The Effect of Light on Plastid Differentiation, Chlorophyll Biosynthesis, and Essential Oil Composition in Rosemary (Rosmarinus officinalis) Leaves and Cotyledons.

Andrea Böszörményi,Anna Skribanek,Melinda Pávai,Katalin Solymosi,Adrienn Dobi

doi:10.3389/fpls.2020.00196

Andrea Böszörményi, Anna Skribanek + Show 3 more

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https://doi.org/10.3389/fpls.2020.00196

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Abstract

It is unclear whether light affects the structure and activity of exogenous secretory tissues like glandular hairs. Therefore, transmission electron microscopy was first used to study plastid differentiation in glandular hairs and leaves of light-grown rosemary (Rosmarinus officinalis “Arp”) plants kept for 2 weeks under ambient light conditions. During our detailed analyses, among others, we found leucoplasts with tubuloreticular membrane structures resembling prolamellar bodies in stalk cell plastids of peltate glandular hairs. To study the effect of darkness on plastid differentiation, we then dark-forced adult, light-grown rosemary plants for 2 weeks and observed occasionally the development of new shoots with elongated internodes and pale leaves on them. Absorption and fluorescence spectroscopic analyses of the chlorophyllous pigment contents, the native arrangement of the pigment-protein complexes and photosynthetic activity confirmed that the first and second pairs of leaf primordia of dark-forced shoots were partially etiolated (contained low amounts of protochlorophyll/ide and residual chlorophylls, had etio-chloroplasts with prolamellar bodies and low grana, and impaired photosynthesis). Darkness did not influence plastid structure in fifth leaves or secretory tissues (except for head cells of peltate glandular hairs in which rarely tubuloreticular membranes appeared). The mesophyll cells of cotyledons of 2-week-old dark-germinated rosemary seedlings contained etioplasts with highly regular prolamellar bodies similar to those in mesophyll etio-chloroplasts of leaves and clearly differing from tubuloreticular membranes of secretory cells. Analyses of the essential oil composition obtained after solid phase microextraction and gas chromatography-mass spectroscopy showed that in addition to light, the age of the studied organ (i.e., first leaf primordia and leaf tip vs. fifth, fully developed green leaves) and the type of the organ (cotyledon vs. leaves) also strongly influenced the essential oil composition. Therefore, light conditions and developmental stage are both important factors to be considered in case of potential therapeutic, culinary or aromatic uses of rosemary leaves and their essential oils.

Highlights

Peculiar cubic phase membrane organizations, termed tubular complexes or tubuloreticular inclusions have been observed in several animal, human or plant cells
Due to their very high surface-to-volume ratio, prolamellar bodies are thought to serve as a membrane reserve that can be quickly converted into a large photosynthetic membrane network upon lightdark transition of for instance seedlings germinating in the soil (Ferroni et al, 2009; Kakuszi et al, 2017) or leaf primordia of buds after bud break (Solymosi and Böddi, 2006; Solymosi et al, 2006, 2012)
Our aim was to check whether such tubuloreticular structures were characteristic for the plastids of the peltate glandular hairs of other medicinally and economically important Lamiaceae species such as for example rosemary (Rosmarinus officinalis) (Borges et al, 2018; De Oliveira et al, 2019) and whether their presence or structure was influenced by darkness

Summary

Introduction

Peculiar cubic phase membrane organizations, termed tubular complexes or tubuloreticular inclusions have been observed in several animal, human or plant cells. The prolamellar bodies present in the etioplasts or etio-chloroplasts of dark-grown plants represent another well-known group of cubic phase membranes present in nature [reviewed in Solymosi and Schoefs (2010), Solymosi and Aronsson (2013), Kowalewska et al (2019)] Due to their very high surface-to-volume ratio, prolamellar bodies are thought to serve as a membrane reserve that can be quickly converted into a large photosynthetic membrane network upon lightdark transition of for instance seedlings germinating in the soil (Ferroni et al, 2009; Kakuszi et al, 2017) or leaf primordia of buds after bud break (Solymosi and Böddi, 2006; Solymosi et al, 2006, 2012). It has to be outlined, that prolamellar bodies represent one subtype of tubuloreticular membrane structures with highly regular spatial organization consisting of tetrahedral units of membrane tubules arranged in strictly geometric manner [reviewed in Solymosi and Schoefs (2010), Solymosi and Aronsson (2013)]

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