The metabolic response of plants to oxygen deficiency

OXYGEN DEFICIENCY IN PLANTS M I N I R E V I E83W The metabolic response of plants to oxygen deficiency Carlos Antônio Ferreira de Sousa1,* and Ladaslav Sodek2 1 Empresa Brasileira de Pesquisa Agropecuária - Embrapa Meio-Norte, Av. Duque de Caxias, 5650, Bairro Buenos Aires, C P 01, 64006-220, Teresina, PI, Brasil; 2 Departamento de Fisiologia Vegetal, Instituto de Biologia, CP 6109, Unicamp, 13083-970, Campinas, SP, Brasil; * Corresponding author: Received: 01/08/2002, Accepted: 02/09/2002 Plants, under natural or experimental conditions, can be subject to a range of O2 concentrations from normal (normoxia) through deficient (hypoxia) to total absence (anoxia). Many metabolic processes are affected by O2 deficiency but the most studied events are those related to respiration and metabolism of N. In the absence of a terminal electron acceptor for the electron transport chain, the tricarboxylic acid cycle functions only partially and in both directions. Acidification of the cytosol occurs and pyruvate, the product of glycolysis, is transformed to lactate and ethanol, which represent the main fermentation reactions in plants. Alanine is the third most important product of anaerobic metabolism, resulting from high rates of amino acid interconversion in which transaminases such as alanine aminotransferase play an important role. The role of alanine accumulation under anaerobiosis is not clear and appears to be independent of the source of N whether NO3-, NH4+ or N2. How nitrate exerts its beneficial effect on tolerance of root hypoxia in waterlogged plants is still not clearly understood. Such aspects of N metabolism pose interesting challenges for future research on metabolic responses of plants to oxygen deficiency. Key words: anoxia, hypoxia, N metabolism, fermentation products. Respostas metabólicas de plantas à deficiência de oxigênio: As plantas, em condições naturais ou experimentais, podem ser submetidas à disponibilidade de O2 que varia desde os teores normais (normoxia), passando pela deficiência (hipoxia) ou até mesmo pela ausência (anoxia). Vários processos metabólicos são afetados pela deficiência de O2, porém os eventos mais estudados são aqueles relacionados à respiração e ao metabolismo de N. Na ausência de um aceptor eletrônico terminal na cadeia de transporte de életrons, o ciclo do ácido tricarboxílico passa a funcionar parcialmente e em ambas as direções. Ocorre a acidificação do citosol e o piruvato, produto da glicólise, é transformado em lactato e etanol, que representam as principais reações fermentativas das plantas. A alanina é o terceiro mais importante produto do metabolismo anaeróbico, sendo resultante de altas taxas de interconversão entre os aminoácidos em que as transaminases, tais como alanina aminotransferase, desempenham um papel importante. O acúmulo de alanina sob anaerobiose parece ser independente da fonte de N: NO3-, NH4+ ou N2 e o seu papel precisa ser esclarecido. Da mesma forma, ainda não está completamente entendido como o NO3- exerce seu efeito benéfico sobre a tolerância radicular à hipoxia em plantas encharcadas. Tais aspectos do metabolismo de N colocam desafios interessantes para as futuras pesquisas sobre as respostas das plantas à deficiência de oxigênio. Palavras-chave: hipoxia, anoxia, metabolismo de N, produtos da fermentação. Abbreviations: ADH (alcohol dehydrogenase); AlaAT (alanine aminotransferase); AspAT (aspartate aminotransferase); ANPs (anaerobic proteins); OAA (oxaloacetic acid); OAA-DC (oxaloacetic acid decarboxylase); ETC (electron transport chain); GabaOT (Gaba oxoglutarate transaminase); Gaba-PT (Gaba pyruvate transaminase); GS/GOGAT (glutamine synthetase/glutamine oxoglutarate amidotransferase); GluDC (glutamate decarboxylase); LDH (lactate dehydrogenase); NTP (nucleotide triphosphate); PAGE (polyacrylamide-gel electrophoresis); PDC (pyruvate decarbolylase); NR/NiR (nitrate/nitrite reductase); TCA cycle (tricarboxylic acid cycle); 2OG (2-oxoglutarate). Braz. J. Plant Physiol., 14(2):83-94, 2002 84 C.A.F. SOUSA AND L. SODEK INTRODUCTION Oxygen is indispensable to higher plants for metabolism and growth. However, under natural or experimental conditions plants can be subjected to a great range of oxygen availability, from normal levels (normoxia) through deficiency (hypoxia) to total absence (anoxia). According to Drew (1997), normoxia prevails when oxygen supply does not limit oxidative phosphorylation. For hypoxia, the partial pressure of oxygen is low enough to limit the production of ATP by mitochondria whereas anoxia is attained when the mitochondrial production of ATP is insignificant compared to that generated by glycolysis and fermentation. Oxygen deficiency of root systems occurs frequently in nature (Kennedy et al., 1992) affecting the majority of plants at some time during their life cycle (Jackson et al., 1982). In the field, roots can be subject to oxygen deficiency soon after strong rainfall, since the soil usually becomes flooded for a short or longer period depending on its drainage capacity (Huang et al., 1994a). In other situations, oxygen deficiency can occur due to the anatomical structure of some tissues that impede gas exchange (Thompson and Greenway, 1991; Perata and Alpi, 1993). Nevertheless the majority of plant tissues can tolerate oxygen deficiency for short periods before suffering irreversible damage (Kennedy et al., 1992). Plants whose root system is flooded can undergo morphological and anatomical changes that enhance gas exchange in an attempt to avoid or minimize oxygen deficiency (Perata and Alpi, 1993). In order to tolerate hypoxic stress, they may further undergo biochemical and metabolic changes. This review will focus on the more important biochemical and metabolic changes relating to the products of fermentation and the N pool together with special emphasis on alanine accumulation and the importance of nitrate in counteracting the adverse effects of oxygen deficiency. Metabolic events affected by oxygen deficiency Oxygen deficiency in plants, brought about by waterlogging of the root system is a very common event in nature. Its consequences vary from the increase in biomass of the shoot in relation to the root (BarrettLennard et al., 1988; Huang and Johnson, 1995) to the loss of plants, due to seasonal flooding (Kennedy et al., Braz. J. Plant Physiol., 14(2):83-94, 2002 1992). The relative reduction in root biomass and the shift in allocation of metabolites to the shoot during flooding are probably the result of a metabolic adaptation aimed at diminishing the demand for oxygen by the root system (Naidoo and Naidoo, 1992; Huang et al., 1994b). Reduction in photosynthetic activity is another consequence of waterlogging and can be attributed to several factors: lower water potential and stomatal conductance; lower activities of photosynthetic enzymes; impaired transport of photoassimilates due to lower sink activity; and lower chlorophyll content (Huang et al (...truncated)