How eco-evolutionary principles can guide tree breeding and tree biotechnology for enhanced productivity
Abstract
Tree breeding and biotechnology can enhance forest productivity and help alleviate the rising pressure on forests from climate change and human exploitation. While many physiological processes and genes are targeted in search of genetically improved tree productivity, an overarching principle to guide this search is missing. Here in this paper, we propose a method to identify the traits that can be modified to enhance productivity, based on the differences between trees shaped by natural selection and ‘improved’ trees with traits optimized for productivity. We developed a tractable model of plant growth and survival to explore such potential modifications under a range of environmental conditions, from non-water limited to severely drought-limited sites. We show how key traits are controlled by a trade-off between productivity and survival, and that productivity can be increased at the expense of long-term survival by reducing isohydric behavior (stomatal regulation of leaf water potential) and allocation to defense against pests compared with native trees. In contrast, at dry sites occupied by naturally drought-resistant trees, the model suggests a better strategy may be to select trees with slightly lower wood density than the native trees and to augment isohydric behavior and allocation to defense. Thus, which traits tomore »
- Authors:
-
- International Institute for Applied Systems Analysis, Laxenburg (Austria). Ecosystems Services and Management Program
- Duke Univ., Durham, NC (United States). Nicholas School of the Environment and Earth Sciences
- Swedish University of Agricultural Sciences,Umeå (Sweden). Department of Forest Ecology and Management and Department of Forest Genetics and Plant Physiology , Umeå Plant Science Centre
- Publication Date:
- Research Org.:
- Duke Univ., Durham, NC (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1454931
- Grant/Contract Number:
- SC0006967; SC0006700
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Tree Physiology
- Additional Journal Information:
- Journal Volume: 34; Journal Issue: 11; Journal ID: ISSN 0829-318X
- Publisher:
- Oxford University Press
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; 54 ENVIRONMENTAL SCIENCES; adaptation; anisohydric; aridity; climate; ecology; evolution; forestry; functional traits; genetic modification; gmo; hydraulics; life history; mathematical model; mortality; risk management; selection; strategy; transpiration; wood
Citation Formats
Franklin, Oskar, Palmroth, Sari, and Nasholm, Torgny. How eco-evolutionary principles can guide tree breeding and tree biotechnology for enhanced productivity. United States: N. p., 2014.
Web. doi:10.1093/treephys/tpu111.
Franklin, Oskar, Palmroth, Sari, & Nasholm, Torgny. How eco-evolutionary principles can guide tree breeding and tree biotechnology for enhanced productivity. United States. https://doi.org/10.1093/treephys/tpu111
Franklin, Oskar, Palmroth, Sari, and Nasholm, Torgny. Sat .
"How eco-evolutionary principles can guide tree breeding and tree biotechnology for enhanced productivity". United States. https://doi.org/10.1093/treephys/tpu111. https://www.osti.gov/servlets/purl/1454931.
@article{osti_1454931,
title = {How eco-evolutionary principles can guide tree breeding and tree biotechnology for enhanced productivity},
author = {Franklin, Oskar and Palmroth, Sari and Nasholm, Torgny},
abstractNote = {Tree breeding and biotechnology can enhance forest productivity and help alleviate the rising pressure on forests from climate change and human exploitation. While many physiological processes and genes are targeted in search of genetically improved tree productivity, an overarching principle to guide this search is missing. Here in this paper, we propose a method to identify the traits that can be modified to enhance productivity, based on the differences between trees shaped by natural selection and ‘improved’ trees with traits optimized for productivity. We developed a tractable model of plant growth and survival to explore such potential modifications under a range of environmental conditions, from non-water limited to severely drought-limited sites. We show how key traits are controlled by a trade-off between productivity and survival, and that productivity can be increased at the expense of long-term survival by reducing isohydric behavior (stomatal regulation of leaf water potential) and allocation to defense against pests compared with native trees. In contrast, at dry sites occupied by naturally drought-resistant trees, the model suggests a better strategy may be to select trees with slightly lower wood density than the native trees and to augment isohydric behavior and allocation to defense. Thus, which traits to modify, and in which direction, depend on the original tree species or genotype, the growth environment and wood-quality versus volume production preferences. In contrast to this need for customization of drought and pest resistances, consistent large gains in productivity for all genotypes can be obtained if root traits can be altered to reduce competition for water and nutrients. In conclusion, our approach illustrates the potential of using eco-evolutionary theory and modeling to guide plant breeding and genetic technology in selecting target traits in the quest for higher forest productivity.},
doi = {10.1093/treephys/tpu111},
journal = {Tree Physiology},
number = 11,
volume = 34,
place = {United States},
year = {Sat Nov 01 00:00:00 EDT 2014},
month = {Sat Nov 01 00:00:00 EDT 2014}
}
Web of Science
Figures / Tables:
Works referenced in this record:
Genetics of superior growth traits in trees are being mapped but will the faster-growing risk-takers make it in the wild?
