How eco-evolutionary principles can guide tree breeding and tree biotechnology for enhanced productivity

Franklin, Oskar; Palmroth, Sari; Nasholm, Torgny

doi:10.1093/treephys/tpu111

How eco-evolutionary principles can guide tree breeding and tree biotechnology for enhanced productivity

Journal Article · Sat Nov 01 00:00:00 EDT 2014 · Tree Physiology

DOI:https://doi.org/10.1093/treephys/tpu111· OSTI ID:1454931

Franklin, Oskar ^[1]; Palmroth, Sari ^[2]; Nasholm, Torgny ^[3]

International Institute for Applied Systems Analysis, Laxenburg (Austria). Ecosystems Services and Management Program; International Institute for Applied Systems Analysis
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

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.

View Accepted Manuscript (DOE)

Research Organization:: Duke Univ., Durham, NC (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)

Grant/Contract Number:: SC0006700; SC0006967

OSTI ID:: 1454931

Journal Information:: Tree Physiology, Journal Name: Tree Physiology Journal Issue: 11 Vol. 34; ISSN 0829-318X

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United States

Language:: English

References (61)

An ecohydrological perspective on drought-induced forest mortality Parolari, Anthony J.; Katul, Gabriel G.; Porporato, Amilcare Journal of Geophysical Research: Biogeosciences, Vol. 119, Issue 5 https://doi.org/10.1002/2013JG002592	journal	May 2014
Trends in wood density and structure are linked to prevention of xylem implosion by negative pressure Hacke, Uwe G.; Sperry, John S.; Pockman, William T. Oecologia, Vol. 126, Issue 4 https://doi.org/10.1007/s004420100628	journal	February 2001
Heterogeneous distribution of soil nutrients increase intra-specific competition in the clonal plant Glechoma hederacea Roiloa, Sergio R.; Sánchez-Rodríguez, Paula; Retuerto, Rubén Plant Ecology, Vol. 215, Issue 8 https://doi.org/10.1007/s11258-014-0338-7	journal	May 2014
Genetic transformation of eucalyptus Girijashankar, V. Physiology and Molecular Biology of Plants, Vol. 17, Issue 1 https://doi.org/10.1007/s12298-010-0048-0	journal	February 2011
Genetic Modification of Short Rotation Popular Wood: Properties for Ethanol Fuel and Fiber Productions Dinus, R. Critical Reviews in Plant Sciences, Vol. 20, Issue 1 https://doi.org/10.1016/S0735-2689(01)80012-5	journal	January 2001
Plant diversity and drought: The role of deep roots Lindh, Magnus; Zhang, Lai; Falster, Daniel Ecological Modelling, Vol. 290 https://doi.org/10.1016/j.ecolmodel.2014.05.008	journal	October 2014
Managing productivity and drought risk in Eucalyptus globulus plantations in south-western Australia White, Donald A.; Crombie, D. Stuart; Kinal, Joe Forest Ecology and Management, Vol. 259, Issue 1 https://doi.org/10.1016/j.foreco.2009.09.039	journal	December 2009
The Brazil Eucalyptus Potential Productivity Project: Influence of water, nutrients and stand uniformity on wood production Stape, Jose Luiz; Binkley, Dan; Ryan, Michael G. Forest Ecology and Management, Vol. 259, Issue 9 https://doi.org/10.1016/j.foreco.2010.01.012	journal	April 2010
Linking definitions, mechanisms, and modeling of drought-induced tree death Anderegg, William R. L.; Berry, Joseph A.; Field, Christopher B. Trends in Plant Science, Vol. 17, Issue 12 https://doi.org/10.1016/j.tplants.2012.09.006	journal	December 2012
Competition effects in cocoa (Theobroma cacao L.) hybrid trials Lachenaud, Ph.; Montagnon, C. Euphytica, Vol. 128, Issue 1, p. 97-104 https://doi.org/10.1023/A:1020669526647	journal	January 2002
Forest biotech and climate change Fenning, Trevor M.; Walter, Christian; Gartland, Kevan M. A. Nature Biotechnology, Vol. 26, Issue 6 https://doi.org/10.1038/nbt0608-615	journal	June 2008
Increasing drought under global warming in observations and models Dai, Aiguo Nature Climate Change, Vol. 3, Issue 1 https://doi.org/10.1038/nclimate1633	journal	August 2012
