Developmental expression of the cucumber Cs-XTH1 and Cs-XTH3 genes, encoding xyloglucan endotransglucosylase/hydrolases, can be influenced by mechanical stimuli

Robert Malinowski,Anna Barczak-Brzyżek,Stephen C Fry,Marcin Filipecki,Anita Wiśniewska,Stefan Malepszy,Sabina Zuzga,Andrzej Noyszewski,Michał Godlewski

doi:10.1007/s11738-018-2707-7

Abstract

The expression of two genes encoding xyloglucan endotransglucosylase/hydrolases (XTHs), Cs-XTH1 and Cs-XTH3, was upregulated during the onset of cucumber somatic embryogenesis. As a means of characterising the developmental regulation of these genes, the activity of the respective upstream regulatory regions was investigated in seedlings and somatic embryos of Arabidopsis thaliana and Cucumis sativus. GUS assays revealed that both genes are under developmental control. In addition, elevated promoter activity was found in the tension-bearing regions of the plant and in response to touch and wounding, which is consistent with the existence of numerous stress-related cis elements in the 5′-regulatory regions. In vivo xyloglucan endotransglucosylase (XET) action assays were performed to gain an overview on the role of XTHs during somatic embryogenesis. The highest XET action was observed in the external cell layers of somatic embryos in the cotyledonary region and in the presumptive region of peg formation. Based on the results, we propose a dual mechanism (one developmental and the second adaptive) for the regulation of Cs-XTH1 and Cs-XTH3 activity wherein the developmental pattern can be modified by mechanical stimuli.

Highlights

The xyloglucan endotransglucosylase/hydrolases (XTHs) are a family of plant genes encoding the xyloglucan transglucosylase/hydrolase enzymes (XTH; EC 2.4.1.207)
We reported that two cucumber XTH genes, CsXTH1 and CsXTH3, were engaged in somatic embryogenesis (Linkiewicz et al 2004; Malinowski et al 2004; Wiśniewska et al 2012)
The nucleotide sequence conservation reaching 75% identity within coding sequence does not extend to the 5′ regulatory regions of CsXTH1 and CsXTH3

Summary

Introduction

The XTHs are a family of plant genes encoding the xyloglucan transglucosylase/hydrolase enzymes (XTH; EC 2.4.1.207). The enzymatic XET and XEH activities have been shown to lead to enhanced viscoelasticity or increased strength when applied to cellulose/xyloglucan biocomposite material mimicking a cell wall structure (Chanliaud et al 2004), and exogenously applied XTHs have been shown to modify the extensibility of real plant cell wall material (Maris et al 2009) These results have provided strong support for previous demonstrations of the ability of these proteins to integrate new xyloglucan molecules (Thompson et al 1997) and to remodel existing xyloglucan molecules (Thompson and Fry 2001) of the cell wall. This type of morphological change, especially when it occurs locally, may be important for plant morphogenesis (Hejnowicz et al 1977; Dumais et al 2004)

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Conclusion