Elsevier

Current Opinion in Biotechnology

Volume 49, February 2018, Pages 73-79
Current Opinion in Biotechnology

Plant secretory structures: more than just reaction bags

https://doi.org/10.1016/j.copbio.2017.08.003Get rights and content

Highlights

  • Plants can produce large quantities of specialized metabolites in dedicated organs.

  • Enzyme isoforms with specific characteristics contribute to this high productivity.

  • Green trichomes are sink organs that use photosynthesis as energy provider.

Plants have a remarkable capacity for the production of a wide range of metabolites. Much has been reported and reviewed on the diversity of these metabolites and how it is achieved, for example through the evolution of enzyme families. In comparison, relatively little is known on the extraordinary metabolic productivity of dedicated organs where many of these metabolites are synthesized and accumulate. Plant glandular trichomes are such specialized metabolite factories, for which recent omics analyses have shed new light on the adaptive metabolic strategies that support high metabolic fluxes. In photosynthetic trichomes such as those of the Solanaceae, these include CO2 refixation and possibly C4-like metabolism which contribute to the high productivity of these sink organs.

Introduction

Plants are known to be masters at generating chemical diversity. One invoked reason for this extraordinary diversity is their sessile nature. Being unable to escape adverse conditions, plants have evolved various processes to compensate for this immobility, one of them being the production of compounds that will protect them against aggressors or an unfavourable environment. An argument often used in articles about the biosynthesis of plant secondary metabolites to justify the work is that by elucidating the biosynthesis pathway it will become possible to make them more readily available by engineering easily cultivable microorganisms such as Escherichia coli or the yeast Saccharomyces cerevisiae. While this argument may hold true for substances produced by rare, endangered or difficult to cultivate species, or for substances that are in particularly low amounts such as Taxol, in many cases the substances of interest are actually present in fairly large quantities in the plant. In Table 1, some examples are given that illustrate this point.

This capacity to produce specialized metabolites in large quantities means that developing processes based on metabolic engineering and fermentation of microorganisms is a tough challenge. A revealing story in this regard is that of the engineering of artemisinic acid, the precursor of the antimalarial artemisinin in yeast. In a series of remarkable metabolic engineering efforts, production of artemisinic acid in yeast reached over 20 g/L [2, 3, 4]. The industrial development of this process was taken over by a non-profit organization and ultimately by the pharmaceutical giant Sanofi-Aventis [5]. Major investments were made in a production facility to supply this compound for the manufacture of anti-malarial medication. However, the production costs were still above those of plant-produced artemisinin and a better organization of artemisinin production by small farmers led to a stabilization of the prices and of the supply. This rendered the fermented route no longer competitive. The production plant was sold, and is now faced with an uncertain future [6]. The lesson of this is that plants can be hard to beat and that it may be worth understanding how they manage to achieve this high productivity. There have been efforts to try and exploit this inherent capacity for metabolic engineering purposes to develop the production of industrial compounds in plants. Current efforts and perspectives for the production of isoprenoids in plant cell factories are reviewed in this issue [7]. The combination of large scale sequencing data, particularly from non-model species, and of recent developments in synthetic biology such as modular assembly schemes based on Golden Gate cloning [8, 9], create exciting opportunities for the production of secondary metabolites in plants. In this regard, one nice and recent example is the gram-scale production of triterpenoids in Nicotiana benthamiana [10].

Many, if not all, plant species possess dedicated organs or tissues where these metabolites are produced and stored, typically in large quantities. These specialized structures can be classified in two major classes based on their localization in the plant: at the surface or internal. At the surface, probably the most broadly represented type of secretory structures are glandular trichomes. They can adopt a myriad of shapes and sizes but have in common the capacity to synthesize large quantities of metabolites and to secrete them at the surface or store them in dedicated compartments depending on the nature of the compounds [11].

Inside the plant, a number of secretory structures or specialized cells dedicated to the biosynthesis and storage of metabolites have been described. These include laticifers, resin ducts, secretory cavities and oil glands. These structures have evolved to accumulate and store large quantities of metabolites or polymers. The purpose of this review is to survey the latest knowledge in our understanding of how these specialized structures work, specifically what are the metabolic features that allow these structures to be so productive. Because most of the work in this area is on glandular trichomes, the content of this review will be strongly biased on these organs.

Section snippets

Transcriptional activation of committed pathways and occurrence of specific isoforms

Probably the clearest feature of secretory structures accumulating a particular class of compounds, is the high transcriptional activation of genes encoding enzymes of the committed pathways for these compounds. In most cases, the compounds which accumulate in these organs are also synthesized there, explaining these high expression levels. For example, in glandular trichomes, this has been a tremendous help to identify and characterize a number of pathways, including those of menthol in

Where do glandular trichomes get their carbon and energy from?

The massive productivity of glandular trichomes for hydrocarbon compounds raises the question of the origin of the carbon and of the energy and reducing power required to drive these biosyntheses. Here, a distinction should be made between green (or photosynthetic) and non-photosynthetic trichomes. Typically peltate trichomes of the Lamiaceae (mint family) are non-photosynthetic [57]. Early labelling studies in peppermint indicated that glucose could be incorporated into terpenes [58]. It was

Does refixation of CO2 via C4 metabolism increase photosynthetic trichome productivity?

Mining of the transcriptome and proteome data revealed that genes typically associated with C4-photosynthesis are overexpressed in tomato trichomes, in particular phosphoenolpyruvate carboxykinase (PEPCK) and plastidial NADP-dependent malate dehydrogenase [41••]. Although PEPCK is typically described as a decarboxylating enzyme involved in gluconeogenesis, it is a reversible enzyme which has high affinity for CO2 at physiological concentrations of cations [64]. Furthermore, one can assume that

Conclusion

The extraordinary capacity of plants to produce large amounts of metabolites in specialized secretory structures is beginning to be unravelled. In addition to high expression levels of committed pathways, dedicated central and energy metabolic networks have evolved to optimize precursor supply and carbon-efficiency. These include the expression of specific enzyme isoforms with adapted kinetic properties or regulatory mechanisms. Interestingly, photosynthetic trichomes are largely auxotrophic

Conflict of interest

The author declares no conflicts of interest.

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

The author gratefully acknowledges the support of the Deutsche Forschungsgemeinschaft (Grant TI800/1-1) and of the Leibniz-Institute of Plant Biochemistry.

I apologize to those whose work was not cited for space reasons.

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