Explaining Intraspecific Diversity in Plant Secondary Metabolites in An
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Review Tansley review Explaining intraspecific diversity in plant secondary metabolites in an ecological context Author for correspondence: Ben D. Moore1, Rose L. Andrew2, Carsten Kulheim€ 3 and William J. Foley3 Ben D. Moore 1 Tel: +61 2 4570 1384 Hawkesbury Institute for the Environment, University of Western Sydney, Locked Bag 1797, Penrith 2751, NSW, Australia; Email: [email protected] 2Department of Botany, University of British Columbia, 3529-6270 University Blvd, Vancouver, BC V6T 1Z4, Canada; 3Research Received: 23 June 2013 School of Biology, Australian National University, Canberra, 0200, ACT, Australia Accepted: 22 August 2013 Contents Summary 1 VII. How and why is chemical diversity maintained? 7 I. Introduction 1 VIII. Evolvability of PSM variation 8 II. PSM variation in time: ontogeny, phenology and induced IX. Evolutionary strategies and plant chemical defence 10 defences 2 X. Conclusions and future directions 12 III. PSM variation through space: the role of environment 3 Acknowledgements 13 IV. Genes and biosynthetic pathways underlying PSM variation 3 References 13 V. Mechanisms for diversification of PSMs 3 VI. Examples of diversity from specific biosynthetic pathways 5 Summary New Phytologist (2013) Plant secondary metabolites (PSMs) are ubiquitous in plants and play many ecological roles. Each doi: 10.1111/nph.12526 compound can vary in presence and/or quantity, and the composition of the mixture of chemicals can vary, such that chemodiversity can be partitioned within and among individuals. Key words: biosynthesis, evolvability, Plant ontogeny and environmental and genetic variation are recognized as sources of chemical herbivore, heritability, plant defence, variation, but recent advances in understanding the molecular basis of variation may allow the transgenic, variance. future deployment of isogenic mutants to test the specific adaptive function of variation in PSMs. An important consequence of high intraspecific variation is the capacity to evolve rapidly. It is becoming increasingly clear that trait variance linked to both macro- and micro-environmental variation can also evolve and may respond more strongly to selection than mean trait values. This research, which is in its infancy in plants, highlights what could be a missing piece of the picture of PSM evolution. PSM polymorphisms are probably maintained by multiple selective forces acting across many spatial and temporal scales, but convincing examples that recognize the diversity of plant population structures are rare. We describe how diversity can be inherently beneficial for plants and suggest fruitful avenues for future research to untangle the causes and consequences of intraspecific variation. with pollinators and mycorrhizal fungi, attracting predators of I. Introduction herbivores, plant–plant signalling and protection against abiotic Plant secondary metabolites (PSMs) are ubiquitous in the plant stressors such as UV-B radiation, frost and drought (Dixon & kingdom, and play myriad ecological roles in defence against Paiva, 1995). Yet, because of their sheer number and diversity, herbivores and pathogens past and present, mediating interactions modes of action remain to be discovered and adaptive Ó 2013 The Authors New Phytologist (2013) 1 New Phytologist Ó 2013 New Phytologist Trust www.newphytologist.com New 2 Review Tansley review Phytologist advantages still await rigorous demonstration for most PSMs, II. PSM variation in time: ontogeny, phenology and presenting an ongoing challenge for ecologists. Like most traits induced defences of organisms, PSMs are variable at all scales including among species, populations, individuals, and different plant parts Much of the qualitative and quantitative PSM variation in a species (Suomela et al., 1995; Holeski et al., 2012a), and it is this occurs among tissue types and ontogenetic stages, and across variation and its causes and consequences that are the subject of circadian and annual cycles (Kim et al., 2011; Holeski et al., this review. 2012a). Optimal defence theory suggests that different plant tissues A plant population can exhibit presence–absence polymor- are defended in accordance with their value to the plant, the costs of phisms for individual PSMs, but more common, and often defence and the risk of herbivore or pathogen attack (Rhoades & overlaid, is quantitative variation in PSM concentrations. The great Cates, 1976). These factors change throughout plants’ ontogeny diversity of PSMs also allows for variation in the number and and, accordingly, so too do PSM concentrations (Barton & evenness of concentrations (i.e. PSM richness and a-chemodiver- Koricheva, 2010). Plant age and size can also influence PSM sity) of PSMs in individual plants as well as qualitative variation concentrations, either as a life history strategy or as a consequence of between individuals and groups (b-chemodiversity). When dis- changing resource availability. Consequently, population age cussing qualitative variation, phenotypes with different PSM structure can also contribute to chemical variation (Moore & profiles are referred to as chemotypes. These perspectives on Foley, 2005; Andrew et al., 2007). chemical variability and diversity are elaborated upon in Support- ing Information Notes S1. 