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Elucidation of biosynthesis pathways of volatile organic compounds (VOCs) in plants is a very active field of research. Since the initial isolation of the limonene synthase and the linalool synthase genes from Mentha spicata and Clarkia breweri (Colby et al., 1993; Dudareva et ah, 1996), dozens of genes involved in the biosynthesis of terpenes, phenylpropanoids/benzenoids and fatty acid derivatives have been characterized in plants belonging to various families. Although most work has been done on angiosperms and conifers, the genetic basis of VOC diversity found in more basal plant lineages is also starting to be investigated (Jia et ah, 2018). Until recently, most studies were focused on identifying the genes and enzymes involved in the biosynthesis of aroma compounds. Early works used model plants such as C. breweri, Antirrhinum majus, Arabidopsis thaliana and Petunia x hybrida or plants of agronomical or horticultural interests such as Solanum lycopersicum and Rosa x hybrida. During the past ten years, as more and more pathways were elucidated, the central question of the evolutionary origin of this chemical diversity arose. In a growing number of cases, impact of gene and/or allele evolution on specialized metabolism has been analyzed in detail. In this chapter, we will describe some of these molecular mechanisms by which a plant can acquire or loose the capacity to synthesize specific VOCs. As illustrations, examples will be selected from different categories of VOCs in various plant families, with an emphasis on scent and aroma compounds from plants of particular agronomical or horticultural interests.


Friends and Foes Interacting with Plants

Plants are sessile organisms, which have, even more than other organisms, exploited chemical diversity to cope with their changing environments. The metabolites that a plant is able to synthesize have crucial roles for its survival in challenging conditions, due to both biotic and abiotic factors. VOCs are particularly important for interactions with pollinators and for defense against enemies. It is generally admitted that plant defense was the initial function of VOCs and that scent emission for the attraction of pollinators evolved later (Raguso, 2009). Defense-related VOCs may have direct effects through toxic properties or act as anti-digestive and anti-nutritive compounds. They may also attract enemies of the herbivores in the now well-known indirect defense phenomena. Accordingly, any mutation of a gene leading to the production of an advantageous volatile compound, or eliminating a disadvantageous compound, increases the plant fitness and thus can be quickly selected.

Flower scent is a strong signal directing pollinators to flowers that can deliver a reward like nectar or pollen. Sometimes the reward for insects is a place used as a nest that favors mating and protection. Scent can also be deterrent or toxic to undesirable visitors like ants, caterpillars, or even bacteria (Muhlemann et al., 2014). Scent is thus considered as a major fitness component, however, due to the complexity of the volatile profiles of many flowers, detailed analysis of the role of individual compounds is difficult.

Community-wide patterns of flower scent signals have rarely been explored. Nevertheless, scent advertisement in a plant community has been shown to be inversely proportional to the population size of pollinators: more scent is emitted by species blooming early in the season, when pollinators are scarce and the emission tends to decrease when more pollinators are present (Filella et al., 2013). The dynamics of seasonal emission of scent leading to the structuration of the plant-pollinator network is thus quite complex. Although it is generally assumed that floral volatiles provide fitness benefits for plants, VOCs may impact both mutualists that pollinate flowers and herbivores that damage them (Boachon et al., 2015). By silencing both benzylacetone biosynthesis and nectar production in N. attenuate! by RNAi approaches, the costs and benefits of these traits for the plant could be evaluated, in relationships with two pollinators and one herbivore (Kessler et al., 2015). This study concluded that both herbivores and pollinators shaped the evolution of floral traits and that it made little sense to study the effects of the ones without considering the effects of the others.

Besides the well described plant-insect interactions, more recent works highlight the influence of plant VOCs on the microbial communities present at the surface of plant tissues (reviewed in Junker and Tholl, 2013). Microbial VOCs have also been shown to influence plant growth or reproduction (Piechulla et al., 2017). The diversity of both beneficial and pathogenic organisms interacting with plants makes it complicated to understand the forces that drive the evolution of VOC biosynthesis and diversity. Furthermore, evolution may occur on genes that directly synthesize VOCs, but also on transcription factors and regulators that are linked to development cycle, to rhythmicity, or to response to environmental, biotic or abiotic factors.

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