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Plant Physiology and Plant Molecular Biology 44, 283-307

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Plant Physiology and Plant Molecular Biology 44, 283-307 PDF hosted at the Radboud Repository of the Radboud University Nijmegen The following full text is a publisher's version. For additional information about this publication click this link. http://hdl.handle.net/2066/15945 Please be advised that this information was generated on 2021-10-10 and may be subject to change. Plant, Cell and Environment (1996) 19, 1423-1430 Sensitivity to ethylene: the key factor in submergence-induced shoot elongation of Rumex M. BANGA, C.W.P.M. BLOM & L.A.C.J. VOESENEK Department of Ecology, University of Nijmegen, Toernooiveld, 6525 ED Nijmegen, the Netherlands ABSTRACT such as Callitriche plcitycarpa (Musgrave, Jackson & Ling 1972), Ranunculus sceleratus (Musgrave & Walters 1973), Rosettes of flooding-resistant Rumex palustris plants show Oryzci scitiva (Metraux & Kende 1983), Nymphoides a submergence-induced stimulation of elongation, which is peltatci (Ridge & Amarasinghe 1984) and Rumexpalustris confined to the petioles of young leaves. This response (Voesenek & Bloin 1989b). Unlike most terrestrial plants, increases the probability of survival. It is induced by ethy­ amphibians can survive short periods of submergence lene that accumulates in submerged tissues. Flooding- although they need to protrude above the water surface for intolerant Rumex acetosella plants do not show this longer-term survival and reproduction (Ridge 1987). Since response. We investigated whether differences in shoot most plants continuously produce small amounts of ethy­ elongation between the species, between old and young lene, submergence leads to accumulation by physical leaves and between the petiole and leaf blade of a R. palus­ entrapment by the surrounding water (Musgrave et al. tris plant result from differences in internal ethylene con­ 1972; Voesenek et al. 1993). In submerged amphibious centration or in sensitivity to the gas. Concentrations of plants, this entrapped ethylene enhances shoot elongation free and con jugated ACC in petioles and leaf blades of R. which restores leaf-air contact. This is an important mech­ palustris indicated that ethylene is synthesized throughout anism to increase the chances of survival (Laan & Blom the submerged shoot, although production rates varied 1990; van der Sman et al. 1991). locally. Nevertheless, no differences in ethylene concentra­ Species of the genus Rumex form a gradient from strictly tion were found between submerged leaves of various terrestrial to amphibious, ranging from R. acetosella, ages. In contrast, dose-response curves showed that only which grows on dry sandy soils, to R. palustris, a species elongation of young petioles of R. palustris was sensitive to from frequently Hooded mud-flats along the riverside ethylene. In R. acetosella, elongation of all leaves was (Blom et al. 1994). In vegetative rosettes of flooding-resis­ insensitive to ethylene. We conclude that variation in ethy­ tant R. palustris, submergence stimulates shoot elongation. lene sensitivity rather than content explains the differ­ This response is stronger in younger leaves, particularly ences in submergence-induced shoot elongation between the petioles (Voesenek & Blom I989a,b; Banga, Blom & the two Rumex species and between leaves of R. palustris. Voesenek 1995). In rosettes of flooding-intolerant R. ace­ tosella, which are never flooded under natural conditions, Key-words: Rumex palustris; Rumex acetosella; Polygonaceae; leaf elongation is neither stimulated nor inhibited when docks; ethylene sensitivity; shoot elongation; submergence. plants are submerged in the laboratory ( Banga et al. 1995). Submerged R. palustris and R. acetosella plants accu­ INTRODUCTION mulate ethylene to similar levels (Blom et al. 1994). Moreover, large variations in the ethylene concentration The gaseous hormone ethylene plays many roles during between leaves of various ages or between leaf blades and plant development. For example, seedlings of many dicots petioles of R. palustris are unlikely, since this species are able to penetrate compacted soil more readily as a probably possesses an internal interconnected gas-space result of the so-called ‘triple response’ to ethylene, which system. Only if ethylene production rates varied strongly is a combination of radial expansion and inhibition of elon­ between shoot organs would some variation in the ethylene gation and the tightening of the apical hook. In adult plants, concentration within a submerged R. palustris shoot occur. ethylene regulates the ripening of fruits, senescence of It is our hypothesis that differences in the submergence- leaves, the subsequent abscission of plant parts and various induced elongation response between species (R. palustris