journal, November 2014
- Nasholm, T.; Palmroth, S.; Ganeteg, U.
- Tree Physiology, Vol. 34, Issue 11
Influence of water deficit on the molecular responses of Pinus contorta x Pinus banksiana mature trees to infection by the mountain pine beetle fungal associate, Grosmannia clavigera
journal, December 2013
- Arango-Velez, A.; Gonzalez, L. M. G.; Meents, M. J.
- Tree Physiology, Vol. 34, Issue 11
A generic model of thinning and stand density effects on forest growth, mortality and net increment
journal, January 2009
- Franklin, Oskar; Aoki, Kentaro; Seidl, Rupert
- Annals of Forest Science, Vol. 66, Issue 8
Competitive interactions across a soil fertility gradient in a multispecies forest
journal, March 2013
- Coates, K. David; Lilles, Erica B.; Astrup, Rasmus
- Journal of Ecology, Vol. 101, Issue 3
Genomic and physiological approaches to advancing forest tree improvement
journal, July 2008
- Nelson, C. D.; Johnsen, K. H.
- Tree Physiology, Vol. 28, Issue 7
Towards optimizing wood development in bioenergy trees: Research review
journal, December 2011
- Nieminen, Kaisa; Robischon, Marcel; Immanen, Juha
- New Phytologist, Vol. 194, Issue 1
Effects of tree Density and Stand age on Carbon Allocation Patterns in Postfire Lodgepole pine
journal, April 2004
- Litton, Creighton M.; Ryan, Michael G.; Knight, Dennis H.
- Ecological Applications, Vol. 14, Issue 2
A New Method to Assess Competition in Coffee Clonal Trials with Single-Tree Plots in Côte d'Ivoire
journal, January 2001
- Montagnon, C.; Flori, A.; Cilas, C.
- Agronomy Journal, Vol. 93, Issue 1
Yield–trait performance landscapes: from theory to application in breeding maize for drought tolerance
journal, November 2010
- Messina, Carlos D.; Podlich, Dean; Dong, Zhanshan
- Journal of Experimental Botany, Vol. 62, Issue 3
An ecohydrological perspective on drought-induced forest mortality
journal, May 2014
- Parolari, Anthony J.; Katul, Gabriel G.; Porporato, Amilcare
- Journal of Geophysical Research: Biogeosciences, Vol. 119, Issue 5
The variability of stomatal sensitivity to leaf water potential across tree species indicates a continuum between isohydric and anisohydric behaviours
journal, May 2014
- Klein, Tamir
- Functional Ecology, Vol. 28, Issue 6
Mortality Rates of 205 Neotropical Tree and Shrub Species and the Impact of a Severe Drought
journal, February 1995
- Condit, Richard; Hubbell, Stephen P.; Foster, Robin B.
