The Effect of Hybridization on Secondary Metabolites and Herbivore Resistance: Implications for the Evolution of Chemical Diversity in Plants
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Phytochem Rev (2011) 10:107–117 DOI 10.1007/s11101-010-9194-9 The effect of hybridization on secondary metabolites and herbivore resistance: implications for the evolution of chemical diversity in plants Dandan Cheng • Klaas Vrieling • Peter G. L. Klinkhamer Received: 29 January 2010 / Accepted: 17 August 2010 / Published online: 1 September 2010 Ó The Author(s) 2010. This article is published with open access at Springerlink.com Abstract The diversity of secondary metabolites parental SMs in hybrids generally is constrained by (SMs) has been poorly understood from both a that in parental plants, but transgressive expression mechanistic and a functional perspective. Hybridiza- was present in some hybrids. Hybrids may be as tion is suggested to contribute to the evolution of susceptible (resistant) as the parents or more suscep- diversity of SMs. In this paper we discuss the effects tible than the parents, but rarely more resistant than of hybridization on SMs and herbivore resistance by the parents. However, different hybrid classes (F1, evaluating the literature and with special reference to F2, backcrossing and mixed genotypes) show differ- our own research results from the hybrids between ent patterns in relation to herbivore resistance. The Jacobaea vulgaris (syn. Senecio jacobaea) and variation in SMs and herbivore resistance occurring Jacobaea aquatica (syn. Senecio aquaticus). We also in hybrids could be explained by complicated genetic review the possible genetic mechanism which causes mechanisms rather than a simple one-gene model. the variation of SMs and herbivore resistance in Most previous work in this field only reported mean hybrids. Most SMs in hybrids are present in the trait values for hybrid classes and few studies focused parents as well. But hybrids may miss some parental on genotype differences within hybrid classes. Our SMs or have novel SMs. The concentration of 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 D. Cheng (&) Á K. Vrieling Á P. G. L. Klinkhamer the evolution of chemical diversity in plants. Plant Ecology and Phytochemistry Section, Institute of Biology, Leiden University, Sylviusweg 72, 2300 RA Leiden, The Netherlands Keywords Chemical defense Á Pyrrolizidine e-mail: [email protected] alkaloids Á Jacobaea vulgaris Á Jacobaea aquatica K. Vrieling e-mail: [email protected] Abbreviations P. G. L. Klinkhamer AFLP Amplified fragment length polymorphism e-mail: [email protected] BC Backcrossing dw Dry weigh of plant material D. Cheng PA Pyrrolizidine alkaloid Institute of Ecology & Environmental Science, School of Environmental Studies, China University QTL Quantitative Trait Locus of Geosciences, Lumo Road 388, 430074 Wuhan, China SM Secondary metabolite 123 108 Phytochem Rev (2011) 10:107–117 Introduction (3) express novel SMs that are absent in each parent or (4) express a parental SM in other tissues than the parents. The last two are regarded as novelty. Rieseberg The role of hybridization with respect to the origin of and Ellstrand (1993) showed that, among 743 SMs biodiversity has been debated for over a century. identified in parents and their F1 hybrids of 21 genera Recent research indicates that hybridization plays a from 24 studies, 68% were present both in the hybrids role in the generation of novel traits, transgressive and their parents, 27% only occurred in parental plants, segregation, introgression of traits between species and 5% of the SMs were only found in the hybrids. The and speciation itself (e.g. Stebbins 1959; Arnold 1992; frequency of novelty was ca. 8% in later generation Rieseberg and Carney 1998). Furthermore hybridiza- hybrids and even higher (ca.18%) in hybrid-derived tion may contribute to the success of invasive species species. The survey by Orians (2000) based on 31 and cause the displacement and extinction of local studies including 80 hybrid crosses showed that at least species (Huxel 1999; Prentis et al. 2007). To elucidate one specific SM was missing in the hybrids in ca. 60% of the diversity in SMs and plant resistance from an the crosses and at least one novel SM was found in ca. ecological and evolutionary perspective, hybrids are 40% of the crosses. We extended the reviews of regarded as a good study system (Fritz et al. 1999; Rieseberg and Ellstrand (1993) and Orians (2000)by Orians 2000). In this paper we will focus on the including 7 studies published from 2000 to 2010. From consequences of hybridization for the generation of these studies we scored the presence and absence of SMs qualitative and quantitative variation in secondary in different hybrid classes. The combined results show chemistry and