Enhanced Sensitivity to Ethylene in Nitrogen- or Phosphate-Starved Roots of Zea mays L. during Aerenchyma Formation

Abstract

Adventitious roots of maize (Zea mays L. cv TX 5855), grown in a well-oxygenated nutrient solution, were induced to form cortical gas spaces (aerenchyma) by temporarily omitting nitrate and ammonium (-N), or phosphate (-P), from the solution. Previously this response was shown (MC Drew, CJ He, PW Morgan [1989] Plant Physiology 91: 266-271) to be associated with a slower rate of ethylene biosynthesis, contrasting with the induction of aerenchyma by hypoxia during which ethylene production is strongly stimulated. In the present paper, we show that aerenchyma formafion induced by nutrient starvation was blocked, under noninjurious conditions, by addition of low concentrations of Ag+, an inhibitor of ethylene action, or of aminoethoxyvinyl glycine, an inhibitor of ethylene biosynthesis. When extending roots were exposed to low concentrations of ethylene in air sparged through the nutrient solution, N or P starvation enhanced the sensitivity to exogenous ethylene at concentrations as low as 0.05 microliters ethylene per liter air, promoting a more rapid and extensive formation of aerenchyma than in unstarved roots. We conclude that temporary deprivation of N or P enhances the sensitivity of ethylene-responsive cells of the root cortex, leading to cell lysis and aerenchyma.The roots of many plant species, especially those well adapted to wetland conditions, respond to inadequate oxygenation of their environment by formation of aerenchyma (16,17). In maize, lysigenous aerenchyma can form in young seminal (18) as well as nodal (adventitious) roots (11,12) when they extend under conditions of hypoxia into nutrient solution that is partially oxygen deficient. Aerenchyma, comprising an interconnected series ofgas-filled cavities or lacunae (1 1), improves the internal aeration of the roots (13). At an early stage in aerenchyma formation, cells of the root cortex, located about 10 mm behind the apex, undergo premature lysis and disintegration to form lacunae (7). Hypoxia stimulates ethylene biosynthesis, and the increase in internal ethylene concentration is closely associated with induction of cell lysis and aerenchyma formation (1,11 (10,19). In an earlierpaper, we examined cell lysis and ethylene biosynthesis in the root tip of maize during temporary deficiency of N or P and compared the responses to those induced by hypoxia (10). We found that temporary shortage of these nutrients consistently inhibited the rate of ethylene production of the excised tips to only one-half to one-third that of unstarved controls. The activity of ACC3 synthase and the ACC concentration were likewise depressed by N or P starvation. Induction of cell lysis by nutrient starvation, unlike hypoxia, was thus not related to a greater endogenous concentration of ethylene.In the present study, we used inhibitors of ethylene biosynthesis and ethylene action to determine whether ethylene is associated with the onset of cell lysis in nutrient-deprived roots. We also examined the response of such roots to exogenous ethylene. We show that nutr...

Induction of Enzymes Associated with Lysigenous Aerenchyma Formation in Roots of Zea mays during Hypoxia or Nitrogen Starvation

“…temporary deprivation of N or P does not stimulate the ethybene biosynthetic pathway (Figs. 5 and 6; see also Drew et al, 1989) but greatly enhances the sensitivity of ethylene-responsive cells of the root cortex, leading to cell lysis and a.erenchyma formation (He et al, 1992). The present resulls implicate ethylene in the induction of cellulase activity, w e n under conditioins where ethylene biosynthesis is slowed.…”

“…90-37264-5523. * Corresponding author; fax 1-409-845-0627. 861 depresses it (Drew et al, 1989); instead, they strongly enhanced the sensitivity of cortical cells to ethylene, causing a more rapid lysis of cells in the presence of very low concentrations of the gas (He et al, 1992). As with hypoxia, inhibitors of ethylene-mediated responses (Ag' or AVG) block aerenchyma formation in roots growing in N-or P-deficient solution, suggesting that ethylene is involved in aerenchyma formation under these conditions as well (He et al, 1992).…”

Respostas morfológicas em Guibourtia hymenifolia (Moric.) J. Leonard (Fabaceae) e Genipa americana L. (Rubiaceae), submetidas ao estresse por deficiência nutricional e alagamento do substrato

“…He et al (1992) também verificaram a influência do estado nutricional sobre as respostas morfo-anatômicas em raízes de milho. Kolb et al (1998) estudando as respostas de Sebastiania commersoniana (Baillon) Smith & Downs, ao alagamento, verificaram maior conteúdo de amido nas células parenquimáticas corticais nas plantas controle em relação às plantas mantidas alagadas por 60 dias.…”

“…He et al (1992) verificaram que a deficiência temporária de nitrogênio e fósforo em plantas de milho alagada, aumenta a sensibilidade de tecidos da raíz ao etileno exógeno promovendo a lise celular e formação de aerênquima. Já Santiago & Paoli (2003) estudando as respostas de Adelia membranifolia (Müll.…”

Hormone sensitivity and plant adaptations to flooding

“…In these three plant species, ethylene sensitizes the tissue to gibberellin (MuSGRAVEet al 1972, Musgrave & W alters 1973, Raskin & Kende 1984a. Another example of the importance of shifts in hormone sensitivity is the increase in sensitivity to ethylene of N or P starved roots of Zea mays L. Deprivation of N and P enhances the sensitivity of ethylene-responsive cells of the root cortex, leading to aerenchyma formation (He et al 1992).…”