- Ecological Monographs, Vol. 65, Issue 4
Resource limitation in a competitive context determines complex plant responses to experimental resource additions
journal, November 2013
- Farrior, Caroline E.; Tilman, David; Dybzinski, Ray
- Ecology, Vol. 94, Issue 11
Proteins for Transport of Water and Mineral Nutrients across the Membranes of Plant Cells
journal, April 1999
- Chrispeels, Maarten J.; Crawford, Nigel M.; Schroeder, Julian I.
- The Plant Cell, Vol. 11, Issue 4
COMPETITION AMONG EUCALYPTUS TREES DEPENDS ON GENETIC VARIATION AND RESOURCE SUPPLY
journal, October 2008
- Boyden, Suzanne; Binkley, Dan; Stape, José Luiz
- Ecology, Vol. 89, Issue 10
Genomic selection for growth and wood quality in Eucalyptus: capturing the missing heritability and accelerating breeding for complex traits in forest trees
journal, February 2012
- Resende, Marcos D. V.; Resende, Márcio F. R.; Sansaloni, Carolina P.
- New Phytologist, Vol. 194, Issue 1
Any trait or trait-related allele can confer drought tolerance: just design the right drought scenario
journal, September 2011
- Tardieu, F.
- Journal of Experimental Botany, Vol. 63, Issue 1
Condensed tannin biosynthesis and polymerization synergistically condition carbon use, defense, sink strength and growth in Populus
journal, December 2013
- Harding, S. A.; Xue, L. -J.; Du, L.
- Tree Physiology, Vol. 34, Issue 11
Transpiration modulates phosphorus acquisition in tropical tree seedlings
journal, August 2011
- Cernusak, L. A.; Winter, K.; Turner, B. L.
- Tree Physiology, Vol. 31, Issue 8
The Ball-Berry-Leuning and Tardieu-Davies stomatal models: synthesis and extension within a spatially aggregated picture of guard cell function
journal, November 2002
- Dewar, R. C.
- Plant, Cell and Environment, Vol. 25, Issue 11
Climate and weather influences on spatial temporal patterns of mountain pine beetle populations in Washington and Oregon
journal, November 2012
- Preisler, Haiganoush K.; Hicke, Jeffrey A.; Ager, Alan A.
- Ecology, Vol. 93, Issue 11
Plant diversity and drought: The role of deep roots
journal, October 2014
- Lindh, Magnus; Zhang, Lai; Falster, Daniel
- Ecological Modelling, Vol. 290
Risk-taking plants: Anisohydric behavior as a stress-resistance trait
journal, July 2012
- Sade, Nir; Gebremedhin, Alem; Moshelion, Menachem
- Plant Signaling & Behavior, Vol. 7, Issue 7
Herbivory and Plant Defenses in Tropical Forests
journal, November 1996
- Coley, P. D.; Barone, J. A.
- Annual Review of Ecology and Systematics, Vol. 27, Issue 1
Managing productivity and drought risk in Eucalyptus globulus plantations in south-western Australia
journal, December 2009
- White, Donald A.; Crombie, D. Stuart; Kinal, Joe
- Forest Ecology and Management, Vol. 259, Issue 1
Let the concept of trait be functional!
journal, May 2007
- Violle, Cyrille; Navas, Marie-Laure; Vile, Denis
- Oikos, Vol. 116, Issue 5
Tragedy of the commons as a result of root competition
journal, August 2001
- Gersani, Mordechai; Brown, Joel s.; O'Brien, Erin E.
- Journal of Ecology, Vol. 89, Issue 4
Strategy Space and the Disturbance Spectrum: A Life‐History Model for Tree Species Coexistence
journal, July 2000
- Loehle, Craig
- The American Naturalist, Vol. 156, Issue 1
The importance of wood traits and hydraulic conductance for the performance and life history strategies of 42 rainforest tree species
journal, November 2009
- Poorter, Lourens; McDonald, Imole; Alarcón, Alfredo
- New Phytologist, Vol. 185, Issue 2
Linking definitions, mechanisms, and modeling of drought-induced tree death
journal, December 2012
- Anderegg, William R. L.; Berry, Joseph A.; Field, Christopher B.