stress responses (Abeles, Morgan & Saltveit 1992). and R. acetosella), between leaves of various ages and In most terrestrial plants, ethylene inhibits stem and leaf between the petiole and leaf blade are not caused by varia­ elongation (Abeles et al. 1992). However, it stimulates tion in ethylene concentrations, but are related to differ­ shoot elongation in many aquatic and amphibious species, ences in ethylene sensitivity, defined as the response to exogenously applied hormone (Trewavas 1981; Weyers, Correspondence: Minke Banga, Department of Ecology, University Paterson & A’Brook 1987). The experiments described in of Nijmegen, Toernooiveld, 6525 ED Nijmegen, The Netherlands. this paper test this hypothesis. © 1996 Blackwell Science Ltd 1423 1424 M. Banga e tal Firstly, localization of ethylene biosynthesis in sub­ tration of conjugated ACC (= MACC + GACC), a portion merged R. palustris plants was investigated, to determine of the aqueous extract was hydrolysed in 1-84 mol dm“3 whether ethylene production rates vary markedly between HC1 at 100 °C for 3 h and then neutralized with NaOH leaves of different ages or between leaf blades and petioles. according to Hoffman et al. (1983). ACC was determined Direct determination of the sites of ethylene synthesis in using the method described by Lizada & Yang (1979) with submerged plants is impossible because ethylene can only internal standardization. In the assay ACC is chemically be measured in the gas phase. Therefore, we chose to mea­ converted in equimolar amounts of ethylene which was sure concentrations of free and conjugated ACC (l- determined on a Chrompack Packard gas chromatograph aminocyclopropane-l-carboxylic acid) in petioles and leaf model 438 A fitted with a Porapack Q column (length blades. ACC is the immediate precursor of ethylene 100 cm) at 60 °C packed to 0-34 g cm"3 and a flame ioniza­ (Adams & Yang 1979). ACC can also be irreversibly con­ tion detector. The difference in ACC content before and jugated to stable MACC [ l-(malonylamino)cyclopropane- after hydrolysis was taken as the concentration of conju­ l-carboxylic acid; Amrhein et al. 1981; Hoffman & Yang gated ACC. All concentrations were determined on a fresh 1982; Hoffman, Liu & Yang 1983] or GACC |l-(y-glu- weight basis. tamylamino)cyclopropane-l-carboxylic acid; Martin et al. From an extra set of 60 similar plants, fresh/dry weight 1995]. Ethylene concentrations per se were measured in ratios were quantified for all plant pails and treatments. Each submerged R. palustris leaves of various ages to investi­ sample consisted of two petioles or leaf blades and three gate whether ethylene concentration gradients exist within replications were used. The ratios were used to calculate submerged plants. Finally, ethylene dose-response curves concentrations on a dry weight basis. The effects of submer­ were used to quantify the ethylene sensitivities of petioles gence on the concentrations of free and conjugated ACC and leaf blades of the two Rumex species. were tested statistically by /-tests (Sokal & Rohlff 1981). MATERIALS AND METHODS Endogenous ethylene concentrations Plant materials and growth conditions To prevent confounding of ethylene production rates by the activity of soil micro-organisms (Arshad & Seeds of Rumex palustris Sm. and R. acetosella L. col­ Frankenberger 1990), the soil was gently removed from lected from field populations around Nijmegen. The the roots before measurements were made. To determine Netherlands, were incubated on moist filter paper in Petri endogenous ethylene concentrations in leaves of various dishes under a 12 h day/12 h night regime (PPFR 25 /J\no\ ages, all leaves but one [leaf 3, leaf 4 or leaf 5 (= youngest irf2 s-1; 25-27/10 °C) for 7-10 d. Seedlings were then leaf)] were removed. Groups of three or four R. palustris transferred to 200 cm3 pots filled with a mixture of sand leaves of the same age were placed together on 100 cm and standard peat-based potting compost ( 1:1 v/v) and glass vials filled with ballotini and 15 cnr of tap water grown in a growth chamber (16 h day/8 h night; PPFR according to Horton (1992). A vial without plant material 180 ¿iinol m“2 s'1; 20-22 °C; 40-70% RH) lor 15-22 d, was used as a zero-ethylene reference. Vials were placed and sprayed daily with 10 cnr tap water. Plants were used individually in open 600 cm3 glass cuvettes that contained when the fifth leaf was emerging. All experiments were 400 cm' of tap water, but the plant material was not yet performed under similar temperature and light conditions submerged. Wound ethylene production lasted for 8-10 li to those described for the growth chamber. (data not shown). Therefore, the start of submergence treatment was delayed for 16 h. After 24 h submergence, when ethylene accumulation is Assay for ACC and conjugates very high, the endogenous ethylene
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