Seasonal changes in fructan accumulation in the underground organs of Gomphrena marginata Seub. (Amaranthaceae) under rock-field conditions

Silva, Fernanda Gomes da; Cangussu, Lílian Mendes Borburema; Paula, Sandro Lânio Abreu de; Melo, Geraldo Aclécio; Silva, Emerson Alves

Abstract

Rock field plant species present several adaptations to the climatic characteristics and seasonality of this habitat. In this study, we evaluate under field conditions the seasonal changes in non-structural carbohydrate accumulation in tuberous organs of Gomphrena marginata. Tuber fragments of plants of G. marginata were sampled monthly for a year (August 2010 to July 2011) in a rock-field area in southeastern Brazil. Quantitative analyses of total fructose, fructo-oligosaccharides, fructo-polysaccharides, reducing sugars and free proline were carried out. Qualitative analyses of carbohydrates were also performed by thin layer chromatography (TLC) and high performance anion exchange chromatography (HPAEC/PAD). Soil moisture was evaluated by gravimetry and plant water status was evaluated by measuring the relative water content (RWC) and water potential (Ψw) of underground organs. Throughout the analyzed period, a well-marked seasonality of fructan accumulation was observed in tuberous roots of G. marginata correlating significantly with seasonal changes in soil water availability. In the rainy period (October to February), the content of fructo-polysaccharides decrease while during the dry and quiescent growth period (April to September) a high accumulation of fructo-polysaccharides was observed without changes in the RWC of tuberous roots, suggesting that cell osmoregulation contributed to water status maintenance in G. marginata. Our study presents a second species of Amaranthaceae that accumulates fructans as its main reserve carbohydrate, which can be an important strategy for survival in an environment characterized by a long dry period.

