The effect of hybridization on secondary metabolites and herbivore resistance: implications for the evolution of chemical diversity in plants

Abstract

The diversity of secondary metabolites (SMs) has been poorly understood from both a mechanistic and a functional perspective. Hybridization is suggested to contribute to the evolution of diversity of SMs. In this paper we discuss the effects of hybridization on SMs and herbivore resistance by evaluating the literature and with special reference to our own research results from the hybrids between Jacobaea vulgaris (syn. Senecio jacobaea) and Jacobaea aquatica (syn. Senecio aquaticus). We also review the possible genetic mechanism which causes the variation of SMs and herbivore resistance in hybrids. Most SMs in hybrids are present in the parents as well. But hybrids may miss some parental SMs or have novel SMs. The concentration of parental SMs in hybrids generally is constrained by that in parental plants, but transgressive expression was present in some hybrids. Hybrids may be as susceptible (resistant) as the parents or more susceptible than the parents, but rarely more resistant than the parents. However, different hybrid classes (F1, F2, backcrossing and mixed genotypes) show different patterns in relation to herbivore resistance. The variation in SMs and herbivore resistance occurring in hybrids could be explained by complicated genetic mechanisms rather than a simple one-gene model. Most previous work in this field only reported mean trait values for hybrid classes and few studies focused on genotype differences within hybrid classes. Our study in Jacobaea hybrids showed transgressive segregation in most SMs and herbivore resistance. To summarize, our article shows that hybridization may increase the variation of SMs and affect herbivore resistance, which may partially explain the evolution of chemical diversity in plants.

Fig. 1

Division of test of secondary metabolite (SM) expression (a) and herbivore resistance in hybrid plants (b) over the different categories in percentages of the total. Numbers on the top of the bars indicate the number of SMs or herbivore resistance tests. For SM expression: ND no difference, Im intermediate expression, D dominant expression, U under expression, O over expression. For herbivore resistance: ND no difference, A additive resistance, D dominant resistance, S susceptible, R resistant. Data resources are shown in Tables 1 and 2. For detailed information see the text

Fig. 2

Division of tests of herbivore resistance in hybrid plants over the different categories in percentages of the total. a F1 hybrid populations, b F2 hybrid populations, c BC backcross populations, d MX mixed hybrid populations. Numbers on the top of bars indicate the number of tests. ND no difference, A additive resistance, D dominant resistance, S susceptible, R resistant. Data resources are shown in Table 2. For detailed information see the text

Fig. 3

Distribution of genotype means of a total PA concentration, b senecionine concentration, c jacobine concentration and d thrips damage in the shoots of J. aquaticus, J. vulgaris, F1 and F2 hybrids. Total PA includes free bases and N-oxides. For senecionine and jacobine only the free base concentration is given. Symbols above the bars indicate the position of parental and F1 genotype. Filled triangle J. aquatica parent, filled inverted triangle J. vulgaris parent, filled square F1-A, filled diamond F1-B. Data from Cheng et al. (unpublished)