- Trends in Plant Science, Vol. 17, Issue 12
Balancing the costs of carbon gain and water transport: testing a new theoretical framework for plant functional ecology
journal, November 2013
- Prentice, I. Colin; Dong, Ning; Gleason, Sean M.
- Ecology Letters, Vol. 17, Issue 1
Genetic strategies for dissecting complex traits in biomass willows (Salix spp.)
journal, November 2013
- Hanley, S. J.; Karp, A.
- Tree Physiology, Vol. 34, Issue 11
Heterogeneous distribution of soil nutrients increase intra-specific competition in the clonal plant Glechoma hederacea
journal, May 2014
- Roiloa, Sergio R.; Sánchez-Rodríguez, Paula; Retuerto, Rubén
- Plant Ecology, Vol. 215, Issue 8
Overexpression of a Plasma Membrane Aquaporin in Transgenic Tobacco Improves Plant Vigor under Favorable Growth Conditions but Not under Drought or Salt Stress
journal, January 2003
- Aharon, Refael; Shahak, Yosepha; Wininger, Smadar
- The Plant Cell, Vol. 15, Issue 2
Trends in wood density and structure are linked to prevention of xylem implosion by negative pressure
journal, February 2001
- Hacke, Uwe G.; Sperry, John S.; Pockman, William T.
- Oecologia, Vol. 126, Issue 4
Molecular and physiological responses to abiotic stress in forest trees and their relevance to tree improvement
journal, April 2014
- Harfouche, A.; Meilan, R.; Altman, A.
- Tree Physiology, Vol. 34, Issue 11
Least‐Cost Input Mixtures of Water and Nitrogen for Photosynthesis
journal, January 2003
- Wright, Ian J.; Reich, Peter B.; Westoby, Mark
- The American Naturalist, Vol. 161, Issue 1
The world-wide ‘fast-slow’ plant economics spectrum: a traits manifesto
journal, February 2014
- Reich, Peter B.
- Journal of Ecology, Vol. 102, Issue 2
Improving plant stress tolerance and yield production: is the tonoplast aquaporin SlTIP2;2 a key to isohydric to anisohydric conversion?
journal, November 2008
- Sade, Nir; Vinocur, Basia J.; Diber, Alex
- New Phytologist, Vol. 181, Issue 3
Competition effects in cocoa (Theobroma cacao L.) hybrid trials
journal, January 2002
- Lachenaud, Ph.; Montagnon, C.
- Euphytica, Vol. 128, Issue 1, p. 97-104
Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought?
journal, June 2008
- McDowell, Nate; Pockman, William T.; Allen, Craig D.
- New Phytologist, Vol. 178, Issue 4
Forest fine-root production and nitrogen use under elevated CO 2 : contrasting responses in evergreen and deciduous trees explained by a common principle
journal, January 2009
- Franklin, Oskar; McMURTRIE, Ross E.; Iversen, Colleen M.
- Global Change Biology, Vol. 15, Issue 1
A model analysis of the influence of root and foliage allocation on forest production and competition between trees
journal, March 1993
- King, D. A.
- Tree Physiology, Vol. 12, Issue 2
Genetic transformation of eucalyptus
journal, February 2011
- Girijashankar, V.
- Physiology and Molecular Biology of Plants, Vol. 17, Issue 1
Integrating plant hydraulics and gas exchange along the drought-response trait spectrum
journal, October 2014
- Manzoni, S.
- Tree Physiology, Vol. 34, Issue 10
Modeling carbon allocation in trees: a search for principles
journal, January 2012
- Franklin, O.; Johansson, J.; Dewar, R. C.