fructans; osmoregulation; seasonality

Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant and Soil 39:205-207.
Blake GR (1965) Bulk density. In: Black CA, Evans DD, White JL, Ensminger LE, Clark FE (eds.). Methods of soil analysis, p. 374-390. American Society of Agronomy, Madison.
Carvalho MAM, Dietrich SMC (1993) Variation in fructan content in the undergound organs of Vernonia herbacea (Vell.) Rusby at different phenological phases. New Phytologist 123:735-740.
Carvalho MAM, Pinto MM, Figueiredo-Ribeiro RCL (1998) Inulin production by Vernonia herbacea as influenced by mineral fertilization and time of harvest. Revista Brasileira de Botânica 21:281-285.
Carvalho MAM, Zaidan LBP, Dietrich SMC (1997) Growth and fructan contents in plants of Vernonia herbacea (Asteraceae) regenerated from rhizophores. New Phytologist 136:153-161.
Chaves-Filho JT, Stacciarini-Seraphin E (2001) Alteração no potencial osmótico e teor de carboidratos solúveis em plantas jovens de lobeira (Solanum lycocarpum St.-Hil.) em resposta ao estresse hídrico. Revista Brasileira de Botânica 24:199-204.
Coutinho LM (2002) Eugen Warming e o Cerrado brasileiro: um século depois. In: Klein AL (org), p. 77-91. UNESP, Imprensa Oficial do Estado de São Paulo, São Paulo.
Dias-Tagliacozzo GM (1995) Frutanos de Vernonia herbaceae (Vell) Rusby: Variações em função da temperatura e da disponibilidade de água. Tese de doutorado. Universidade Estadual de Campinas, Campinas.
Dias-Tagliacozzo GM, Itaya NM, Carvalho MAM, Figueiredo-Ribeiro RCL, Dietrich SMC (2004) Fructans and water suppression on intact and fragmented rhizophores of Vernonia herbacea Brazilian Archives of Biology and Technology 47:363-373.
Edelman J, Jefford TG (1968) The mechanism of fructosan metabolism in higher plants as exemplified in Helianthus tuberosus New Phytologist 67:517-531.
Figueiredo-Ribeiro RCL (1993) Distribuição, aspectos estruturais e funcionais dos frutanos, com ênfase em plantas herbáceas do cerrado. Revista Brasileira de Fisiologia Vegetal 5:203-208.
Garcia PMA (2009) Variações no metabolismo de frutanos em Vernonia herbacea (Vell) Rusby (Asteraceae) em resposta ao déficit hídrico e sua relação com a tolerância à seca. Dissertação de mestrado. Instituto de Botânica da Secretaria do Meio Ambiente de São Paulo, São Paulo.
Garcia PMA, Asega AF, Silva EA, Carvalho, MAM (2011) Effect of drought and re-watering on fructan metabolism in Vernonia herbaceae (Vell.) Rusby. Plant Physiology and Biochemistry 49:664-670.
Hendry GAF, Wallace RK (1993) The origin, distribution and evolutionary significance of fructans. In: Suzuki M, Chatterton JN (eds). Science and Technology of Fructan, CRC Press, Boca Raton.
Hu CA, Lin WW, Valle D (1996) Cloning, characterization and expression of cDNAs encoding human D1-pyrroline-5-carboxylate dehydrogenase. The Journal of Biological Chemistry. 271:9795-9800.
Isejima EM, Figueiredo-Ribeiro RCL (1993) Fructan variations in tuberous roots of Viguiera discolor Baker (Asteraceae): the influence of phenology. Plant and Cell Physiology 34:723-727.
Jermyn MA (1956) A new method for determination of ketohexoses in presence of aldohexoses. Nature 177:38-39.
Maggio A, Miyazaki S, Veronese P, Fujita T, Ibeas JI, Damsz B, Narasimhan ML, Hasegawa PM, Joly RJ, Bressan RA (2002) Does proline accumulation play a active role in stress-induced growth reduction? The Plant Journal 31:699-712.
Mantovani W, Martins FR (1988) Variações fenológicas das espécies do cerrado da Reserva Biológica de Moji-Guaçú, Estado de São Paulo. Revista Brasileira de Botânica 11:101-112.
McCree KJ, Fernández CJ (1989) Simulation model for studying physiological water stress responses of whole plants. Crop Science 29:353-360.
Miller, GL (1959) Use of dinitrosalicylle acid for determination of reducing sugar. Analytcal Chemistry 11:426-428.
Paiva R, Oliveira LM (2006) Fisiologia e Produção Vegetal. UFLA, Lavras.
Phang JM (1985) The regulatory functions of proline and pyrroline-5-carboxilic acid. Current Topics in Cellular Regulation 25:92-132.
Pollock CJ, Cairns AJ, Sims IM, Housley TL (1996) Fructans as reserve carbohydrates in crop plants. In: Zamski E, Shaffer AA (eds) Photoassimilate distribution in plants and crops: source - sink relationships, p. 97-113. Marcel Dekker, New York.
Pollock CJ, Chatterton NJ (1988) Fructans. In: Preiss J (ed) The biochemistry of plants: a comprehensive treatise, p.109-140. Academic Press, New York.
Pollock CJ, Jones T (1979) Seasonal patterns of fructan metabolism in forage grasses. New Phytologist 83:9-15.
Ribeiro JF, Walter BMT (1988) Fitofisionomias do Bioma Cerrado. In: Sano SM, Almeida SP (org.). Cerrado: ambiente e flora. Planaltina, Embrapa-CPAC, p.89-166.
Ritsema T, Smeekens S (2003) Engineering fructan metabolism in plants. Journal of Plant Physiology 160:811-820.
Sharma P, Dubey RS (2005) Modulation of nitrate reductase activity in rice seedlings under aluminium toxicity and water stress: role of osmolytes as enzyme protectant. Journal of Plant Physiology 162:854-862.
Siqueira JC (1991) O gênero Gomphrena L. (Amaranthaceae) no Brasil. Tese de doutorado. Universidade Estadual de Campinas, Campinas-SP.
Spollen WG, Nelson CJ (1994) Response of fructan to water deficit in growing leaves of tall fescue. Plant Physiology 106:329-336.
Taiz L, Zeiger E (2010) Plant Physiol, 5^th edn. Sinauer Associates, Sunderland.
Tertuliano MF, Figueiredo-Ribeiro RCL (1993) Distribution of fructose polymers in herbaceous species of Asteraceae from the cerrado. New Phytologist 123:741-749.
Valliyodan B, Nguyen HT (2006) Understanding regulatory networks and engineering for enhanced drought tolerance in plants. Current Opinion in Plant Biology 9:1-7.
Vieira CC, Figueiredo-Ribeiro RCL (1993) Fructose-containing carbohydrates in the tuberous root of Gomphrena macrocephala St. Hil. (Amaranthaceae) at different phenological phases. Plant, Cell and Environment 16:919-928.
Weatherley PE (1950) Studies in the water relations of cotton plant. I. The field measurement of water deficits in leaves. New Phytologist 49:81-97.
Wise CS, Dimler RJ, Davis HA, Rist CE (1955) Determination of easily hydrolysable fructose units in dextran preparation. Analytical Chemistry 27:33-36.