Fitness and its role in evolutionary genetics Orr, H. Allen Nature Reviews Genetics, Vol. 10, Issue 8 https://doi.org/10.1038/nrg2603	journal	August 2009
Tragedy of the commons as a result of root competition Gersani, Mordechai; Brown, Joel s.; O'Brien, Erin E. Journal of Ecology, Vol. 89, Issue 4 https://doi.org/10.1046/j.0022-0477.2001.00609.x	journal	August 2001
The Ball-Berry-Leuning and Tardieu-Davies stomatal models: synthesis and extension within a spatially aggregated picture of guard cell function Dewar, R. C. Plant, Cell and Environment, Vol. 25, Issue 11 https://doi.org/10.1046/j.1365-3040.2002.00909.x	journal	November 2002
A coupled model of stomatal conductance, photosynthesis and transpiration Tuzet, A.; Perrier, A.; Leuning, R. Plant, Cell and Environment, Vol. 26, Issue 7 https://doi.org/10.1046/j.1365-3040.2003.01035.x	journal	July 2003
A generic model of thinning and stand density effects on forest growth, mortality and net increment Franklin, Oskar; Aoki, Kentaro; Seidl, Rupert Annals of Forest Science, Vol. 66, Issue 8 https://doi.org/10.1051/forest/2009073	journal	January 2009
Transgenic Populus Trees for Forest Products, Bioenergy, and Functional Genomics Ye, Xia; Busov, Victor; Zhao, Nan Critical Reviews in Plant Sciences, Vol. 30, Issue 5 https://doi.org/10.1080/07352689.2011.605737	journal	September 2011
Strategy Space and the Disturbance Spectrum: A Life‐History Model for Tree Species Coexistence Loehle, Craig The American Naturalist, Vol. 156, Issue 1 https://doi.org/10.1086/303369	journal	July 2000
Least‐Cost Input Mixtures of Water and Nitrogen for Photosynthesis Wright, Ian J.; Reich, Peter B.; Westoby, Mark The American Naturalist, Vol. 161, Issue 1 https://doi.org/10.1086/344920	journal	January 2003
Yield–trait performance landscapes: from theory to application in breeding maize for drought tolerance Messina, Carlos D.; Podlich, Dean; Dong, Zhanshan Journal of Experimental Botany, Vol. 62, Issue 3 https://doi.org/10.1093/jxb/erq329	journal	November 2010
Any trait or trait-related allele can confer drought tolerance: just design the right drought scenario Tardieu, F. Journal of Experimental Botany, Vol. 63, Issue 1 https://doi.org/10.1093/jxb/err269	journal	September 2011
A model analysis of the influence of root and foliage allocation on forest production and competition between trees King, D. A. Tree Physiology, Vol. 12, Issue 2 https://doi.org/10.1093/treephys/12.2.119	journal	March 1993
Genomic and physiological approaches to advancing forest tree improvement Nelson, C. D.; Johnsen, K. H. Tree Physiology, Vol. 28, Issue 7 https://doi.org/10.1093/treephys/28.7.1135	journal	July 2008
Transpiration modulates phosphorus acquisition in tropical tree seedlings Cernusak, L. A.; Winter, K.; Turner, B. L. Tree Physiology, Vol. 31, Issue 8 https://doi.org/10.1093/treephys/tpr077	journal	August 2011
Modeling carbon allocation in trees: a search for principles Franklin, O.; Johansson, J.; Dewar, R. C. Tree Physiology, Vol. 32, Issue 6 https://doi.org/10.1093/treephys/tpr138	journal	January 2012
Investigating the drought-stress response of hybrid poplar genotypes by metabolite profiling Barchet, G. L. H.; Dauwe, R.; Guy, R. D. Tree Physiology, Vol. 34, Issue 11 https://doi.org/10.1093/treephys/tpt080	journal	October 2013
Genetic strategies for dissecting complex traits in biomass willows (Salix spp.) Hanley, S. J.; Karp, A. Tree Physiology, Vol. 34, Issue 11 https://doi.org/10.1093/treephys/tpt089	journal	November 2013
Condensed tannin biosynthesis and polymerization synergistically condition carbon use, defense, sink strength and growth in Populus Harding, S. A.; Xue, L. -J.; Du, L. Tree Physiology, Vol. 34, Issue 11 https://doi.org/10.1093/treephys/tpt097	journal	December 2013
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 Arango-Velez, A.; Gonzalez, L. M. G.; Meents, M. J. Tree Physiology, Vol. 34, Issue 11 https://doi.org/10.1093/treephys/tpt101	journal	December 2013
