJ, Ross JJ, Quittenden LJ, Davies NW, Reid JB (2012) Hormonal changes during non-climacteric ripening in strawberry. Journal of Experimental Botany 63:4741-4750.

[31] Tanaka K, Asami T, Yoshida S, Nakamura Y, Matsuo T, Okamoto S (2005) Brassinosteroid homeostasis in Arabidopsis is ensured by feedback expressions of multiple genes involved in its metabolism. Plant Physiology 138:1117-1125.

[32] Vanlerberghe GC (2013) Alternative oxidase: a mitochondrial respiratory pathway to maintain metabolic and signaling homeostasis during abiotic and biotic stress in plants. International Journal of Molecular Sciences 14:6805-6847.

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

[34] Voesenek LA, Harren FJ, Bögemann GM, Blom CW, Reuss J (1990) Ethylene production and petiole growth in rumex plants induced by soil waterlogging: the application of a continuous flow system and a laser driven intracavity photoacoustic detection system. Plant Physiology 94:1071-1077.

[35] Wills RBH, Widjanarko SB (1995) Changes in physiology, composition and sensory characteristics of Australian papaya during ripening. Australian Journal of Experimental Agriculture 35:1173-1176.

[36] Zaharah SS, Singh Z, Symons GM, Reid JB (2012) Role of brassinosteroids, ethylene, abscisic acid, and indole-3-acetic acid in mango fruit ripening. Journal of Plant Growth Regulation 31:363-372.