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Molecular population genetics of inducible defense genes in Populus tremula
Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences.
2012 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Plant-herbivore interactions are among the most common of ecological interactions. It is therefore not surprising that plants have evolved multiple mechanisms to defend themselves, using both constitutive chemical and physical barriers and by induced responses which are only expressed after herbivory has occurred. Herbivores, on the other hand, respond to these plant defenses by evolving counter-adaptations which makes defenses less effective or even useless. Adaptation can occur at different geographical scales, with varying coevolutionary interactions across a spatially heterogenous landscape. By looking at the underlying genes responsible for these defensive traits and herbivore related phenotypic traits, it is possible to investigate the coevolutionary history of these plant- herbivore interactions. Here I use molecular population genetic tools to investigate the evolutionary history of several inducible defense genes in European Aspen (Populus tremula) in Sweden. Two genes, belonging to the Polyphenol oxidase gene-family (PPO1 and PPO2), show skews in their site frequency spectrum together with patterns of diversity and divergence from an outgroup which correspond to signatures of adaptive evolution (Paper II). 71 single nucleotide polymorphisms (SNPs) from seven inducible defense genes (PPO1-PPO3, TI2-TI5) show elevated levels of population differentiation compared to control genes (genes not involved in plant defense), and 10 of these defense SNPs show strong signatures of natural selection (Paper III). These 71 defense SNPs also divides a sample of Swedish P. tremula trees into three distinct geographical groups, corresponding to a Southern, Central and Northern cluster, a patterns that is not present in control SNPs (Paper III). The same geographical pattern, with a distinct Northern cluster, is also observed in several phenotypic traits related to herbivory in our common garden in Sävar (Paper IV). These phenotypic traits show patterns of apparent local maladaptation of the herbivore community to the host population which could indicate the presence of “information coevolution” between plants and herbivores (Paper IV). 15 unique defense SNPs also show significant associations to eight phenotypic traits but the causal effects of these SNP associations may be confounded by the geographic structure found in both the underlying genes and in the phenotypic traits. The co-occurrence of population structure in both defense genes and herbivore community traits may be the result from historical events during the post-glacial recolonization of Sweden.

Abstract [sv]

Interaktioner mellan växter och herbivorer är bland de vanligaste ekologiska interaktionerna och det är därför inte förvånande att växter har utvecklat flera olika mekanismer för att försvara sig. Dessa försvarsmekanismer består både av konstitutiva kemiska och fysiska barriärer så väl som inducerade försvar som bara är uttryckta efter att en växt har blivit skadad genom betning. Herbivorerna å sin sida svarar på dessa försvar genom att utveckla motanpassningar som gör växternas försvar mindre effektiva eller till och med verkningslösa. Dessa anpassningar kan ske över olika geografiska skalor beroende på om de samevolutionära interaktionerna varierar i ett rumsligt heterogent landskap. Genom att studera de underliggande gener som kontrollerar dessa försvarsegenskaper tillsammans med herbivorrelaterade fenotypiska egenskaper är det möjligt att undersöka den samevolutionära historien av interaktionerna mellan växter och herbivorer. Här använder jag mig av molekylärpopulationsgenetiska verktyg för att undersöka den evolutionära historien i flera inducerade försvarsgener hos asp (Populus tremula) i Sverige. Två gener, som tillhör genfamiljen Polyphenol-oxidaser (PPO1 och PPO2), uppvisar ett frekvensmönster som man förväntar sig vid positiv selektion. Detta mönster kan också ses i dessa geners diversitet samt i divergens från en utgrupp (Uppsats II). 71 ”single nucleotide polymorphisms” (SNPar) från 7 inducerade försvarsgener (PPO1-PPO3, TI2-TI5) visar förhöjda nivåer av populationsdifferentiering jämfört med kontrollgener (gener som inte är involverade i trädens försvar), och 10 av dessa försvars-SNPar visar även tecken på naturlig selektion (Uppsats III). Dessa 71 försvars-SNPar delar in ett urval av svenska aspar i tre distinkta geografiska grupper som beskriver ett sydligt, centralt och nordligt kluster som inte förekommer hos kontroll-SNPar (Uppsats III). Samma geografiska mönster, med ett distinkt nordligt kluster, återfinns däremot i ett antal fenotypiska egenskaper som är relaterade till herbivori i ett odlingsförsök utanför Sävar (Uppsats IV). Dessa fenotypiska egenskaper visar tecken på lokal felanpassning hos herbivorsamhället till den lokala värdpopulationen, vilket kan indikera förekomsten av ett ”samevolutionärt informationsutbyte” mellan växter och herbivorer (Uppsats IV). 15 unika försvars-SNPar påvisar också signifikanta associationer med 8 olika fenotypiska egenskaper, men om dessa har en verklig effekt eller inte är svårt att säga på grund av den geografiska strukturen som förekommer både hos de underliggande generna och hos de fenotypiska egenskaperna. Att denna populationsstruktur förekommer hos både försvarsgener och egenskaper som är förknippade med herbivorsamhället kan däremot vara ett resultat av historiska händelser som skett under aspens post-glaciala återkolonisation av Sverige.

Place, publisher, year, edition, pages
Umeå: Umeå Universitet , 2012. , 34 p.
Keyword [en]
Populus, herbivore defense, adaptation, population genetics, population structure, association mapping, complex traits
National Category
Evolutionary Biology Ecology Genetics
Research subject
evolutionär genetik
Identifiers
URN: urn:nbn:se:umu:diva-54361ISBN: 978-91-7459-415-7 (print)OAI: oai:DiVA.org:umu-54361DiVA: diva2:519239
Public defence
2012-05-16, KBC-huset, Stora hörsalen, KB3B1, Umeå Universitet, Umeå, 10:00 (English)
Opponent
Supervisors
Available from: 2012-04-25 Created: 2012-04-24 Last updated: 2015-04-29Bibliographically approved
List of papers
1. Using association mapping to dissect the genetic basis of complex traits in plants
Open this publication in new window or tab >>Using association mapping to dissect the genetic basis of complex traits in plants
2010 (English)In: Briefings in Functional Genomics & Proteomics, ISSN 1473-9550, E-ISSN 1477-4062, Vol. 9, no 2, 157-165 p.Article in journal (Refereed) Published
Abstract [en]

Association or linkage disequilibrium mapping has become a very popular method for dissecting the genetic basis of complex traits in plants. The benefits of association mapping, compared with traditional quantitative trait locus mapping, is, for example, a relatively detailed mapping resolution and that it is far less time consuming since no mapping populations need to be generated. The surge of interest in association mapping has been fueled by recent developments in genomics that allows for rapid identification and scoring of genetic markers which has traditionally limited mapping experiments. With the decreasing cost of genotyping future emphasis will likely focus on phenotyping, which can be both costly and time consuming but which is crucial for obtaining reliable results in association mapping studies. In addition, association mapping studies are prone to the identification of false positives, especially if the experimental design is not rigorously controlled. For example, population structure has long been known to induce many false positives and accounting for population structure has become one of the main issues when implementing association mapping in plants. Also, with increasing numbers of genetic markers used, the problem becomes separating true from false positive and this highlights the need for independent validation of identified association. With these caveats in mind, association mapping nevertheless shows great promise for helping us understand the genetic basis of complex traits of both economic and ecological importance.

Keyword
association mapping, complex traits, genotyping, plants, population structure
Identifiers
urn:nbn:se:umu:diva-32949 (URN)10.1093/bfgp/elp048 (DOI)000276191200009 ()20053815 (PubMedID)
Available from: 2010-03-31 Created: 2010-03-31 Last updated: 2017-12-12Bibliographically approved
2. Molecular population genetics of elicitor-induced resistance genes in European aspen (Populus tremula L., Salicaceae)
Open this publication in new window or tab >>Molecular population genetics of elicitor-induced resistance genes in European aspen (Populus tremula L., Salicaceae)
2011 (English)In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 6, no 9, e24867- p.Article in journal (Refereed) Published
Abstract [en]

Owing to their long life span and ecological dominance in many communities, forest trees are subject to attack from a diverse array of herbivores throughout their range, and have therefore developed a large number of both constitutive and inducible defenses. We used molecular population genetics methods to examine the evolution of eight genes in European aspen, Populus tremula, that are all associated with defensive responses against pests and/or pathogens, and have earlier been shown to become strongly up-regulated in poplars as a response to wounding and insect herbivory. Our results show that the majority of these defense genes show patterns of intraspecific polymorphism and site-frequency spectra that are consistent with a neutral model of evolution. However, two of the genes, both belonging to a small gene family of polyphenol oxidases, show multiple deviations from the neutral model. The gene PPO1 has a 600 bp region with a highly elevated K(A)/K(S) ratio and reduced synonymous diversity. PPO1 also shows a skew toward intermediate frequency variants in the SFS, and a pronounced fixation of non-synonymous mutations, all pointing to the fact that PPO1 has been subjected to recurrent selective sweeps. The gene PPO2 shows a marked excess of high frequency, derived variants and shows many of the same trends as PPO1 does, even though the pattern is less pronounced, suggesting that PPO2 might have been the target of a recent selective sweep. Our results supports data from both Populus and other species which have found that the the majority of defense-associated genes show few signs of selection but that a number of genes involved in mediating defense against herbivores show signs of adaptive evolution.

