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Importance of tannins for responses of aspen to anthropogenic nitrogen enrichment
Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC). (Benedicte Riber Albrectsen)ORCID iD: 0000-0003-4802-5509
2016 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Boreal forests are often strongly nitrogen (N) limited. However, human activities are leading to increased N inputs into these ecosystems, through atmospheric N deposition and forest fertilization. N input into boreal forests can promote net primary productivity, increase herbivore and pathogen damage, and shift plant species composition and community structure. Genetic diversity has been suggested as a key mechanism to promote a plant species’ stability within communities in response to environmental change. Within any plant population, specific traits (e.g. growth and defense traits) can vary substantially among individuals, and a greater variation in traits may increase chances for the persistence of at least some individuals of a population, when environmental conditions change. One aspect of plant chemistry that can greatly vary among different genotypes (GTs) are condensed tannin (CTs). These secondary metabolites have been suggested to affect plant performance in many ways, e.g. through influencing plant growth, the interactions of plants with herbivores and pathogens, and through affecting litter decomposition, and hence the return of nutrients to plants. To investigate how genotypic variation in foliar CT production may mediate the effects that anthropogenic N enrichment can have on plant performance and litter decomposition, I performed a series of experiments. For these experiments, aspen (Populus tremula) GTs with contrasting abilities to produce foliar CTs (i.e. low- vs. high-tannin producers) were grown under 3 N conditions, representing ambient N (+0 kg ha-1), upper level atmospheric N deposition (+15 kg ha-1), and forest fertilization rates (+150 kg ha-1). This general experimental set-up was once established in a field-like environment, from which natural enemies were excluded, and once in a field, in which enemies were present. In my first two studies, I investigated tissue chemistry and plant performance in both environments. I observed that foliar CT levels decreased in response to N in the enemy‑free environment (study I), but increased with added N when enemies were present (study II). These opposing responses to N may be explained by differences in soil N availability in the two environments, or by induction of CTs after enemy attack. Enemy damage generally increased in response to N, and was higher in low-tannin than in high-tannin plants across all N levels. Plant growth of high‑tannin plants was restricted under ambient and low N conditions, probably due to a trade-off between growth and defense. This growth constraint for high‑tannin plants was weakened, when high amounts of N were added (study I and II), and when enemy levels were sufficiently high, so that benefits gained through defense could outweigh the costs of defense production (study II). Despite those general responses of low- and high‑tannin producers to added N, I also observed a number of individual responses of GTs to N addition, which in some case were not connected to the intrinsic ability of the GTs to produce foliar CTs. In study III, gene expression levels in young leaves and phenolic pools of the plants that were grown in the enemy‑free environment were studied. This study revealed that gene control over the regulation of the phenylpropanoid pathway (PPP) was distributed across the entire pathway. Moreover, PPP gene expression was higher in high-tannin GTs than in low‑tannin GTs, particularly under ambient N. At the low N level, gene expressions declined for both low- and high-tannin producers, whereas at the high N level expression at the beginning and the end of the PPP was upregulated and difference between tannin groups disappeared. Furthermore, this study showed that phenolic pools were frequently uncorrelated, and that phenolic pools were only to some extent related to tannin production and gene expression. In study IV, I investigated the decomposability of litter from the field plants. I found that N enrichment generally decreased mass loss, but there was substantial genetic variation in decomposition rates, and GTs were differentially responsive to added N. Study IV further showed that CTs only had a weak effect on decomposition, and other traits, such as specific leaf area and the lignin:N ratio, could better explain genotypic difference in mass loss. Furthermore, N addition caused a shift in which traits most strongly influenced decomposition rates. Collectively, the result of these studies highlight the importance of genetic diversity to promote the stability of species in environments that experience anthropogenic change.

Abstract [sv]