the possible effects on hybrids fitness in that 24.2% of the 1,112 SMs studied were not present in relation to herbivore resistance. We asked the follow- the hybrids, 5.5% were novel SMs only present in the ing questions: (1) Do hybrids have a greater qualitative hybrids and 70.3% were present in both the parents and or quantitative variation of SMs and herbivore resis- hybrids (Table 1). Adding more studies did not change tance relative to the parental taxa? (2) Does this pattern the results obtained by the previous review suggesting differ between different classes of hybrids? (3) Is the that the data are solid (Table 1,chi-square= 2.8, variation in SMs and herbivore resistance determined df = 2, P = 0.24). by simple genetic mechanisms? From an evolutionary point of view it is important to know if among a hybrid Quantitative variation of SMs in hybrids population some individuals show more extreme trait values than either of the parental species. Unfortu- Orians (2000) divided the quantitative variation of nately, most studies reported mean trait values for the concentration of SMs in F1 hybrids relative to the hybrid classes and only very few studies focused on parents in five categories: (1) higher than in either genotype differences within hybrid classes. Finally, parent (O-overexpression); (2) intermediate between we therefore, will summarize the development of our those of the two parental taxa (Im-intermediate research on Jacobaea hybrids as a case study with expression); (3) lower than in either parent special attention on within hybrid genotype variation. (U-underexpression); (4) similar to that in one of Hybridization occurs frequently in Senecio and Jac- the two parental taxa (D-dominance expression); or obaea species. The interaction of herbivorous insects and (5) not different from either parent when the parents plants of these species in relation to the pyrrolizidine show similar concentrations (ND-no difference). alkaloids (PAs) have been intensively studied (van der From an evolutionary point of view, we think the Meijden et al. 1989, 1992; Vrieling et al. 1991; Hartmann fourth category (Dominance) should be divided to 1999; Macel et al. 2002, 2005; Leiss et al. 2009a). two subcategories: Dl-dominance to the lower parent and Dh-dominance to the higher parent. A meta- The effect of hybridization on SMs analysis of 5 studies showed that among the 96 parental SMs present in the F1 hybrids, most are Qualitative variation of SMs in hybrids either expressed at concentrations similar to one of the parents or at intermediate concentrations (33 and Hybrids may: (1) express all of the SMs of the parental 29%, respectively), some are over expressed (19%), taxa; (2) fail to express certain parental SMs; while others occur at lower concentrations than in 123 Phytochem Rev (2011) 10:107–117 Table 1 Qualitative and quantitative variation of the secondary metabolites (SMs) in hybrid plants Taxa SM Hybrid Quanlitative variation Quantitative variation Reference class Missing Complementary Novel ND Im Dl Dh U O SMs SMs SMs Allium cepa 9 A. kermesinuma Cysteine sulfoxides and F1 0 26 0 7 8 4 1 2 4 Storsberg et al. (2004) volatile sulfur compounds Corymbia citriodora subsp. Hexane extracts of leaves F1 17 29 5 0 7 1 2 0 4 Nahrung et al. (2009) variegata 9 C. torellianab Citrus meyerii 9 C. limon cv. Essential oils F1 5 55 1 38 5 7 4 1 1 Verzera et al. (2005) Cavone C. medica 9 C. limon cv. Cavone F1 1 49 0 39 3 4 3 0 0 Eucalyptus globulusc Sideroxylonal and F1(SN) 0 6 0 0 0 1 0 1 4 O’Reilly-Wapstra et al. macrocarpal F1(NS) 0 6 0 1 0 1 3 0 1 (2005) Eucalyptus. grandis 9 Essential oils F1 14 10 3 0 7 1 0 1 1 Toloza et al. (2008) E. camaldulensisd E. grandis 9 E. tereticornisd F1 15 10 3 0 5 0 1 2 2 Quercus. gambelii 9 Q. griseae Ellagitannins F1 0 10 0 0 5 0 0 5 0 Yarnes et al. (2008) BC(gr) 0 10 0 2 4 2 0 1 1 BC(ga) 0 10 0 3 4 1 1 1 0 Salix caprea 9 S. repens Phenolic glucosides F1 0 7 0 0 2 4 1 0 0 Hallgren et al. (2003) F2 0 7 0 0 5 0 2 0 0 BC(c) 0 7 0 0 0 6 1 0 0 BC(r) 0 7 0 1 5 0 1 0 0 Results previous reviews:(qualitative data from 217 533 49 5 28 32f 13 18 Rieseberg and Ellstrand Rieseberg and Ellstrand 1993 and quantitative data (1993), Orians (2000) from Orians 2000) Total 269 782 61 96 88 84f 27 36 Percentage 24.2% 70.3% 5.5% 29.0% 26.6% 25.4%f 8.2% 10.9% F1, F2, BC (pure species parents indicated by the first or first two letters), ND (no difference from both of the parents), Im (intermediate between the parents), Dl (similar to the lower parent), Dh (similar to the higher parent), U (underexpression), O (overexpression) a The average concentration of individual SMs of 6 F1 hybrids b SMs appearing in [50% of hybrid individuals scored as present and those appearing \50% scored as missing c Intraspecies hybrids of two geographically distinct populations (races) of E.