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Optimal partitioning theory revisited: Nonstructural carbohydrates dominate root mass responses to nitrogen

Under optimal partitioning theory (OPT), plants preferentially allocate biomass to acquire the resource that most limits growth. Within this framework, higher root mass under low nutrients is often assumed to reflect an allocation response to build more absorptive surface. However, higher root mass...

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Published in:Ecology (Durham) 2010, Vol.91 (1), p.166-179
Main Authors: Kobe, Richard K, Iyer, Meera, Walters, Michael B
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description Under optimal partitioning theory (OPT), plants preferentially allocate biomass to acquire the resource that most limits growth. Within this framework, higher root mass under low nutrients is often assumed to reflect an allocation response to build more absorptive surface. However, higher root mass also could result from increased storage of total nonstructural carbohydrates (TNC) without an increase in non‐storage mass or root surface area. To test the relative contributions of TNC and non‐storage mass as components of root mass responses to resources, we grew seedlings of seven northern hardwood tree species (black, red, and white oak, sugar and red maple, American beech, and black cherry) in a factorial light × nitrogen (N) greenhouse experiment. Because root mass is a coarse metric of absorptive surface, we also examined treatment effects on fine‐root surface area (FRSA). Consistent with OPT, total root mass as a proportion of whole‐plant mass generally was greater in low vs. high N. However, changes in root mass were influenced by TNC mass in all seven species and were especially strong in the three oak species. In contrast, non‐storage mass contributed to increased total root mass under low N in three of the seven species. Root morphology also responded, with higher fine‐root surface area (normalized to root mass) under low vs. high N in four species. Although biomass partitioning responses to resources were consistent with OPT, our results challenge the implicit assumption that increases in root mass under low nutrient levels primarily reflect allocation shifts to build more root surface area. Rather, root responses to low N included increases in: TNC, non‐storage mass and fine‐root surface area, with increases in TNC being the largest and most consistent of these responses. The greatest TNC accumulation occurred when C was abundant relative to N. Total nonstructural carbohydrates storage could provide seedlings a carbon buffer when respiratory or growth demands are not synchronized with photosynthesis, flexibility in responding to uncertain and fluctuating abiotic and biotic conditions, and increased access to soil resources by providing an energy source for mycorrhizae, decomposers in the rhizosphere, or root uptake of nutrients.
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Within this framework, higher root mass under low nutrients is often assumed to reflect an allocation response to build more absorptive surface. However, higher root mass also could result from increased storage of total nonstructural carbohydrates (TNC) without an increase in non‐storage mass or root surface area. To test the relative contributions of TNC and non‐storage mass as components of root mass responses to resources, we grew seedlings of seven northern hardwood tree species (black, red, and white oak, sugar and red maple, American beech, and black cherry) in a factorial light × nitrogen (N) greenhouse experiment. Because root mass is a coarse metric of absorptive surface, we also examined treatment effects on fine‐root surface area (FRSA). Consistent with OPT, total root mass as a proportion of whole‐plant mass generally was greater in low vs. high N. However, changes in root mass were influenced by TNC mass in all seven species and were especially strong in the three oak species. In contrast, non‐storage mass contributed to increased total root mass under low N in three of the seven species. Root morphology also responded, with higher fine‐root surface area (normalized to root mass) under low vs. high N in four species. Although biomass partitioning responses to resources were consistent with OPT, our results challenge the implicit assumption that increases in root mass under low nutrient levels primarily reflect allocation shifts to build more root surface area. Rather, root responses to low N included increases in: TNC, non‐storage mass and fine‐root surface area, with increases in TNC being the largest and most consistent of these responses. The greatest TNC accumulation occurred when C was abundant relative to N. 