Vinca drug components accumulate exclusively in leaf exudates of Madagascar periwinkle

Roepke, Jonathan; Salim, Vonny; Wu, Maggie; Thamm, Antje M. K.; Murata, Jun; Ploss, Kerstin; Boland, Wilhelm; Luca, Vincenzo De

doi:10.1073/pnas.0911451107

Cited by 168 publications

(150 citation statements)

References 27 publications

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“…2 and 5). These data contrast with previously published reports that showed most catharanthine localized in the wax layer of the leaf tissue (31,32). The reasons for these differences are unclear but may reflect differences between cultivars or differences between leaf and stem tissue.…”

Section: Discussioncontrasting

confidence: 56%

Cell-specific localization of alkaloids in Catharanthus roseus stem tissue measured with Imaging MS and Single-cell MS

Yamamoto

Takahashi

Mizuno

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

111

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Catharanthus roseus (L.) G. Don is a medicinal plant well known for producing antitumor drugs such as vinblastine and vincristine, which are classified as terpenoid indole alkaloids (TIAs). The TIA metabolic pathway in C. roseus has been extensively studied. However, the localization of TIA intermediates at the cellular level has not been demonstrated directly. In the present study, the metabolic pathway of TIA in C. roseus was studied with two forefront metabolomic techniques, that is, Imaging mass spectrometry (MS) and live Single-cell MS, to elucidate cell-specific TIA localization in the stem tissue. Imaging MS indicated that most TIAs localize in the idioblast and laticifer cells, which emit blue fluorescence under UV excitation. Single-cell MS was applied to four different kinds of cells [idioblast (specialized parenchyma cell), laticifer, parenchyma, and epidermal cells] in the stem longitudinal section. Principal component analysis of Imaging MS and Single-cell MS spectra of these cells showed that similar alkaloids accumulate in both idioblast cell and laticifer cell. From MS/MS analysis of Single-cell MS spectra, catharanthine, ajmalicine, and strictosidine were found in both cell types in C. roseus stem tissue, where serpentine was also accumulated. Based on these data, we discuss the significance of TIA synthesis and accumulation in the idioblast and laticifer cells of C. roseus stem tissue. A lkaloids constitute one of the largest groups of specialized metabolites, many of which have biological functions that are indispensable, not only for plants themselves but also for human health. Approximately 20% of plant species are known to contain alkaloids (1). The significant value of alkaloids as medicines or luxury items in human life has attracted widespread interest from researchers in a range of scientific fields. These researchers have extensively studied how plant-specialized metabolites are produced at cellular and tissue levels (2). The reports indicate that biosynthetic pathways of plant specialized metabolites often involve multiple cell types that are biochemically and morphologically distinct (3,4

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Section: Discussioncontrasting

confidence: 56%

Cell-specific localization of alkaloids in Catharanthus roseus stem tissue measured with Imaging MS and Single-cell MS

Yamamoto

Takahashi

Mizuno

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

111

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“…In Arabidopsis, camalexin has antifungal properties and aids defense against pathogens including Botrytis cinerea, Alternaria brassicicola, and Sclerotinia sclerotiorum (Thomma et al, 1999;Ferrari et al, 2007;Stotz et al, 2011). Berberine, catharanthine, gossypol, momilactones, phytocassanes, and sanguinarine also have antimicrobial properties and confer tolerance to plant pathogens (Stermitz et al, 2000;Puckhaber et al, 2002;Umemura et al, 2003;Fukuta et al, 2007;Roepke et al, 2010;Obiang-Obounou et al, 2011). In addition to the involvement in auxin signaling (Brown et al, 2001;Buer and Muday, 2004), flavonols are protectants against UV light stress (Li et al, 1993;Bieza and Lois, 2001;Emiliani et al, 2013) and herbivores (Wuyts et al, 2006a;Onkokesung et al, 2014).…”

Section: Biological Relevance Of Wrky-regulated Specialized Metabolitesmentioning

confidence: 99%

Regulation of Specialized Metabolism by WRKY Transcription Factors

2014

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WRKY transcription factors (TFs) are well known for regulating plant abiotic and biotic stress tolerance. However, much less is known about how WRKY TFs affect plant-specialized metabolism. Analysis of WRKY TFs regulating the production of specialized metabolites emphasizes the values of the family outside of traditionally accepted roles in stress tolerance. WRKYs with conserved roles across plant species seem to be essential in regulating specialized metabolism. Overall, the WRKY family plays an essential role in regulating the biosynthesis of important pharmaceutical, aromatherapy, biofuel, and industrial components, warranting considerable attention in the forthcoming years.

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“…The discovery of VmPiNMT and RsPiNMT was in part based on an interesting strategy for identifying the biochemical functions of different members of the g-TLMT class of enzymes by harvesting potential MIA substrates from the leaf surfaces of plants that accumulate them and using them for biochemical activity testing (Roepke et al, 2010; Fig. 2).…”

Section: Discussionmentioning

confidence: 99%

A Picrinine N-Methyltransferase Belongs to a New Family of γ-Tocopherol-Like Methyltransferases Found in Medicinal Plants That Make Biologically Active Monoterpenoid Indole Alkaloids

Levac

Cázares

et al. 2016

Plant Physiol.

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Members of the Apocynaceae plant family produce a large number of monoterpenoid indole alkaloids (MIAs) with different substitution patterns that are responsible for their various biological activities. A novel N-methyltransferase involved in the vindoline pathway in Catharanthus roseus showing distinct similarity to g-tocopherol C-methyltransferases was used in a bioinformatic screen of transcriptomes from Vinca minor, Rauvolfia serpentina, and C. roseus to identify 10 g-tocopherol-like N-methyltransferases from a large annotated transcriptome database of different MIA-producing plant species (www.phytometasyn.ca). The biochemical function of two members of this group cloned from V. minor (VmPiNMT) and R. serpentina (RsPiNMT) have been characterized by screening their biochemical activities against potential MIA substrates harvested from the leaf surfaces of MIA-accumulating plants. The approach was validated by identifying the MIA picrinine from leaf surfaces of Amsonia hubrichtii as a substrate of VmPiNMT and RsPiNMT. Recombinant proteins were shown to have high substrate specificity and affinity for picrinine, converting it to N-methylpicrinine (ervincine). Developmental studies with V. minor and R. serpentina showed that RsPiNMT and VmPiNMT gene expression and biochemical activities were highest in younger leaf tissues. The assembly of at least 150 known N-methylated MIAs within members of the Apocynaceae family may have occurred as a result of the evolution of the g-tocopherol-like N-methyltransferase family from g-tocopherol methyltransferases.

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Vinca drug components accumulate exclusively in leaf exudates of Madagascar periwinkle

Cited by 168 publications

References 27 publications

Cell-specific localization of alkaloids in Catharanthus roseus stem tissue measured with Imaging MS and Single-cell MS

Cell-specific localization of alkaloids in Catharanthus roseus stem tissue measured with Imaging MS and Single-cell MS

Regulation of Specialized Metabolism by WRKY Transcription Factors

A Picrinine N-Methyltransferase Belongs to a New Family of γ-Tocopherol-Like Methyltransferases Found in Medicinal Plants That Make Biologically Active Monoterpenoid Indole Alkaloids

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