Publication Dates

Publication in this collection
23 June 2015
Date of issue
2013

History

Received
12 Mar 2013
Accepted
16 Mar 2013

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

[1] Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant and Soil 39:205-207.

[2] Blake GR (1965) Bulk density. In: Black CA, Evans DD, White JL, Ensminger LE, Clark FE (eds.). Methods of soil analysis, p. 374-390. American Society of Agronomy, Madison.

[3] Carvalho MAM, Dietrich SMC (1993) Variation in fructan content in the undergound organs of Vernonia herbacea (Vell.) Rusby at different phenological phases. New Phytologist 123:735-740.

[4] Carvalho MAM, Pinto MM, Figueiredo-Ribeiro RCL (1998) Inulin production by Vernonia herbacea as influenced by mineral fertilization and time of harvest. Revista Brasileira de Botânica 21:281-285.

[5] Carvalho MAM, Zaidan LBP, Dietrich SMC (1997) Growth and fructan contents in plants of Vernonia herbacea (Asteraceae) regenerated from rhizophores. New Phytologist 136:153-161.

[6] Chaves-Filho JT, Stacciarini-Seraphin E (2001) Alteração no potencial osmótico e teor de carboidratos solúveis em plantas jovens de lobeira (Solanum lycocarpum St.-Hil.) em resposta ao estresse hídrico. Revista Brasileira de Botânica 24:199-204.

[7] Coutinho LM (2002) Eugen Warming e o Cerrado brasileiro: um século depois. In: Klein AL (org), p. 77-91. UNESP, Imprensa Oficial do Estado de São Paulo, São Paulo.

[8] Dias-Tagliacozzo GM (1995) Frutanos de Vernonia herbaceae (Vell) Rusby: Variações em função da temperatura e da disponibilidade de água. Tese de doutorado. Universidade Estadual de Campinas, Campinas.

[9] Dias-Tagliacozzo GM, Itaya NM, Carvalho MAM, Figueiredo-Ribeiro RCL, Dietrich SMC (2004) Fructans and water suppression on intact and fragmented rhizophores of Vernonia herbacea Brazilian Archives of Biology and Technology 47:363-373.

[10] Edelman J, Jefford TG (1968) The mechanism of fructosan metabolism in higher plants as exemplified in Helianthus tuberosus New Phytologist 67:517-531.

[11] Figueiredo-Ribeiro RCL (1993) Distribuição, aspectos estruturais e funcionais dos frutanos, com ênfase em plantas herbáceas do cerrado. Revista Brasileira de Fisiologia Vegetal 5:203-208.

[12] Garcia PMA (2009) Variações no metabolismo de frutanos em Vernonia herbacea (Vell) Rusby (Asteraceae) em resposta ao déficit hídrico e sua relação com a tolerância à seca. Dissertação de mestrado. Instituto de Botânica da Secretaria do Meio Ambiente de São Paulo, São Paulo.

[13] Garcia PMA, Asega AF, Silva EA, Carvalho, MAM (2011) Effect of drought and re-watering on fructan metabolism in Vernonia herbaceae (Vell.) Rusby. Plant Physiology and Biochemistry 49:664-670.

[14] Hendry GAF, Wallace RK (1993) The origin, distribution and evolutionary significance of fructans. In: Suzuki M, Chatterton JN (eds). Science and Technology of Fructan, CRC Press, Boca Raton.

[15] Hu CA, Lin WW, Valle D (1996) Cloning, characterization and expression of cDNAs encoding human D1-pyrroline-5-carboxylate dehydrogenase. The Journal of Biological Chemistry. 271:9795-9800.