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Psychology</subject><subject>General aspects</subject><subject>greenhouse experimentation</subject><subject>Greenhouses</subject><subject>hardwood</subject><subject>Maple sugar</subject><subject>Models, Biological</subject><subject>mycorrhizae</subject><subject>Nitrogen</subject><subject>Nitrogen - pharmacology</subject><subject>nitrogen content</subject><subject>nutrient content</subject><subject>nutrient uptake</subject><subject>nutrients</subject><subject>optimal partitioning theory</subject><subject>photosynthesis</subject><subject>Plant ecology</subject><subject>Plant Leaves - drug effects</subject><subject>Plant Leaves - metabolism</subject><subject>Plant roots</subject><subject>Plant Roots - drug effects</subject><subject>Plant Roots - metabolism</subject><subject>Plant Stems - drug effects</subject><subject>Plant Stems - metabolism</subject><subject>Plants</subject><subject>Prunus</subject><subject>rhizosphere</subject><subject>Roots of functions</subject><subject>Seedlings</subject><subject>Soil resources</subject><subject>Species Specificity</subject><subject>storage</subject><subject>surface area</subject><subject>Surface areas</subject><subject>Theory</subject><subject>total nonstructural carbohydrates</subject><subject>trees</subject><subject>Trees - classification</subject><subject>Trees - metabolism</subject><issn>0012-9658</issn><issn>1939-9170</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2010</creationdate><recordtype>article</recordtype><recordid>eNp9kl-L1DAUxYso7rj64AdQi6DiQ9d7k0ya-CbD-gcW90H3waeSpulsxk7TTVJlvr13mNEFQQMhgfM75ya5KYrHCGeoNLwBXQGw-gzvFAvUXFcaa7hbLACQVVou1UnxIKUN0ECh7hcnDLgCBnJRfL-cst-aoZxMzD77MPpxXeZrF-KujO6HTz677m35OYwpx9nmORJsTWzD9a6LJrtUdmHrR9qVMYRcbk1K5EwTOUjMoRx9jmHtxofFvd4MyT06rqfF1fvzr6uP1cXlh0-rdxeVFZLLSuhaOmlb2zKOLfZMs1bp2qJijguxFF2rFLPSobSgLRdc1Nj1srPW4lI7flq8OuROMdzMLuVm65N1w2BGF-bU1JyrGoSoiXz5X5IhR5qSwOd_gZswx5FuQQwdDusaCHp9gGwMKUXXN1Okt427BqHZN6oB3ewb1SCxT4-Bc7t13R_yd2cIeHEETLJm6KMZrU-3HFuC0FoTJw7cTz-43b8rNuerbwwQNCLKffyTg22Tcoi3sUspETgn_dlB701ozDpS6asv5Jf0h7RWXPFfJUq89A</recordid><startdate>2010</startdate><enddate>2010</enddate><creator>Kobe, Richard K</creator><creator>Iyer, Meera</creator><creator>Walters, Michael B</creator><general>Ecological Society of America</general><scope>FBQ</scope><scope>IQODW</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QG</scope><scope>7SN</scope><scope>7SS</scope><scope>7ST</scope><scope>7T7</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>K9.</scope><scope>P64</scope><scope>RC3</scope><scope>SOI</scope><scope>M7N</scope><scope>7X8</scope></search><sort><creationdate>2010</creationdate><title>Optimal partitioning theory revisited: Nonstructural carbohydrates dominate root mass responses to nitrogen</title><author>Kobe, Richard K ; Iyer, Meera ; Walters, Michael B</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4636-4976e6cbcb231b1f292b897c182e34454db882c6e16c09c343471df6dccc159e3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2010</creationdate><topic>Animal and plant ecology</topic><topic>Animal, plant and microbial ecology</topic><topic>Biological and medical sciences</topic><topic>Biomass</topic><topic>biomass allocation</topic><topic>biomass partitioning</topic><topic>Carbohydrate Metabolism</topic><topic>Carbohydrates</topic><topic>carbon</topic><topic>dry matter partitioning</topic><topic>Ecology</topic><topic>energy</topic><topic>Experiments</topic><topic>Fagus grandifolia</topic><topic>fine root surface area</topic><topic>fine roots</topic><topic>Flowers &amp; plants</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>General aspects</topic><topic>greenhouse experimentation</topic><topic>Greenhouses</topic><topic>hardwood</topic><topic>Maple sugar</topic><topic>Models, Biological</topic><topic>mycorrhizae</topic><topic>Nitrogen</topic><topic>Nitrogen - pharmacology</topic><topic>nitrogen content</topic><topic>nutrient content</topic><topic>nutrient uptake</topic><topic>nutrients</topic><topic>optimal partitioning theory</topic><topic>photosynthesis</topic><topic>Plant ecology</topic><topic>Plant Leaves - drug effects</topic><topic>Plant Leaves - metabolism</topic><topic>Plant roots</topic><topic>Plant Roots - drug effects</topic><topic>Plant Roots - metabolism</topic><topic>Plant Stems - drug effects</topic><topic>Plant Stems - metabolism</topic><topic>Plants</topic><topic>Prunus</topic><topic>rhizosphere</topic><topic>Roots of functions</topic><topic>Seedlings</topic><topic>Soil resources</topic><topic>Species Specificity</topic><topic>storage</topic><topic>surface area</topic><topic>Surface areas</topic><topic>Theory</topic><topic>total nonstructural carbohydrates</topic><topic>trees</topic><topic>Trees - classification</topic><topic>Trees - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kobe, Richard K</creatorcontrib><creatorcontrib>Iyer, Meera</creatorcontrib><creatorcontrib>Walters, Michael B</creatorcontrib><collection>AGRIS</collection><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Environment Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>ProQuest Health &amp; Medical Complete (Alumni)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>Environment Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>MEDLINE - Academic</collection><jtitle>Ecology (Durham)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kobe, Richard K</au><au>Iyer, Meera</au><au>Walters, Michael B</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Optimal partitioning theory revisited: Nonstructural carbohydrates dominate root mass responses to nitrogen</atitle><jtitle>Ecology (Durham)</jtitle><addtitle>Ecology</addtitle><date>2010</date><risdate>2010</risdate><volume>91</volume><issue>1</issue><spage>166</spage><epage>179</epage><pages>166-179</pages><issn>0012-9658</issn><eissn>1939-9170</eissn><coden>ECGYAQ</coden><abstract>Under optimal partitioning theory (OPT), plants preferentially allocate biomass to acquire the resource that most limits growth. 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However, changes in root mass were influenced by TNC mass in all seven species and were especially strong in the three oak species. In contrast, non‐storage mass contributed to increased total root mass under low N in three of the seven species. Root morphology also responded, with higher fine‐root surface area (normalized to root mass) under low vs. high N in four species. Although biomass partitioning responses to resources were consistent with OPT, our results challenge the implicit assumption that increases in root mass under low nutrient levels primarily reflect allocation shifts to build more root surface area. Rather, root responses to low N included increases in: TNC, non‐storage mass and fine‐root surface area, with increases in TNC being the largest and most consistent of these responses. The greatest TNC accumulation occurred when C was abundant relative to N. Total nonstructural carbohydrates storage could provide seedlings a carbon buffer when respiratory or growth demands are not synchronized with photosynthesis, flexibility in responding to uncertain and fluctuating abiotic and biotic conditions, and increased access to soil resources by providing an energy source for mycorrhizae, decomposers in the rhizosphere, or root uptake of nutrients.</abstract><cop>Washington, DC</cop><pub>Ecological Society of America</pub><pmid>20380206</pmid><doi>10.1890/09-0027.1</doi><tpages>14</tpages></addata></record>
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source Wiley; JSTOR
subjects Animal and plant ecology
Animal, plant and microbial ecology
Biological and medical sciences
Biomass
biomass allocation
biomass partitioning
Carbohydrate Metabolism
Carbohydrates
carbon
dry matter partitioning
Ecology
energy
Experiments
Fagus grandifolia
fine root surface area
fine roots
Flowers & plants
Fundamental and applied biological sciences. Psychology
General aspects
greenhouse experimentation
Greenhouses
hardwood
Maple sugar
Models, Biological
mycorrhizae
Nitrogen
Nitrogen - pharmacology
nitrogen content
nutrient content
nutrient uptake
nutrients
optimal partitioning theory
photosynthesis
Plant ecology
Plant Leaves - drug effects
Plant Leaves - metabolism
Plant roots
Plant Roots - drug effects
Plant Roots - metabolism
Plant Stems - drug effects
Plant Stems - metabolism
Plants
Prunus
rhizosphere
Roots of functions
Seedlings
Soil resources
Species Specificity
storage
surface area
Surface areas
Theory
total nonstructural carbohydrates
trees
Trees - classification
Trees - metabolism
title Optimal partitioning theory revisited: Nonstructural carbohydrates dominate root mass responses to nitrogen
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