Molecular and physiological responses to abiotic stress in forest trees and their relevance to tree improvement Harfouche, A.; Meilan, R.; Altman, A. Tree Physiology, Vol. 34, Issue 11 https://doi.org/10.1093/treephys/tpu012	journal	April 2014
Integrating plant hydraulics and gas exchange along the drought-response trait spectrum Manzoni, S. Tree Physiology, Vol. 34, Issue 10 https://doi.org/10.1093/treephys/tpu088	journal	October 2014
Genetics of superior growth traits in trees are being mapped but will the faster-growing risk-takers make it in the wild? Nasholm, T.; Palmroth, S.; Ganeteg, U. Tree Physiology, Vol. 34, Issue 11 https://doi.org/10.1093/treephys/tpu112	journal	November 2014
Overexpression of a Plasma Membrane Aquaporin in Transgenic Tobacco Improves Plant Vigor under Favorable Growth Conditions but Not under Drought or Salt Stress Aharon, Refael; Shahak, Yosepha; Wininger, Smadar The Plant Cell, Vol. 15, Issue 2 https://doi.org/10.1105/tpc.009225	journal	January 2003
Proteins for Transport of Water and Mineral Nutrients across the Membranes of Plant Cells Chrispeels, Maarten J.; Crawford, Nigel M.; Schroeder, Julian I. The Plant Cell, Vol. 11, Issue 4 https://doi.org/10.1105/tpc.11.4.661	journal	April 1999
The variability of stomatal sensitivity to leaf water potential across tree species indicates a continuum between isohydric and anisohydric behaviours Klein, Tamir Functional Ecology, Vol. 28, Issue 6 https://doi.org/10.1111/1365-2435.12289	journal	May 2014
Competitive interactions across a soil fertility gradient in a multispecies forest Coates, K. David; Lilles, Erica B.; Astrup, Rasmus Journal of Ecology, Vol. 101, Issue 3 https://doi.org/10.1111/1365-2745.12072	journal	March 2013
The world-wide ‘fast-slow’ plant economics spectrum: a traits manifesto Reich, Peter B. Journal of Ecology, Vol. 102, Issue 2 https://doi.org/10.1111/1365-2745.12211	journal	February 2014
Balancing the costs of carbon gain and water transport: testing a new theoretical framework for plant functional ecology Prentice, I. Colin; Dong, Ning; Gleason, Sean M. Ecology Letters, Vol. 17, Issue 1 https://doi.org/10.1111/ele.12211	journal	November 2013
Let the concept of trait be functional! Violle, Cyrille; Navas, Marie-Laure; Vile, Denis Oikos, Vol. 116, Issue 5 https://doi.org/10.1111/j.0030-1299.2007.15559.x	journal	May 2007
Forest fine-root production and nitrogen use under elevated CO ₂ : contrasting responses in evergreen and deciduous trees explained by a common principle Franklin, Oskar; McMURTRIE, Ross E.; Iversen, Colleen M. Global Change Biology, Vol. 15, Issue 1 https://doi.org/10.1111/j.1365-2486.2008.01710.x	journal	January 2009
Strategies of a Bornean tropical rainforest water use as a function of rainfall regime: isohydric or anisohydric?: Strategies of a tropical rainforest water use Kumagai, Tomo'Omi; Porporato, Amilcare Plant, Cell & Environment, Vol. 35, Issue 1 https://doi.org/10.1111/j.1365-3040.2011.02428.x	journal	October 2011
Towards a worldwide wood economics spectrum Chave, Jerome; Coomes, David; Jansen, Steven Ecology Letters, Vol. 12, Issue 4 https://doi.org/10.1111/j.1461-0248.2009.01285.x	journal	April 2009
Optimal nitrogen allocation controls tree responses to elevated CO ₂ Franklin, Oskar New Phytologist, Vol. 174, Issue 4 https://doi.org/10.1111/j.1469-8137.2007.02063.x	journal	June 2007
Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? McDowell, Nate; Pockman, William T.; Allen, Craig D. New Phytologist, Vol. 178, Issue 4 https://doi.org/10.1111/j.1469-8137.2008.02436.x	journal	June 2008
Improving plant stress tolerance and yield production: is the tonoplast aquaporin SlTIP2;2 a key to isohydric to anisohydric conversion? Sade, Nir; Vinocur, Basia J.; Diber, Alex New Phytologist, Vol. 181, Issue 3 https://doi.org/10.1111/j.1469-8137.2008.02689.x	journal	November 2008
The importance of wood traits and hydraulic conductance for the performance and life history strategies of 42 rainforest tree species Poorter, Lourens; McDonald, Imole; Alarcón, Alfredo New Phytologist, Vol. 185, Issue 2 https://doi.org/10.1111/j.1469-8137.2009.03092.x	journal	November 2009
Biomass allocation to leaves, stems and roots: meta-analyses of interspecific variation and environmental control: Tansley review Poorter, Hendrik; Niklas, Karl J.; Reich, Peter B. New Phytologist, Vol. 193, Issue 1 https://doi.org/10.1111/j.1469-8137.2011.03952.x	journal	November 2011
Towards optimizing wood development in bioenergy trees: Research review Nieminen, Kaisa; Robischon, Marcel; Immanen, Juha New Phytologist, Vol. 194, Issue 1 https://doi.org/10.1111/j.1469-8137.2011.04011.x	journal	December 2011
Genomic selection for growth and wood quality in Eucalyptus: capturing the missing heritability and accelerating breeding for complex traits in forest trees Resende, Marcos D. V.; Resende, Márcio F. R.; Sansaloni, Carolina P. New Phytologist, Vol. 194, Issue 1 https://doi.org/10.1111/j.1469-8137.2011.04038.x	journal	February 2012
Forests trapped in nitrogen limitation - an ecological market perspective on ectomycorrhizal symbiosis Franklin, Oskar; Näsholm, Torgny; Högberg, Peter New Phytologist, Vol. 203, Issue 2 https://doi.org/10.1111/nph.12840	journal	May 2014
A new look at water transport regulation in plants Martínez-Vilalta, Jordi; Poyatos, Rafael; Aguadé, David New Phytologist, Vol. 204, Issue 1 https://doi.org/10.1111/nph.12912	journal	July 2014
Tree life history strategies: the role of defenses Loehle, Craig Canadian Journal of Forest Research, Vol. 18, Issue 2 https://doi.org/10.1139/x88-032	journal	February 1988
Herbivory and Plant Defenses in Tropical Forests Coley, P. D.; Barone, J. A. Annual Review of Ecology and Systematics, Vol. 27, Issue 1 https://doi.org/10.1146/annurev.ecolsys.27.1.305	journal	November 1996
Effects of tree Density and Stand age on Carbon Allocation Patterns in Postfire Lodgepole pine Litton, Creighton M.; Ryan, Michael G.; Knight, Dennis H. Ecological Applications, Vol. 14, Issue 2 https://doi.org/10.1890/02-5291	journal	April 2004
COMPETITION AMONG EUCALYPTUS TREES DEPENDS ON GENETIC VARIATION AND RESOURCE SUPPLY Boyden, Suzanne; Binkley, Dan; Stape, José Luiz Ecology, Vol. 89, Issue 10 https://doi.org/10.1890/07-1733.1	journal	October 2008
Climate and weather influences on spatial temporal patterns of mountain pine beetle populations in Washington and Oregon Preisler, Haiganoush K.; Hicke, Jeffrey A.; Ager, Alan A. Ecology, Vol. 93, Issue 11 https://doi.org/10.1890/11-1412.1	journal	November 2012
Resource limitation in a competitive context determines complex plant responses to experimental resource additions Farrior, Caroline E.; Tilman, David; Dybzinski, Ray Ecology, Vol. 94, Issue 11 https://doi.org/10.1890/12-1548.1	journal	November 2013
A New Method to Assess Competition in Coffee Clonal Trials with Single-Tree Plots in Côte d'Ivoire Montagnon, C.; Flori, A.; Cilas, C. Agronomy Journal, Vol. 93, Issue 1 https://doi.org/10.2134/agronj2001.931227x	journal	January 2001
Mortality Rates of 205 Neotropical Tree and Shrub Species and the Impact of a Severe Drought Condit, Richard; Hubbell, Stephen P.; Foster, Robin B. Ecological Monographs, Vol. 65, Issue 4 https://doi.org/10.2307/2963497	journal	February 1995
Risk-taking plants: Anisohydric behavior as a stress-resistance trait Sade, Nir; Gebremedhin, Alem; Moshelion, Menachem Plant Signaling & Behavior, Vol. 7, Issue 7 https://doi.org/10.4161/psb.20505	journal	July 2012

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How eco-evolutionary principles can guide tree breeding and tree biotechnology for enhanced productivity

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