Place, publisher, year, edition, pages
Public Library of Science, 2011
National Category
Biological Sciences
Identifiers
urn:nbn:se:umu:diva-50727 (URN)10.1371/journal.pone.0024867 (DOI)21949772 (PubMedID)
Available from: 2011-12-20 Created: 2011-12-20 Last updated: 2017-12-08Bibliographically approved
3. Geographic structure and adaptive population differentiation in herbivore defence genes in European aspen (Populus tremula L., Salicaceae)
Open this publication in new window or tab >>Geographic structure and adaptive population differentiation in herbivore defence genes in European aspen (Populus tremula L., Salicaceae)
2012 (English)In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 21, no 9, 2197-2207 p.Article in journal (Refereed) Published
Abstract [en]

When a phenotypic trait is subjected to spatially variable selection and local adaptation, the underlying genes controlling the trait are also expected to show strong patterns of genetic differentiation since alternative alleles are favored in different geographical locations. Here we study 71 SNPs from seven genes associated with inducible defense responses in a sample of P. tremula collected from across Sweden. Four of these genes (PPO2, TI2, TI4 and TI5) show substantial population differentiation and a PCA conducted on the defense SNPs divides the Swedish population into three distinct clusters. Several defense SNPs show latitudinal clines, although these were not robust to multiple testing. However, five SNPs (located within TI4 and TI5) show strong longitudinal clines that remain significant after multiple test correction. Genetic geographical variation, supporting local adaptation, has earlier been confirmed in genes involved in the photoperiod pathway in P. tremula, but this is, to our knowledge, one of the first times that geographic variation has been found in genes involved in plant defense against antagonists.

Place, publisher, year, edition, pages
Blackwell Publishing, 2012
Keyword
adaptation, herbivore defence, population genetics, population structure, Populus
National Category
Genetics Evolutionary Biology
Research subject
evolutionär genetik
Identifiers
urn:nbn:se:umu:diva-54299 (URN)10.1111/j.1365-294X.2012.05524.x (DOI)
Available from: 2012-04-24 Created: 2012-04-24 Last updated: 2017-12-07Bibliographically approved
4. Population differentiation in arthropod community structure and phenotypic association with inducible defense genes in European Aspen (Populus tremula L., salicaceae)
Open this publication in new window or tab >>Population differentiation in arthropod community structure and phenotypic association with inducible defense genes in European Aspen (Populus tremula L., salicaceae)
Show others...
(English)Manuscript (preprint) (Other academic)
Abstract [en]

Plant-herbivore interactions are known to vary across a landscape due to both variation in abiotic and biotic factors. Such spatial variation tends to promoting local adaption of plants to the prevailing herbivore regime. Here we use data from a common garden to look for patterns across populations in the abundance and diversity of herbivorous insects. We also screen for variation in the untargeted metabolome of the foliage of a subset of the same trees. We also search for phenotypic associations between genetic variation in a number of wound-induced genes and phenotypic variation in herbivore abundance, diversity and in metabolomes. We observe significant genetic variation in a number of herbivore-related traits but low correlations between traits. We do observe substantial genetic structure in both herbivore community structure and in metabolic profiles and this structure is aligned with genetic structure we have previously documented for a set of defense genes. We also identify a number of significant associations between SNPs from wound-induced defense genes and a number of the herbivore traits and metabolic profiles. However, these associations are likely not causal, but are rather caused by the underlying population structure we observe. These results highlight to the importance of historical processes and the need to better understand both the current-day geographic distribution of different herbivore species as well as the post-glacial colonization history of both plants and herbivores.

Keyword
adaptation, arthropod community, population structure, association mapping, Populus
National Category
Genetics Evolutionary Biology Ecology
Research subject
evolutionär genetik
Identifiers
urn:nbn:se:umu:diva-54302 (URN)
Available from: 2012-04-24 Created: 2012-04-24 Last updated: 2015-04-29Bibliographically approved

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