Boreala skogar är ofta mycket kväve (N) begränsade. Men mänskliga aktiviteter leder till ökad N tillförsel i dessa ekosystem, både genom depostition av N från atmosfären och skogsgödsling. N-tillförsel i boreala skogar kan främja netto primärproduktionen men även leda till ökade skador från naturliga fiender (herbivorer och patogener) samt skiftningar i växtartsammansättning. Genetisk mångfald har föreslagits som en viktig mekanism för att främja en växtarts stabilitet inom samhällen som upplever miljöförändringar. Inom varje växtpopulation kan specifika egenskaper (t.ex. tillväxt och försvar) varierar kraftigt mellan individer och en större variation i egenskaper kan öka chanserna för att åtminstone några individer från en population överlever ifall miljöförhållandena förändras. En aspekt av växtkemi som i hög grad kan variera mellan olika genotyper (GT) är bladens kondenserade tanniner (KT). Dessa sekundära metaboliter har föreslagits påverka växtens prestationsförmåga på många sätt, t.ex. genom att påverka tillväxt, interaktioner mellan växter och herbivorer eller patogener och genom att påverka förna nedbrytning, och följaktligen återbördandet av näringsämnen till kretsloppet. För att undersöka hur genotypiska variation i KT produktion kan påverka de effekter som antopogent N kan ha på växtens prestationsförmåga och förna nedbrytning, utförde jag en serie experiment. Jag studerade olika asp (Populus tremula) GT med olika förmåga att producera KT (låg- och hög-tannin producenter). Växterna odlades i tre olika N förhållanden, som representerade ambient N nivå (+0 kg ha-1), atmosfärisk N deposition = låg nivå (+15 kg ha-1), och skogsgödsling = hög nivå (150 kg ha‑1). Dessa GT etablerades i en fält-liknande miljö där naturliga fiender uteslutits och i ett fält där naturliga fiender var närvarande. I mina första två studierna undersökte jag vävnadskemi och växternas prestationsförmåga i de båda miljöerna. Jag observerade att KT nivåerna sjönk till följd av N‑tillsats i den fiende-fria miljön (studie I), men ökade med N-tillsats ifall fiender var närvarande (studie II). Dessa motsatta reaktioner på N-tillsats kan förklaras av skillnader i N-tillgång mellan de två odlingsplatserna eller genom ökad KT produktion som respons på angrepp. Skador orsakade av herbivorer och patogener ökade generellt till följd av N‑tillsats och var högre i låg-tannin än i hög‑tannin producerande GT oavsett N‑förhållande. Tillväxten hos växter från högtannin GT begränsades i ambient- och låg N-tillsats förhållanden, troligen på grund av att avvägning mellan tillväxt och försvar förskjutits emot försvar. Den begränsade tillväxten i hög-tannin växter minskade om stora mängder N tillsattes (studie I och II) och om antalet fiender var tillräckligt högt så att nyttan av försvaret kunde uppväga kostnaderna för försvarsproduktionen (studie II). Trots dessa generella respons hos låg- och hög-tannin GT till följd av N‑tillsats observerade jag även ett antal individuella respons hos GT som i vissa fall var orelaterade till växters förmåga att producera KT. I studie III undersöktes genuttrycksnivåer och fenolinnehåll i blad från växter som odladats i en miljö där naturliga fiender exkluderats. Denna studie visade att fenylpropanoidsyntesvägen (FPV) regleras genom kontroll av många av de undersökta FPV-generna. Dessutom var FPV genuttryck högre i hög-tannin GT än i låg-tannin GT, särskilt vid ambient N. Vid låg N-tillsats minskade genuttrycket av FPV-gener i både låg- och hög-tannin producenter, medan hög N-tillgång ledde till att gener i början och slutet av FPV uppreglerades och till att skillnaderna mellan tannin grupperna försvann. Dessutom visade studien att de separata fenol-poolerna ofta var okorrelerade med varandra och att fenol-poolerna bara till viss del var korrelerade med KT produktion och FPV-genutryck. I studie IV undersökte jag nedbrytningshastigheten för förnan från fältodlade aspar. Jag upptäckte att N-tillsats generellt minskade viktförlusten men att det fanns en betydande genetisk variation mellan GT och att dessa även var olika mottagliga för tillsatt N. Studie IV visade vidare att KT endast hade en svag effekt på nedbrytning och att andra egenskaper såsom specifik bladyta och lignin:N ratio kunde bättre förklara den genotypiska skillnaden i viktförlust. Dessutom orsakade N‑tillsats en förskjutning av vilka egenskaper som mest påverkade förnans nedbrytningshastighet. Sammanfattningsvis visar mina studier på vikten av genetisk mångfald för att främja växtartens stabilitet i miljöer som upplever antropogena förändringar.

