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

Abstract

The plant hormone ethylene is an important signal in plant growth responses to environmental cues. In vegetative growth, ethylene is generally considered as a regulator of cell expansion, but a role in the control of meristem growth has also been suggested based on pharmacological experiments and ethylene-overproducing mutants. In this study, we used transgenic ethylene-insensitive and ethylene-overproducing hybrid aspen (Populus tremula ؋ tremuloides) in combination with experiments using an ethylene perception inhibitor [1-methylcyclopropene (1-MCP)] to demonstrate that endogenous ethylene produced in response to leaning stimulates cell division in the cambial meristem. This ethylenecontrolled growth gives rise to the eccentricity of Populus stems that is formed in association with tension wood.plant hormones ͉ secondary xylem ͉ tension wood ͉ vascular cambium ͉ wood development T he vascular cambium is the meristem that produces secondary xylem and phloem by periclinal cell divisions, and it is responsible for wood production and stem diameter growth in trees. Cambial growth rate along the trunk is correlated with leaf biomass and crown structure (1). Superimposed on this intrinsic control, cambial growth is also strongly influenced by environment, where mechanical and gravitational loads imposed by wind and leaning are important (2). Wind sway induces increased diameter growth that protects against stem breakage (3), whereas a static lean results in a localized growth response known as tension wood (TW) in dicotyledonous angiosperms. TW is formed on the upper side of the leaning stem, resulting in characteristic asymmetric growth, and it serves to correct the stem position (4). In addition to the striking increase in cambial cell divisions, TW has an altered anatomy, and the fibers form an additional inner, cellulose-rich, gelatinous secondary cell wall layer (G layer) (5).Experiments with ethylene applications have revealed that this volatile plant hormone has the potential to both inhibit and stimulate growth (6). Its synthesis from S-adenosylmethionine through the action of 1-aminocyclopropane-1-carboxylate (ACC) synthase (ACS) and ACC oxidase (ACO) is triggered in vegetative tissues in response to many environmental cues. To date, concepts of ethylene function in vegetative growth have mainly implicated its role in primary tissue and cell expansion (6). However, ethylene biosynthesis increases during TW formation because of an asymmetric induction of ACO (7,8), and application of ethylene has been shown to stimulate cambial growth both in trees and herbaceous species (9, 10). 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 (11-13). Moreover, the ethylene-overproducing Arabidopsis mutant eto1 exhibits aberrant cell divisions in the quiescent center of the root (14). However, experiments where ethylene homeostasis is artificially manipulated by a...

Transcriptome analysis provides insights into wood formation during larch tree aging

“…More information about the molecular mechanisms by which ethylene controls wood formation has been reported (Andersson-Gunneras et al 2003;Love et al 2009;Vahala et al 2013). These data indicate that the linear cell growth mode may be common to cotton fibers and xylem cells and facilitate the study of the regulatory network of xylem cell growth.…”

“…Here, we found that LaMYB44 had the same expression pattern as LaERFs, supporting its involvement in this mode. In addition, overexpression of PttACO1 stimulates cambial cell division in poplar (Love et al 2009). So these data provide more information about the function of MYB in wood formation besides controlling secondary wall biosynthesis (Demura and Fukuda 2007;Ye and Zhong 2015).…”

Components Acting Downstream of Short Day Perception Regulate Differential Cessation of Cambial Activity and Associated Responses in Early and Late Clones of Hybrid Poplar

“…For example, several putative ethylene response factors and genes involved in ethylene biosynthesis are differentially regulated in the two clones (Supplemental Table S2). Ethylene has been implicated in the regulation of dormancy induction (Ruonala et al, 2006;Ruttink et al, 2007) and cambial cell division (Love et al, 2009). Taken together, these observations suggest that the clones differ in their regulation of multiple hormonal pathways that control the timing of cambial growth cessation under SDs.…”

Diversity and cis-element architecture of the promoter regions of cellulose synthase genes in Eucalyptus

“…Yazaki et al (2003) found the MYB1AT element to be involved in Arabidopsis dehydration stress response while investigating gibberellic acid (GA) and abscisic acid (ABA) responses in rice. GA has also been found to play a role in cambial cell differentiation and xylem development (Love et al 2009) pointing to the co-regulation of genes involved in xylogenesis. This putative MYB-like element may also be important as a number of MYB transcription factors have been identified as key members of the transcriptional network regulating the secondary cell wall formation (Goicoechea et al 2005;Demura and Fukuda 2007;Legay et al 2010;Zhong et al 2010).…”