[16] Isejima EM, Figueiredo-Ribeiro RCL (1993) Fructan variations in tuberous roots of Viguiera discolor Baker (Asteraceae): the influence of phenology. Plant and Cell Physiology 34:723-727.

[17] Jermyn MA (1956) A new method for determination of ketohexoses in presence of aldohexoses. Nature 177:38-39.

[18] Maggio A, Miyazaki S, Veronese P, Fujita T, Ibeas JI, Damsz B, Narasimhan ML, Hasegawa PM, Joly RJ, Bressan RA (2002) Does proline accumulation play a active role in stress-induced growth reduction? The Plant Journal 31:699-712.

[19] Mantovani W, Martins FR (1988) Variações fenológicas das espécies do cerrado da Reserva Biológica de Moji-Guaçú, Estado de São Paulo. Revista Brasileira de Botânica 11:101-112.

[20] McCree KJ, Fernández CJ (1989) Simulation model for studying physiological water stress responses of whole plants. Crop Science 29:353-360.

[21] Miller, GL (1959) Use of dinitrosalicylle acid for determination of reducing sugar. Analytcal Chemistry 11:426-428.

[22] Paiva R, Oliveira LM (2006) Fisiologia e Produção Vegetal. UFLA, Lavras.

[23] Phang JM (1985) The regulatory functions of proline and pyrroline-5-carboxilic acid. Current Topics in Cellular Regulation 25:92-132.

[24] Pollock CJ, Cairns AJ, Sims IM, Housley TL (1996) Fructans as reserve carbohydrates in crop plants. In: Zamski E, Shaffer AA (eds) Photoassimilate distribution in plants and crops: source - sink relationships, p. 97-113. Marcel Dekker, New York.

[25] Pollock CJ, Chatterton NJ (1988) Fructans. In: Preiss J (ed) The biochemistry of plants: a comprehensive treatise, p.109-140. Academic Press, New York.

[26] Pollock CJ, Jones T (1979) Seasonal patterns of fructan metabolism in forage grasses. New Phytologist 83:9-15.

[27] Ribeiro JF, Walter BMT (1988) Fitofisionomias do Bioma Cerrado. In: Sano SM, Almeida SP (org.). Cerrado: ambiente e flora. Planaltina, Embrapa-CPAC, p.89-166.

[28] Ritsema T, Smeekens S (2003) Engineering fructan metabolism in plants. Journal of Plant Physiology 160:811-820.

[29] Sharma P, Dubey RS (2005) Modulation of nitrate reductase activity in rice seedlings under aluminium toxicity and water stress: role of osmolytes as enzyme protectant. Journal of Plant Physiology 162:854-862.

[30] Siqueira JC (1991) O gênero Gomphrena L. (Amaranthaceae) no Brasil. Tese de doutorado. Universidade Estadual de Campinas, Campinas-SP.

[31] Spollen WG, Nelson CJ (1994) Response of fructan to water deficit in growing leaves of tall fescue. Plant Physiology 106:329-336.

[32] Taiz L, Zeiger E (2010) Plant Physiol, 5^th edn. Sinauer Associates, Sunderland.

[33] Tertuliano MF, Figueiredo-Ribeiro RCL (1993) Distribution of fructose polymers in herbaceous species of Asteraceae from the cerrado. New Phytologist 123:741-749.

[34] Valliyodan B, Nguyen HT (2006) Understanding regulatory networks and engineering for enhanced drought tolerance in plants. Current Opinion in Plant Biology 9:1-7.

[35] Vieira CC, Figueiredo-Ribeiro RCL (1993) Fructose-containing carbohydrates in the tuberous root of Gomphrena macrocephala St. Hil. (Amaranthaceae) at different phenological phases. Plant, Cell and Environment 16:919-928.

[36] Weatherley PE (1950) Studies in the water relations of cotton plant. I. The field measurement of water deficits in leaves. New Phytologist 49:81-97.

[37] Wise CS, Dimler RJ, Davis HA, Rist CE (1955) Determination of easily hydrolysable fructose units in dextran preparation. Analytical Chemistry 27:33-36.

Brasil

Brasil

Seasonal changes in fructan accumulation in the underground organs of Gomphrena marginata Seub. (Amaranthaceae) under rock-field conditions

Abstract

Publication Dates

History