Place, publisher, year, edition, pages
Umeå: Umeå University , 2016. , 57 p.
Keyword [en]
aspen, foliar condensed tannins, genetic variability, anthropogenic nitrogen enrichment, plant growth, plant defense, litter decomposition, Populus tremula
Keyword [sv]
asp, kondenserade tanniner, genetisk variabilitet, antropogent kväve, tillväxt, växtförsvar, förna nedbrytning, Populus tremula
National Category
Forest Science Ecology Soil Science
Research subject
biology, Environmental Science; Ecological Botany; Entomology; Physiological Botany; Population Biology
Identifiers
URN: urn:nbn:se:umu:diva-120248ISBN: 978-91-7601-505-6 (print)OAI: oai:DiVA.org:umu-120248DiVA: diva2:927526
Public defence
2016-06-07, KBC3A9 (Lilla Hörsalen), KBC huset, Umeå universitet, Umeå, 10:00 (English)
Opponent
Supervisors
Available from: 2016-05-17 Created: 2016-05-12 Last updated: 2016-05-26Bibliographically approved
List of papers
1. Genotypic tannin levels in Populus tremula impact the way nitrogen enrichment affects growth and allocation responses for some traits and not for others
Open this publication in new window or tab >>Genotypic tannin levels in Populus tremula impact the way nitrogen enrichment affects growth and allocation responses for some traits and not for others
2015 (English)In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 10, no 10, e0140971Article in journal (Refereed) Published
Abstract [en]

Plant intraspecific variability has been proposed as a key mechanism by which plants adapt to environmental change. In boreal forests where nitrogen availability is strongly limited, nitrogen addition happens indirectly through atmospheric N deposition and directly through industrial forest fertilization. These anthropogenic inputs of N have numerous environmental consequences, including shifts in plant species composition and reductions in plant species diversity. However, we know less about how genetic differences within plant populations determine how species respond to eutrophication in boreal forests. According to plant defense theories, nitrogen addition will cause plants to shift carbon allocation more towards growth and less to chemical defense, potentially enhancing vulnerability to antagonists. Aspens are keystone species in boreal forests that produce condensed tannins to serve as chemical defense. We conducted an experiment using ten Populus tremula genotypes from the Swedish Aspen Collection that express extreme levels of baseline investment into foliar condensed tannins. We investigated whether investment into growth and phenolic defense compounds in young plants varied in response to two nitrogen addition levels, corresponding to atmospheric N deposition and industrial forest fertilization. Nitrogen addition generally caused growth to increase, and tannin levels to decrease; however, individualistic responses among genotypes were found for height growth, biomass of specific tissues, root: shoot ratios, and tissue lignin and N concentrations. A genotype's baseline ability to produce and store condensed tannins also influenced plant responses to N, although this effect was relatively minor. High-tannin genotypes tended to grow less biomass under low nitrogen levels and more at the highest fertilization level. Thus, the ability in aspen to produce foliar tannins is likely associated with a steeper reaction norm of growth responses, which suggests a higher plasticity to nitrogen addition, and potentially an advantage when adapting to higher concentrations of soil nitrogen.

National Category
Botany
Identifiers
urn:nbn:se:umu:diva-111477 (URN)10.1371/journal.pone.0140971 (DOI)000363248400088 ()26488414 (PubMedID)
Available from: 2015-12-09 Created: 2015-11-13 Last updated: 2017-12-01Bibliographically approved
2. Differences in constitutive tannin-level influence Populus tremula genotypes’ responses to anthropogenic N-enrichment
Open this publication in new window or tab >>Differences in constitutive tannin-level influence Populus tremula genotypes’ responses to anthropogenic N-enrichment
(English)Manuscript (preprint) (Other academic)
National Category
Ecology
Identifiers
urn:nbn:se:umu:diva-120374 (URN)
Available from: 2016-05-16 Created: 2016-05-16 Last updated: 2016-05-16
3. Genetic variation of foliar tannins determines how soil nitrogen impacts phenylpropanoid pathway regulation in aspen
Open this publication in new window or tab >>Genetic variation of foliar tannins determines how soil nitrogen impacts phenylpropanoid pathway regulation in aspen
Show others...
(English)Article in journal (Other academic) Submitted
National Category
Ecology
Identifiers
urn:nbn:se:umu:diva-120376 (URN)
Available from: 2016-05-16 Created: 2016-05-16 Last updated: 2016-05-16
4. The effect of anthropogenic nitrogen enrichment on litter decomposition differs among contrasting Populus tremula L. genotypes
Open this publication in new window or tab >>The effect of anthropogenic nitrogen enrichment on litter decomposition differs among contrasting Populus tremula L. genotypes
(English)Article in journal (Other academic) Submitted
National Category
Ecology
Identifiers
urn:nbn:se:umu:diva-120377 (URN)
Available from: 2016-05-16 Created: 2016-05-16 Last updated: 2016-05-16

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