- Tree Physiology, Vol. 32, Issue 6
A new look at water transport regulation in plants
journal, July 2014
- Martínez-Vilalta, Jordi; Poyatos, Rafael; Aguadé, David
- New Phytologist, Vol. 204, Issue 1
Fitness and its role in evolutionary genetics
journal, August 2009
- Orr, H. Allen
- Nature Reviews Genetics, Vol. 10, Issue 8
Tree life history strategies: the role of defenses
journal, February 1988
- Loehle, Craig
- Canadian Journal of Forest Research, Vol. 18, Issue 2
Transgenic Populus Trees for Forest Products, Bioenergy, and Functional Genomics
journal, September 2011
- Ye, Xia; Busov, Victor; Zhao, Nan
- Critical Reviews in Plant Sciences, Vol. 30, Issue 5
Genetic Modification of Short Rotation Popular Wood: Properties for Ethanol Fuel and Fiber Productions
journal, January 2001
- Dinus, R.
- Critical Reviews in Plant Sciences, Vol. 20, Issue 1
Forests trapped in nitrogen limitation - an ecological market perspective on ectomycorrhizal symbiosis
journal, May 2014
- Franklin, Oskar; Näsholm, Torgny; Högberg, Peter
- New Phytologist, Vol. 203, Issue 2
Towards a worldwide wood economics spectrum
journal, April 2009
- Chave, Jerome; Coomes, David; Jansen, Steven
- Ecology Letters, Vol. 12, Issue 4
Forest biotech and climate change
journal, June 2008
- Fenning, Trevor M.; Walter, Christian; Gartland, Kevan M. A.
- Nature Biotechnology, Vol. 26, Issue 6
The Brazil Eucalyptus Potential Productivity Project: Influence of water, nutrients and stand uniformity on wood production
journal, April 2010
- Stape, Jose Luiz; Binkley, Dan; Ryan, Michael G.
- Forest Ecology and Management, Vol. 259, Issue 9
Optimal nitrogen allocation controls tree responses to elevated CO 2
journal, June 2007
- Franklin, Oskar
- New Phytologist, Vol. 174, Issue 4
Biomass allocation to leaves, stems and roots: meta-analyses of interspecific variation and environmental control: Tansley review
journal, November 2011
- Poorter, Hendrik; Niklas, Karl J.; Reich, Peter B.
- New Phytologist, Vol. 193, Issue 1
Strategies of a Bornean tropical rainforest water use as a function of rainfall regime: isohydric or anisohydric?: Strategies of a tropical rainforest water use
journal, October 2011
- Kumagai, Tomo'Omi; Porporato, Amilcare
- Plant, Cell & Environment, Vol. 35, Issue 1
A coupled model of stomatal conductance, photosynthesis and transpiration
journal, July 2003
- Tuzet, A.; Perrier, A.; Leuning, R.
- Plant, Cell and Environment, Vol. 26, Issue 7
Investigating the drought-stress response of hybrid poplar genotypes by metabolite profiling
journal, October 2013
- Barchet, G. L. H.; Dauwe, R.; Guy, R. D.
- Tree Physiology, Vol. 34, Issue 11
Increasing drought under global warming in observations and models
journal, August 2012
- Dai, Aiguo
- Nature Climate Change, Vol. 3, Issue 1
Works referencing / citing this record:
An evolutionary ecology perspective to address forest pathology challenges of today and tomorrow
journal, March 2016
- Desprez-Loustau, Marie-Laure; Aguayo, Jaime; Dutech, Cyril
- Annals of Forest Science, Vol. 73, Issue 1
Insect outbreak shifts the direction of selection from fast to slow growth rates in the long-lived conifer Pinus ponderosa
journal, June 2017
- de la Mata, Raul; Hood, Sharon; Sala, Anna
- Proceedings of the National Academy of Sciences, Vol. 114, Issue 28
The importance of intraspecific variation in tree responses to elevated [CO 2 ]: breeding and management of future forests
journal, May 2016
- Ainsworth, Elizabeth A.
- Tree Physiology, Vol. 36, Issue 6
An evolutionary ecology perspective to address forest pathology challenges of today and tomorrow
journal, March 2016
- Desprez-Loustau, Marie-Laure; Aguayo, Jaime; Dutech, Cyril
- Annals of Forest Science, Vol. 73, Issue 1
Figures / Tables found in this record: