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.
• Hybridization can lead to novel qualitative or quantitative variation of secondary metabolite (SM) expression that can have ecological and evolutionary consequences. • We measured pyrrolizidine alkaloid (PA) expression in the shoots and roots of a family including one Jacobaea vulgaris genotype and one Jacobaea aquatica genotype (parental genotypes), two F1 hybrid genotypes, and 102 F2 hybrid genotypes using liquid chromatography–tandem mass spectrometry (LC-MS/MS). • We detected 37 PAs in the roots and shoots of J. vulgaris, J. aquatica and the hybrids. PA concentrations and compositions differed between genotypes, and between roots and shoots. Three otosenine-like PAs that only occurred in the shoots of parental genotypes were present in the roots of F2 hybrids; PA compositions were sometimes novel in F2 hybrids compared with parental genotypes, and in some cases transgressive PA expression occurred. We also found that PAs from within structural groups covaried both in the roots and in the shoots, and that PA expression was correlated between shoots and roots. • Considerable and novel variation present among F2 hybrids indicates that hybridization has a potential role in the evolution of PA diversity in the genus Jacobaea, and this hybrid system is useful for studying the genetic control of PA expression.
Biological invasion is regarded as one of the greatest environmental problems facilitated by globalization. Some hypotheses about the invasive mechanisms of alien invasive plants consider the plant–herbivore interaction and the role of plant defense in this interaction. For example, the “Shift Defense Hypothesis” (SDH) argues that introduced plants evolve higher levels of qualitative defense chemicals and decreased levels of quantitative defense, as they are released of the selective pressures from specialist herbivores but still face attack from generalists. Common groundsel (Senecio vulgaris), originating from Europe, is a cosmopolitan invasive plant in temperate regions. As in other Senecio species, S. vulgaris contains pyrrolizidine alkaloids (PAs) as characteristic qualitative defense compounds. In this study, S. vulgaris plants originating from native and invasive ranges (Europe and China, respectively) were grown under identical conditions and harvested upon flowering. PA composition and concentration in shoot and root samples were determined using Liquid Chromatography-Tandem Mass Spectrometry (LC-MS/MS). We investigated the differences between native and invasive S. vulgaris populations with regard to quantitative and qualitative variation of PAs. We identified 20 PAs, among which senecionine, senecionine N-oxide, integerrimine N-oxide and seneciphylline N-oxide were dominant in the roots. In the shoots, in addition to the 4 PAs dominant in roots, retrorsine N-oxide, spartioidine N-oxide and 2 non-identified PAs were also prevalent. The roots possessed a lower PA diversity but a higher total PA concentration than the shoots. Most individual PAs as well as the total PA concentration were strongly positively correlated between the roots and shoots. Both native and invasive S. vulgaris populations shared the pattern described above. However, there was a slight trend indicating lower PA diversity and lower total PA concentration in invasive S. vulgaris populations than native populations, which is not consistent with the prediction of SDH.
Increasing evidence has confirmed the importance of plant-associated bacteria for plant growth and productivity, and thus it is hypothesized that interactions between bacteria and alien plants might play an important role in plant invasions. However, the diversity of the bacterial communities associated with invasive plants is poorly understood. We therefore investigated the diversity of rhizospheric and endophytic bacteria associated with the invasive annual plant Senecio vulgaris L. (Asteraceae) based on 16S rRNA gene data obtained from 57 samples of four Senecio vulgaris populations in a subtropical mountainous area in central China. Significant differences in diversity were observed between plant compartments. Specifically, the rhizosphere harbored many more bacterial operational taxonomic units and showed higher alpha diversity than the leaf and root endospheres. The relative abundance profiles of the bacterial community composition differed substantially between the compartments and populations, especially at the phylum and family levels. However, the top five phyla (Proteobacteria, Firmicutes, Bacteroidetes, Actinobacteria, and Acidobacteria) accounted for more than 90% of all the bacterial communities. Moreover, similar endophytic communities with a shared core set of bacteria were observed from different Senecio vulgaris populations. Heavy-metal-resistant, phosphate-solubilizing bacteria (Brevundimonas diminuta), nitrogen-fixing bacteria (Rhizobium leguminosarum), and cold-resistant bacteria (Exiguobacterium sibiricum) were present in the endosphere at relatively high abundance. This study, which reveals the structure of bacterial communities and their putative function in invasive Senecio vulgaris plants, is the first step in investigating the role of plant–bacteria interactions in the invasion of this species in China.