1. Herbivore-induced changes in PSMs Particularly against specialists, the effectiveness of defence is rarely determined by summing concentrations across broad PSM Biotic interactions often change PSM profiles and net production classes and more often linked to specific individual compounds by inducing defensive responses. Induction can occur locally at the which sometimes account for small fractions of total defence site of attack or infection, or can be systemic (Kessler & Baldwin, allocation (Adler et al., 1995), emphasizing the importance of 2002). A growing list of examples also demonstrate persistent, qualitative PSM diversity. The effectiveness of PSMs as herbivore transgenerational induction of PSMs by herbivory on maternal deterrents can also be influenced by plant nutritional quality, as plants, mediated by epigenetic mechanisms including DNA herbivores titrate nutritional reward against the cost of ingesting methylation, histone modification, smRNAs and enhanced PSMs (Au et al., 2013). homologous recombination (Holeski et al., 2012b). Inducible Diversity in the specificity of biochemical interactions between chemical defence may allow plants to avoid any costs associated plants and their enemies parallels PSM diversity. For example, with defence when enemies are absent, while constitutively defended digoxin is highly specific, targeting the Na+/K+ ATPases (Katz et al., plants must pay these costs whether or not defences are required 2010), whereas tannins bind many diverse proteins. Terpenes act as (Karban & Baldwin, 1997; Mithofer & Boland, 2012); however, direct defences through generalized toxicity and as receptor-specific maintaining the capacity to induce defences may also be costly. cues to attract parasitoids (indirect defence), so both quantitative Changes to PSM synthesis can also be induced remotely by and qualitative diversity influence the ecological interactions of volatile emissions from con- or heterospecific neighbours that are plants possessing these compounds. Small structural variations can under herbivore attack (Baldwin et al., 2006). Despite extensive also have vastly different effects. For example, specific ellagitannin efforts, few of the signalling molecules have been identified (Jander identity influences redox conditions in caterpillar guts (Appel, & Clay, 2011) beyond salicylates and jasmonates (Erb et al., 2012), 1993; Salminen & Karonen, 2011). These observations emphasize and reactive oxygen molecules such as hydrogen peroxide that the use of cost–benefit analyses to explain quantitative PSM (Orozco-Cardenas et al., 2001). Jasmonate signalling is widespread variation will probably fail if the group of PSMs considered is too and has been well characterized in plants including Arabadopsis inclusive. thaliana, tomato (Lycopersicon esculentum) and Nicotiana attenuata All chemical phenotypic variation is attributable to the effects of (Turner et al., 2002). Wild tobacco (N. attenuata) plants treated genes, environment and the interaction of these, and this extends to with methyl jasmonate increase production of nicotine and are phenotypic variation with plant ontogeny and phenology. Here, we attacked less often by herbivores, although induction exacts a cost to first review how PSMs respond in time and space to plants’ biotic seed production if herbivores are absent (Baldwin, 1998). Attack and abiotic interactions with their environment. We then address signals are propagated and amplified by signalling molecule the genetic and molecular basis of PSM qualitative diversity, with cascades that travel between cells, through the phloem of plants an emphasis on the insights to be gained into PSM diversity from and through the atmosphere to neighbouring plants and to natural manipulating the genes that are ultimately responsible. Having enemies of the plants’ attackers (Degenhardt et al., 2003). described the phenomenon of PSM variation, we turn to how Previously attacked plants and their neighbours may be ‘primed’ quantitative genetic variation contributes to PSM quantitative to a higher alert level than na€ıve plants by the detection of a variety variation, discuss the evolvability of trait means and variances and of volatile organic compounds (VOCs), including green leafy finally consider the ecological