Transient Exposure to Ethylene Stimulates Cell Division and Alters the Fate and Polarity of Hypocotyl Epidermal Cells

Abstract

After transient exposure to the gaseous hormone ethylene, dark-grown cucumber (Cucumis sativus) hypocotyls developed unusual features. Upon ethylene's removal, the developing epidermis showed significant increases in cell division rates, producing an abundance of guard cells and trichomes. These responses to ethylene depended on the stage of development at the time of ethylene exposure. In the upper region of the hypocotyl, where cells were least differentiated at the onset of ethylene treatment, complex, multicellular protuberances formed. Further down the hypocotyl, where stomata and trichomes were beginning to develop at the onset of ethylene exposure, an increase in the number of stomata and trichomes was observed. Stomatal complexes developing after the ethylene treatment had a significant increase in the number of stomatal subsidiary cells and the number of cells per trichome increased. Analysis of division patterns in stomatal complexes indicated that exposure to ethylene either suspended or altered cell fate. Ethylene also altered cell division polarity, resulting in aberrant stomatal complexes and branched trichomes. To our knowledge, the results of this study demonstrate for the first time that transient treatment with physiological concentrations of ethylene can alter cell fate and increase the propensity of cells to divide.Ethylene regulates a variety of physiological and biochemical processes in plants, such as fruit ripening, senescence, abscission, sex determination, root initiation, and cell elongation (Abeles et al., 1992). Ethylene also regulates the size and stature of plants in response to various environmental cues (Abeles, 1973;Kieber, 1997). Its effects on dark-grown seedling development, described initially as the triple response, include increased radial growth of the root and stem, reduced root and stem elongation, and abnormal horizontal stem growth (Neljubow, 1901;Knight et al., 1910). The term triple response, as it is now commonly used, includes exaggeration in the curvature of the apical hook instead of abnormal horizontal growth (Bleecker et al., 1988;Guzman and Ecker, 1990 and references therein). The triple response of Arabidopsis has been exploited for characterizing the ethylene signal transduction system by identifying numerous mutants that either phenocopy the triple response in the absence of exogenous ethylene or fail to respond properly to ethylene (Guzman and Ecker, 1990).The dramatic stimulation of radial swelling of stems and roots by ethylene has led to physiological studies and cellular analyses of this phenomenon (Burg and Burg, 1966;Lang et al., 1982;Bleecker et al., 1988;Abeles et al., 1992;Baskin and Williamson, 1992;Kieber, 1997). Depending on the timing of ethylene's application, the physiological condition, seedling age, and the plant species concerned, either promotive (Ku et al., 1970;Lehman et al., 1996;Smalle et al., 1997) or inhibitory (Kieber et al., 1993) effects on organ elongation have been reported. For young developing dicot seedlings, ethylene has ...

Ethylene is an endogenous stimulator of cell division in the cambial meristem of Populus

“…The inhibition of this response in trees where ethylene perception was reduced (transgenic and 1-MCP-treated wild type) further showed that it was mediated through ethylene receptors. Application experiments have also demonstrated a potential for ethylene to stimulate endoreduplication in hypocotyls of Arabidopsis and cucumber (11)(12)(13), cell division activity, and the induction of cell cyclerelated genes in adventitious root formation and in the intercalary meristem of deepwater rice (25,26). In line with these observations, overproduction of ethylene in Arabidopsis roots due to the loss of function of ETO1 [encoding a BTB/POZ protein that regulates ACS5 stability, and hence elevated ethylene biosynthesis, through ubiquitin E3 ligase complex (27)] not only inhibited root elongation but also induced additional cell division in the quiescent center, and a function for endogenous ethylene in postembryonic stem cell division was postulated (14).…”

“…Additional observations also support a potential role for ethylene in cell division. Applied ethylene stimulated endoreduplication in cucumber hypocotyls and growth of the intercalary meristem in deepwater rice (11)(12)(13). Moreover, the ethylene-overproducing Arabidopsis mutant eto1 exhibits aberrant cell divisions in the quiescent center of the root (14).…”

Effects of light and ethylene on endogenous hormones and development of Catasetum fimbriatum (Orchidaceae)

“…Light-grown plants, on the other hand, show limited longitudinal shoot growth, rapidly forming short and round pseudobulbs and normal green leaves (Suzuki and Kerbauy, 1999). Several effects of ethylene on shoot growth (Cary et al, 1995), cell division (Kazama et al, 2004) and hormone levels (Peres et al, 1999) have been reported. Up to now, experiments conducted to explore plant growth and development controlled by internal cues, such as hormonal balance, and by external factors have not, unfortunately, yielded conclusive information.…”

The POLARIS Peptide of Arabidopsis Regulates Auxin Transport and Root Growth via Effects on Ethylene Signaling

“…For example, auxin can suppress cytokinin biosynthesis (Nordströ m et al, 2004), auxin and cytokinin can act synergistically to induce ethylene biosynthesis (Vogel et al, 1998), and ethylene can modify auxin responses and meristem function (Morgan and Gausman, 1966;Suttle, 1988;Visser et al, 1996;Haver et al, 2002;Vandenbussche et al, 2003;Souter et al, 2004;Stepanova et al, 2005). Depending on the exposure, ethylene can either inhibit or promote cell division and influence cell fate (Kazama et al, 2004), and in part it acts through interactions with DELLA proteins (Achard et al, 2003). The roles of actin and tubulin components are also receiving much attention, both as being modified by hormones and signaling pathways (Lang et al, 1982;Cyr, 1991;Lloyd et al, 1996;Gardiner et al, 2001;Hussey, 2004) and as themselves being implicated as regulators of hormonal signaling systems (Geldner et al, 2001).…”